Wastewater quality and required water quality for

irrigation purposes
Pierre P. Renault, Sabine Houot, Enrique Barriuso, Chrystelle Langlais

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Pierre P. Renault, Sabine Houot, Enrique Barriuso, Chrystelle Langlais. Wastewater quality and
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Wastewater quality
and required
water quality for
irrigation purposes

Pierre Renault

January 2014
 Wastewater quality and required water quality for irrigation purposes AGADAPT

AgAdapt R&D Project / Wastewater quality and required water quality for
irrigation purposes

Authors: Pierre RENAULT Date: March 2014

Division: Wastewater and Environment

Reference:

Recipients

André CHANZY INRA – AgAdapt Coordinator

Liliana DI PIETRO INRA – EMMAH Leader

Guy RICHARD INRA – Leader of the Environment and Agronomy Division

Jean-François SOUSSANA DRI&P – ARI Program management

Chrystelle LANGLAIS CIRSEE (SUEZ Environment) – KIC Partner

Authors Scientific validation Final validation

Pierre RENAULT Liliana DI PIETRO Guy RICHARD

Final acceptance

Level of confidentiality

This document is the property of INRA. It cannot be used or disclosed without prior written
permission.

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AGADAPT Wastewater quality and required water quality for irrigation purposes

Report summary:

This review summarizes the main issues related to wastewater reuse for agricultural
irrigation. It discusses successively the reuse itself, the sanitary, environmental and agricultural
hazards caused by human pathogens and chemicals in wastewater, the economic sustainability
of wastewater reuse, and the means either legal (guidelines or regulations and standards) or
economic (tariffs, subsidies, taxes) to promote wastewater reuse while minimizing the risks.
Proposals are made in the conclusion to improve and promote wastewater reuse in a more
rational framework. As human enteric viruses are more and more often incriminated in human
outbreaks, Appendix 1 provides a review on their fate in the environment.
Although wastewater reuse can address simultaneously problems in water quantity and quality,
it remains low in most of the European countries. Wastewater is preferentially reused for crop
irrigation in South European countries having a high Water Stress Index, high water needs for
crops and large volumes of wastewater produced (Cyprus, Malta, Spain and Italy), and reuse
will increase further in these countries. Wastewater reuse remains low in South European
countries having a lower water stress index (Greece, France and Portugal), but it should
increase because of global warming and the increase in frequency of extreme droughts. In more
Northern European countries where water deficit for crops is lower or non-existent, wastewater
may be reused locally for irrigation (e.g. in Germany) and/or in other sectors such as urban and
industry sectors (e.g. in Belgium); several large cities and conurbations depend on recharging
the surface and ground water bodies by treated wastewater. We have obtained nearly no
information on wastewater reuse in Bulgaria that has one of the highest water stress index of
European countries.
Public acceptance is good, but some opposition exists ("psychologically repugnant", "lack of
purity", "can cause disease") and justifies information to prevent project failure. Actual risks
include sanitary, environmental and agricultural hazards; they result from the presence in raw
sewage of human pathogens and various inorganic and organic compounds. Although it is
possible to produce water of almost any quality desired from wastewater, cost-effectiveness of
treatments must be ensured. In order to protect conventional water resources, reduce the risks
inherent in the use of wastewaters to tolerable levels, and insure the economic sustainability of
reuse projects, the management of conventional and alternative water resources requires
appropriate regulations and standards, as well as economic policy. Since water requirements,
properties of raw wastewaters, and human resistance to pathogens vary with regions, it would
not be appropriate to use the same regulations and standards in all European countries.
However, the current diversity of rules is not scientifically justified and lead to inequalities.
Europe could propose guidelines with maximum tolerated risks and a methodological framework
to elaborate regional or national regulations and standards that account for local specificities. A
distinction should then be performed between crops for local markets or for export.
New tools to support decisions such as computer programs are required. They have to account
simultaneously for treatments, hazards, and cost-benefit considerations (with the monetary
valuations of changes in human health, environment and crops), whereas existing tools only
address part of the problem: they include models for quantitative microbial risk assessment,
decision support systems for the configuration of wastewater treatment plants, and methods for
the monetary valuation of the positive and negative changes in the environment. In addition,

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 Wastewater quality and required water quality for irrigation purposes AGADAPT

there are still gaps in knowledge and not enough data or parameters estimated correctly to
ensure the reliability of these models. First, the fate of pollutants (including pathogens) is not
enough known and described to properly inform quantitative microbial risk assessment; second,
the monetary valuation of environmental changes is recent and probably requires a step back
with, where possible, a comparison of methods; third, several studies have questioned the
relevance of standards in selected microbial indicators and recent methodological
developments suggest that the direct monitoring of some pathogens would be more appropriate
in the next years.

Key words: wastewater, reuse, irrigation, hazards, enteric pathogens, chemical pollutants,
regulations, guidelines, standards, economic sustainability, cost-effectiveness,
yuck factor

Contributors:

Pierre Renault*: INRA, UMR 1114 EMMAH, Domaine Saint Paul, Site Agroparc, CS 40 509,
84914 Avignon Cedex 9, France (E-mail:[email protected];
Tel.: +33(0)4 32.72.22.23; Fax: +33 (0)4.32.72.22.10)
Sabine Houot, Enrique Barriuso: UMR INRA-AgroParisTech Environnement et Grandes
Cultures (Equipe Sol), BP 01, 78850 Thiverval-Grignon, France
([email protected] and [email protected])
Chrystelle Langlais: SUEZ-Environnement, CIRSEE, 38 rue du Président Wilson, 78230 Le
Pecq, France ([email protected])

*: Correspondance [email protected]

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AGADAPT Wastewater quality and required water quality for irrigation purposes

TABLE OF CONTENTS

Introduction: wastewater recycling as a mean to cope problems in water quantity and quality ... 7
Hazards related to wastewater reuse for irrigation ................................................................... 14
Technological hazards.......................................................................................................... 17
Health/sanitary hazards ........................................................................................................ 19
Biological hazards (viruses, bacteria, protozoa and helminth eggs) .................................. 19
Major human enteric and water-based pathogens ........................................................ 20
Quantitative microbial risk assessment ......................................................................... 24
Bioindicators of human pathogens................................................................................ 27
Chemical hazards ............................................................................................................. 29
Environmental and agricultural hazards ................................................................................ 30
Economic sustainability of wastewater reuse in irrigation: an overview .................................... 31
Regulations: the need for stronger scientific basis ................................................................... 33
The need of new matrix of multi-criteria requirements for water reuse at regional scales ......... 37
Conclusions ............................................................................................................................. 39
References .............................................................................................................................. 42
References from the authors ................................................................................................ 42
External References ............................................................................................................. 42
Appendix 1: Virus fate in the environment ................................................................................ 68
Appendix 2: Organic contaminants in wastewaters .................................................................. 75
Introduction: main sources of organic contaminants in wastewaters ..................................... 75
Organic contaminants in the environment; link with wastewaters ......................................... 77
Efficiency of organic pollutant removal in WWTP.................................................................. 78
Organic pollutant fate in the environment after wastewater spreading .................................. 80
Risk due to the organic contaminants in irrigation wastewaters ............................................ 81
Contamination of conventional water resources ................................................................ 81
Uptake from soils and plants contamination by organic pollutants ..................................... 83
Ecotoxic effect of organic contaminants ............................................................................ 84
Concluding remarks ............................................................................................................. 85

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Wastewater quality and required water quality for irrigation purposes AGADAPT

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AGADAPT Wastewater quality and required water quality for irrigation purposes

Wastewater quality and required water quality

for irrigation purposes

By Pierre Renault
INRA-UAPV UMR Environnement Méditerranéen et Modélisation des Agro-Hydrosystèmes,
Avignon, France

Introduction: wastewater recycling as a mean to cope

problems in water quantity and quality

The world is facing increasing problems of limited water resources (Scheierling et al.,
2010; Escobar, 2010; Anderson, 2006; Lazarova and Asano, 2005) illustrated by the water
stress index (Bixio et al., 2006), the depletion of groundwater tables (Cao et al., 2013; Taylor et
al., 2012; Frederick, 2006) and the increase in the Palmer drought severity index (Bates et al.,
2008). They result from population growth – e.g. in North Africa (Qadir et al., 2010; Ouanouki et
al., 2009), in Jordan (Alfarra et al., 2011) and in arid West States of the USA –, from Earth
global warning as in South European Countries (Bixio et al., 2006) – e.g. in Greece (García-
Ruiz et al., 2011), Italy (García-Ruiz et al., 2011; Van der Bruggen, 2010; Giungato et al., 2010)
and Spain (Estrela and Vargas, 2012; García-Ruiz et al., 2011; Pedrero et al., 2010; Esteban
and De Miguel, 2008) –, from increasing urbanization (Kennedy et al., 2012; Bates et al., 2008)
– e.g. in Windhoek (Du Pisani, 2006), San Diego (Steirer and Thorsen, 2013) and Mexico City
(Tortajada and Castelán, 2003) –, the main problem being then to have water available at the
right place and the right time with the required quality (Angelakis et al., 1999), and from the
increase of recreational uses (Sinclair et al., 2009; Hamilton et al., 2007b). Frederick (2006)
estimated that about 10% of the world’s agricultural food output depends on non-renewable
groundwater supplies, with water tables falling a meter or more annually in parts of Mexico,
India, China, the USA, and several other countries. The world is facing simultaneously a
decrease in the quality of conventional waters (Van der Bruggen, 2010) subject to chemical
and microbiological pollutions (Bradbury et al., 2013; Van der Bruggen, 2010; Craun et al.,
2006; Tillaut et al., 2004; Cournot et al., 2001). The overexploitation of coastal aquifers has led
to their salinization (Giungato et al., 2010). And the discharge of inadequately treated
wastewater (Leverenz et al., 2011; Okoh et al., 2007), usually only after a secondary treatment
in Europe (European Commission, 2011; Commission of the European Communities, 1998;
CEC, 1991), but sometimes after a lighter treatment, see without treatment especially in several
developing countries (Raschid-Sally and Jayakody, 2008; Ensink and van der Hoek, 2006;
Downs et al., 1999), has led to contaminations of rivers and aquifers by mineral and organic
chemicals (Leverenz et al., 2011), as well as human pathogens (helminth eggs, protozoa,
bacteria and viruses) (Pachepsky et al, 2011; Servais et al., 2009). In the European Community,

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these problems may be increased by the imperfect compliance (European Commission, 2011)
with the Council Directive 91/271/EEC (CEC, 1991) and by the increase of the populations of
large cities – e.g. Milan (Mazzini et al., 2013) –. The poor quality of conventional water has led
to human recreational or drinkable waterborne outbreaks (Craun et al. 2010; Sinclair et al.,
2009; Reynolds et al., 2008; Craun et al., 2006; Calderon et al., 2005), to various environmental
effects like decrease in the biodiversity of rivers, soil compaction, eutrophication (Thomas et al.,
2010; WHO-EC, 2002), and it may affect other human activities – e.g. tourism –. More than
energy, the scarcity and quality of water will limit further growth of established
economies and the development of new ones (Van der Bruggen, 2010), as it is already the
case for China (Yi et al., 2011).

Several actions to cope problems of water quantity and quality can be considered: an
improved maintenance of drinkable water mains and sewers to reduce leakage and
contaminations (Craun et al., 2010; Reynolds et al., 2008), the reduction of irrigation that often
explains most of water consumption (Jiménez and Asano, 2008) through changes in land use
and agricultural practices, the sustainable discharge of wastewater in the environment, and the
transportation of conventional water over long distances as already performed – e.g. in the US
(Fort and Nelson, 2012), Israel (Tal, 2006), Spain (Downward and Taylor, 2007), between the
state of Johore in Malaysia and Singapore (King, 2011; Tortajada, 2006), and between Turkey
and Cyprus with a 107 km long pipeline that will go undersea and that should be completed in
2014 –. These actions may be completed by the reuse of wastewater (Bixio et al., 2008) for
irrigation (Angelakis and Durham, 2008), industrial purposes (Van der Bruggen, 2010; Levine
and Asano, 2002), urban uses (Van der Bruggen, 2010), domestic uses like toilet flushing (Van
der Bruggen, 2010; Radcliffe, 2004) and drinking (Leverenz and al., 2011; Du Pisani, 2006). At
the Earth scale, Van der Bruggen (2010) estimates than 60%, 30% and 10% of all reuse
applications are to be found in agricultural irrigation, in industries (especially cooling water and
process water recycling), and in irrigation of parks, sport field or for groundwater recharge by
percolation, respectively. These proportions are broadly consistent with the proportions of
conventional water uses: e.g., Levine and Asano (2002) noted that industrial water use
comprises about 25% of all worldwide water withdrawals. It is the objective of countries to
reclaim all the collected wastewaters – e.g. Cyprus (Papaiacovou and Papatheodoulou, 2013;
Fatta and Anayiotou, 2007; Fatta et al., 2005) and Israel (Brenner, 2012; Friedler, 2001) –. If all
wastewaters would be collected and reclaimed, their reuse could correspond to more
than about 5-15% of the country water consumptions. Wastewater reuse can be
supplemented by the more expensive desalination of salt or brackish water (Ghaffour et al.,
2013; Peñate and García-Rodríguez, 2012; Lattemann et al., 2011; Garud et al., 2011), the
desalination of treated wastewaters by reverse osmosis being also used to decrease their
salinity for irrigation – e.g. in Alicante wastewater treatment plant, Spain (Renault et al., 2013) –.

Although wastewater reuse in agricultural irrigation has been an old practice – e.g. in
Ancient Egypt and China (Van der Bruggen, 2010; Angelakis and Koutsoyiannis, 2003) and in
ancient Greece and the island of Crete (Lofrano and Brown, 2010; Angelakis et al., 2005) –, it
was not until the last quarter of the 20th century that water reuse appeared on the
international agenda, at first in industrialized countries such as America and Europe (Van

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AGADAPT Wastewater quality and required water quality for irrigation purposes

der Bruggen, 2010). Lofrano and Brown (2010) proposed a review on the evolution of
wastewater management through the ages with a special emphasis to its impacts on human
health and environment. Initially, it was no less than direct reuse of wastewater without any
treatment, apart from possible dilution (Van der Bruggen, 2010), as it is still the case on today in
numerous places like Pakistan (Ensink and van der Hoek, 2006), Mexico (Dows et al., 2000,
1999), and in several developing countries (Raschid-Sally and Jayakody, 2008); and common
practices exist in the developing world for families to reuse own wastewater, often for irrigation
(Van der Bruggen, 2010). In the Middle Age in large cities of Europe, severe problems arose
with surface water quality due to city population growth as rivers generally were used
simultaneously as sewers and for water supply. Several cholera outbreaks were thus observed
in London – e.g. in 1854 (Brody et al., 2000) –, Paris – e.g. in 1832 (Kudlick, 1999) –, and in
other big cities. In Amsterdam, problems have been amplified after the construction of a dam on
the Amstel River to prevent intrusion of saline water of the Flevo Lake, as the city's ring of
canals was soon highly polluted by discharge of wastewater (Van der Bruggen, 2010). It was
not until the 16th century that measures were taken (Van der Bruggen, 2010), which include the
establishment of sewage farms to "purify" wastewater by infiltration into the soil (Crook et al.,
2005; Asano, 2002): in Germany since about 1550 (Asano, 2006), the United Kingdom since
1700 (Asano, 2006), and in France near Paris in 1872 (Brissaud, 2002; Védry et al., 2001).
Wastewater reuse in industry developed only during the 20th century (Levine and Asano, 2002).
The dominant water-using industries include electric power generation, petroleum refining, and
production of steel, paper, chemicals and allied products; water is used for processing, washing,
cooling – almost two-thirds of all industrial water –, and/or transporting products or materials.
Industrial reuse have been in place in the USA since the 1940s, with chlorinated domestic
wastewater effluent used for steel processing, and in Japan in 1951 where the purified water of
the Mikawashima Wastewater Treatment Plant in Tokyo was reused as process water for a
paper mill (Levine and Asano, 2002). The rapid industrial growth in Japan in the 1970s resulted
in competition for water between industry and agriculture for available water sources, and about
80% of industrial process water in Japan was reused in 2000 (Levine and Asano, 2002). In
China, the 1989 average rate of industrial water reuse was reported to be about 56% among 82
major cities, with a maximum reuse of 93% (Levine and Asano, 2002). Progressively,
wastewater was also reused as recreational water, as early in 1965, the Santee, California
recreational lakes, supplied with reused wastewater, were opened for swimming (Asano, 1998).
Since this time, there have been several other examples (Sinclair et al., 2009; Craun et al.,
2005). Until today, there have been only a few projects of potable wastewater reuse (Gerrity et
al., 2013; Rodriguez et al., 2009a). The most famous example of Direct Potable Reuse (DPR),
i.e. theoretically pipe-to-pipe, is in Windhoek, Namibia, since 1969 with increment in 1997
(Du Pisani, 2006), but other projects are operational, – e.g. at Cloudcroft, New Mexico, a tiny
mountain resort town that mingles reclaimed water with local well water (Leverenz and al.,
2011) –, or are planned – e.g. at Big Springs, Texas, (Leverenz et al., 2011) –. The failure of the
initial project in San Diego in 1998 illustrates the difficulties for the public to accept direct
contact with wastewater, the water department’s initiative being derided at this time as "toilet to
tap" (Staub et al., 2011). Progressive changes in San Diego (Steirer and Thorsen, 2013)
resulted firstly from subsequent water shortages and rationing, from the water department's that
began reaching out to customers with discussion groups and public meetings, from the

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awareness of inhabitants that conventional waters receive treated wastewaters, and from the
choice of indirect potable reuse option with treated wastewater first stored in San Vicente
Reservoir. Indirect potable reuse (IPR), i.e. after blending with conventional water and a long
storage underground or in reservoirs, is more widespread and several projects are operational
(Rodriguez et al., 2009a), one of the most famous project being the Water Factory 21 in Orange
County West District, California (Leverenz et al., 2011; Van der Bruggen, 2010), but funnelling
reclaimed water into water supplies is being considered in other cities like Miami, Florida, and
Denver, Colorado; in the North of Virginia, reclaimed water has flowed into the Occoquan
Reservoir for three decades (Rose et al., 2001). In Asia, the NEWater project is to reduce
Singapore dependency to Malaysia and officials consider that 15% of water originates from
treated effluent; most of the treated wastewater is for irrigation or manufacturing but a small
proportion is introduced to raw water reservoirs since 2003 for indirect potable reuse (Van der
Bruggen, 2010). In Belgium, indirect potable reuse is carried out by the local drinking company
IWVA in the Torreele/St-André project to supply potable water to the cities of De Panne,
Koksijde, Nieuwport, Veume and Alveringem (Van Houtte et al., 2012), and large cities, such as
London and Berlin depend on recharging the surface and groundwater bodies by treated
wastewater (Paul and Blunt, 2012; Rygaard et al., 2011; Angelakis, 2011). More generally, the
use of wastewater for groundwater recharge (Levantesi et al., 2010; Foster and Chilton, 2004;
Asano and Cotruvo, 2004; Brissaud, 2003) may indirectly contribute to potable water supply,
even if it is firstly to fulfil other objectives. De facto, indirect potable reuse is occurring widely, as
conventional water used to produce tap water has often the discharge of treated or untreated
wastewater, but usually is not acknowledged. Until now, the proportion of wastewater that is
reused has remained generally low: at the Earth level, even agricultural reuse represents
only less than 1% in volume of the total demand of water by this sector (Jiménez and
Asano, 2008; Wade Miller, 2006).

Wastewater reuse in irrigation may address simultaneously water quantity and

quality problems (Qadir et al., 2010; Angelakis and Durham, 2008; Hamilton et al., 2007b;
Wade Miller, 2006; Bixio et al., 2006; Anderson, 2006; Asano, 2002 Friedler, 2001; Angelakis et
al., 1999; Asano and Levine, 1996, among others), as irrigation often explains most of country
water consumption (Van der Bruggen, 2010) and pollutants may be degraded or retained by
soils. In addition, wastewater may contain fertilizing compounds (Ensink and van der Hoek,
2006) that lead farmers sometimes prefer to use untreated sewage rather than treated
wastewater in developing countries like China, Mexico, Peru, Egypt, Lebanon, Morocco, India
and Vietnam (Jiménez et al., 2010; Sophocleous et al., 2009; Keraita et al., 2008), as more
extensively explained for Pakistan (Ensink and van der Hoek, 2006) and Mexico (Scott et al.,
2000; Downs et al., 2000; Downs et al., 1999). Numerous papers have proposed overviews on
the state of the art on wastewater reuse for irrigation on the Earth (Hochstrat and EUREAU
members, 2011; Van der Bruggen, 2010; Qadir et al., 2010b; EUREAU, 2009; Angelakis and
Durham, 2008; Raschid-Sally and Jayakody, 2008; O’Connor et al., 2008; Jiménez and Asano,
2008; Bixio et al., 2008; Keraita et al., 2008; Hamilton et al., 2007b; MED WWR WG, 2007;
Bixio et al., 2006; Toze, 2006; Bixio et al., 2005; Aoki et al., 2005; Massoud et al., 2003;
Hussain et al., 2002; Angelakis and Bontoux, 2001; Angelakis et al., 1999). Unfortunately, the
nature of available information greatly differs with regions, leading to difficulties in comparisons

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AGADAPT Wastewater quality and required water quality for irrigation purposes

and clear reporting; e.g. large parts of Asia were not included in the survey established by Bixio
et al. (2005). In addition, small projects that predominate in several countries, including most of
the underdeveloped countries, are not considered in surveys, leading to data without statistical
significance (Bixio et al., 2005). Large-scale projects are mostly used for landscape and
agricultural irrigation, whereas small-scale projects often have urban, recreational, or
environmental uses; many relatively small-scale projects can be found in Japan, in contrast to
the USA where water reclamation is mainly dominated by medium- to large-scale projects (Bixio
et al., 2005). Nowadays, there are great differences among countries regarding the
proportion of wastewater collected in sewers (Raschid-Sally and Jayakody, 2008; Hamilton et
al., 2007b), the existence and nature of a subsequent treatments (Jiménez and Asano, 2008;
Keraita et al., 2008; Bixio et al., 2008; Hamilton et al., 2007b) – irrigation may use raw
wastewater (Raschid-Sally, 2010; Ensink and van der Hoek, 2006; Downs et al., 1999), diluted
wastewater without treatment (Raschid-Sally, 2010; Keraita et al., 2008) or treated wastewater,
and treatments also greatly vary between pre-treatments and advanced tertiary treatments –,
and the proportion of wastewater reused in irrigation (Hamilton et al., 2007b). Water recycling
in irrigation is particularly practiced in world regions suffering water scarcity, such as
the Near East and Middle East, Mediterranean countries, Australia, the southwest USA,
and densely populated regions like Japan (Lazarova and Asano, 2013; Bdour et al., 2009;
Keraita et al., 2008; Radcliffe, 2004). It is also practised in regions with severe restrictions
on disposal of treated wastewater effluents, such as Florida (O’Connor et al., 2008). Bixio et
al. (2005) identified large water reuse projects– defined as above 0.5 Mm3.y-1 reclaimed water
for unrestricted use or 2.5 Mm3.y-1 for restricted use – in Japan (over 1800), the USA (over 800),
the EU (over 200), Australia (over 450), and around 100 sites In the Mediterranean and Middle
East area, whereas 50 sites were found in Latin America and 20 in sub-Saharan Africa. Most of
Asia (including China in which wastewater reuse is important (Chang and Ma, 2012; Yi et al.,
2011)) was not included in their survey. Lazarova and Asano (2013) proposed estimates of the
annual amount of reclaimed wastewater of about 5410 and 2770 Mm3.y-1 for China and United
States of America, respectively. Other estimates for China are slightly lower although of the
same order of magnitude (Yi et al., 2011). In Europe, wastewater reuse in irrigation is
practised mainly in Cyprus (nearly 100% of treated wastewater), Malta (with a target of 25%
of treated wastewater (Mangion, 2012)), Spain (Iglesias et al., 2010; Iglesias Esteban and
Ortega de Miguel, 2008), Italy (Mangion, 2012) and to a lesser extent in Greece (Guardiola-
Claramonte et al., 2012) with Crete Island (Agrafioti and Diamadopoulos, 2012), France
(Guardiola-Claramonte et al., 2012) in inland, coastal, and island areas – e.g. in the Noirmoutier
Island (Fazio et al., 2013)), in Germany and some other countries (Guardiola-Claramonte et
al., 2012; Van der Bruggen, 2010; EUREAU, 2004). Wastewater reuse seems to be negligible in
Bulgaria (Hochstrat et al., 2006), although it has one of the highest water stress indexes among
European countries (i.e. over 60%) (Bixio et al., 2006), but we found nearly no information on
reuse in this country. Belgium which has also a high water stress index (over 40%) reuses
wastewater mainly for urban and industrial uses (Bixio et al., 2008). Near Europe, wastewater
reuse in irrigation is important in Israel (Tal, 2006), in Turkey and in some Mediterranean
countries of the Middle East and North Africa (Qadir et al., 2010; Keraita et al., 2008).
Reclaimed wastewater may be used through drip irrigation (Capra and Scicolone, 2007),

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 Wastewater quality and required water quality for irrigation purposes AGADAPT

sprinkler irrigation, and flooding – e.g. for paddy rice fields as in the south of Valencia, Spain
(Renault et al., 2013) –.

Strategies chosen for wastewater reuse are highly variable in terms of requirements
for environmental protection and human health, as may be illustrated by the respective
choices of California and Mexico. In the USA, southern states (Florida, Texas, New Mexico,
Arizona, California, Colorado and Nevada) are the most active in water recycling, with California
and Florida recycling approximately one half of USA recycled wastewater (Van der Bruggen,
2010; Crook et al., 2005). For most of the four decades beginning in 1970, the arid West was
the fastest-growing region in the USA, e.g. the population of Nevada quintupled in that period
while Arizona’s nearly quadrupled, the continued population growth being unmatched by growth
in water storage capacity. The situation is such that, in California, San Diego rainfalls meet only
about 15% of the needs and most of the water is imported from the Colorado River and the
Sacramento-San Joaquin River Delta (Tchobanoglous, 2012). Wastewater recycling projects in
California have been thus booming, with ca. 600 Mm3.y-1 of recycled water being used across
over 4800 locations from 234 wastewater treatment plants (Van der Bruggen, 2010). However,
the development of programs for planned reuse of wastewater within the California began in the
early part of the 20th century (Asano, 2006): by 1910, 35 California communities were already
using sewer water for irrigation; the city of Bakersfield has used reclaimed water since 1912 to
irrigate corn, barley, alfalfa, cotton, and pasture (Asano, 2006), and in 1929, the city of Pomona
initiated a project using reclaimed wastewater for the domestic irrigation of lawns and gardens.
In 1970, water reclamation was formally encouraged in the California State Water Code (Asano,
1998); public health laws were progressively developed, leading to the publication of the so-
called Title 22 (State of California, 2000) and the Purple Book (State of California, 2001), which
are a collection of guidelines, rules, and standards corresponding to a zero tolerance that have
been used later elsewhere as basis for regulations and standards (Bixio et al., 2008). The
largest volumes are used for agricultural irrigation, and thereafter for landscape irrigation (Crook
et al., 2005) – the nearly opposite proportions being observed in Florida (Crook et al., 2005) –,
other applications including industrial reuse, groundwater recharge (Asano and Cotruvo, 2004),
seawater barrier, recreation and wildlife, and indirect potable reuse. Irrigation is mainly for corn,
barley, alfalfa, cotton, and pasture (Van der Bruggen, 2010). By contrast in Mexico, only a small
proportion of wastewater is treated before their reclaim and reuse (Keraita et al., 2008), and
wastewater is recycled in irrigation and considered for its fertilizing value in Guanajuato (Keraita
et al., 2008; Scott et al., 2000) and in the Mezquital Valley (Jiménez, 2005). Farmers generally
prefer untreated wastewater rather than treated water due to its fertilizing value that enable
them to increase their rents for between 135 to 780 US$.ha-1.y-1 (Keraita et al., 2008; Jiménez,
2005; Scott et al., 2000). A study comparing vegetable production using freshwater and
untreated wastewater in Haroonabad, Pakistan, found that the gross margins were significantly
higher for wastewater (US$150 per hectare), because farmers spent less on chemical fertilizer
and achieved higher yields (Jiménez et al., 2010; Hussain et al., 2002).

The awareness that water recycling is a possible partial or total answer to the
growing water needs is increasing, all the more that in water-stressed regions, water
conflicts are already appearing, although sometimes still hidden (Van der Bruggen, 2010).

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For examples, the California State Water Code stated in 1970 that "it is the intention of the
Legislature that the State undertake all possible steps to encourage development of water
reclamation facilities so that reclaimed water be available to help meet the growing water
requirements of the State" (Asano, 2006; Asano and Levine, 1996) and, in the U.S., a milestone
event was the passage of the Federal Water Pollution Control Act in 1972 (later renamed 'the
CleanWater Act') "to restore and maintain the chemical, physical, and biological integrity of the
Nation’s waters" with the ultimate goal of zero discharge of pollutants into navigable, fishable,
and/or swimmable waters (Asano, 2006). The European Communities declared in 1991 that
"treated wastewater shall be reused whenever appropriate. Disposal routes shall minimize the
adverse effects on the environment" (CEC, 1991). Water recycling is the only possible
solution in several situations, as in continental areas without exploitable underground water
resources, like in Windhoek, Namibia (du Pisani, 2006), and the reuse of wastewater can also
be a way to cope with the problems of water quality, the decrease in quality being one of the
most important cause of the decrease in quantity (Lazarova and Azano, 2013) as in China,
which is now facing very serious problems of water and soil pollution (Yi et al., 2011). The
proportion of wastewater that is reused has remained generally low until now (Jiménez
and Asano, 2008), but there is a significant potential for an increased utilisation of reclaimed
wastewater in European countries, specifically in the Mediterranean region, as showed by
simulations considering some scenarios of water availability and uses (Hochstrat et al., 2006).

Thus, the objectives of the rest of this report are:

1. To identify key success factors, constraints and milestones to develop wastewater
reuse in Europe. Constraints include economic sustainability, public acceptance, and
potential risks for human health, the environment, and agricultural productions. Regulations
and standards can simultaneously limit these risks and encourage the use of wastewater,
as well as the economic policy (water price, taxes and subsidies). However, inadequate
regulations and standards may be additional constraints. Positive interactions between
stakeholders, including leaders of farmer associations are barely mentioned in this report,
although they are an important key success factor; it is developed in work package W3.2;
2. to propose in the conclusion of this report a list of multi-criteria requirements for
using treated wastewater in irrigation by integrating national regulations, reuse water
scheme management constraints, health and agronomic constraints, etc..
This reports mainly based on (i) a bibliographic review (with several papers issued from
European projects like AQUAREC and MEDAMARE), (ii) European & National regulations
(including those on non-European countries/states), (iii) Feedback of each partner personal
experiences, and (iv) available results of the WP3.2.

This review has been complicated by inaccurate data and contradictions between
recent papers; inaccuracies and contradictions deal with permitted uses, regulations and
standards for irrigation, and surface areas irrigated with treated wastewaters for several
countries. They have resulted from the significant and rapid changes in wastewater reuse in
several European countries during the last decade, from the lack of recent reviews and data
compilation at National level for most European countries and, sometimes, from the difficulty of
access to national regulations and standards. Probably the most complete and actualized

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informations are for Spain (Iglesias et al., 2010; Iglesias Esteban and Ortega de Miguel, 2008);
by contrast, we don't find recent National review of the state of the art in Italy since the 'old'
reviews of Barbagallo et al. (2001) and Bonomo et al. (1999), although recent regional
informations exist – e.g. for the south of Milan (Mazzini et al., 2013), other parts of the Po valley
(Verlicchi et al., 2012), the Apulia (Giungato et al., 2010), and Sicilia (Cirelli et al., 2012) –. As
examples on encountered errors: (1) the unauthorized aquifer recharge with wastewaters in
Cyprus (paper in 2012), while effluent from Paphos wastewater treatment plant are entirely
used for Ezousa aquifer recharge (Papaiacovou and Papatheodoulou, 2013); (2) over 4000 ha
of agricultural fields irrigated with wastewater in Italy (paper in 2007), whereas more than
3000 ha are concerned in the South of Milan, to which one has to add irrigated surface areas at
least in other part of the Pô valley, in Apulia, Emilia Romagna, Sicilia (Cirelli et al., 2012) and
Sardania; (2) the recommendations of the Conseil Supérieur d'Hygiène Publique de France
(CSHPF, 1991) as current French regulations (paper in 2013), whereas current regulations and
standards are from 2010 (Ministère de la Santé et des Sports, 2010). We hope to have avoided
these pitfalls, and we have often preferred remaining cautious about numerical values.

Hazards related to wastewater reuse for irrigation

Hazards related to wastewater reuse for irrigation include health/sanitary risks,

environmental risks and agricultural risks. They result from wastewater content in
pathogens and chemicals.

Raw wastewaters may contain human enteric pathogens, i.e. viruses (Symonds et al.,
2009), bacteria (Pachepsky et al, 2011), protozoa (Tzipori and Widmer, 2008), and helminth
eggs (Gupta et al., 2009; Ensink and van der Hoek, 2006), that may resist to wastewater
treatments (Gupta et al., 2009; Ryu et al., 2007; Gerba and Smith, 2005; Gerba, 1999;
Amahmid et al., 1999). Wastewater treatment plant workers may be infected as illustrated by
antibodies against hepatitis A and/or hepatitis B detected in a significantly higher proportion of
workers than of control population in Thessaloniki, Greece (Arvanitidou et al., 2004), although
contrasted results have been found in Naples (Montuori et al., 2009). Pathogens have caused
drinking and recreational waterborne outbreaks in developed countries like U.S. (Cann et al.,
2013; Craun et al., 2012; Sinclair et al., 2009; Reynolds et al., 2008; Craun et al., 2006;
Maunula et al., 2005; Calderon et al., 2005; Craun et al., 2005) and Europe (Lopman et al.,
2003; Koopmans et al., 2000), and they can contaminate agricultural products during irrigation,
even with conventional waters (Pachepsky et al., 2011). In addition to enteric pathogens,
increased temperature and stagnant water may favour the growth of human non-enteric
water-based pathogens, like Legionella, Mycobacterium and Naegleria fowleri (Cann et al.,
2013; Reynolds et al., 2008).

Raw wastewaters contain also various mineral chemicals (Toze, 2006b; Unkovich et
al., 2006) and organic pollutants (Toze, 2006b; Toze, 2006a). High contents in sodium cation

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have detrimental effects on the structure of soils (Mazzini et al., 2013), and high concentrations
in sodium, chloride and borate ions are toxic for plants (Unkovich et al., 2006). Generally, heavy
metals are of little concern for irrigation with treated wastewaters, unless wastewater is of
industrial origin and/or is not sufficiently treated (Toze, 2006b). Organic pollutants include
chemicals of personal care products, various pharmaceutical products (Nikolaou et al.,
2007; Hernando et al., 2006), bisphenol A and phthalates (Barnabé et al., 2008; Clara et al.,
2010; Dargnat et al., 2009). When a unique sewer network collects both house wastewaters
and runoff waters, wastewaters may also contain pesticides (Gasperi et al., 2008b;
Blanchoud et al., 2007) and polycyclic aromatic hydrocarbons (Palmquist and Hanaeus,
2005). The removal efficiency of wastewater treatment plants varies with compounds and
treatment trains (Watkinson et al., 2007), and several studies noted the presence of organic
contaminants in the environment – e.g. antibiotic in watershed (Watkinson et al., 2009) –.
Solvents are produced during disinfection by chlorine (Kim et al., 2003) and toxins may
be synthesized by cyanobacteria whose blooms are favoured by wastewater, especially in
ponds (Furtado et al., 2009; Barrington and Chadouani, 2008; Saqrane et al., 2008; Gehringer
et al., 2003; Sivonen and Jones, 1998). Impacts on human health remain uncertain for irrigation
reuse. They may a priori result from pharmaceutically active compounds and a large number of
compounds that are known or suspected endocrine disruptors (Toze, 2006b). Concentrations
of most organic pollutants in urban raw or treated wastewaters are generally below the
toxic levels for humans, but potential problems may result from the combined effects of
several pollutants and/or their cumulative consequences over long-term periods.

The use of untreated wastewater has led to local or regional disastrous effects, such
as in the Po valley the loss of permeability and the contamination of soils as well as a decrease
in the biodiversity of surface water bodies, and 30% of the pollution in the northern portion of the
Adriatic Sea south of Venice before the implantation Nosedo and San Rocco wastewater
treatment plants in the south of Milan (Mazzini et al., 2013). By contrast, the success of
several existing projects of treated wastewater reuse in irrigation has comforted the
opinion that wastewater recycling may be considered as a 'zero-risk' practice, when
properly treated (Lazarova and Asano, 2013). However, there are neither enough
experimental evidences (including epidemiological studies) nor enough works on relevant
processes to know whether wastewater management in reclaiming projects in Europe is
sufficient to prevent health risks. First, it is often a challenge to attribute disease outbreaks
to specific exposure routes (i.e. foodborne, waterborne, airborne or through nearly direct
faecal to oral way (Todd et al., 2008)) due to other contributing factors, especially in developing
countries with a poor hygiene, sanitation and reduced access to safe drinking water (Drechsel
et al., 2012), and numerous case of diseases are not recorded (Reynolds et al., 2008). Second,
the exposure of sensible populations to human enteric pathogens may be fatal for them,
these populations representing more than 25% of the humans in countries like the U.S.
(Reynolds et al., 2008). Third, importations of agricultural products from developing
countries increase the risks because of irrigation with water generally of lower quality (Hunter
et al., 2009) and because microorganisms that participate to the normal intestinal flora of local
populations like several Escherichia coli may have a pathogenic effect on foreign populations.
Fourth, there are new emerging microbial and chemical contaminations – e.g. hepatitis E

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virus (Koopmans and Duizer, 2004), severe acute respiratory syndrome (SARS) which moves
from the bat population to other animals and humans (Gundy et al., 2009; Bennett, 2006), multi
antibioresistant bacteria like Escherichia coli (Cantón et al., 2008), emergent virus strains (La
Rosa et al., 2012; Yen et al., 2011), endocrine disruptors and pharmaceutical compounds
including antibiotics (Leverenz et al., 2011; Barnes et al., 2008; Al-Rifai et al., 2007; Karthikeyan
and Meyer, 2006), solvents generated by chlorine oxidation treatments (Lee and von Gunten,
2010; Kim et al., 2003) –.

It may be distinguished between upstream technological risks related to wastewater

treatment, distribution and quality changes between the outlet of wastewater treatment plant
and the point of use, from downstream hazards related to undesirable effects of reuse on
human health, environment and agriculture (Figure 1).

UPSTREAM HAZARDS DOWNSTREAM HAZARDS

Biological
Technological hazards Health hazards
Chemical
Wastewater treatment
Distribution network operability
(Material, monitoring, storage)
Irrigation devices Wastewater Agricultural/
applications Environmental hazards

Usages

Societal hazards

Technological /
Wastewater treatment Economical constraints
plant specifications Regulations / Guidelines

Figure 1: Hazards linked with wastewater reclaiming in irrigation.

Additional risks deal with the economic sustainability of wastewater reuse, and the
acceptance or rejection of wastewater reclaiming by inhabitants (Leverenz et al., 2011; Cain,
2011; SOFRES, 2006). Even for direct potable water reuse, public acceptance may be good as
in Windhoek, Namibia, (du Pisani, 2006); the failure of direct potable reuse in San Diego,
California, (Staub et al., 2011) is almost fixed now thanks to several changes (Steirer and
Thorsen, 2013; Shipps, 2013): inhabitants accept wastewater reuse all the more water deficit is
an actual threat, water managers greatly communicate with consumers, and it becomes clear
that recycled water is not a direct 'toilet to tap' transfer but that treatments insure a water of
quality often higher than that of conventional waters and indirect potable reuse is now proposed.
We will not discuss social acceptance further in this report, but it cannot be overlooked.

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Technological hazards

Technological hazards include risks of inadequate wastewater treatments, of cross

contamination between potable water mains and treated wastewater distribution network,
of development of facultative enteric human pathogens and water-based pathogens in
this network, and of biofilm with clogging hazards.

Today, technically proven wastewater treatment and water purification processes

exist to produce water of almost any quality desired, and the quality of reclaimed water can
exceed conventional drinking water quality based on most conventional parameters (Norton-
Brandão et al., 2013; Asano, 2006; Asano, 1998). Efficient treatments are some tertiary ones,
including physicochemical coagulation/flocculation, filtrations – especially ultra or nano-filtration
(Pierre et al., 2010; Röhricht et al., 2010) including membrane bioreactor (Sima et al., 2011),
and reverse osmosis (Peñate and García-Rodríguez, 2012; Garud et al, 2011), as sand filtration
may be not sufficient for viruses (CFPTEP, 2010a; CFPTEP, 2010b) although some results are
correct (Aronino et al., 2009) –, high UV radiation levels (Simonet and Gantzer, 2006b) or long
stays in shallow lagoons that may lead to similar results, and chemical disinfection – e.g. with
ozone (Martínez et al., 2011), hydrogen peroxide (Barrington and Chadouani, 2008), peracetic
acid (Kitis, 2004), and chlorine or hypochlorite although they may lead to the production of
solvent as by-products (Kim et al., 2003) –. However in the European context, current
treatments don't totally eliminate microbial and chemical pollutions due to costs; and
progress have still to be made to identify robust new methods of purifying water at lower cost
and with less energy, while at the same time minimizing the use of chemicals and impact on the
environment (Shannon et al., 2008). Several papers have reported large quantities of some
human enteric viruses in raw and treated wastewaters – e.g. for the 5 wastewater treatment
plants around Roma (La Rosa et al., 2010), in a wastewater treatment plant in the south of the
Netherlands (Van den Berg et al., 2005), and for the Leipzig wastewater treatment plant (Pusch
et al., 2005).

Failures in treatments may result from their lack, their inadequacy for specific microbial
or chemical contaminants, or their deficiency caused by a dysfunction of the plant or by
temporary water overflows. Municipal water systems can be overburdened by extreme rainfall
events, as sewer systems often carry both storm water and wastewater (Cann et al., 2013;
Figueras and Borrego, 2010). Similar reasons and the discharge of the excess wastewater
directly into surface water bodies explain correlations between extreme rainfall events and
waterborne disease outbreaks from drinking water (Cann et al., 2013). Although non-compliant
treated wastewater should not be used, the frequency of water analyses and the waiting time for
results make it impossible to react in real time to failures of quality. Treated wastewater may be
stored in reservoirs or lagoons before irrigation. The storage is often regarded as an additional
treatment enabling to break organic contaminants difficult to degrade in generally approximately
1 day of transit in the wastewater treatment plant. Especially for lagoons or reservoirs of small
depth, solar UV radiations may accelerate some transformations, including the alteration of

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virus RNA or DNA (Fong and Lipp, 2005; Gerba et al., 2002; Fujioka and Yoneyama, 2002).
Unfortunately, lagoons or reservoirs may be contaminated by some of the human enteric
pathogens as Salmonella enteritidis (typhoid, diarrhea) and Campylobacter jejuni (diarrhea)
from birds and Cryptosporidum (diarrhea) from cattle (Reynolds et al., 2008); in addition,
wastewater favours blooms of cyanobacteria (Barrington and Chadouani, 2008) synthesizing
neurotoxins and carcinogenic hepatotoxins (Sivonen and Jones, 1998) and, in several
countries, water coming from ponds without special treatment contains microcystins that have
an impact both on the growth and the development of crops (Furtado et al., 2009; Gehringer et
al., 2003; Saqrane et al., 2008).

Leaks in treated wastewater distribution and sometimes interconnections with

conventional water distribution systems, especially when using a unique pipe network of
irrigation alternatively supplied with treated wastewater and conventional water, may led to
contaminations of conventional water (Reynolds et al., 2008) and/or the environments (McKay,
2011). Groundwater contamination may also originate from household wells (Borchardt et al.,
2003). Available statistics on potable water mains may probably be partly transposed to treated
water distribution systems, especially in the U.S. even well-run water distribution systems
experience about 25-30 breaks per 160 km of piping per year and the percent of leakage
ranges between <10% to as high as 32% (Reynolds et al., 2008). Reynolds et al. (2008) also
noted that at least 20% of the potable water mains is below the water table; probably the
proportion is lower for treated wastewater distribution pipes, but leaks below the water table is
probably the worst situation in terms of contamination of groundwater and/or drinking water in
urban context. Possible growth in pipe networks of human enteric pathogens not totally
eliminated during wastewater treatments deals with some pathogens, including Escherichia
coli (Pachepsky et al., 2012), as all human enteric viruses, most human enteric protozoa and
several bacteria are obligatory parasites. In addition, increased temperature and stagnant
water favour the growth of human water-based pathogens, like Legionella (pneumonia,
respiratory infections), Mycobacterium (however, some Mycobacterium, including the
tuberculosis and the leprosy organisms, are obligate parasites and are not found as free-living
members of the genus) and Naegleria fowleri (causing primary amoebic meningoencephalitis
(PAM), fortunately rare, of primary concern because of high fatality rate in diagnosed cases
(>95%)) (Cann et al., 2013; Reynolds et al., 2008). If microbial biofilms seems not lead to clog
pipes, biofouling has been identified as a major contributor to emitter clogging in drip
irrigation systems using reclaimed wastewater (Pachepsky et al., 2012; Capra and
Scicolone, 2007); it lead to proposal the structure of the emitters (Yan et al., 2009).However in
some contexts, drip emitter clogging may be higher for irrigation with conventional water than
with reclaimed water (Cirelli et al., 2012)..

Other technological hazards exist, including those intended to the internal reuse of grey
waters for garden irrigation, and the reclaiming of industrial wastewaters, especially for many
low-income countries with challenges of emerging industrial sectors or mining activities while
institutional, technical and/or regulatory capacities for wastewater treatment are not yet in place;
industrial effluents pose a threat to humans and the environment (Simmons et al., 2010).

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Health/sanitary hazards

Numerous factors affect sanitary/health hazards. They depend on the domestic and/or
industrial origins of wastewater that induce first microbial risks or chemical risks, respectively,
although chemical risks may also be induced by domestic waters – e.g. antibiotics in Cyprus
conventional waters (Papaiacovou and Papatheodoulou, 2013) –. They also depend on the
local importance of pathogens – e.g. hepatitis A is endemic in North Africa countries (Kamal
et al., 2010; Gharbi-Khelifi et al., 2006) and in some European countries like Albania (Divizia et
al., 2005), widespread in some other European countries like Greece (Arvanitidou et al., 2004),
and nearly absent in most of the other European countries except after contaminations due to
international exchanges (Hollinger et Emerson, 2007); helminth eggs may prevail in Pakistan
(Ensink and van der Hoek, 2006) and India (Gupta et al., 2009) –. They also depend on
seasonal variations of some infections (Lal et al., 2012; Jagai et al., 2012; Yen et al., 2011;
Gharbi-Khelifi et al., 2006; Chikhi-Brachet et al., 2002) although this seasonality is not
necessarily found for virus in raw and treated wastewaters – e.g. bacteria (Fracchia et al.,
2006), winter vomiting disease with Norovirus (Myrmel et al., 2006; Van den Berg et al., 2005),
Rotavirus (Myrmel et al., 2006), hepatitis A virus in Tunisia (Gharbi-Khelifi et al., 2006) –. In
tropical climates, human enteric viruses, especially enteroviruses, are isolated throughout the
year and in some cases are more prevalent during rainy seasons (Fong and Lipp, 2005). And in
Texas, seasonal levels of human enteric viruses in wastewater were highest during late
summer, coinciding with the time of substantial crop irrigation: polioviruses were the
predominant enteroviruses recovered during spring monitoring, while Coxsackie B viruses
comprised the majority of identified isolates recovered in summer (Moore et al., 1988). Similar
variations have been obtained for Campylobacter, Salmonella, vero-cytotoxigenic Escherichia
coli, Cryptosporidium and Giardia for various locations in temperate developed countries (Lal et
al., 2012). By contrast, Norovirus outbreak activity is higher between November and March in
the U.S. (Yen et al., 2011). Even with seasonal variations in wastewaters, biofilm may enable
the persistence of Norovirus and Enteroviruses (Skraber et al., 2009). They also depend on
wastewater treatments (Bixio et al., 2005), agricultural practices (crops, irrigation type (mode,
frequency and volumes), local specificities (soil type, wind, tree edges and distance to public
paths), and irrigation method (Hamilton et al., 2006). They also depend on the populations
(race, age structure and demography, socioeconomic and educational levels), their lifestyles
(food consumption, hygiene and mobility …) (Hamilton et al., 2006), and their health that may
be taken into account for quantitative microbial risk assessment dealing with the consumption of
food irrigated by wastewater (WHO, 2006a). Sanitary/health hazards also depend on the
dilution of wastewater with conventional ones (Van der Bruggen, 2010).

Biological hazards (viruses, bacteria, protozoa and helminth eggs)

Although not directly related to wastewaters, waterborne outbreaks caused by enteric

pathogens in drinking waters (Craun et al., 2010; Hoffman et al., 2009; Zhuang et Jin, 2008;
Reynolds et al., 2008; Craun et al., 2006; Gerba, 1999) or recreational waters (swimming

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pools, lakes, lagoons, rivers and thermal station) (Sinclair et al., 2009; Hamilton et al., 2007;
Craun et al., 2005) help identify risks of wastewater reuse in irrigation, since they partly
result from the contaminations of conventional water by wastewater. Although drinking water in
the U.S. is among the safest in the world, 780 waterborne outbreaks were reported from 1971 to
2006 that were caused by chemical contaminants (11.5%), viruses (8.2%), bacteria (16.6%),
protozoa (18.3%), mixed (0.8%) and unidentified agents (44.6%) (Craun et al., 2010).
Waterborne outbreaks caused by unidentified agents are mainly acute gastrointestinal illness,
the characteristics of these outbreaks being often consistent with a viral aetiology (Reynolds et
al., 2008). Outbreaks reported for 1971-2006 have resulted in 577094 cases of illness and 93
deaths (Craun et al., 2010), but the true impact of drinking water contaminations is much higher:
Morris and Levein (1995) estimated that 7 million people become hill and more than 1000
die each year in the U.S. as a result of waterborne microbial infection, and Colford et al.
(2006) estimated there to be 4.3-11.7 million cases of acute gastrointestinal illness attributable
to public drinking water systems in the United States each year. To our knowledge, there is no
equivalent review to those of Craun et al. (2010) and Reynolds et al. (2008) for European
countries; partial informations are accessible for countries – e.g. for France (Bonnin et al., 2012;
ANOFEL Cryptosporidium National Network, 2010; INVS, 2004; INVS, 2001), for The
Netherlands (Svraka et al., 2007) –.

The primary concern in agricultural food consumption deals with uncooked

vegetables (Bos et al., 2010; WHO, 2006), e.g. salads, carrots and onions, and restricted
irrigation is necessary depending on water quality and management, but it may be hard to
implement (Keraita et al., 2010). Other concerns deal with the risk of contamination of farmers
or neighbouring inhabitants by bioaerosols emitted during sprinkler irrigation and agricultural
work, particularly in windy conditions, and with the risk for human pathogen to reach
underground water or surface water bodies without being inactivated (George et al., 2004).
Unfortunately, only a few studies have dealt with human contamination though bioaerosol
emitted during either sprinkling irrigation, during wind events after sludge application (Baertsch
et al., 2007) or flood irrigation (Paez-Rubio et al., 2005), and during activated sludge treatments
(Heinonen-Tanski et al., 2009; Fracchia et al., 2006; Sigari et al., 2006) and lead to regulations
that are not scientifically sound (Lazarova and Brissaud, 2007); in addition for enteric pathogens
transmitted by air way, airborne disease, except for Legionella pneumophila and SARS virus,
there is a lack of knowledge to assess the actual transfer from the respiratory to the gastro-
enteric track and assumptions are performed in quantitative microbial risk assessment on soil
particle ingestion and their level of contamination (Mara et al., 2007).

Major human enteric and water-based pathogens

Currently, more than 140 human enteric pathogens may be transmitted by water route
(Reynolds et al., 2008); they include viruses (Carducci et al., 2009), bacteria (Pachepsky et al,
2011), protozoa (Mota et al., 2009; Tzipori and Widmer, 2008), cyanobacteria (Sivonen and
Jones, 1998), and helminth eggs (Gupta et al., 2009; Ensink and van der Hoek, 2006).

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Table 1: Most common enteric human pathogens and water-based pathogens in drinking water
(The name of water-based pathogens are bold and underlined).
Virus* Bacteria* Protozoa* Helminth eggs**

Norovirus Vibrio cholerae Giardia Lamblia Ascaris,

Sapprovirus Salmonella spp. Cryptosporidium parvum hookworms,
Paraechovirus Shigella spp. Entamoeba histolitica Taenia spp.
Enterovirus: Toxigenic Escherichia coli Cyclospora cayetanensis Schistosoma spp.
(69-71, Poliovirus, Campylobacter spp. Isospora belli
Coxsackievirus, Yersinia enterocolitica Microsporidia
Echovirus) Plesiomonas shigelloides Ballentidium coli
Reovirus Legionella Toxoplasma gondii
Adenovirus Heliobacter pylori Naegleria fowleri
Hepatitis A Virus
Hepatitis E Virus
Rotavirus
Astrovirus
Picobirnavirus
Coronavirus
*: based on Reynolds et al. (2008) for drinking water in U.S. context; **: based on Bos et al.
(2010)

Among them, one has to distinguish on the one hand obligatory pathogens (all human
enteric viruses and helminths, several bacteria and protozoa), from facultative pathogens that
may also develop in soil and/or water – e.g. Legionella pneumophila (Berthelot et al., 2009)
and Naegleria fowleri (Reynolds et al., 2008) –, on the other hand pathogens specific to
humans from zoonotic pathogens (Gerba and Smith, 2005). A list of the most common
enteric and water-based pathogens in drinking water is proposed in Table 1. The same
pathogens are also found in food-related illness and death (Mead et al., 1999).

Nearly at the same time in 2008-2009, the U.S. Environmental Protection Agency (US-EPA)
and the American Water Works Association (AWWA) each proposed unregulated Contaminant
Candidate Lists (CCL) for drinking water by using quite different methodologies according to the
same 3 following criteria (Hoffman et al., 2009): (i) the contaminant may have an adverse effect
on the human health; (2) it is known to occur or there is a substantial likelihood that it will occur
in public water systems with a frequency and at levels of public health concern; and (3)
regulation of such a contaminant would present a meaningful opportunity for the reduction of
health risk. The final Contaminant Candidate List of the U.S. Environmental Protection Agency
in 2009 (U.S.-EPA, 2009) is similar to the List of the American Water Works Association
(Table 2) with common pathogens: 3 groups of viruses (Caliciviruses (includes Norovirus)
Enteroviruses (Coxsackieviruses and Echoviruses), Hepatitis A virus), 5 groups of bacteria
(Campylobacter jejuni, Escherichia coli (0157), Legionella pneumophila, Mycobacterium avium,
Salmonella enterica), and 1 group of protozoa (Shigella sonnei). The U.S. Environmental
Protection Agency considers Cyanobacteria (blue-green algae), other freshwater algae, and

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their toxins only through toxins in the final Contaminant Candidate List 3 (US EPA, 2009), since
they affect human health only through toxin excreted in waters (Sivonen and Jones, 1998).

Table 2: Final Third Drinking Water Contaminant Candidate List (CCL 3) (US-EPA, 2009) and
alternative proposal of the American Water Works Association (Hoffman et al., 2009)
Final CCL 3(US-EPA, 2009) AWWA list (Hoffman et al., 2009)

Adenovirus
Caliciviruses (includes Norovirus) Caliciviruses (Norovirus)
Campylobacter jejuni Campylobacter-like organisms
Enterovirusess Enteroviruses
(include Poliovirus, Coxsackievirus (include Coxsackievirus and Echovirus)
and Echovirus)

Escherichia coli (0157) Toxigenic Escherichia coli

Helicobacter pylori
Hepatitis A virus Hepatitis A virus
Legionella pneumophila Legionella pneumophilia
Mycobacterium avium Mycobacterium avium
Naegleria fowleri
Rotavirus
Salmonella enterica Salmonella enterica
Shigella sonnei Shigella spp.
Vibrio cholerae

Viruses are obligate, intracellular parasites (Fong and Lipp, 2005; Sobsey and Meschke,
2003). Most of human enteric viruses are naked viruses (Fong and Lipp, 2005) that may
survive a long time in water environments (weeks to months) (La Rosa et al., 2012), with the
well-known exception of the severe acute respiratory syndrome (SARS) virus which is an
enveloped virus that may be considered as enteric and that is more rapidly inactivated in water
and wastewater at ambient temperatures (Gundy et al., 2009). Most of them are human
specific, except hepatitis E virus with infections suggested from pigs from almost identical
viruses (Koopmans and Duizer, 2004) and infection proven from deer (Tei et al., 2003), and the
severe acute respiratory syndrome virus which moves from the bat population to other animals
and humans (Gundy et al., 2009; Bennett, 2006). Viruses of greatest concern in water (and their
associative illnesses) include the group of Enteroviruses with Poliovirus, Coxsackievirus and
Echovirus (diarrhoea, meningitis, myocarditis, fever, respiratory disease, nervous system
disorders, birth defects), hepatitis A virus (hepatitis, liver damage and jaundice), Norovirus
(diarrhoea), Astrovirus (diarrhoea), Adenovirus (diarrhoea, respiratory disease, eye infections.
heart disease), and Rotavirus (diarrhoea) (Rodríguez‐Lázaro et al., 2012). In practice,
however, the most commonly reported foodborne viral infections are viral gastroenteritis and
less frequently hepatitis A (Seymour and Appleton, 2001). Viruses have the greatest infectivity,
requiring the fewest number to cause infection of all waterborne microorganisms (Morin and
Picoche, 2008), and they are excreted in the faeces in the largest numbers up to 1011-1012.g-1
faeces for sick and healthy carriers (Maunula et al., 2013; La Rosa et al., 2012; Da Silva et al.,

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2010; Reynolds et al., 2008; Fong and Lipp, 2005; Koopmans and Duizer, 2004) and several
weeks after the illness period (Maunula et al., 2013; Da Silva et al., 2007). They are not
efficiently removed by conventional filtration and they are more resistant to disinfectants
than bacteria (CFPTEP, 2010a; CFPTEP, 2010b; Aronino et al., 2009; Petrinca et al., 2009; Da
Silva et al., 2008), although some studies shows an high efficiency of treatments with
differences in the decrease of GI and GII Norovirus groups (Da Silva et al., 2007) or of the
nearly complete treatment train in the Upper Occoquan Sewage Authority Water Reclamation
Plant that protect the Occoquan Reservoir (Rose et al., 2001). Viruses are detected in raw
wastewaters as well as in treated wastewaters at the exit of wastewater treatment plants – e.g.
in 5 wastewater treatment plants around Rome (La Rosa et al., 2010), in 2 wastewater
treatment plants in the southwest of the Netherlands (Van den Berg et al., 2005), for Leipzig
(Pusch et al., 2005), for Rio de Janeiro in Brazil (Villar et al., 2007), and in Norway for Oslo area
and elsewhere (Myrmel et al., 2006) –. This may explain why they are also found in
conventional surface waters and groundwaters. Because of their small size (0.02-0.1 µm) and
ease of transport in the subsurface, viruses are of primary concern in groundwaters (Reynolds
et al., 2008). They are known to be the causative agent in 8.2% of drinking water outbreaks
reported in recent years in the U.S. (Craun et al., 2010) to which probably most of the 44.6% of
outbreaks of undetermined etiology have to be added. The overall method to extract and detect
viruses in foods using molecular tools could be divided into three different steps: (1) virus
elution and clarification from substrates, (2) concentration of the viruses (Hamza et al., 2009;
Croci et al., 2008; Liu et al., 2007; Villar et al., 2006; Dubois et al., 2006; Katayama et al., 2002;
Jothikumar et al. 1995; Tsai et al., 1993), and (3) RNA or DNA extraction and purification,
amplification, detection of amplified products, and confirmation of the results (Croci et al., 2008).
For each of these steps various methods exist. Among the methodological difficulties: the
easiness to obtain GC enumerations but the difficulties to estimate the proportion of viruses that
remain infectious (Nuanualsuwan and Cliver, 2002), although some PCR methods are proposed
to discriminate between infectious and non-infectious viruses (Bhattacharya et al., 2004;
Nuanualsuwan and Cliver, 2002).Other detection methods exist, including virus cultivation that
enables to enumerate infectious viruses, but that is also fastidious and that is still not possible
for several viruses including Norovirus. Due to the potential great concern of viruses in raw and
treated wastewaters, we add to this review a more complete in Appendix 1.

Bacteria are prokaryotic, single-celled organisms, ranging in size from 0.1 to 10 µpm
(Reynolds et al., 2008). Enteric bacteria are able to colonize the human intestinal and
gastrointestinal tract. Generally, enteric bacteria do not survive long in the environment,
although some have resistant spores or can form dormant stages that aid in their survival.
Waterborne outbreaks caused by enteric bacteria primarily occur because of failed or absent
treatment processes. Waterborne enteric bacteria of greatest concern in water (and their
associative illnesses) include Salmonella (typhoid, diarrhoea), Shigella (diarrhoea),
Campylobacter (diarrhoea, nervous system disorders), Vibrio cholerae (diarrhoea), and
enterotoxigenic Escherichia coli (via produced toxins: diarrhoea, kidney failure, haemorrhagic
colitis) (Gupta et al., 2008), Helicobacter pylori (duodenal and gastric ulcers, infections can lead
to gastric cancer (Reynolds et al., 2008)), and Mycobacterium avium (lung infection,
disseminated infection in severely immunocompromised peoples). Although the contribution of

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the waterborne route of exposure to the disease is uncertain, studies have found 10%-60% of
individual groundwater wells contaminated with Helicobacter pylori (Park et al., 2001).
Legionella pneumophila (lung diseases) is an important water-based bacteria that may develop
in stagnant water at warm temperature (Reynolds et al., 2008); in the U.S., 6 water-associated
outbreaks were recorded in 2001-2002 (Reynolds et al., 2008). Other water-based pathogens
include Leptospira spp. (Leptospirosis) and Burkholderia pseudomallei (acute and chronic forms
of melioidosis; symptoms may include pain in chest, bones, or joints; cough; skin infections,
lung nodules and pneumonia) (endemic areas include particularly Thailand and northern
Australia).

Enteric protozoa are single-celled animals that live in the gastrointestinal tract of infected
individuals (Reynolds et al., 2008). They range in size from 1 to I00 µm and produce an
environmentally stable cysts or oocysts that survive for long intervals in wastewater, aquatic and
terrestrial environments. The thick cyst or oocyst walls are highly resistant to disinfectants used
in conventional water treatment. Waterborne enteric protozoa of primary concern in water (and
their associative illnesses) include Cryptosporidium (parvum, hominis …) (Xiao, 2010) and
Giardia (lamblia, Instestinalis …) (Amahmid et al., 1999); they are implied in dysentery
diseases, infections of the liver, lungs, pericardium, skin and brain. A well-known example of
Cryptosporidium outbreak is the outbreak that took place in Milwaukee, Wisconsin in 1993
(Hoxie et al., 1997; Mac Kenzie et al., 1994). Entamoeba histolytica is another parasite that
causes 40000-100000 deaths annually in the World (Ackers and Mirelman, 2006); in the large
bowel, infections that are exclusively luminal are asymptomatic, and clinical amoebiasis only
occur when the parasite penetrates the colon wall, causing flask-shaped ulcers that lead to
amoebic dysentery. Much less frequently, Entamoeba spread through the portal vein to the liver
(amoebic liver abscess) and, very rarely, disseminate to other sites. Cyclospora caryentensis is
another parasite that has been linked to a possible waterborne outbreak in the U.S. (Mansfield
and Ciajadhar 2004). Naegleria fowleri (primary amoebic meningoencephalitis) is a water-based
pathogen of primary concern because of a high fatality rate in diagnosed cases. Two deaths
occurred in an outbreak of Naegleria in 2002 (Reynolds et al., 2008). Cysts of the three species
are resistant to desiccation, temperature, pH variations and chlorination. Enteric protozoa are of
major concerns for operators involved in recycling wastewaters; they may be easily removed by
filtrations.

While helminths are a major problem in some countries (Gupta et al., 2009; Ensink and van
der Hoek, 2006; Amahmid et al., 1999), they seem less and less important in others, to such an
extent that helminth eggs have disappeared from the French standards in 2010 (MSS, 2010).
The most common species are Ascaris lumbricoides, hookworms, Enterobius vermicularis,
Trichostrongylus spp., Taenia spp., Hymenolepis nana and Dicrocoelium dendriticum.

Quantitative microbial risk assessment

Quantitative microbial risk assessment (QMRA) tools permit a priori to assess the risk of
exposure, infection and disease of peoples via pathogens in food, water or air (Schijven et al.,

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2013; Pachepsky et al., 2011; Hunter et al., 2003; Petterson and Ashbolt, 2003). They can take
into account the disappearance of pathogens over the entire chain from water treatment to the
potential exposure of peoples (Mara, 2011; Mara et al., 2010; Stine et al., 2005). Considering a
number of disability adjusted life years (DALY) per case of disease (pcd) that may vary with
regions (Institute for Health Metrics and Evaluation. 2013; WHO, 2006a; WHO, 2004), these
tools allow to compare the effects of different pathogens, to take into account different
pathogens simultaneously, and to achieve tolerable targets of disability adjusted life years
(DALY) per person per year (pppy) by satisfying required microbial reductions either exclusively
during wastewater treatment or by combining the effects of treatment to pathogen decay after
irrigation before and after harvest (WHO, 2006a; Stine et al., 2005).

The quantitative microbial risk assessment is based on the initial mathematical model for
drinking water (Fewtrell and Bartram, 2001; Haas et al., 1999; Haas et al., 1993) issued from
chemical risk assessment approaches. It combines 3 types of considerations (Haas et al.,
1999): the exposure assessment (i.e. the number of pathogen ingested during an exposure
event through food, water or air ways), the dose-response assessment (i.e. the relationship
between infection probability and the number of pathogens ingested), and risk characterization
(i.e. the probability of illness (see death) for infected peoples). A framework to adapt to country
or regional contexts has been proposed (Scheierling et al., 2010; WHO, 2006a). Considering a
tolerable disability adjusted life years per person per year and the disability adjusted life years
per case of disease, one has (i) to estimate the required level of reduction of pathogens initially
present in raw wastewater (step 1: calculation of the tolerable disease and infection risks per
person per year; step 2: calculation of the tolerable infection risk and dose of ingested
pathogens per exposure event; step 3: calculation of the level of reduction of pathogens
required to achieve the health targets), (ii) specify how pathogen reduction would be achieved
by wastewater treatment commonly in conjunction with other heath protection measures, and
(iii) to verify that the targets have been achieved through bioindicators or pathogen themselves.
Deterministic models of quantitative microbial risk assessment have been proposed (Hamilton
et al., 2007a), but quantitative microbial risk assessment tools may be combined with stochastic
simulations (Karavarsamis and Hamilton, 2010; Mara and Sleigh, 2010; Mara et al., 2007;
Hamilton et al., 2006; Hamilton and Stagnitti, 2006; Sleigh and Mara, 2003) to account for the
random distribution of some of the context parameters, e.g. the structure of the population (age,
body mass, socioeconomic, racial, and geographic demography) and the depending daily
consumption (US-EPA, 2003; US-EPA, 1997).

The World Health Organization proposed this tool to help countries develop their own
regulations and standards (WHO, 2006a), partly in response to criticism of too liberal previous
guidelines in 1989 (WHO, 1989) compared to those of the U.S. Environmental Protection
Agency (USEPA/USAID 1992). This recommendation was based on some works (Fattal et al.,
2004; Sleigh and Mara, 2003; Blumenthal et al., 2003; Blumenthal et al., 2000; Tanaka et al.,
1998; Shuval et al., 1997; Asano et al., 1992 among others) and it followed the adoption of
QMRA in the Australian national water recycling guidelines (EPHC/NRMMC/AHMC, 2006).
Additional applications of quantitative microbial risk assessments to wastewater reuse for
irrigation have been published later. They give a first overview of risks resulting from the

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ingestion of crops irrigated by wastewater as a function of the pathogens and their

concentrations in the effluent – e.g. viruses (Mara and Sleigh, 2010c; Mara and Sleigh, 2010b;
Mara et al., 2007; Hamilton et al., 2006; Stine et al., 2005; Petterson et al., 2001), bacteria
(Stine et al., 2005), protozoa (Mota et al., 2009), and helminths (Mara and Sleigh, 2010a; Mara
and Sleigh, 2010b) –, the crops – e.g. lettuce (Mara et al., 2007; Hamilton et al., 2006; Stine et
al., 2005; Petterson et al., 2001),cucumber (Hamilton et al., 2006), broccoli (Hamilton et al.,
2006), cabbage (Hamilton et al., 2006), cantaloupe (Stine et al., 2005), and pepper (Stine et al.,
2005) –, the irrigation type (subsurface, furrow, or drip irrigation), and other practices such as
the delay between the last irrigation and the harvest, postharvest washing/disinfection, and the
preparation of food (Hamilton et al., 2006). Inhalation (and the involuntary ingestion) by farmers
or neighbouring inhabitants of aerosolized soil particles have been discussed for highly
mechanised and manual cropping systems (Mara et al., 2007). Some papers proposed updates
from the WHO guidelines (Mara et al., 2010), and Maimon et al. (2010) proposed a review on
the risks resulting from different current guidelines.

The value for the tolerable DALY (10-6 pppy) proposed in the WHO guidelines (WHO,
2006a) and in the Australian national water recycling guidelines (EPHC/NRMMC/AHMC, 2006),
as currently retained as for drinking water (WHO, 2006a), may be too restrictive in most of the
developing countries (Mara and Sleigh, 2010c), and other threshold values have been
proposed: 10-5 (Mara and Sleigh, 2010c) and 10-4 pppy (Mara, 2013; Mara, 2011; Mara and
Sleigh, 2010b; Stine et al., 2005) among others. On the one hand, other routes of contamination
can largely predominate – e.g. even with raw wastewater used for spinach and Cauliflower
irrigation in Pakistan, unhygienic post-harvest handling was the major source of produce
contamination (Ensink and van der Hoek, 2006), and other contaminations in the market may
result from the use of contaminated freshening water (WHO, 2006a) –. On the other hand, a too
low threshold value would lead to additional costs that may be disproportionate with regard to
the expected health gain and unrealistic for several developing countries (Blumenthal et al.,
2000). An increase in the tolerable DALY per person per year from 10-6 to 10-5-10-4, would then
lead to very simple wastewater treatment systems to achieve a single-log unit pathogen
reduction as the balance of the required total pathogen reduction (i.e. 103-105) can be easily
achieved by very reliable post-treatment health-protection control measures (pathogen die-off
and produce washing or disinfection) (Mara and Sleigh, 2010b-c). As proposed by the World
Health Organization (WHO, 2006), tolerable DALY should be adapted to national or regional
contexts, and possibly distinguish agricultural production for local consumption from those for
export. The Californian standard of 2.2 total coliforms (roughly 1 E. coli) per 100 ml and the
recommendation of USEPA & USAID (1992) for an ‘undetectable’ level of E. coli in 100 ml result
in Rotavirus infection risks of 10-6-10-8 pppy. Such low levels of risk are difficult to justify
epidemiologically, and they are unlikely to be cost effective in protecting health (Mara et al.,
2007). However, the usefulness of quantitative microbial risk assessment is dependent upon the
quality and appropriate use of available data for describing the occurrence, persistence and
human dose-response of pathogens (Petterson and Ashbolt, 2003). First, QMRA approach
requires to correctly measure or estimate the initial amounts of pathogens in the raw
wastewater and their actual fates during wastewater treatments, storage in ponds or reservoirs,
distribution of reclaimed wastewater and after irrigation (before and after harvest); processes

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are still misunderstood and/or poorly quantified (virus internalization in edible parts of crops
eaten crude (Wei et al., 2011; Urbanucci et al., 2009; Chancellor et al., 2006; Oron et al., 1995)
and virus attachment at the surface of vegetables (Vega et al., 2005); pathogen transfer from
respiratory track to gastro-enteric track among others as implicitly assumed by Mara et al.
(2007) and demonstrated in other contexts (Marks et al., 2000), as pathogens may be present
in bioaerosols (Fracchia et al., 2006; Carducci et al., 2000; Brandi et al., 2000); the effect of
washing edible parts of foods (Mara, 2013; WHO, 2006a among others) whose effects may be
overestimated with regard to fine works on works on some crops (Gerba and Kennedy, 2007)
and on other types of surfaces (Barker et al., 2004)), and several constants remain imprecise as
those to estimate pathogen decays during and after treatment (Mara, 2013). Second, estimating
exposure, infection and disease risks simultaneously requires having a good description of
human comportments (nutrition, sanitary habits, movements and body protection …) as partly
available for some countries (U.S. Environmental Protection Agency, 2003; U.S. Environmental
Protection Agency, 1997) but not everywhere. Third, real time detections of actual human
pathogens remains difficult and expensive, although great progresses have been done in
molecular methods, and the enumeration of bioindicators instead of actual pathogens may be
criticized (see below); this last point is complex to solve as ‘reference’ pathogens (e.g.,
Norovirus, Campylobacter, Cryptosporidium, Ascaris) can be chosen but tolerable DALY pppy
may led to pathogen concentrations so low especially for viruses – e.g. 5 10-3 Rotavirus/L
(WHO, 2006a) – that they cannot be detected without preliminary great concentrations.
Bioindicator concentrations are usually greatly higher but their correlation with actual pathogen
concentrations and fates is questionable (see below).

Similarly as for microbial risks, quantitative chemical risk assessment may be applied to
organic pollutant in wastewaters. The approach may be based on acceptable concentration of
pollutant, i.e. zero effect concentration, rather than disability adjusted life years (DALY) (Weber
et al., 2006). And other approaches of risk assessment combining physiochemical,
environmental properties and toxicity of the 200 most commonly prescribed drugs, as well as
common antibiotics and lipid regulating drugs that were not within the top 200, has been used to
rank different risks (Cooper et al., 2008). Unfortunately and similarly to microbial risk
assessment, there is currently a lack of information concerning the effects of antibiotics to
critically assess potential risks for environmental discharge and water recycling (Watkinson et
al., 2007).

Bioindicators of human pathogens

Bioindicators are used as indexes of the presence and concentration of human

pathogens in raw and treated wastewaters as well as in conventional, recreational and drinking
waters; they are also used to assess/control the reliability of plant treatments and identify
the origin of water. Their use can be justified by the great number and the diversity of human
pathogens in waters, their dangerousness, and difficulties in their enumeration; bioindicators
are easier, faster and cheaper to isolate, cultivate and identify (Keegan et al., 2009).
Moreover, pathogen concentrations not-measurable without first concentrate the

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suspensions are often beyond maximum tolerable thresholds that may be calculated by
quantitative microbial risk assessment (QMRA) for a tolerated disability adjusted life years
(DALY) of 10-6 per person per year; this is especially the case for human enteric viruses – e.g.
5 10-3 Rotavirus.L-1 proposed in an example proposed by the World Health Organization (WHO,
2006a) –. By contrast bioindicators are more abundant; the same example assumes that there
are 105-107 Escherichia coli per Rotavirus (WHO, 2006a). The most common indicators for
microbial water quality and human health risk assessment are total coliform, faecal coliform or
Escherichia coli, and faecal enterococcus (Levantesi et al., 2010; Ministère de la Santé et des
Sports, 2010; Jiang, 2006); other ones include spores of anaerobic sulphite-reducing bacteria
(Ministère de la Santé et des Sports. 2010), Clostridium spores (Levantesi et al., 2010) and F-
specific RNA phages (Ministère de la Santé et des Sports. 2010). To address some of their
deficiencies outlined below, others bioindicators have been proposed without being retained to
our knowledge: somatic coliphages and Bacteroides phages to replace the F-specific phages
(Leclerc et al. 2000), Escherichia faecalis to replace Escherichia coli (Fujioka and Yoneyama,
2002). Unfortunately, no bioindicator can mimic the behaviour and characteristics of the
true pathogens (Payment and Locas, 2011; Symonds et al., 2009; Keegan et al., 2009;
Petrinca et al., 2009; Salgot et al., 2003; Sinton et al., 2002; Moore et al., 1988), only about 3%
of individual humans carry the F-specific RNA phages and their abundance in wastewater
treatment plants may result from their multiplication in sewage (Leclerc et al. 2000), and there is
little concordance in the sample volumes (from 1 to 400 L for bacteriophages), in the
concentration methods and in the phage detection methods, thus making comparisons
extremely difficult (Leclerc et al. 2000). Several works noted no or poor relationships between
classical faecal bioindicators and pathogens in drinking waters (Figueras and Borrego, 2010), in
sewage and/or reclaimed wastewaters (Payment and Locas, 2011; Levantesi et al., 2010;
Carducci et al., 2009; Haack et al., 2009; Villar et al., 2007; Harwood et al., 2005; Leclerc et al.
2000), in surface waters (Payment and Locas, 2011; Skraber et al., 2004; Metcalf et al., 1995),
in groundwater (Payment and Locas, 2011;), and in treated wastewater for irrigation (Holvoet et
al., 2014). More precisely in sewage, even with very high levels of microorganisms, no
mathematical correlation can predict the type or concentration of any pathogen (Payment
and Locas, 2011). Difference between pathogen and bioindicator resistances to plant
treatments contribute also to the lack of correlation – e.g. Adenoviruses have been found to be
significantly more stable than faecal indicator bacteria and other enteric viruses during UV
treatment (Jiang, 2006); Escherichia coli is so sensitive to sunlight inactivation that it should not
be used to monitor recreational waters for the presence of human enteric viruses (Fujioka and
Yoneyama, 2002) –. After discharge in the environment, direct correlation becomes
biologically improbable as dilution, transport, and different inactivation rates occur in various
environments (Payment and Locas, 2011). This may lead to false alert and to lack of alert,
as at Milwaukee where drinking water contamination lead over 400000 people to be infected
with cryptosporidium in 1993 (Mac Kenzie et al., 1994). However, bioindicators are still useful as
a measure of risk (Holvoet et al., 2014; Payment and Locas, 2011). Moreover, several authors
noticed that bioindicators may be useful to assess/control the reliability of plant treatments
while mentioning differences between the fates of bioindicators and pathogens during some
treatments (Lucena et al., 2004; Vilanova et al., 2004; Ashbolt et al., 2001). Today, we can
assume that the monitoring of bioindicators may be replaced shortly by the direct detection of

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pathogenic microorganisms (Figueras and Borrego, 2010). , including for example human
enteric viruses (Bosch et al., 2008). New developments in molecular techniques with real-time
or quantitative PCR, Multiplex PCR and genetic microarrays would probably enable faster
determination of pathogen themselves, with much more information on their viability and
infectivity (Yeh et al., 2009; Stratton and Matthews, 2009). Especially, methods for virus
extraction, concentration, and enumeration have quickly evolved during the last 10 years
(Mattison et Bidawid, 2009; Rodríguez et al., 2009b; Hamza et al., 2009; Bosch et al., 2008;
Croci et al., 2008; Morin and Picoche, 2008; Oillic et al., 2007; Da Silva et al., 2007; Liu et al.,
2007; Villar et al., 2006; Dubois et al., 2006; Villar et al., 2006; Dubois et al., 2006; Fong et Lipp.
2005; He et Jiang, 2005; Katayama et al., 2002; Jothikumar et al. 1995; Tsai et al., 1993).

Chemical hazards

Raw wastewaters may contain various chemicals including mineral compounds (N

compounds, phosphates, chloride, sodium, borate, trace metals …) (Leverenz et al., 2011;
Toze, 2006b; Unkovich et al., 2006), and organic pollutants (Toze, 2006b; Toze, 2006a). N-
compounds and phosphates may favour river eutrophication (Thomas et al., 2010; WHO-EC,
2002), while they are important nutrients for crops. Possible high contents in sodium cation
have detrimental effects on the structural stability of soils, their compactness and their
water permeability (Mazzini et al., 2013), and high concentrations in sodium, chloride and
borate ions are toxic for plants (Unkovich et al., 2006). Heavy metals are of little concern for
irrigation with treated wastewaters as most of those in raw sewage are immobilized on the
biosolid fraction (sludge …) during classical treatments (Toze, 2006b). However, some authors
recommended to use an additional treatment process to decrease the level of metals in the
sewage irrigation water (Afifi et al., 2011) and, when wastewater is of industrial origin and/or is
not sufficiently treated, heavy metals would need to be considered (Toze, 2006b; Foster and
Chilton, 2004), notably lead, chromium, cadmium (Foster and Chilton, 2004), – e.g. as in India
(Sridhara Chary et al., 2008) and probably in the past in China, with as a lasting effect due to
the very low mobility of metals in soils (Khan et al., 2008) –. Organic pollutants are often
considered as 'emerging pollutants', i.e. new chemicals without regulatory status and which
impacts on environment and human health are poorly understood for the U.S. Environmental
Protection Agency (Deblonde et al., 2011). Organic pollutants from house wastewaters
include chemicals of personal care products, various pharmaceutical products
(antibiotics, lipid regulator agents, anti-inflammatory drugs, -blockers, cancer therapeutics,
contraceptives and other hormones) (Barnes et al., 2008; Chefetz et al., 2008; Al-Rifai et al.,
2007; Nikolaou et al., 2007; Conn et al., 2006; Hernando et al., 2006; Karthikeyan and Meyer,
2006; Barnes et al., 2004), bisphenol A and phthalates (Barnabé et al., 2008; Clara et al.,
2010; Dargnat et al., 2009). When a unique urban sewer network collects both house
wastewaters and runoff waters during rainy events, wastewaters may also contain pesticides
(Gasperi et al., 2008b; Blanchoud et al., 2007) and polycyclic aromatic hydrocarbons
(Palmquist and Hanaeus, 2005). In addition, solvents are produced during disinfection by
chlorine (Kim et al., 2003). And neurotoxins and carcinogenic hepatotoxins may be
synthesized by cyanobacteria (Sivonen and Jones, 1998) from which blooms are favoured by

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wastewater (Barrington and Chadouani, 2008); in several countries, water coming from ponds
without special treatment contains microcystins that have an impact both on the growth and the
development of crops (Gehringer et al., 2003; Saqrane et al., 2008). Concentrations of most
organic pollutants in urban wastewaters (raw or treated) are generally below the toxic
levels for humans, but potential problems may result from the combined effects of several
pollutants and/or their cumulative consequences over long-term periods, all the more that
some pharmaceuticals and personal care products are very persistent in the environment
and/or can accumulate in plants. The great diversity of compounds leads to fragmentary
knowledge on their environmental fate and impacts. Impacts on aquatic ecosystems have been
the most discussed (Gros et al., 2010). Impacts on human health remain uncertain for irrigation
reuse. They may a priori result from pharmaceutically active compounds and a large number of
compounds that are known or suspected endocrine disruptors: they include the estradiol
compounds commonly found in the contraceptive pill, phytoestrogens, pesticides, industrial
chemicals such as bisphenol A and nonylphenol, and heavy metals (Toze, 2006b).
Groundwater contamination may be direct from residential septic systems (Swartz et al., 2006).
The removal efficiency of treatment trains in wastewater treatment plants varies between
compounds and treatments trains (Watkinson et al., 2007), and several studies noted the
presence of organic contaminants in the environment – e.g. antibiotic in watershed (Watkinson
et al., 2009) –. Due to the potential concern of organic pollutants in raw and treated
wastewaters, we add to this review a more detailed review on the diversity and the
environmental fate of organic contaminants in Appendix 2.

Environmental and agricultural hazards

Irrigation with wastewater partly protects rivers, aquifers and the sea from direct
discharge of wastewaters into these water bodies. Other well-known environmental benefits
include the recovery of nutrients for agriculture, and the sustainability of water resource
management.

However, the use of untreated wastewater has led sometimes to local or regional
disastrous effects. As a European example, Milan is the largest European project for
agricultural irrigation reuse. Irrigation is taken from streams and a network of intermeshed
ditches and canals developed by Cistercian monks in which raw wastewaters were discharged
until recently; the system has been completed with derivation canals from Lugano and Maggiore
lakes. The doubling of Milan population since the late 19th century together with 1 M daily
workers has led to huge amount of wastewater, loss of permeability and contamination of soils,
and 30% of the pollution in the northern portion of the Adriatic Sea south of Venice, until
Nosedo and San Rocco wastewater treatment plants have been operational in 2003 and 2004,
respectively (Mazzini et al., 2013).

Environmental hazards may result from the salinity and sodicity of wastewaters that affect
soil structural stability, soil structure and soil mechanical strength (Sou/Dakouré et al., 2013;
Qadir and Drechsel, 2010; Vogeler, 2009; Tal, 2008; Gharaibeh et al., 2007; Toze, 2006; Gerba

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and Smith, 2005) and indirectly soil air and water permeabilities, as well as soil aeration. The
excessive salinity and sodicity of wastewaters lead sometimes farmer associations to mix water
desalinized by reverse osmosis to other treated wastewater to insure acceptable water electrical
conductivity (Renault et al., 2013). Hazards also result from the toxicity for plants of high salinity
and high levels of chlorine, sodium and boron (Tal, 2008; Hamilton et al., 2007; Unkovich et al.,
2006; GWRC Report, 2005; Angelakis et al., 1999). At least wastewaters may contain toxic
compounds, by emerging organic substances (disruptors endocrine, pharmaceuticals including
antibiotics ...) (Leverenz et al., 2011, Barnes et al., 2008, Al-Rifai et al., 2007; Karthikeyan and
Meyer, 2006). They may affect the environmental biodiversity (), the growth and yield of crops,
and/or accumulate in plants (Dolliver et al., 2007; Boxall et al., 2006; Kumar et al., 2005) or
animals (Rimkus et al., 1997).

Indirectly, wastewater reuse may induce several changes that have to be explicitly taken
into account for decision with cost-benefit approaches: drinking water supply, recreational
activities, jobs ….

Economic sustainability of wastewater reuse in irrigation:

an overview

Cost-benefit analyses are important to insure the economic sustainability of

wastewater reuse for crop irrigation and optimize the choice of expenditure items. As an
example; the city of San Diego is now going to reuse indirectly wastewater as potable water
(Steirer and Thorsen, 2013), since costs of potable reuse are lower than costs of nonpotable
reuse and desalination, and cost of importing water which remains smaller is anticipated to rise
faster and to become comparable to reuse by 2030 (Trussell et al., 2012). Other costs-benefits
analyses have been performed at regional or country level – e.g. in Israel (Haruvy, 1997) –. On
the one hand for human health protection, it is important to know whether additional
expenditures must be made, and where they must be made (on wastewater treatments, on
the production of agricultural products and their commercialization, at the level of consumers). It
is important to take into account simultaneously all positive or negative impacts on crops (e.g.
their yields and qualities), on the environment (e.g. the biodiversity in water bodies, the
structural stabilities of soils and their effects on soil compaction, permeability to water, aeration
...), and indirectly on other sectors of the economy (tourism, recreational activities, employment
…). On the other hand, it is important to know how to use economic incentives to promote
the reuse of wastewater, including tariffs, subsidies and taxes (Van der Bruggen, 2010).
Although the ‘polluter pays’ principle is widely accepted in most OECD countries, polluters in
Europe currently pay only for treatments required for the discharge of wastewater in
conventional water bodies; the cost of additional (regenerating) treatments required to remove
remaining contaminants before reuse can be charged partly or totally to farmers or public
authorities. It may increase the economic burden of wastewater reuse in agriculture beyond the
point which most agriculture crops can carry and it may result in blocking the rational economic

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development of water recycling and reuse. Therefore in several places, regenerated water is
sold at very low prices, e.g. in Milan (Mazzini et al., 2013), Cyprus (Papaiacovou et al., 2013)
and Tunisia (Qadir et al., 2010b).

Economic considerations begin to participate to decisions by comparing cost of additional

treatments (Molinos-Senante et al., 2013; Iglesias et al., 2010) to direct and indirect benefits
(Lavee, 2013, 2011; Molinos-Senante et al., 2010). Such analyses can be performed at national
or regional levels by comparing alternative scenarios (Lavee, 2013). Costs of additional
water treatments may be estimated (Molinos-Senante et al., 2013; Iglesias et al., 2010) in
order to optimize treatment technologies. Operational costs deal with energy, chemicals, labour,
maintenance and sludge and grit disposal (Mazzini et al., 2013). Total cost per m3 of treated
wastewater is usually much higher than the plant unit is small (Hernández-Sancho and Sala-
Garrido, 2009), but it greatly depends on the local context, making comparisons difficult
between wastewater treatment plants. France has many very small wastewater treatment plants
(Golla et al., 2010): in 2011, only 17.3 % of the 19300 plants corresponded to French
agglomerations of more than 2000 equivalent habitants, while 17% of the stations deal with
more than 90% of the pollution produced (MEDDE, 2013). Beyond about 5.4 million homes
were not connected to the public sewage in 2012 (MEDDE, 2012). Decision support systems
(DSS) with monetary valuations of costs exist for the selection and design of wastewater
treatments (Hamouda et al., 2009; Hidalgo et al. 2007), but there is still a need to develop
integrated decision support systems that are generic, usable and consider a system analysis
approach (Hamouda et al., 2009).

Taking into account the impact of practices on health, the environment and crops
requires to assign a monetary value to these effects. Monetary valuation of disease gave
place to several papers about 20 years (Remoundou and Koundouri, 2009). By contrast until
recently, monetary valuation of environmental benefits were restricted to some items – e.g.
nitrate leaching (Haruvy, 1997)) –, whereas many social and environmental costs have been
difficult to quantify (Hamouda et al., 2009). Since a few years, new methods of monetary
valuation have been proposed, including contingent valuations (Dupont, 2013; Alcon et al.,
2012), estimation of shadow prices for the pollutants removed in a treatment process
(Hernández-Sancho et al., 2010; Molinos-Senante et al., 2010) and others (Lavee, 2011).

The use of such methods leads already to some interesting results although their
generic value is questionable. As a first example, Shuval (2008) combined a quantitative
microbial risk assessment to a cost effectiveness analysis: he estimated that treating
wastewater to meet the US-EPA/US-AID guidelines (US-EPA/US-AID, 1992) would result in an
additional cost, of some $ 500 000 to $ 1 000 000 per case of disease prevented compared to
WHO standard. As a second example, Lavee (2011) examined the costs and benefits
associated with possible alternative wastewater treatment standards in Israel; it was found that
switching from the current standards to more demanding standards would indeed achieve a net
benefit to the national economy, estimated at US$0.1235/m3 of treated wastewater. Of course,
the results of Lavee greatly differ from those of Fine et al., (2006) who didn't account for
environmental impacts.

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Therefore, it seems important to develop integrated decision support systems that

are generic, usable and consider a system analysis approach (Hamouda et al., 2009). And
in their objectives for updating their guidelines, the U.S. Environmental Protection Agency would
like to have focus on international project economic benefits (Bastian, 2012).

Regulations: the need for stronger scientific basis

Some 50 countries in the world irrigate about 10 million hectares of crops with
raw/untreated wastewater producing about 12% of the world food crops (Shuval, 2008); they
include China, Mexico, India, Chile, Syria, Pakistan, Colombia, Argentina, several USA states,
Ghana, Vietnam, Peru, Turkey, Morocco, Egypt, Kuwait, Sudan, Tunisia, Nepal and Bolivia,
although several of them also use treated wastewater in irrigation (Keraita et al., 2008). China,
India, Pakistan and Mexico are among the largest countries in this group, and also those most
often mentioned for large-scale industrial water pollution and irrigation with highly polluted water
(Jiménez and Asano, 2008). This practice is made possible by the lack of guidelines,
regulations, and standards or their non-compliance; it provides vital work for hundreds of
thousands of poor farmers and essential food for malnourished populations, but it often results
simultaneously in massive disease transmission (Shuval, 2008). In Europe, several countries
have no regulations or guidelines dealing with reuse for irrigation: Austria, Czech Republic,
Denmark, Estonia, Finland, Iceland, Ireland, Latvia, Lithuania, Luxembourg, Norway, Slovenia,
Slovakia, Sweden, Switzerland, and the Netherlands. We can add to this list several others that
are still contemplating regulations or guidelines (Belgium, Bulgaria, Hungary, Malta, Poland,
Romania, and UK) (Angelakis, 2012), Malta criteria being already in preparation since 2011
(Angelakis, 2012). The lack of regulations/guidelines in these countries generally results from
the recycling of wastewater for other uses – e.g. in industry in Belgium (Bixio et al., 2008) – or
from the lack of reuse. A probable exception is Bulgaria that has still no regulation, while its
water stress index is higher than 60% (Bixio et al., 2005), but there have not been any specific
investigations related to wastewater reuse in this country (Angelakis et al., 2007). By contrast,
other European countries have regulations or guidelines dealing with wastewater reuse
in irrigation: Italy (since 1976 with the water Protection Act in 1976 that was replaced in 2003
by the Ministry Decree, D.M. n°185/03 (Mazzini et al. (2013))), France (since 1991 (CSHPF,
1991) modified with an 'arrêté' in 2010 (Ministère de la Santé et des Sports, 2010) and currently
discussed to be improved again), Germany (since 1999 (Jiménez and Asano, 2008)), Cyprus
(since 2005 (Decree 269/2005) for small agglomerations completed in 2007 with standards set
through disposal permits for large agglomerations (Decree 263/2007)), Portugal (since 2006,
standards NP 4434 (Marecos do Monte, 2010; Marecos do Monte, 2008)), Spain (since 2007)
(Angelakis, 2012), and Greece (since 2011 (Papaiakovou et al., 2011)).

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Some reviews have traced the history of the regulations on wastewater reuse in irrigation
(Angelakis, 2012; Paranychianakis et al., 2011; Papaiakovou et al., 2011; Shuval, 2008), and
the recent guidelines of the U.S. Environmental Protection Agency give an insight into
regulations or guidelines and standards of different countries/states (US-EPA, 2012).
Wastewater reuse for irrigation was practiced in the World without regulations or
guidelines before 1918. At this time, the California State Board of Public Health promulgated
the initial Regulation Governing Use of Sewage for Irrigation Purpose, pertaining to irrigation of
non-edible and cooked crops with sewage effluents (Angelakis, 2012; Asano, 2006; Ongerth
and Jopling, 1977) and, in 1933, the State Department of Health in California allowed the
irrigation of vegetables if the wastewater was oxidized (made non-putrescible) and reliably
disinfected or filtered to meet bacterial standard is approximately the same as the current
drinking water standard. California has continually revised its regulations and standards since
that time to address additional applications, advances in treatment technology, and increased
knowledge in microbiology and public health protection (Angelakis, 2012; Crook and Surampalli,
1996; Ongerth and Ongerth, 1982), and publish the so-called Title 22 (State of California, 2000)
and the Purple Book (State of California, 2001), which are a collection of guidelines, rules,
and standards corresponding to a "zero tolerance" (e.g. 2.2 TC/100 mL of treated
wastewater for unrestricted irrigation of vegetable crops normally eaten raw). They have been
used later elsewhere as basis for regulations and standards (Bixio et al., 2008). Currently,
California has the most comprehensive regulations pertaining to the public health aspects of
reuse (Zhang, 2012). In recognition of the value of reclaimed water, the U.S. Environmental
Protection Agency published guidelines for wastewater reuse, with progressively more stringent
standards (initially proposed in 1980, then updated in 1992, 2004 and 2012 (US-EPA, 2012;
Crook and Surampalli, 1996). Standards proposed in 1992 together with the US Agency for
International Development for unrestricted irrigation include 'No FC detection in 100 mL' (US-
EPA/US-AID, 1992), regardless of technical feasibility, of cost effectiveness for other areas of
the world, and of the "natural" river water or water at approved bathing beaches in the United
States or Europe microbial quality. The State of Florida already adopted 'No detectable E.
coli/100 ml for crops consumed raw' in 2003 (Papaiakovou et al., 2011). In the U.S., 25 states
had regulations, 16 guidelines, 9 nothing governing the practice of reuse of treated wastewater
covering several but not all uses of wastewater in 2003 (Bastian, 2012). Some other countries
have adopted a "zero risk" regulations, including Israel with its first regulations in 1952
(Shuval, 2008; Brissaud, 2008; Asano, 2006) and increasing with its revision in 1978 and 1999
(i.e. <1 FC/100 ml for unrestricted irrigation in 1999), in Greece (Papaiakovou et al., 2011;
Hochstrat et al., 2011) and Australia before 2006 (ARMCANZ-ANZECC-NHMRC, 2000); such
option is generally not economically or technically feasible in developing countries
(Shuval, 2008). In Europe, Italy and Cyprus have established the highest standards, but not as
severe as U.S. standards. Cyprus imposes < 5 faecal coliforms/100 mL in 80% of samples for
unrestricted irrigation for small agglomerations. In Italy, it is interesting to note the Law decree
n°152 in 2003 (Ministry Decree, D.M. n°185/03) set less restrictive rules (<10 E. coli/100 mL in
80% of samples for unrestricted irrigation than the water Protection Act in 1976 (<2 total
coliforms in all samples before for unrestricted irrigation). By contrast, the World Health
Organisation (WHO) proposed first in 1973 Guidelines with standards (<100 FC/100 ml in
80% of samples for unrestricted irrigation) for wastewater reuse (WHO, 1973). Standards were

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added in the 1989 in WHO Health Guidelines for the Use of Wastewater in Agriculture and
Aquaculture for wastewater irrigation of vegetables eaten raw (<1000 faecal coliforms (FC)
/100 mL and <1 helminth egg /L of effluent) (WHO, 1989), based on reviews requested in 1982
by the World Bank and the World Health Organization on new epidemiological and
technological evidence regarding health risks associated with wastewater irrigation (Shuval et
al. 1986, Feachem et al, 1983; Strauss and Blumenthal, 1989). The new guidelines have
become widely accepted by international agencies including the FAO, UNDP, UNEP and the
World Bank, and have been adopted by several countries like Texas State in 1990 (75
FC/100 mL) (Papaiakovou et al., 2011), France (Ministère de la Santé et des Sports, 2010;
CSHPF, 1991) and Spain ((Royal Decree 1620/2007, 2007) Iglesias et al., 2010; Iglesias
Esteban and Ortega de Miguel, 2008) and number of developing, as well as developed
countries. In 2006, the World Health Organization has experienced a major turning point in
its proposals with the use of quantitative microbial risk assessment as basis for decision
(WHO, 2006a,b), partly in response to criticism of too liberal previous guidelines in 1989 (WHO,
1989) compared to those of the U.S. Environmental Protection Agency (USEPA/USAID 1992).
The group involved in the preparation of this third edition of guidelines has concluded that these
new risk assessment studies validated the WHO (1989) of 1000 E. Coli/100ml for unrestricted
irrigation of most vegetable and salad crops eaten uncooked. And Shuval et al. (2008)
estimated that treating wastewater to meet the U.S.-EPA/U.S.-AID guidelines (1992) would
result in an additional cost, of some $ 500,000 to $ 1,000,000 per case of disease prevented.
Some countries have adopted the quantitative microbial risk assessment as a tool in their
federal guidelines like Australia after 2006 (Power, 2010; EPHC/NRMMC/AHMC, 2006) and
Canada (Huot, 2008). Unfortunately, the QMRA attractive approach still suffers today from lack
of data and knowledge (see above). Thus, regulations or guidelines and standards (selected
indicators associated thresholds) greatly differ between countries, and these differences are
not easily understood without taking into account the acceptability of practices and the level of
development of countries (e.g. Ongerth and Ongerth, 1982; Ongerth and Jopling 1977).

The targets of regulations (or guidelines) and standards are first to protect public
health, i.e. secure wastewater reuse for agricultural product consumers as well as farmers,
neighbouring inhabitants and walkers (Paranychianakis et al., 2011). They should also protect
the environment – especially soils and water bodies – and agricultural productions (in quality
and quantity), while environmental risks are either ignored or underrepresented (Maimon et al.,
2010) and most of the standards focus on microbial health parameters, those dealing with
environmental and crops being commonly not included in standards (e.g. nutrients for plants,
salts, toxic organics, trace elements) (Paranychianakis et al., 2011). Guidelines, regulations
and relevant standards may also encourage wastewater reuse. In 1970, the California State
Water Code stated that "it is the intention of the Legislature that the State undertake all possible
steps to encourage development of water reclamation facilities so that reclaimed water may be
available to help meet the growing water requirements of the State" (California Water Code,
section 512) and the California Water Code (section 13551) states that no one shall use water
from any source of quality suitable for potable domestic use for non-potable uses, if suitable
recycled water is available. Similarly, the European Communities Commission Directive
declared that "treated wastewater shall be reused whenever appropriate. Disposal routes shall

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minimize the adverse effects on the environment" (CEC, 1991). During the last quarter of the
20th century, the benefits of promoting water reuse as a means of supplementing water
resources have been recognized by most state legislatures in the USA as well as by the
European Union (Asano, 2006). A first way is prohibit wastewater discharge in surface water
bodies or to impose more stringent standards (Paranychianakis et al., 2011); another way is to
limit the amount of conventional water use or to link permits to the progressive use of alternative
water sources (Van der Bruggen, 2010). In addition, non-regulatory measures like taxes on
conventional water and/or subsidies on treated wastewater and for additional infrastructures
may also favour wastewater reuse. However, inadequate regulations may prevent initiatives
in wastewater reuse in irrigation, as it has been clearly observed in Italy until 2003. In France,
a similar analysis has been proposed before and after the new regulation (Ministère de la Santé
et des Sports, 2010) by Lazarova and Brissaud (2007), Blin et al. (2008) and Molle et al. (2012);
and a modification of this regulation being studied since about for 12 months.

Regulations or guidelines and standards on wastewater reuse in irrigation may address

wastewater treatment, the quality of treated wastewater (chemical and biological properties)
at the outlet of the wastewater treatment plant or at the point of use, the modalities of
irrigation (crop, irrigation method, delay between the last irrigation and harvest, setback
distances and/or edge required …), the traceability, the controls, the alert procedures in case of
malfunction, and the public (inhabitants, education …) information. Currently, treatments and
quality requirements generally depend on the crop (non-food or food crop, food crop eaten raw
or cooked, edible parts in direct contact or not with irrigation water, delay between the last
irrigation and harvest). They may also depend on the soil and the proximity of peoples. In only a
few regulations like the French 2010 regulation (Ministère de la Santé et des Sports, 2010), the
soil content in trace metal elements affect the possibility to use wastewater. Different qualities of
wastewaters are generally defined. As the appropriateness of current microbial indicators are
often criticised (see before), additional treatments is sometimes seen as a valuable alternative
to too much controls that may be regarded as unsustainable with regard to cost.

The establishment of regulations and standards at the European scale is

questionable although it is supported by several authors (Gatel, 2012; Angelakis, 2012;
Angelakis 2011; Angelakis et al., 2003). Such regulations or guidelines and standards could
contribute to improve the management of water resources and increase the protection of public
health and environment, to avoid useless restrictions and disadvantages of national regulations
(Angelakis, 2012), (iii) encourage the use of alternative water sources, and finally (iv) enhance
the agricultural productivity in Southern European countries. However, regulations have to take
into account actual health and environmental hazards that vary with regions and countries.
Hazards caused by wastewater irrigation have to be compared to other sources of hazards, and
to the cost for reducing these risks – e.g. product handling in markets (Ensink and van der
Hoek, 2007) –.

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The need of new matrix of multi-criteria requirements for

water reuse at regional scales

Wastewater reuse practice has to insure sanitary safety, as well as economic and
environmental sustainabilities whereas scientific knowledge is still often insufficient.
Currently, there are inconsistencies in the rationale of current standards to control hazards in
wastewater reuse (Salgot et al., 2006): namely the adequacy of control parameters (retained
microbial (and sometimes chemical) indicators), a lack of definition of the appropriate sampling
points, the number and periodicity of samples and analysis, and the cost of the analytical work
(Salgot et al., 2006). Risks have to be quantitatively assessed, since a 'zero risk' policy may
lead to excessive costs and a serious misallocation of expenditures (Shuval, 2008).

We suggest retaining water categories adapted by Salgot et al. (2006) with regard to
special final uses (Table 3), as they distninguish 4 cateogries with greatly differing risks
microbial contaminations. Such subdivisions could be refined according to other criteria, e.g. the
time elapsed between the last irrigation and harvest (WHO, 2006), post-harvest treatments
(WHO, 2006), and distances criteria (MSS, 2010).

Table 3: Microbial and chemical water quality categories for different types of irrigation of
wastewater reused (from CEDEX (1997) adapted by Salgot et al. (2006))
Microbial Chemical
Specific final use
category category

I 1  Private garden irrigation.

II 1  Irrigation of open access landscape areas (parks, golf courses, sport

fields, etc.).
 Irrigation of greenhouse crops.
 Irrigation of raw consumed food crops. Fruit trees sprinkler irrigated.
 Unrestricted irrigation.

IV 1  Irrigation of pasture.
 Irrigation of indusrial crops for canning industry and crops not raw-
consummed.
 Irrigation of fruit-trees except by sprinkling.
 Irrigation of industrial crops, nurseries, fodder, cereals and
oleaginous seeds.

V 1  Irrigation of forested areas, landscape areas and restricted access

areas. Forestry.

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Dealing with microbial hazards for humans, the detection of human pathogens may be
costly, the maximum tolerable concentrations may be very low with regard to detection
thresholds for the most sensitive methods (especially for viruses (WHO, 2006)), and the time
needed to produce results may be long. One has therefore to propose solutions that combine (i)
preventive risk management concepts (especially Hazard Analysis Critical Control Point
(HACCP)) and good reuse practices to reduce the number of controls (Salgot et al., 2006), (ii)
cheap and fast measurements of parameters easily monitored and partly depending on the
organic load and the treatment train of wastewater (e.g. turbidity, total suspended solids, BOD,
COD), (iii) fast measurements of traditional faecal indicators (Escherichia coli and bioindicators
more resistant to treatments: e.g. Enterococcus faecalis, spores of Clostridium perfringens,
viruses (bacteriophage), and (iv) maybe during high risk periods the enumeration of some
actual human pathogens in raw wastewaters, especially 1 or 2 viruses (Noroviruses, Hepatitis A
viruses, Enteroviruses, Adenoviruses and/or Rotaviruses) and protozoa (Giardia Lamblia cysts
and Cryptosporidium parvum oocysts), although it would be better to measure water-based
pathogens at the point of use (Legionella, Naegleria fowleri). Epidemiological methods seem not
to be good tools for assessing health risks, since they are not sensitive enough to “tease out”
cases that might be associated with recycled water. Threshold values in new standards should
be based on quantitative microbial risk assessments and cost-benefit analysis insuring the
economic sustainability of reuse and the best use of money. Thresholds should not to be the
same between regions and countries; moreover, standards should differ between products for
the local market and for export.
Dealing with soil and crop protection, some parameters may be monitored easily before
irrigation in lagoons or storage reservoirs (pH, electrical conductivity), and other ones may be
measured sometimes (sodium absorption ratio (SAR)). Mineral compounds that may be toxic for
plants (chloride, sodium, boron) should be measured rarely as their concentration in wastewater
is probably nearly constant. As long as wastewaters are of domestic origin, we suggest to check
(maybe once a year or every 2 years) for the accumulation of heavy metals in soils rather than
measuring their concentrations in treated wastewater, since most of them are adsorbed on
microbial sludge.
By contrast, difficulties inherent in emerging organic substances result partly to their high
number and diversity. Two complementary approaches may be proposed. The first is to monitor
concentrations of some compounds in treated effluents; they have to be minimized with respect
to the origin of the sewage (domestic, urban and/or industrial) and cover a broad spectrum of
chemicals. The second is the use of bioassays on the oestrogenic (and other) activities of all
compounds in treated effluents (Richard et al., 2014; Körner et al., 2001).

If microbial and chemical standards should not be the same everywhere, methods to define
them could be shared. They may be based on the use of a decision support system combining
a model describing the environmental fate of contaminants, a quantitative risk assessment and
cost-benefit approach, all interacting with decision support systems for the optimization
treatment trains in wastewater treatment plants.

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Conclusions

Wastewater reuse for crop irrigation may simultaneously address water quantity and
quality problems; it is implemented in regions where conventional water resources are too
limiting and/or the discharge of (treated) wastewater has too much impact on the environment,
especially in coastal areas and Islands where tourism is of first concern (Fazio et al., 2013).
While wastewater reuse is already important in some countries/states including California (Van
der Bruggen, 2010), Israel (Tal et al., 2006), and Cyprus (Papaiacovou et al., 2013), it remains
generally low. In Europe, wastewater is preferentially reused for crop irrigation in South
European countries having a high Water Stress Index, high water needs for crops and large
volumes of wastewater produced (Cyprus, Malta, Spain and Italy), and reuse will increase
further in these countries, even in Cyprus where it is currently limited by the collect and
treatment of wastewaters (Papaiacovou et al., 2013). Wastewater reuse remains low or
negligible in South European countries having a lower water stress index (Greece, France and
Portugal), but it should increase because of global warming and the increase in frequency of
extreme droughts. In more Northern European countries where water deficit for crops is lower or
non-existent, wastewater may be reused locally for irrigation (e.g. in Germany) and/or in other
sectors such as urban and industry sectors (e.g. in Belgium (Van der Bruggen, 2010)); and
several large cities and conurbations depend on recharging surface water and groundwater
bodies by treated wastewater, leading de facto to indirect potable reuse, although it is usually
not acknowledged. We have obtained nearly no information on wastewater reuse in Bulgaria
that has one of the highest water stress index of European countries.

Wastewater may be reused for various activities: agricultural or landscape irrigation,

industrial uses, urban reuse, recreational uses, aquifer recharge, and indirect or direct potable
reuse. The type of use has to be discussed with regard to local water needs, cost-benefit
considerations and possible conflicts. Conflicts may result from competing uses in countries
with a high water demand – e.g. between irrigation and industrial uses in Japan (Van der
Bruggen, 2010) –, and from greatly differing quality needed for several simultaneous uses and
the allocation of treatment costs – e.g. in the South of Valencia, Spain, where water from El
Pindo wastewater treatment plant simultaneously irrigates submerged rice fields and supplies
Albefura lake (Renault et al., 2013) –. Public acceptance is generally good for reuse in
irrigation and for other uses, with the exception of direct potable reuse (Ormerod and Scott,
2012; Cain, 2011; Leverenz et al., 2011; Sofres, 2006; Ongerth and Ongerth, 1982; Ongerth
and Jopling, 1977) although some 'success stories' exist in direct potable reuse as in Windhoek
(Namibia) (du Pisani, 2006). However, some opposition exists. They are often explained by
the 'yuck factor' (Macpherson, 2013; Leong, 2010), corresponding to a psychological aversion
with the following expressions retained in surveys: "psychologically repugnant", "lack of purity",
"can cause disease" (Ongerth and Jopling, 1977). Another explaination is that public opposition
would result from social and cultural perceptions of risk (Ormerod and Scott, 2012). The 2
preceding explanations justify more information dealing with water cycle, water treatments
and the actual risks in order to prevent project failure.

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Actual risks include sanitary, environmental and agricultural hazards that result from
the presence in raw sewage of human pathogens and various inorganic and organic
compounds. Although it is possible to produce water of almost any quality desired from
wastewater (Norton-Brandão et al., 2013), cost-effectiveness of treatments have to be ensured.
The management of conventional and alternative water resources requires appropriate
regulations and standards, as well as economic policy. While the diversity of current rules
between European countries seems not scientifically justified and leads to inequalities,
differences between regions in water requirements, raw wastewater properties and human
resistance to pathogens justify having regulations adapted to regional contexts, and Ashbolt et
al. (2001) to tailor indicator choice to local circumstances when translating international
guidelines into local standards. The European Union could propose guidelines with
maximum tolerated risks and a methodological framework to elaborate regional or
national regulations and standards that account for local specificities, in the same spirit that
the World Health Organization encourages national governments to adapt their guidelines to
their own socioeconomic and environmental realities (Ensink and van der Hoek, 2007). A
distinction should then be performed between crops for local markets or for export.

Some separate tools exist to optimise wastewater treatment, assess quantitatively microbial
risks or estimate the balance between benefits and costs, including a monetary valuation of
environmental changes, but new tools combining risk assessment, treatment optimisation
and cost-benefit considerations are required to support decisions dealing with the
definition of new regulations and standards as well as economic policy (tariffs, taxes, subsidies
…). In the current state of knowledge, a first generation of combined tools can be proposed,
but they would have to evolve in order to (i) incorporate new data, processes and pathways of
contamination, (ii) add emerging microbial or chemical contaminants, and (iii) adapt to possible
changes in standards (indicators themselves, their maximum tolerable quantities and/or their
minimum removal rate).

The relevance of microbial indicators has to be discussed. Their use to characterize

the efficiency of treatments is probably relevant as long as several bioindicators having
different sensitivities to different treatments are used simultaneously. The major limitations of
microbial indicators generally used are first weak correlations with the level of pathogens
in wastewater and second their fate in the environment that may differ from the fate of
pathogens. In particular, they are generally not correlated with the levels of enteric viruses that
are increasingly considered as the etiologic agents of human enteric infections. An alternative
could be to detect directly some pathogens (Bosch et al., 2008) from a list established using
a methodology as that of the U.S. Environmental Protection Agency and the American Water
Works Association. This choice is currently hampered by the low levels of enteric pathogens
and the very low thresholds of tolerable concentrations; they may require the concentration of
water samples prior to pathogen detection and the use of molecular methods. But great
technological progresses have been performed, including those using DNA microarrays on
silicone nanostructures (e.g. Oillic et al., 2007), and molecular methods would allow to obtain
results quickly. Another alternative would be to partly replace microbial controls with more

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advanced treatments and/or more controls on some treatments (e.g. by measuring the
residual content in disinfectant), all the more that treatments will probably have to become more
stringent, partly to avoid environmental discharge of water too much contaminated by
chemicals. In the case of separate sewage networks for domestic wastewaters and rain runoff
without industrial wastewaters, indicators of emerging organic pollutants have probably to
be chosen among chemicals from personal care products, pharmaceutical products, bisphenol
A and phthalates; otherwise they must cover a broad spectrum of toxicological and ecological
risks as well as possible technical disorders (Salgot et al., 2006).

Additional knowledge is needed to optimize wastewater reuse. First, it is important to

better understand and describe the processes implied in microbial contaminations in
order to improve quantitative microbial risk assessment: via air (aerosolization, atmospheric
speciation of pathogens, inactivation/mortality and transport in the atmosphere, redeposition,
transfer from human respiratory tract to gastro-intestinal track), via food (internalisation through
the roots, the leaf stomata and/or injuries in the aerial parts of plants), and via water to some
extent to better assess the reactive transport of pathogens from soil surface to underlying
aquifer. It is also important to assess the combined effects of organic pollutants on
human health and environmental biodiversity, as well as their cumulative consequences
over long-term periods, as concentrations of most of them in urban wastewaters are generally
below the toxic levels for humans. Quantitative microbial risk assessment and quantitative
chemical risk assessment need also informations on population habits (food, displacements,
protection of farmers during field labour …) that are probably not available in each European
country. Second, new probe methodologies are required to monitor in situ microbial and
chemical contaminations in real time and at low costs, whereas current cost greatly vary
between microorganisms, as well as between organic micro-pollutants (Salgot et al., 2006).
Third, the monetary valuation of the changes resulting from wastewater reuse (human
health, environment, recreational activities, industry, jobs …) must be refined, especially the
monetary valuation of environmental changes, which is recent and may result from different
calculation procedures.

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Appendix 1: Virus fate in the environment

By Pierre Renault
INRA-UAPV UMR Environnement Méditerranéen et Modélisation des Agro-Hydrosystèmes,
Avignon, France

Viruses are obligate, intracellular pathogens (Fong and Lipp, 2005; Sobsey and
Meschke, 2003). Outside of the cells they may infect, virus particles (virions) consist of the
genetic material (viral RNA or DNA) wrapped by a protein coat (viral capside) and, in some
cases, an external envelope of lipids that surrounds the capside. Most of human enteric
viruses are naked viruses, i.e. without lipidic coating (Fong and Lipp, 2005); they are then
very resistant in the environment and to certain water treatments (Carducci et al., 2009), and
they may survive a long time in water environments (weeks to months) (La Rosa et al.,
2012). An exception is the well-known severe acute respiratory syndrome (SARS) virus, which
is an enveloped virus, i.e. with a lipidic coating, that may be considered as enteric and that is
rapidly inactivated in water and wastewater at ambient temperatures (Gundy et al., 2009;
Bennett, 2006). Most of human enteric viruses are human specific, except hepatitis E virus
with infections from pigs suggested from almost identical viruses (Koopmans and Duizer, 2004)
and infection proven from deer (Tei et al., 2003), and the severe acute respiratory syndrome
virus which moves from the bat population to other animals and humans (Gundy et al., 2009;
Bennett, 2006). The most notable viruses are hepatitis A virus (HAV) (hepatitis, liver
damage and jaundice), and the Calicivirus, especially the Norovirus genus (diarrhoea), and in
a lesser extent the Rotavirus (diarrhoea) (Rodríguez‐Lázaro et al., 2012; Carducci et al., 2009;
Koopmans and Duizer, 2004). Other viruses of greatest concern in water (and their associative
illnesses) include the group of Enteroviruses with Poliovirus, Coxsackievirus and Echovirus
(diarrhoea, meningitis, myocarditis, fever, respiratory disease, nervous system disorders, birth
defects), Astrovirus (diarrhoea) and Adenovirus (diarrhoea, respiratory disease, eye
infections. heart disease) (Rodríguez‐Lázaro et al., 2012). They have been involved in
waterborne outbreaks via drinking water (Hoffman et al., 2009; Zhuang and Jin, 2008; Craun et
al., 2006; Gerba, 1999) and recreational waters (swimming pools, lakes, lagoons, rivers and
thermal station) (Sinclair et al., 2009; Calderon et al., 2005; Craun et al., 2005). The most
commonly reported foodborne viral infections lead to gastroenteritis and less frequently hepatitis
A (Seymour and Appleton, 2001). Norovirus, Enteroviruses (Coxsackievirus and Echovirus) and
hepatitis A virus are among the 12 human pathogens listed in the 'Contaminant Candidate List'
established by the U.S. Environmental Protection Agency in 2008 (US-EPA, 2009), and among
the 11 human pathogens retained nearly at the same time by the American Water Works
Association (AWWA) (Hoffman et al., 2009); In addition, Adenovirus and Poliovirus are in the
first list, whereas Rotavirus is in the second one. The hepatitis A virus and the Norovirus have
been detected in wastewaters at the entrance and the exit of wastewater treatment plants (Da
Silva et al., 2011; La Rosa et al., 2010; Petrinca et al., 2009; Van den Berg et al., 2005; Pusch

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et al., 2005). They have been also detected sometimes in soils and underground waters
(Parashar et al., 2011; Reynolds et al., 2008; Borchardt et al., 2003).

The epidemiology of the Hepatitis A virus varies with the public hygiene and the water
treatment. There are endemic zones in Africa (Kamal et al., 2010; Gharbi-Khelifi et al., 2006)
and in some European countries like Albania (Divizia et al., 2005), where human populations
are exposed to this virus from childhood; viral infections are then generally asymptomatic or
lead to not acute disease (Yong and Son, 2009; Pinto et al., 2007). In regions like Tunisia,
hepatitis A virus infections seem to be cyclic with maximum in winters that may result from
heavy winter rainfalls, lower temperature than in summer, the use of unsanitised sludge as crop
fertilizer, and higher (infected) shellfish consumption (Gharbi-Khelifi et al., 2006). With the
development of this country, asymptomatic infections in young children have tended to
decrease, and more severe disease with even deadly forms of infection have tended to appear
among adults, clinical manifestations seeming to increase with age (Gharbi-Khelifi et al., 2006).
In regions with higher public health, viral infections result first from the Hepatitis A virus
importation from endemic regions via travellers or foods that are eaten crude or only slightly
cooked (seashells, onions, lettuce, spinach, tomatoes, raspberries …) (Hollinger and Emerson,
2007); human adults then develop acute forms of the disease, see rarely fulminant forms (Yong
and Son, 2009; Pinto et al., 2007). Two hepatitis A outbreaks affecting more than 800
individuals were reported in western France (between December 1992/March 1993 (Nuiaouet et
al., 1993) and in the Italian lake district between November 2002 and February 2003 (Divizia et
al., 2005). The great genetic and antigenic variabilities of the Norovirus, and their dynamic
behaviour render difficult their detection and characterization (Green, 2007) and don't enable
humans to immunize themselves (Atmar, 2010; Green, 2007). Gastroenteritis resulting from
Norovirus infections (also called ‘winter vomiting disease’) are generally not severe. They often
combine diarrhea and vomiting, and affect all the age groups (Green, 2007). They explain in
several developed countries more than 80% of gastroenteritis outbreaks for adults (Koopmans
et al., 2000) and more than 90% of nonbacterial outbreaks (Green, 2007). Several
contaminated foods are incriminated (Green, 2007; Koopmans and Duizer, 2004). Infections
vary with seasons (Yen et al., 2011; Chikhi-Brachet et al., 2002) although this seasonality is not
necessarily found for virus in raw and treated wastewaters (Myrmel et al., 2006; Van den Berg
et al., 2005).

Viruses have the greatest infectivity of all waterborne microorganisms: a few number
of them (about 101-102 pfu) being sufficient to cause infection (Morin and Picoche, 2008;
Hollinger and Emerson, 2007; Green, 2007), while they are excreted in the faeces in the
largest numbers, i.e. up to 1011-1012.g-1 faeces for sick and healthy carriers (Maunula et al.,
2013; La Rosa et al., 2012; Da Silva et al., 2011; Reynolds et al., 2008; Fong and Lipp, 2005;
Koopmans and Duizer, 2004) and several weeks after the illness period (Maunula et al., 2013;
Da Silva et al., 2007). In the USA, 8.2% of drinking waterborne outbreaks recorded between
1911 and 2006 had a well identified viral origin and other 44.6% corresponded to acute
gastroenteritis with an undetermined etiology (Craun et al., 2010) that were compatible with viral
infections (Reynolds et al., 2008). In France, some foodborne outbreaks resulting from water

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contamination by viruses were noted in the city of Gourdon (Lot) in August 2000 (INVS, 2001)
and in Isère department in November 2002 (INVS, 2004).

Viruses may be transmitted by direct contamination (faecal-oral) or indirect

contamination via contaminated environmental surfaces (Vasickova et al., 2010; Barker et al.,
2004) or more generally via contaminated food or drinkable water (Vega et al., 2005; Koopmans
and Duizer, 2004; Pallansch, 2001) after transport in the environment (surface, waters, soils).
Transmission via air has also been noted (Ziros et al., 2011; Marks et al., 2000; Caul, 1994).
The transmission of enteric viruses present in wastewaters via the environment has been
neglected for a long time with regard to their direct transmission (faecal-oral), and with regard to
other pathogen transmission (bacteria and parasites like protozoa and helminths) for which
detection/enumeration methods exist since more time (Koopmans and Duizer, 2004). With the
recent development of detection methods based on molecular biology that are very sensitive
and that may be applied on environmental samples, the environmenntal transmission of human
viruses has become an emerging problematic (Rodríguez‐Lázaro et al., 2012; Cliver, 2010;
Carducci et al., 2009; Costafreda et al., 2006; Widdowson et al., 2005; Brooks et al., 2005;
Fong and Lipp, 2005; Bhattacharya et al., 2004; Koopmans and Duizer, 2004; Metcalf et al.,
1995) and human viruses are more and more often incriminated in human outbreaks
(Koopmans and Duizer, 2004; Gerba, 1999).

Human enteric viruses are not efficiently removed by conventional filtration and they
are more resistant to disinfectants than bacteria (CFPTEP, 2010a; CFPTEP, 2010b;
Aronino et al., 2009; Petrinca et al., 2009; Da Silva et al., 2008; Koopmans and Duizer, 2004),
although some studies have shown the high efficiency of some treatments – e.g. the removal of
Norovirus with differences in the decrease of GI and GII Norovirus groups (Da Silva et al.,
2007), and the nearly complete removal of viruses by the treatment train in the Upper Occoquan
Sewage Authority Water Reclamation Plant that protect the Occoquan Reservoir (Rose et al.,
2001) –. Viruses are detected in raw wastewaters as well as in treated wastewaters at the exit
of wastewater treatment plants – e.g. for 5 wastewater treatment plants around Rome (La Rosa
et al., 2010), for 2 wastewater treatment plants in the southwest of the Netherlands (Van den
Berg et al., 2005), for the wastewater treatment plant of Leipzig (Pusch et al., 2005), for Rio de
Janeiro in Brazil (Villar et al., 2007), and for Oslo area and elsewhere in Norway (Myrmel et al.,
2006) –. This may partly explain why they are also found in conventional surface waters and
groundwaters. Because of their small size (0.02-0.1 µm) and ease of transport in the
subsurface, viruses are of primary concern in groundwaters (Reynolds et al., 2008).

Supplied during irrigation by wastewaters, human enteric viruses may be dispersed

in the atmosphere as bioaerosols, or transported within the soil towards the aquifers
(Zhuang and Jin, 2008; Reynolds et al., 2008; Gerba, 1999) and other environmental
reservoirs (surface water bodies, roots of plants …). The hepatitis A virus and the Norovirus
may be absorbed and internalised in the roots of onions and lettuce and are thereafter
recovered in their bulb and leaves, respectively (Wei et al., 2011; Urbanucci et al., 2009; Wei et
al., 2009; Chancellor et al., 2006). In the soil, virus fate depends on their transport, their
adsorption on solids (Da Silva et al., 2011; Syngouna and Chrysikopoulos, 2010; Zhuang and

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Jin, 2008; Guan et al., 2003; Dowd et al., 1998; Vilker et al., 1983; Moore et al., 1981; Taylor et
al., 1981), and their inactivation (i.e. either their disappearance or the loss of their infection
potential) (Murray and Laband, 1979). Transport, immobilisation/mobilisation and inactivation
depend on each other: virus may be transferred either free or adsorbed on a colloid (Syngouna
and Chrysikopoulos, 2010; Zhuang and Jin, 2008), and virus inactivation may be slowed
(Schaub and Sagik, 1975; Gerba, 1999) or accelerated by their adsorption on some minerals,
especially on metal oxides (Zhuang and Jin, 2008; Murray and Laband, 1979).

We group here the too rare works that have dealt with the fate of human enteric
viruses in the Environment with those that used bacteriophages as models, although there
are differences between the behaviours of bacteriophages and human enteric viruses of the
Enterovirus genus, as well as between viruses within the Enterovirus genus (Coxsachievirus,
Enterovirus, Poliovirus and Echovirus) (Goyal and Gerba, 1979; Gerba et al., 1981).
Several studies have dealt with the adsorption of viruses on solids. Although a few ones
have focused on real soils (Bradley et al., 2011; Taylor et al., 1981; Moore et al., 1981), the
majority have considered pure materials as models of solid behaviour: metal oxides
(Zhuang and Jin, 2008; Buining et al., 1994; Murray and Laband, 1979), clays such as kaolinite
and montmorillonite (Syngouna and Chrysikopoulos, 2010; Lipson and Stotzky, 1983; Vilker et
al., 1983; Taylor et al., 1981), silica (Taylor et al., 1981; Murray and Laband, 1979) and
organic compounds (Zhuang and Jin, 2003). To our knowledge, the effect of the soil structure
has not been studied. Viruses that were used were bacteriophages (MS2, X174, PRD1 …)
differing from each other by their dimension (Dowd et al., 1998), their isoelectric point (Michen
and Graule, 2010), their wettability (Dowd et al., 1998) and residues of amino-acids on the
surface of the capsid (Syngouna and Chrysikopoulos, 2010). A few actual human pathogens
have been used: the Poliovirus (Taylor et al., 1981; Moore et al., 1981; Murray and Laband,
1979) and other viruses also belonging to the Enterovirus genus (Enterovirus, Coxsachievirus,
Echovirus) (Gerba, 1999), the possibility to cultivate them in vitro permitting to assess their
infectious behaviour. Some alternatives to the use of human pathogen viruses have emerged.
On the one hand, animal viruses have been used as surrogates of human viruses: the murine
Mengovirus as a surrogate of the hepatitis A virus (Costafreda et al., 2006), the feline Calicivirus
as a surrogate of the human Norovirus (Park et al., 2011; Bae and Schwab, 2008), and more
recently, the murine Norovirus as another surrogate of the human Norovirus (Park et al., 2011;
Hewitt et al., 2009; Bae and Schwab, 2008). On the other hand, virus-like particles (VLP) quite
similar to actual viruses may be constructed for some viruses by synthetizing in vitro the
capsidal recombinant proteins issued from the same virus that self-assemble: this is the case
for the Norovirus (Da Silva et al., 2011; Goodridge et al., 2004) and the Rotavirus, although the
actual structure of Rotavirus capside is more complex and is not perfectly reproduced by virus-
like particles (Charpilienne et al., 2001). Temperature effects have been studied only a little,
whereas these effects indirectly inform on the hydrophilic/hydrophobic forces involved in
adsorption (Syngouna and Chrysikopoulos, 2010) and climate affects Norovirus epidemiology
(Lopman et al., 2009). Studies on virus immobilisation have often focused on equilibrium
reached after periods of about 1 hour (Moore et al., 1981) or some days (Syngouna and
Chrysikopoulos, 2010), but recent works define the attachment efficiency as the actual to
maximal absorption (in non-limiting conditions) rate ratio (Da Silva et al., 2011). Only a few

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studies have dealt with the reversibility of the immobilisation (Zhuang and Jin, 2008; Loveland
and al., 1996; Murray and Laband, 1979). Murray and Laband (1979) followed the
remobilisation of intact (infectious) Poliovirus, the proteins that are constitutive of their capsid
being labelled with 14C and their RNA being labelled with 3H; they assessed the implication of
the physicochemical denaturation on virus inactivation. Some mathematical models have been
proposed, including models that account for spatial heterogeneities in advection-convection,
geochemistry and inactivation in solution and at solid surface (Tufenkji, 2007; Bhattacharjee et
al., 2002; Schijven and Hassanizadeh, 2000). And some studies compared experimental data
and model simulations, but model hypotheses could be criticised (Zhuang and Jin, 2008; Guan
et al., 2003; Chu et al., 2001). Empirical models also exist for virus inactivation in other matrix
and extreme conditions with regard to soil classical ones, like hepatitis A virus in acidified
berries (Deboosere et al., 2010) and hepatitis A virus and Norovirus on inert solid surfaces (Kim
et al., 2012).

Virus immobilisation depends (i) on the virus itself (Syngouna and Chrysikopoulos, 2010;
Michen and Graule, 2010; Zhuang and Jin, 2008; Goodridge et al., 2004; Guan et al., 2003;
Dowd et al., 1998; Gerba et al., 1981; Goyal and Gerba, 1979; Chlumecka et al., 1977), the viral
strain for the Norovirus (Da Silva et al., 2011) or a change in the virus conformation under
certain circumstances for the Poliovirus (Taylor et al., 1981), (ii) on soil solid nature (Bradley et
al., 2011; Zhuang and Jin, 2008; Zhuang and Jin, 2003; Moore et al., 1981; Murray and Laband,
1979), and (iii) on the soil solution properties (pH, ionic strength, mineral ions, organic
compounds) (Da Silva et al., 2011; Cao et al., 2010; Zhuang and Jin, 2003; Dowd et al., 1998;
Taylor et al., 1981). Forces involved in virus adsorption are of various natures. They include
electrical forces (Schaldach et al., 2006), the virus and soil inert particles charges varying with
the pH and the ionic composition of the solution (Cao et al., 2010; Van Voorthuizen et al., 2001;
Sposito, 1998; Chorover and Sposito, 1995; Gerba et al., 1981); they are attractive when the pH
is between the isoelectric point of the virus and the isoelectric point of the soil particle (Goyal,
1979), the retention intensity being then often inversely proportional to the pH (Syngouna and
Chrysikopoulos, 2010). The salinity may affect (Cao et al., 2010), and organic compounds may
counter act the effect of an increase of salinity (Cao et al., 2010). A few solids, like Fe oxides,
have high isoelectric points that favour virus adsorption over a larger range of pH (Syngouna
and Chrysikopoulos, 2010). However, adsorption may also exist if electric repulsion is reduced
by the presence of divalent cations (Ca2+, Mg2+) (Da Silva et al., 2011) or an increase in the
ionic strength of the solution (Sposito, 1998), and/or when other forces counterbalance this
repulsion: van der Waals forces (Chattopadhyay and Puls, 2000), hydrophilic/hydrophobic
attractions (Van Voorthuizen et al., 2001) …. Some anions also affect virus immobilisation: Cl-
seems to be the most favourable to virus immobilisation, HPO42- and HCO3- may favour or
disfavour virus immobilization depending on the virus itself and the physicochemical conditions
(Da Silva et al., 2011). Forces involved in colloid adsorption may also include
hydrophobic/hydrophilic forces (Crist et al., 2005). DLVO theory (Derjaguin, Landau, Verwey et
Overbeek) describe some of these forces but ignore other forces that may be sometimes more
important (Attinti et al., 2010; Syngouna and Chrysikopoulos, 2010) and ignore the physical
retention of the larger viruses (Dowd et al., 1998) and of viral aggregates in conditions favouring
virus aggregation (Da Silva et al., 2011). The inability of the DLVO theory (Hermansson, 1999)

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to model the retention of some bacteria suggests that processes are ignored, including clogging
of the pores and retention by particle roughness (Jacobs et al., 2007). Virus adsorption at the
air-water interface may be taken into account in unsaturated systems (Chu et al., 2001), as also
noted for bacteria (Schäfer et al., 1998).

Only a few works have dealt with virus inactivation in soils (Zhao et al., 2008) and few
is known on their survival and inactivation (Rzeżutka and Cook, 2004; Gerba, 1999). Virus
adsorption on solids can slow (Schaub and Sagik, 1975; Gerba, 1999), or accelerate virus
inactivation. Virus inactivation at the surface of metal oxides can be fast (Zhuang and Jin,
2008; Murray and Laband, 1979); it may be accelerated by factors favouring indirectly virus
adsorption, including a decrease of soil moisture and soil sterilization (Zhao et al., 2008), a
decrease in soil solution pH (Zhuang and Jin, 2008) and a decrease in other compounds that
may be adsorbed at the surface of oxides (e.g. phosphates (Zhuang and Jin, 2008)); by
contrasts, compounds may may favor specifc attachments and inhance virus inactivation (e.g.
carbonate (Zhuang and Jin, 2008)). Virus inactivation has been studied in other matrix and in
extreme conditions with regard to those prevailing in soils, including the inactivation of hepatitis
A virus in acidified berries at high temperatures (Deboosere et al. 2010), and more generally
virus inactivation in foods by traditional and novel technologies (Hirneisen et al., 2010). Various
processes may explain viral inactivation: viral RNA or DNA damage (with or without preliminary
release of viral RNA or DNA from the capside; virus antigen damage, separation between viral
DNA or RNA and the capsid; in special laboratory contexts Poliovirus RNA separated from the
capsid may still infect host cells (Nuanualsuwan and Cliver, 2003).

By contrast, nearly nothing is known on virus fate in the atmosphere. Studies on

atmospheric fluxes of biocolloids have begun only recently and enumerating the specific content
in bacteria and viruses remain difficult (Georgakopoulos et al., 2009; Georgakopoulos et al.,
2008; Verreault et al., 2008). Some studies deal with airborne transmission of viruses in hospital
(Caul, 1994), and in the vicinity of wastewater treatment plants (Ziros et al., 2011). Several
factors affecting survival and mobility are known or greatly suspected: (i) the relative humidity
and temperature (Kim et al., 2012; Donaldson, 1972; Akers and Hatch, 1968; De Jong and
Winkler, 1968; Akers et al., 1966), (ii) sunlight or UV radiations (Park et al., 2011; Simonet and
Gantzer, 2006b; Thurston-Enriquez et al., 2003; Sinton et al., 2002; Fujioka and Yoneyama,
2002), and (iii) oxidants (ozone (Tseng and Li, 2006), free radicals OH …). Inactivation by solar
UV radiation of bacteriophage and polioviruses in marine water reported by Fong and Lipp
(2005), and inactivation of adenovirus, coliphage MS-2, and feline calicivirus in buffered
demand-free (BDF) water and groundwater (Thurston-Enriquez et al., 2003); however, they
noticed that viruses are more resilient than many other pathogens to UV radiations and that
viruses with double-strand DNA or RNA are extremely stable when exposed to UV because
their undamaged DNA or RNA strand may serve as a template for repair by host enzymes
(Thurston-Enriquez et al., 2003; Gerba et al., 2002).

Difficulties in virus detection and enumeration result first from their low infectious
doses (101-102 viruses) (Morin and Picoche, 2008; Hollinger and Emerson, 2007; Green, 2007),
and the very low tolerable concentration threshold – e.g. 5 10-3 Rotavirus/L to insure less

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than 10-6 Disability Adjusted Life Years (DALY) per person per year (pppy) (WHO, 2006) –.
Additional difficulties result from the extraction of viruses from solid matrix (soil, food …)
that are always partial, and the enumeration of infectious viruses that remains impossible
for viruses not yet culturable – e.g. Norovirus –. The overall method to extract and detect
viruses could be divided into three different steps: (1) virus elution and clarification from
substrates, (2) virus concentration (Hamza et al., 2009; Croci et al., 2008; Liu et al., 2007; Villar
et al., 2006; Dubois et al., 2006; Katayama et al., 2002; Jothikumar et al. 1995; Tsai et al.,
1993), and (3) virus enumeration. For each of these steps various methods exist. Virus
enumeration has greatly evolved during the last decades with molecular biology (PCR, RT-
PCR, quantitative RT-PCR …) (Mattison and Bidawid, 2009; Villar et al., 2007; Da Silva et al.,
2007; Costafreda et al. 2006; Brooks et al., 2005; Bhattacharya et al., 2004; Metcalf et al.,
1995). In the environment, virus enumeration depends simultaneously on their elution and
extraction from solids and their subsequent concentration which may lead to simultaneously
concentrate PCR inhibitors in some methods (Hamza et al., 2009; Croci et al., 2008; Dubois et
al. 2006). Cultivation methods are fastidious, and require the availability of target cells, fast
enough virus replication and observable cytopathic effects. As it is difficult to estimate the
proportion of viruses that remain infectious (Nuanualsuwan and Cliver, 2002), some PCR
methods have been proposed to discriminate between infectious and non-infectious viruses
(Bhattacharya et al., 2004; Nuanualsuwan and Cliver, 2002). However, it depend on the mode
of inactivation of viruses and their effect on viral RNA or DNA (Simonet and Gantzer, 2006a).
Other methods of detection and enumeration exist like immunochromatographic assays for the
detection of human Rotavirus (Bon et al., 2006), Characterization and purification of viruses
using chromatofocusing applied on bacteriophages (Brorson et al., 2008).

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Appendix 2: Organic contaminants in wastewaters

By Enrique Barriuso and Sabine Houot

INRA-AgroParisTech UMR Environnement et Grandes Cultures, 78850 Thiverval-Grignon,
France

Introduction: main sources of organic contaminants in wastewaters

Organic contaminants (OC) in wastewaters come from several sources. We mainly

focus on OC in domestic wastewaters, although wastewater treatment plants (WWTP) often
receive a mixture of domestic and industrial waters, as well as runoff waters during rainy events.
As a consequence of the diversity and complexity of OC, there is an abundant literature but only
a few general papers, while others deal with case studies that are difficult to generalize since
they depend on the experimental conditions and treatment trains in WWTPs.

Components of personal care products used in large quantities are widely found in
raw wastewaters (bath additives, shampoos, hair tonic, skin care products, hair sprays, soaps,
sun screens, perfumes, aftershaves …). Other compounds issued from personal care products
and found in sewage include parabens (alkyl-p-hydroxybenzoates) that are among the most
widely used antimicrobial preservative (for cosmetics, toiletries, pharmaceuticals and even
foodstuffs), the triclosan (a chlorinated diphenyl ether) used as antiseptic agent and
preservative (for toothpaste, footwear, handsoap, acne creams …), the byphenylol and the
chlorophene also used as preservatives and disinfectants. Pharmaceutical products most
commonly detected in the treated effluents worldwide include antibiotics, lipid regulator agents,
anti-inflammatory drugs, ß-blockers, cancer therapeutics, contraceptives and other hormones
(Hernando et al., 2006; Nikolaou et al., 2007). Some pharmaceuticals and personal care
products are very persistent in the environment (e.g. blood lipid regulators such as clofibric acid,
X-ray contrast media and musks). Phthalates are other ubiquitous OC in the environment.
They have been used for 50 years and 3 million tons are produced per year around the world.
They are present in many products, for examples in plastics (e.g. PVC) as plasticizers to make
them flexible and improve both impact and cold resistances, and in cosmetics as fixative agents
to increase the penetrating power of a product into the skin or to prevent cracking of nails. The
most used phthalate is DEHP (di-2-ethylhexyl phthalate) especially for fragrances, food
containers, blood bags, catheters or bibbers; it is also the most quantified in wastewater
(Barnabé et al., 2008; Dargnat et al., 2009; Clara et al., 2010). The concentration in wastewater
varied from 10 to 200 µg/L (Fromme et al., 2002; Vogelsang et al., 2006; Gasperi et al., 2008a).
Pesticides are also found in wastewaters. Although the largest amounts are used for
agriculture, they are also used in urban areas to protect infrastructures (buildings, roads,

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streets, railway tracks, gardens …). When used in urban areas, especially on impermeable
surfaces, pesticides may move into sewers during runoff events. Blanchoud et al. (2007)
revealed that 80% to 100% of the diuron applied on impervious surfaces could potentially be
remobilized during a rainfall event. These authors estimated also than the urban and agriculture
wastewaters contribution to the pesticide water pollution was equivalent in Marne watershed.
Others biocids are widely used in urban areas for material protection. Depending on the
existence of combined or separate urban sewer networks for house wastewater and rainwater,
pesticide can directly contaminate or not wastewaters (Gerecke et al., 2002). Gasperi et al.
(2008b) identified the origin of OC and metals into the sewerage system of Paris. Of the 66
elements investigated (based on the list established in European Decision no. 2455/2001/EC),
33 and 40 priority substances could be observed in raw sewage and wet weather effluents,
respectively. Chlorobenzenes and most of the pesticides always remained below the limit of
quantification, while the majority of other OC assessed were identified within the μg/L range
(Gasperi et al., 2008b). Runoff via atmospheric inputs and/or surface leaching was found to
induce a wider range of OC and lead to higher concentrations of certain PAHs (3–4 rings
PAHs), pesticides (diuron and oxadiazon, and to a lesser extent, of diazinon, propiconazole and
terbutryn) and organotin compounds (Gasperi et al., 2008b). PAHs found in wastewater are
indicators of pyrolytic inputs (mainly coming from the use of fuels in house heating and
transport). PAH concentrations reported in the literature for domestic wastewaters ranged
between 0.02 to 0.89 μg/L (Palmquist and Hanaeus, 2005). Other ubiquous persistent organic
pollutants are the PCBs; however, articles concerning their concentrations in wastewater are
the rarest (Miège et al., 2009).

Glassmeyer et al. (2005) tried to regroup statistically OC depending on their occurrence

and detection frequencies. OC with similar use were frequently grouped together. For
example, the pharmaceuticals trimethoprim, sulfamethoxazole, dehydronifedipine,
diphenhydramine, diltiazem, and carbamazepine were all grouped together. Other notable
groupings were (i) faecal sterols, cholesterol, coprostanol, and sitosterol, (ii) caffeine and its
metabolite, and (iii) the musks tonalide and galaxolide. The most unexpected result for
Glassmeyer et al. (2005) was that acetaminophen appeared grouped with the two
microorganisms, Escherichia coli and Enterococci, and not the other pharmaceuticals.
Compounds that are typically only used by humans, such as the pharmaceuticals
carbamazepine and diphenhydramine, and even caffeine, would be potential candidates as
indicators of water of human origin (Chen et al., 2002; Buerge et al., 2003; Clara et al., 2004;
Glassmeyer et al., 2005). It is also the case of sterols, mainly the coprostanol (Glassmeyer et
al., 2005).

Focazio et al. (2008) propose to divide OC detected in wastewater into 16 groups:

steroids, non-prescription drugs, fragrances and flavors, antibiotics, pesticides, other
prescription drugs, fire retardants, plasticizers, insect repellent, detergent metabolites,
disinfectant, cosmetics, polynuclear aromatic hydrocarbons (PAH), solvents,
dyes/resins/fuels and antioxidants. Each group includes various compounds that often
distinguish from each other by very different chemical structures, physico-chemical properties,

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and degradation products issued from the human metabolism or from biological or chemical
degradation into sewers or WWTP.

The academic interest in recent decades for the presence of pharmaceutical residues in
wastewater results in a large number of publications on this subject (Miège et al., 2009). The
molecules studied are the most commonly prescribed antibiotics (ciprofloxacin, doxycyclin,
norfloxacin, trimethoprim and sulfamethoxazole) and analgesics and anti-inflammatory drugs
(diclofenac, ibuprofen, and naproxen) (Miège et al., 2009), the number of studies decreasing for
the phthalates with DEHP and BBP, and finally bisphenol A. Molecules least cited in the
literature are contrast agents, ß-blockers, lipid regulators and finally diuretics (Miège et al.,
2009). We have selected some results in order to point out the main figures on the occurrence
and fate of OC linked to the wastewater, and to assess potential risks related to the irrigation
with wastewater. Concentrations of most OC in urban wastewaters (raw or treated) are
generally below the toxic levels for humans, but potential problems may result from the
combined effects of several pollutants and/or their cumulative consequences over long-
term periods, either directly or indirectly through modifications of ecosystems (e.g. several soil
microorganisms acquiring antibiotic resistance). This last point is not treated here; it would be
probably more pertinent in the case of manure or animal effluent spreading.

Organic contaminants in the environment; link with wastewaters

As wastewaters explain most the environmental dispersion of pharmaceuticals, their

monitoring in the environment can give interesting informations, as highlighted in the review of
Monteiro and Boxall (2010), the monitoring work of Gros et al. (2010) on 73 pharmaceuticals,
and a review on the presence and persistence of pharmaceuticals in the environment, with data
from more than 150 references (Glassmeyer et al., 2008).

Focazio et al. (2008) analysed U.S. surface waters and groundwaters, and detected 63 OC
among 100 listed in at least 1 water sample; they assumed that OC originated from
wastewaters. The maximum number of compounds detected in the same site was 31 and the
median number of compounds detected per site was 4. In surface water, the 5 most
frequently detected OC were cholesterol (59% of positive samples, natural sterol), metolachlor
(53%, herbicide), cotinine (51%, nicotine metabolite), β-sitosterol (37%, natural plant sterol) and
1,7-dimethylxanthine (27%, caffeine metabolite). In groundwater, the 5 most frequently detected
chemicals were tetrachloroethylene (24%, solvent), carbamazepine (20%, pharmaceutical),
bisphenol A (20%, plasticizer), 1,7-dimethylxanthine (16%, caffeine metabolite) and tri(2-
chloroethyl)phosphate (12%, fire retardant). Non-prescription drugs (including caffeine, 1,7-
dimethylxanthine, cotinine, ibuprofen and acetominophen) were detected more frequently than
any other of the 15 groups in surface water; only 3 groups (biogenic steroids, detergent
metabolites, and solvents) had individual chemical maximum concentrations exceeding 2 μg/L,
whereas 7 groups (including antibiotics, non-prescription drugs, and other prescription drugs)
had maximum concentrations lower than 0.5 μg/L.

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Another interesting review by Deblonde et al. (2011) mainly focused on bisphenol A, 6

phthalates and 50 pharmaceuticals (including drugs for human health and disinfectants). The
molecules studied were the most commonly prescribed antibiotics (ciprofloxacin, doxycyclin,
norfloxacin, trimethoprim and sulfamethoxazole), analgesics and anti-inflammatory drugs
(diclofenac, ibuprofen, and naproxen), whereas the least cited molecules are contrast agents, ß-
blockers, lipid regulators and diuretics (Miège et al., 2009). In the review of Deblonde et al.
(2011), the concentrations of OC in the influent of WWTPs ranged from 0.007 to 56.63 μg/L.
Caffeine concentration in influent was the highest among the concentrations of molecules
investigated (average of 56.63 μg/L). The concentrations of ofloxacin were the lowest, and
varied between 0.007 and 2.275 μg/L in the influent treatment plant. Tetracycline, ibuprofen,
contrast products, caffeine, and codeine were found in effluents of WWTPs (Deblonde et al.,
2011), also phthalates are always found (Dargnat et al. (2009) found phthalates concentrations
around 2 μg/L). The metronidazole and norfloxacin were found at concentrations below
0.05 μg/L in the effluent (Clara et al., 2010).

Efficiency of organic pollutant removal in WWTP

Several studies have discussed the removal efficiency of wastewater treatment trains, that
corresponds to the ratio of output-to-input OC concentration (Bolong et al., 2009; Gros et al.,
2010; Fatta-Kassinos et al., 2011a; Jelic et al., 2011; Gao et al., 2012). Removal efficiency
depends on OC themselves, treatment train and seasonal variations in OC concentrations
(Vieno et al., 2005; Takao et al., 2008), as well as climatic conditions that affect for example
water fluxes in the WWTP. Runoff dramatically reduces the OC removal rate: in a period of
increased influent flow, the removal rate dropped to below 5% from over 60% previously
(Ternes, 1998). The variability of removal efficiency can be pointed out also by comparing
published results for the same OC: removal efficiency varies from 17% (Rosal et al., 2010) to
98% (Peng et al., 2006) for sulfamethoxazole, from 12% (Spongberg and Witter, 2008) to 80%
(Karthikeyan and Meyer, 2006) for tetracycline, from 4.3% to 72% (Rosal et al., 2010) for
erythromycin.

Two main mechanisms may be involved in the OC removal: sorption on sludge (or on other
specific sorbents) and biodegradation (Carballa et al., 2004). Sorption on sewage sludge is the
main removal process for hydrophobic OC having high sorption capacities, e.g. for several
pharmaceuticals: fluoroquinolones (Golet et al., 2003) and tetracyclines (Kim et al., 2005). By
contrast, sorption is negligible for most polar pharmaceuticals, the main possible removal
process being then biodegradation, e.g. for acetaminophen, caffeine, salbutamol and salicylic
acid whose degradation efficiency can exceed 90% in WWTP (Gomez et al., 2007; Jones et al.,
2007). Others pharmaceuticals are hardly removed as gemfibrozil and fenofibric (Bendz et al.,
2005), the ß-blockers acebutolol and sotalol (Vieno et al., 2006), the fluoroquinolones
ciprofloxacin and norfloxacin (Lindberg et al., 2006; Vieno et al., 2006), and the iodinated X-ray
contrast media iomeprol and iopromide (Ternes et al., 2007). Very low removals (<40%) were
also reported for carbamazepine, diatrizoate, iopamidol and roxithromycin (Bendz et al., 2005;
Bernhard et al., 2006; Vieno et al., 2006; Ternes et al., 2007). Radjenovic et al. (2009) found

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also that antiepileptic carbamazepine and diuretic hydrochlorothiazide are recalcitrant to

biodegradation in the WWTP. The low degradation (<30%) of carbamazepine in WWTP was
confirmed by Miao et al. (2005). Lincomycin was also another pharmaceutical little degraded
(17%) (Karthikeyan and Meyer, 2006). Deblonde et al. (2011) found removal rates ranging from
0% (contrast media) to 97% for caffeine (psycho-stimulant) that may be considered as an
indicator of human origin, whose concentration in influent is often the highest among the OC
investigated.

Additional tertiary treatments may allow improving OC removal efficiency. Yang et al.
(2011) followed the concentration of 19 pharmaceutically active compounds and personal care
products in primary effluent (i.e. after pre-treatment) and after each step of the following tertiary
treatment train: membrane filtration – adsorption on granular activated carbon - ozone oxidation.
Caffeine and acetaminophen were found at the highest concentrations in the primary effluent
(∼105 ng/L), followed by ibuprofen (∼104 ng/L), sulfamethoxazole and a DEET (∼103 ng/L), and
other compounds (concentrations on the order of several hundred of ng/L). After activated
sludge treatment and membrane filtration, the concentrations of caffeine, acetaminophen,
ibuprofen, phthalate, tetracycline, and 17α-ethynylestradiol had decreased by more than 90%.
Erythromycin and carbamazepine, which were resistant to biological treatment, were eliminated
by 74 and 88%, on average, by adsorption on granular activated carbon. Ozonation may oxidize
most of the remaining compounds by >60%, except primidone and phthalate. Of the initial 16
compounds detected in the primary effluent, only sulfamethoxazole, primidone, caffeine and
DEET were frequently detected in the final effluent, but at concentrations about 10–100 ng/L.
The incomplete removal in the sewage treatment plants can be related to the low concentration
of each compound, possibly not enough in relation to the catabolic enzyme affinities of sewage
microbiota (Daughton and Ternes, 1999). Thus, reduction of concentration by dilution with fresh
water can reduce the efficacy of biological treatment, suggesting treating specific pollutions at
the source, rather than in WWTP collecting all wastewaters (Joss et al., 2006). Unfortunately,
some OC have a chemical structure resisting to conventional wastewater treatments (phenols,
chlorinated hydrocarbons, some pesticides …).

Among the personal care products, fragrances (musks) are ubiquitous contaminants,
persistent and bioaccumulative, that are sometimes highly toxics (amino musk transformation
products are toxicologically significant) (Daughton and Ternes, 1999). Musks are refractory to
biodegradation that explains why there are difficult to remove in the wastewater treatment
plants. Because synthetic musks are ubiquitous, used in large quantities, introduced into the
environment almost exclusively via treated sewage effluent, and are persistent and
bioconcentrated, they are indicators for the presence of other personal care products (Rimkus
et al., 1997; Gatermann et al., 1998; Daughton and Ternes, 1999).

A general problem concerns the elimination of polar OC as acidic pharmaceuticals, but

also other acidic compounds like some pesticides and benzotriazoles which belong to the list
of high production volume chemicals. Benzotriazoles are largely used as corrosion inhibitors
in many industrial applications, but also in households (dishwashing agents); their elimination
efficiency in WWTP ranged between 20 to 70% (Weiss et al., 2006) and they are regularly

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discharged with municipal wastewater (Reemtsma et al., 2010). Among pesticides, azoles used
as fungicides are often found in the wastewater, with a limited efficiency of the WWTP (between
30 and 65% of elimination) (Stamatis et al., 2010). The dilution may be the only mechanism
to reduce the concentration of some polar OC that are neither biodegradable nor retained
by any of the natural or technical barriers in the WWTP. A typical and well documented
example of such a compound is ethylenediaminotetraacetate (EDTA), a chelating agent used in
industrial processes as well as in consumer products. EDTA is not biodegradable under
environmental conditions and may only be destructed by photolysis of its iron-complex in a
natural environment. The effluents of 8 municipal WWTP in Western Europe were analysed
over 10 months by liquid-chromatography−mass spectrometry for the occurrence of 36 polar
pollutants, including household and industrial chemicals, pharmaceuticals, and personal care
products. In a long-term study of the effluents of three WWTP. Reemtsma et al. (2006) showed
that polar OC, sulfophenylcarboxylates and EDTA were detected above 10 μg/L on average,
while benzotriazoles, benzothiazole-2-sulfonate, diclofenac, and carbamazepine showed mean
concentrations of 1−10 μg/L, followed by some fire retardants, naphthalene disulfonates, and
personal care products in the range of 0.1−1 μg/L. Half of the determined polar OC were not
significantly removed in tertiary wastewater treatment (Reemtsma et al., 2006).

For some OC, the practices linked to the treatment of wastewater are the main sources of
these OC in the environment, especially for some chlorinated compound produced during
chlorine disinfection.

The degradability of a given OC can be described by laboratory experiments allowing the

calculation of the rate constants of degradation (kbio) considering that kinetic of pseudo first
order. Using this approach, Joss et al. (2006) proposed the identification of three groups of OC
according to their degradation constant: compounds with k bio<0.1 L.g-1.d−1 are not removed to a
significant extent (<20%), compounds with kbio>10 L.g-1.d−1 are greatly transformed (>90%) and
in-between moderate removal is expected. Briefly, only 4 targets compounds (ibuprofen,
paracetamol, 17ß-estradiol and estrone) of the 35 compounds studied are degraded by more
than 90%, while 17 compounds (including macrolides and sulfonamides) were removed by less
than 50% during biological wastewater treatment (Joss et al., 2006).

Organic pollutant fate in the environment after wastewat er

spreading

Several studies investigated the occurrence and distribution of pharmaceuticals in soil

irrigated with reclaimed water (Kinney et al., 2006; Ternes et al., 2007; Gielen et al., 2009).

Sorption on soils is an important process conditioning the OC fate in soils, as it

regulates leaching. Because of the large spectra of molecular properties, sorption properties
may greatly vary between compounds of a group of OC: e.g. the compilation of antibiotics
sorption coefficients (Kd) showed that they vary between 0.2 and 6000 L/kg, which correspond

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to very mobile and immobile compounds, respectively. In general, sulfonamide antibiotics and
organophosphate biocides are mobile in the environment, whereas tetracycline, macrolide
and fluoroquinolone antibiotics exhibit low mobility (Boxall, 2008). In a study by Chefetz et
al. (2008), the sorption-desorption behaviour and the mobility of carbamazepine, naproxen and
diclofenac were studied in soil layers sampled from a plot irrigated with both freshwater and
wastewater. Carbamazepine and diclofenac were significantly retarded in the 0-5 cm soil layer
rich in soil organic matter (OM). Carbamazepine was not affected by the water type, whereas
diclofenac exhibited a higher retardation factor in the freshwater leaching system. Naproxen
exhibited significantly lower retardation factors than diclofenac but with a similar trend. In the 5-
15 cm soil sample containing low OM, naproxen was highly mobile while carbamazepine and
diclofenac were still retarded. In the 15-25 cm sample, all compounds exhibited their lowest
retardation factors. Sorption data suggested that OM governs the studied OC interactions with
the soil samples. Both the quantity and the physicochemical nature of soil OM affect
sorption interactions (Chefetz et al., 2008). This study suggests that carbamazepine and
diclofenac can be classified as slow mobile compounds in OM-rich soil layers. When these
compounds pass this layer and/or are introduced into OM-poor soils, their mobility increases
significantly. This emphasizes the potential transport of pharmaceuticals to groundwater due to
intensive irrigation with reclaimed wastewater in OM-poor soils (Chefetz et al., 2008).

OC degradation in soil is another important process conditioning the capacity of

soils to eliminate OC. However, persistent, non-degradable OC can be accumulated in soils,
as for example phthalate esters which have accumulated in agricultural soils irrigated by
wastewater in China (Zeng et al., 2008): phthalates were detected in all soil samples with the
concentrations ranging from 0.195 to 33.6 μg/g and mainly originate from wastewater irrigation
and sewage sludge application. Excessive accumulation of such compounds in agricultural soils
may not only result in environmental contamination, but leads also to elevated phthalates
uptake by crops, which may affect food quality. Other results found that most antibiotics are
not biodegradable under aerobic conditions (Thiele-Bruhn, 2003; Alexy et al., 2004; Gartiser
et al., 2007). Photolysis can be an additional degradation process depending on the
modalities of wastewater irrigation. Some pharmaceuticals are particularly sensitive to the
photolysis as this is the case of tetracyclines, fluoroquinolones, sulphanilic acid, tylosin,
nitrofuran antibiotics … (Kümmerer, 2009). But most of the works on photodegradation have
been performed in water: photochemical decomposition could play an important role in surface
water as an additional elimination pathway or for effluent treatment (Viola et al., 2004; Edhlund
et al., 2006; Hu and Coats, 2007), but the extrapolation to potential photodegradation at the soil
surface must be done carefully.

Risk due to the organic contaminants in irrigation wastewaters

Contamination of conventional water resources

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Although soil contamination by persistent OC is the first risk to be considered, the OC

accumulated in soils can be transported by leaching and runoff from soil surface into the
groundwater and surface waters after rainfall events (Pedersen et al., 2005; Topp et al.
2008), all the more that the use of sewage sludge as organic amendment or fertilizer in
agricultural fields (Oppel et al., 2004) may be another source of pollution.

However soil acts as a reactor allowing degradation and retardation to leaching of

OC. Little data are available on the persistence and effects in the environment. Although the
continuous introduction of OC into the environment through continuous irrigation or other types
of discharge practices can make them 'pseudo-persistent' (Fatta-Kassino et al., 2011b),
analyses have shown that most organic compounds are rapidly decomposed is soils after
irrigation (Focazio et al., 2008; Duran-Alvarez et al., 2009). Durand-Alvarez et al. (2009)
showed that despite the continuous application of contaminants with wastewater over many
years, the concentrations of acidic pharmaceuticals and endocrine disrupting compounds were
generally lower than those expected considering the input amounts by a single irrigation event.
Only carbamazepine showed evidence of persistence in the soils (Fatta-Kassinos et al.,
2011b). Kinney et al. (2006) found that measurable but low concentrations of pharmaceuticals
can be detected in soil irrigated with reclaimed wastewater. The residues of polycyclic aromatic
hydrocarbons, polychlorinated biphenyls, chlorinated benzenes and phenols were investigated
in soil in a study undertaken by Al Nasir and Batarseh (2008) in a field irrigated with wastewater;
the concentration levels of all targeted compounds (like naphthalene, acenaphthylene,
acenapthene, fluorine, phnanthrene, anthracene, pyrene, chrysene, o-cresol, p-cresol, 2,4-
dimethylphenol, 2,6-dichlorophenol, 2,3,5-trichlorophenol, 2,3,4,6-tetrachlorophenol, etc.) found
in soil irrigated with wastewater were much higher than for the reference site, indicating a
source of contamination due to irrigation with wastewater. The depuration role of soil through
filtration has been evidenced by Xu et al. (2009). These authors showed that after 4 months of
turf field irrigation with reclaimed municipal wastewater, no OC was detected in the leachate
draining through the 89-cm profile. Ibuprofen, naproxen, triclosan, bisphenol A, clofibric acid,
and estrone were detected in the surface to 30-cm soil profiles. The screenings of pollution risk
identified the same 6 compounds as having the potential to contaminate groundwater, and
under conditions of turf grass irrigation, clofibric acid and ibuprofen would be most prone to
cause the pollution. An interesting lysimetric study was done by Ternes et al. (2007). Lysimeters
located in an irrigated agricultural field irrigated with wastewater effluents were monitored with
regard to the occurrence of 52 pharmaceuticals and 2 personal care products. No differences in
pollution of the groundwater were found for soils with and without addition of digested sludge.
Most of the selected OC were never detected in any of the lysimeter, although they were
present in the treated wastewater used for irrigation. However, some OC were detected up to
several μg/L (diatrizoate and iopamidol, the antiepileptic carbamazepine and the antibiotic
sulfamethoxazole) while the acidic pharmaceuticals, musk fragrances, oestrogens and ß-
blockers were likely sorbed or transformed while passing the top soil layer. Anionic species of
pharmaceuticals are mobile in the soils, showed little elimination, and led to risks of
groundwater contamination, whereas most cationic or neutral compounds are efficiently
retained on the soils (Siemens et al., 2008). Scheytt et al. (2007) confirmed that clofibric acid
is a compound highly mobile and persistent. Other pharmaceutical detected after wastewater

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irrigation in the unsaturated zone were primidone and propyphenazone. In the column
experiment in the lab no transformation and no retardation was found for clofibric acid, whereas
diclefenac was degraded (79% of initial amount), and only 37% and 17% of degradation was
found for ibuprofen and propyphenazone, respectively (Scheytt et al., 2007). Siemens et al.
(2008) showed that pharmaceuticals found at high concentrations in the wastewater (>1 µg/L)
had little elimination during soil passage pointing risk of groundwater contamination with
naproxen, ibuprofen and diclofenac as a consequence of wastewater irrigation. In a monitoring
study using wells close to a field irrigated with wastewater. Katz et al. (2009) noted low
concentrations of carbamazepine in water indicating the persistence of this compound in the
subsurface. Avisar et al. (2009) questioned the wastewater reuse practice for irrigation, because
they point out the contamination of the aquifer under land irrigated with treated wastewater
effluents for about 5 decades, they found out that concentrations of the OC in the groundwater
were found to be up to 20 ng/L.

In addition to leaching, runoff is another transfer process resulting into a risk of

surface water contamination. Topp et al. (2008) studied the runoff of pharmaceuticals and
personal care products following application of sewage sludge to an agricultural field. Ibuprofen
and acetaminophen concentrations in the runoff first decreased and then increased, suggesting
that these OC were initially chemically or physically sequestered in the sewage sludge and
subsequently released in the soil. Carbamazepine and triclosan were detected at low
concentrations in a runoff event 266 d after sewage sludge application.

Uptake from soils and plants contamination by organic pollutants

Organic contaminants remaining in surface soils may be uptaken by plants. Very limited
information is available in the literature. Previous research focused primarily on plant uptake of
veterinary pharmaceuticals that are associated with animal wastes and demonstrated their
potential to accumulate in plants, and some data are available on uptake of antibiotics from soil
amended with manure containing antibiotics by carrot roots, lettuce leaves (Boxall et al., 2006)
and corn (Kumar et al., 2005). The highest uptakes of sulfamethazine were found in corn and
lettuce, followed by potato (Dolliver et al., 2007). The low concentration levels into the vegetal
tissues allow deducing a very low health risk. The OC residues, which are reversibly adsorbed
to soil, may be taken up by plants. In a greenhouse experiment, corn took up lasalocid and
monensin. In laboratory experiments, it has been demonstrated the uptake of sulfadimethoxin in
sorghum, pea and corn, and this uptake had an influence on their development (Schneider,
2008). Hydroponic culture plants, incorporated sulfanamide up to a final concentration of 180 to
2000 mg/kg. Roots of corn and sorghum accumulated much more active ingredients than the
shoots. Similar results were obtained for rye, carrot, corn, sorghum and pea in field trials.
Enrofloxacin was also accumulated in μg/g amounts (Schneider, 2008). In the case of a
negative effect on plants as showed by Schneider (2008), it is not clear whether the effect
resulted from the direct damage of the plant by OC or antibiotics effects on soil microorganisms
was responsible for the damage by affecting the plant-microorganism symbiosis (Chander et al.,
2005). The decay in the number of soil bacteria leads to a lack of feed for soil fauna (protozoa,

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nematodes, micro-arthropods) and finally influences soil functions: plant residues are
decomposed slower, denitrification is slower, and therefore nutrients are recycled more slowly
(Migliore et al., 1998). Al Nasir and Batarseh (2008) noted that different plants showed different
uptakes of various OC from a soil irrigated with wastewater. Roots were the most contaminated
part of the plant, while fruits were the least contaminated. The uptake ratios are dependent on
the plant type and the physicochemical properties of organic compounds. In a greenhouse
experiment, Wu et al. (2010) studied the uptake of three pharmaceuticals (carbamazepine,
diphenhydramine, and fluoxetine) and two personal care products (triclosan and triclocarban) by
soybean. Carbamazepine, triclosan, and triclocarban were found concentrated in root tissues
and translocated into above ground parts including beans, whereas accumulation and
translocation for diphenhydramine and fluoxetine was limited. OC introduced by irrigation
appeared to be more available for uptake and translocation than those introduced by
sewage sludge. The uptake from soil to root and translocation from root to leaf may be rate
limited for triclosan and triclocarban and metabolism may occur within the plant for
carbamazepine.

Ecotoxic effect of organic contaminants

Direct ecotoxic effects of OC present in wastewater used for irrigation are not treated in the
literature. Ecotoxicology papers are focused on effects of wastewater on aquatic media. The
reasons are that effluents of WWTP are usually connected to the water resources. As an
example, Gros et al. (2010) showed that susceptibility for pharmaceuticals decreases in the
order algae > daphnia > fish; they concluded that no significant risk could be associated to the
presence of pharmaceuticals in effluents, mainly because of the dilution and low concentrations.
Another example, coupling soil and water compartments is the study of Ternes et al. (2007) that
found that potential estrogenic effects of wastewater disappeared after irrigation, since the most
potent steroid oestrogens were not measurable. Only one paper proposed an original approach
of integrated risk assessment using life cycle impact assessment methods (LCIA) (Muñoz et al.,
2008). This method allows quantifying the potential environmental impacts on ecotoxicity and
human toxicity of wastewater containing priority and emerging pollutants. This methodology was
applied to wastewater influent and effluent samples from a WWTP. Characterization factors
were applied to the average concentration of 98 OC, obtaining impact scores for different
scenarios: discharging wastewater to aquatic recipient, and using it for crop irrigation. The
results show that treated wastewater has a substantially lower environmental impact than the
influent, and that pharmaceuticals and personal care products greatly contribute to toxicity in
this wastewater. Ciprofloxacin, fluoxetine, and nicotine constitute the main personal care
products of concern in this case study, while 2,3,7,8-TCDD, and hexachlorobenzene were the
priority pollutants with highest contribution. When wastewater was released to fresh water
ecosystems, the impact was mainly caused by fluoxetine, triclosan, and ciprofloxacin. Another
scenario considered using wastewater for irrigation and thus releasing it to soil: the impact on
terrestrial ecosystems is in this case mostly due to ciprofloxacin. Finally, the impact on human
health of using wastewater for crop irrigation is mostly due to nicotine and gemfibrozil,

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attributing the impact to nicotine and hexachlorobenzene in the influent, and to 2,3,7,8-TCDD
and hexachlorobenzene in the effluent (Muñoz et al., 2008).

Concluding remarks

Organic contaminants that may be present in raw wastewaters mainly include various
compounds in personal care products, pharmaceuticals, phthalates, as well as some biocides
used for material protection. However when there is a unique urban sewage network that collect
both house wastewaters and runoff waters, they may also contain pesticides and polycyclic
aromatic hydrocarbons (PAH). At least, some organic contaminants (solvents) may be produced
into the WWTP during disinfection by chlorine. A classification has been proposed with the
following 16 groups: steroids, non-prescription drugs, fragrances and flavors, antibiotics,
pesticides, other prescription drugs, fire retardants, plasticizers, insect repellent, detergent
metabolites, disinfectant, cosmetics, polycyclic aromatic hydrocarbons, solvents,
dyes/resins/fuels and antioxidants. Concentrations of most OC in urban wastewaters (raw or
treated) are generally below the toxic levels for humans, but potential problems may result from
the combined effects of several pollutants and/or their cumulative consequences over long-term
periods
The main conclusions concerning the content of pharmaceuticals in wastewaters are:
- Analgesics and anti-flammatories have been widely reported in sewage treatment effluents;
the highest concentrations corresponding to the compounds sold in higher quantities:
ibuprofen, diclofenac, acetaminophen, naproxen …;
- Antiobiotics: macrolides, sulfonamides, tetracycline, fluoroquinolones, chloramphenicol and
trimethoprim have been identified in wastewater, in the inputs of the sewage treatment
plants and in the sewage effluents. The most frequently detected antibiotic in environmental
samples is the metabolite of the macrolide erythromycin (Hirsch et al., 1999). Although
compounds of the penicillin class are used in the highest amounts, they have not generally
been detected in the sewage effluents;
- ß-blockers: metoprolol, propranolol, betaxolol, bisoprolol, carazolol are frequently detected;
- Hormones and steroids: reproductive hormones (estradiol, estrone, hydroxyestrone) and
contraceptive (ethinylestradiol) were generally detected at low concentrations in sewage
effluents;
- Antidepressants: only fluoxetine was detected in sewage effluents;
- Antiepileptics: carbamazepine is the most often used antiepileptic and it and its metabolites
have been frequently detected in sewage effluents at high concentrations.
Dealing with the removal efficiency in wastewater treatment plants and as a general trend of
results in the literature, we can conclude some highlights:
- Psycho-stimulants seem to be easily removed, e.g. about 97% for caffeine (Ternes et al.,
2007);
- The best then removed compounds in WWTP including an activated sludge systems are
phthalates with removal efficiency above 90% (Bendz et al., 2005).
- The removal efficiency is about 71% for bisphenol A and about 50% for antibiotics (Gomez
et al., 2007);

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- Benzotriazoles removal is very variable, ranging between 20 to 70% (Weiss et al., 2006);
- Analgesics, anti-inflammatories and ß-blockers are resistant to treatments (removal
efficiency of 30–40%) (Miège et al., 2009; Deblonde et al., 2011);
- Musks and derivatives are very persistent (Daughton and Ternes, 1999), as EDTA, metal-
complexing agent (Reemtsma et al., 2006);
- Erythromycin and carbamazepine are resistant to biological treatment (Radjenovic et al.,
2009; Yang et al., 2011).

Standards for OC have to be considered in regulations dealing with wastewater reuse for
crop irrigation, the values being established from potential chemical risk assessments. It is
particularly the case for the pharmaceutical products which are secreted after use by humans
and arrive through the sewage system to the wastewater treatment plants (WWTP).

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