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Micro Biology Food Safety

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ASAD ALI

Food safety has emerged as a global challenge, especially affecting developing countries. Major foodborne illnesses in these regions include botulism, shigellosis, campylobacteriosis, E. coli infection, staphylococcus aureus infection, salmonellosis, and listeriosis. These illnesses pose significant threats to human health and economic development. While efforts are being made internationally and locally to address food safety, developing countries continue to face difficulties such as lack of infrastructure, surveillance systems, and resources to curb the high prevalence of foodborne disease.

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1 Introduction Food safety has emerged as a global challenge and most of the developing countries are the victims of the dev- astating perils of foodborne illness. Since, microbes are developing resistance and are able to survive many food production and processing operations thus they pose a potential threat to human health and are regarded as the major sources of foodborne illness. Food safety is well recognized as a primary indicator of economic growth in the developing world therefore, a wave of realization has spurred both at public and government levels for safe food supply.However,the situationstill remains much depress- ing in the developing countries. International organiza- tions are inclined to help developing nations combat food safety issues; hence, numerous NGOs and local consumer groups are teeming in these states to work for food safety. In spite of the recent advancement in the domain of Food Science and Technology and a growing concern raised by various international working groups on food safety, prevalence of foodborne illness still remains a substantial cause of morbidity and preventable death. Developed economies are no exception to the risk of foodborne illness as one-third of the population undergoes this type of illness annually. Moreover, outbreaks in the United States, Australia, Germany, and India are clear indicative of the severity of the problem because30%ofthepopulationinthesecountriessuffered from foodborne illness each year (Tauxe, 1997), and 9.4 million in the United Kingdom (Walker et al., 2003). Similarly, 1200 million cases of diarrheal illness in the US are reported annually involving E. coli, Salmonella spp., Shigella spp., Cyclospora spp., Cryptosporidium spp., Campylobacter jejuni, Clostridium difficile, and other enteric viruses (Guerrant et al., 2001). Prevalence of foodborne illness though not well docu- mented on account of poor monitoring and surveillance REVIEW ARTICLE Microbiological food safety: a dilemma of developing societies Saeed Akhtar1 , Mahfuzur R. Sarker2 , and Ashfaque Hossain3 1 Bahauddin Zakariya University Multan, Department of Food Science and Technology, Multan, Pakistan, 2 Oregon Sate University, Department of Microbiology, Corvallis, Oregon, USA, and 3 University of Hail, College of Health Sciences, Hail, Saudi Arabia Abstract Current food safety issues are deleteriously reshaping the life style of the population in the developing world. Socioeconomic status of the population in poorer economies is one of the major determinants to delineate the availability of safe food to the vulnerable population. Assessment of the prevalence of foodborne illness in developing world is the most neglected area to control disease. Botulism, Shigellosis, Campylobacteriosis, Escherichia coli infection, Staphylococcus aureus infection, Salmonellosis, Listeriosis and Cholerae are extensively prevalent and pose a major threat to human health in underdeveloped communities. The existing food safety status of many African, South Asian, Central, and South American developing countries is distressing therefore; it seems much timely to highlight the areas for the improvement to ensure the supply of safe food to the population in these regions. Extensive literature search at PubMed, Science Direct and Medline was carried out during the current year to catch on relevant data from 1976 to date, using selective terms like food safety, South East Asia, Africa, Central and South America, and foodborne illness etc. Efforts were made to restrict the search to low income countries of these regions with reference to specific foodborne pathogens. This report briefly discusses the present food safety situation in these developing countries and associated consequences as prime issues, suggesting foodborne illness to be the most distressing threat for human health and economic growth. Keywords:  Botulism, Campylobacteriosis, Escherichia coli infection, Staphylococcus aureus infection, Salmonellosis Address for Correspondence: Dr Saeed Akhtar, Bahauddin Zakariya University Multan, Department of Food Science and Technology, Bosan Road, Multan, Pakistan. E-mail: saeedbzu@yahoo.com (Received 25 April 2012; revised 06 October 2012; accepted 17 October 2012) Critical Reviews in Microbiology, 2012; Early Online: 1–13 © 2012 Informa Healthcare USA, Inc. ISSN 1040-841X print/ISSN 1549-7828 online DOI: 10.3109/1040841X.2012.742036 CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
2  S. Akhtar et al. Critical Reviews in Microbiology is recognized as a potential determinant for rapidly declining economic growth in underdeveloped countries. Paucity of literature and statistical data to estimate the economic loss associated with foodborne illness in devel- oping regions is existent and this scarcity of information implies poor surveillance systems that hinder the nations to achieve higher food safety standards. Experience shows that infection control requires plenty of expertise in related fields such as food microbiology, chemistry, and epidemiology etc. Possibly, these skills are available in developing countries but there is no systematic approach available so far to undermine the fast growing incidence of foodborne illness. For example, no significant food- borne illness outbreak has been documented systemati- cally in South Asian or African developing economies so far, though very small epidemiological studies were car- ried out in the past which undeniably could not suffice to estimate the real economic loss. Most of the countries of developing world have no precise foodborne illness mon- itoring and surveillance system to compute economic losses incurred as non-productivity, cost of medication and Disability Adjusted Life Years (DALYs). Extent of mortality among children in developing countries due to diarrhea estimates 1.8 million deaths annually, suggesting a massive economic burden as a result of foodborne illness (WHO, 2005). Economic constraints, political instability, nonexistence of infra- structure and nonadherence with the existing food laws are the significant markers of unsafe food supply. This is further intensified by scantiness of public awareness on health and economic consequences of foodborne illness, illiteracy, poverty, malpractices, and corruption and on top of that legislation that needs to be compatible with the local beliefs and principals in the low income coun- tries. It is particularly important to understand what eco- nomic consequences are ahead if corrective measures are not taken (Henson, 2003). Hardly any developing country would have acquired precise estimates of the burden of foodborne disease because numerous instru- mental reasons deter the correct estimation, for example a majority of the cases especially for diarrheal illness are not reported (Flint et al., 2005). Extensive body of literature confirms number of food- borne disease outbreaks worldwide. Several recent food- borne disease outbreaks are reported in the United States where hygiene and sanitation is much better and the gov- ernmental agencies like local health departments, Center for Disease Control and Prevention (CDC), Federal Regulatory Agencies, Food and Drug Administration (FDA), USDA’s Food Safety and Inspection Service (FSIS), and the Environmental Protection Agency (EPA) are effi- ciently functioning to control foodborne illness. Twenty nine people died in Colorado within a time span of 3 months only i.e. July-September owing to the consump- tion of Del Monte cantaloupe infected with Salmonella spp. (CDC, 2011). FoodborneillnessintheUScausedbyCampylobacter, non-typhi Salmonella spp., E. coli O157, E. coli non-O157 shiga toxin E. coli (STEC) and Listeria mono- cytogenes resulted in a loss of $6.9 billion in terms of medical costs, productivity losses and value of prema- ture deaths in 2000. Correspondingly, an expected loss of $7.2 million is endured for each death of a child dying before the first birthday comparing with one dying at an age of 85 or more (Henson, 2003). These statistics might be virtuously exploited to make a comparison of the economic losses born by the US government with all those services and resources available which practi- cally do not exist in the developing countries of South Asia, Africa, and Central and South America. Therefore, understanding the emerging food safety challenge is rather demanding and requires public health workers and all stakeholders to strive with improved methods to overcome foodborne illness in developing countries (WHO, 2005). Thepresentreviewisanattempttoassimilatefactsand figures with particular emphasis on South Asian, Central and South American and African developing countries to assist governments to develop a food safety roadmap to combat foodborne illness. Bacterial agents and foodborne illness Botulism Four main species of Clostridium produce disease in humans i.e. C. botulinum, C. difficile, C. perfringens, and C. tetani. Foodborne botulism is caused by ingesting minimally processed foods such as canned foods espe- cially prepared at home because heat resistant spores survive in these erroneously handled foods. A potent neurotoxin, found in seven different forms is produced during the growth of C. botulinum resulting in severe neuroparalytic syndrome (Arnon et al., 2001; Skarin et al., 2011). Paralysis begins with blocking motor nerve terminals at the myoneural junction and the resulting conditions lead to death. Nevertheless, the illness is rare and uncommon because the organism thrives in specific conditions of temperature, oxygen, acidity, and water activity. These conditions generally do not exist simul- taneously in a food system to favor the bacterial growth but usually involve health risks with higher mortality rate (Cengiz et al., 2006; Dobbs Austin 1997). Shigellosis Shigellosis, primarily a disease of children and young adults, kills 600,000 children under 5 years of age annu- ally worldwide. The symptoms of shigellosis include fever, abdominal cramps and tenesmus coupled with loose stools containing blood and mucus, eventually resulting in hemolytic uraemic syndrome. S. sonnei, S. boydii, S. flexneri, and S. dysenteriae are the four sero- groups mostly responsible for shigellosis. Thus, shig- ellosis is considered a major public health problem worldwide and is recognized as a global problem (Frost et al., 1981; Hossain et al., 1990; Rosenberg et al., 1976; Sur et al., 2004). CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
Food safety in the developing world  3 © 2012 Informa Healthcare USA, Inc. Campylobacteriosis Campylobacter jejuni is reported as the major cause of gastroenteritis worldwide. Developing countries how- ever, are more prone to campylobacteriosis owing to mishandling of foods, unhygienic water supply, and poor sanitary conditions. Campylobacteriosis is aggravated due to the lack of treatment facilities and health care services in developing countries subsequently distress- ing the impoverished people. The victims generally do not have access to safe drinking water and live in proper sanitary conditions (Coker et al., 2002; Oberhelman Taylor, 1999; Soofi et al., 2011; WHO, 2002). Development of post infection neurological complications due to Campylobacter is another intimidating feature of this organism. Patients suffering from Campylobacter enteri- tis are at increased risk of developing Gullien Barre syndrome (GBS), a serious life-threatening neurological disease (Tam et al., 2007). Escherichia coli infection E. coli is mainly found in the gut of humans, mam- mals, and birds and infection is considered as a reli- able marker of fecal contamination. Enteropathogenic and/or toxigenic microorganisms of intestinal tract of mammalian species are well represented by the presence of E. coli. Majority of the E. coli strains may not be hazardous however,a few of them cause severe intestinal disease in man. Classification of harmful E. coli is generally made on the basis of the production of virulence factors and clinical manifestations (Kaper et al., 2004). Staphylococcus aureus infection Staphylococcus aureus, a most frequent pathogen, is known to be a major cause of foodborne illness (gas- troenteritis). Food poisoning occurs on absorption of staphylococcal enterotoxins and is indicated as abdomi- nal cramps, nausea, vomiting following diarrhea (Le Loir et al., 2003). S aureus is an inhabitant of nostrils, skin and hair of warm-blooded animals and is carried by 30–50% of the human population. The microorganism is capable of growing under a wide range of temperature i.e. 7–48.5°C (Schmitt et al., 1990). Salmonellosis Salmonella spp., a group of Gram-negative enteric bac- teria, is important human food poisoning pathogens in the developed and developing world. Salmonella mainly reside in chicken products however, a wide range of foods have been identified for being contami- nated with these bacteria which subsequently transmit disease in humans particularly children (Flor et al., 2011; Rajashekara et al., 2000). Last decade witnessed increased worldwide incidence of gastrointestinal infections by Salmonella, transmitted through infected poultry flocks, meat, and eggs (Holt et al., 1994). S. enteritidis is known to be the most prevalent and the major cause of human salmonellosis. Approximately, 380 salmonellosis outbreaks resulted in around fifty deaths in United States from 1985 to 1991 (Mishu et al., 1994). Salmonellosis, as a major public health problem, is shown to severely impact socioeconomic status of the sufferers and is also a primary concern for developing countries (Hassan et al., 2008; Razzaque et al., 2009) (Table 1). S. typhi and S. paratyphi, are much more dangerous in developing societies. The bacteria stay within human and are transmitted through consumption of foods infected with patient’s and carrier’s feces. Street vended cultural foods, a commonplace in developing economies, are considered to be the route of S. paratyphi transmission. S. typhi and S. paratyphi, though less prevalent, con- tributed 50% of salmonellosis in the last decade among South-Central Asia and South-East Asian countries (Crump Mintz, 2010; Fangtham Wilde, 2008; Hardy, 2004; Linam Gerber, 2007). Table 1.  Annual burden of diarrhea due to ETEC among children aged up to 4 years in different settings in the developing world. Setting Age group 0–11 month(s) 1–4 year(s) Total 0–4 year(s) Domicile  Total no. of diarrheal cases 429,975,000 868,455,000 1,298,430,000  % of ETEC episodes 14.5 22.5 19.8  No. of diarrheal cases due to ETEC 62,346,375 195,402,380 257,748,755 Outpatient  Total no. of diarrheal cases 50,212,500 74,655,000 124,867,500  % of ETEC episodes 10.9 19.7* 16.2  No. of diarrheal cases due to ETEC 5,473,162 14,707,035 20,180,197 Hospital  Total no. of diarrheal cases 7,312,500 1,890,000 9,202,500  % of ETEC episodes 13.7* 12.9 13.5  No. of diarrheal cases due to ETEC 1,001,812 243,810 1,245,622 All settings  Total no. of diar- rheal cases 487,500,000 945,000,000 1,432,500,000  % of ETEC episodes 14.1 22.2 19.4  No. of diarrheal cases due to ETEC 68,821,349 210,353,225 279,174,574  No. of diarrheal episodes due to ETEC/person/year 0.54 0.47 ND *ETEC was not significantly more often isolated from individuals with diarrhea than from controls. ETEC, enterotoxigenic Escherichia coli; ND, not done. Source: Wennerås and Erling (2004). CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
4  S. Akhtar et al. Critical Reviews in Microbiology Listeriosis Listeria monocytogene, a potentially opportunistic food- borne pathogen, is responsible for infection in popula- tion especially with immunosuppression. High mortality rate is recorded for this pathogen among neonates and adults. Although, infection caused by L. monocyto- gene is rare, even then numerous outbreaks resulting from this pathogen are recorded in the history involv- ing milk, cheese, vegetables, and meat products as the vehicles of transmission. These food commodities are generally considered a source of Listeriosis in 99% cases. Septicemia, meningitis, and loss of fetus are common outcomes of L. monocytogene infection and mortality rate due to Listeriosis accounts for 25% (Slutsker et al., 2000). The organism is unique for its ability to grow at refrigeration temperatures and at a wide range of pH thus poses a threat in food industries producing products with extended shelf life and kept at low temperature (Moretro Langsrud, 2004; WHO, 1988) Vibrio cholerae infection According to World Health Organization, global preva- lence of cholera has amplified resulting in 100,000– 130,000 deaths and covering a dominating part from the developing world in 2010 (Reidl Klose, 2002; WHO, 2010). Cholerae has been identified both epidemic and endemic in many parts of the world especially the coun- tries of the third world where a majority of the cases are not reported. Therefore, it is hard to figure out the correct incidence rate of cholerae in the developing world (Sack et al., 2004). Food safety in South Asian developing countries Food processing and marketing in South Asian coun- tries undergo several stages involving quite a large number of handlers in the market chain. Moreover, modern technologies for processing and storage are lacking and the awareness on food safety for human health among the stakeholders is still missing. Amongst several potential determinants, absence of food safety management systems, good agricultural practices (GAP) and good manufacturing practices (GMP) espe- cially at small scale production and processing has been a known reason for the development of foodborne illness in this region. The street vending of a wide range of food products in most of the resource constrained South Asian countries magnifies the issue manifold and calls for serious efforts to tackle the unique chal- lenge of food safety. The situation of botulism outbreaks in different parts of the world is sufficiently terrifying. Magnitude of the global prevalence of foodborne outbreaks of botulism is increasing especially in the developing economies owing to changing life styles and poor sanitation and hygiene (Rebagliati et al., 2009). Ecological studies show massive botulism outbreaks associated with the consumption of inappropriately prepared indigenous cultural foods. Botulism cases reported in the last few decades e.g. 33 cases with three deaths between 1989 and 2005 in United Kingdom (McLauchlin et al., 2006), 160 foodborne botu- lism outbreaks between 1990 and 2000 in United States (Sobel et al., 2004) and a total of 91 botulism cases in Alaska between 1990 and 2000 (Chiou et al., 2002), clearly indicate that the developed nations with improved deliv- ery of health services and a substantial level of food safety surveillance system are no exception to this issue. Various reports on the prevalence of botulism in India (Agarwal et al., 2004; Dhaked et al., 2002; Lalitha Gopakumar, 2000), implicating several communities consuming canned meat products and fish, demon- strated consequential dominance of the disease in the region. Another massive botulism outbreak afflicting 310 students of a residential school in rural Gujrat, India for consuming ladoo (a local sweet product), curd, but- termilk, sevu (crisp made of gram flour), resulted in 14 deaths (Chaudhry et al., 1998). A total of 209 people in a village in Thailand suffered from ingestion of botulinum toxin through contaminated home-canned bamboo shoots in 2006. Among these, 134 persons were seriously distressed and 42 were placed on mechanical ventilation. That episode of food poisoning was considered to be a massive outbreak of botulism in Northern Thailand and serious concern was raised on international capacity to urgently address the issue (Ungchusak et al., 2007). Similarly, occurrence of botu- lism in China resulted in 421 deaths through 1989 from 15 provinces reporting 2861 cases involved in 745 out- breaks and 986 outbreaks of botulism were reported in Xinjiang, province of China during 1958–1983 sickening 4,377 people of which 548 died (Gao et al., 1990; Shih Chao, 1986). Epidemiological studies demonstrated botulism as a potential human health risk in various parts of Iran. Likewise, occurrence of botulism was reported in the northern province of Iran in 1997 affecting 27 patients withonedeath(Aminzadehetal.,2007;BarariKalantar, 2010; Vahdani et al., 2006). No significant study on outbreaks of botulism has been documented in Bangladesh so far. Unidentified and unreported cases are likely to go unnoticed owing to the absence of any surveillance and reporting mechanism. Data pertaining to C. botulinum incidences in Pakistan are also scant; the cases relating to botulinum outbreaks are hardly diagnosed and recorded. Children under five are the most vulnerable popula- tion fraction severely affected by shigellosis in the devel- oping countries. A substantial number of reports from developing countries including, Pakistan, Bangladesh, Sri Lanka, Maldives, Nepal, Bhutan, Thailand and India evidently indicate shigellosis as the most perilous infec- tion resulting in high morbidity and mortality throughout the year. The high prevalence of shigellosis in developing countries is associated with inappropriate sanitation, hygiene, hot, humid and rainy season and particularly flies ubiquitous in these regions (Agtini et al., 2005; Levine Levine, 1991). Shigellosis affects around 163.2 CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
Food safety in the developing world  5 © 2012 Informa Healthcare USA, Inc. million people in developing countries each year (Kotloff et al., 1999; Sur et al., 2004; WHO, 2005). Other estimates show 414,000 deaths, occurring due to shigellosis in Asia (Legros, 2004) and 1.1 million deaths in developing countries (Niyogi, 2005). Despitethefactthathigherstandardsofsanitationand hygiene are in place in Thailand, 19–37% children under various age groups during 1993–2006 were affected by shigellosis. Population in Bangkok was mainly affected by S. flexneri while S. sonnei clustered around in southern Thailand in 2006 (Bangtrakulnonth et al., 2008) (Table 2). Shigellosis appears to be widely pervasive in Indian subcontinent with S. flexneri to be a common serogroup. Bangladesh is one of the most affected regions in South Asia with regard to foodborne illness. Poverty and natu- ral calamities specifically cyclones are a commonplace and badly affect the socioeconomic status of the popu- lation. Incidence of foodborne illness is a usual event in Bangladesh. Diarrheal episodes in Bangladesh are at the rise particularly during the rainy season (Lobitz et al., 2000; Sack et al., 2004). Prevalence of shigellosis in community settings of Pakistan is alarming and has shown to deleteriously impact the health and wellbeing of the masses. Estimates show 576 000 deaths among children per year in north- ern regions of Pakistan (Bennish, 1991; Soofi et al., 2011; WHO, 1988). In addition to several other contributory factors, ratio- nalreductioninshigellosisincidencesinunderdeveloped countries may be achieved through the improvement of living standards, developing awareness on the compli- cations of foodborne illness and specifically supplying safe water. Moreover, availability of diagnostic facilities at the onset of disease, surveillance and monitoring, implementation of health care policies, awareness on the benefits of hand washing practices to stop transmission of disease from one person to other and introduction of an effective vaccine against Shigella seem to be the effective approaches to reduce shigellosis in the region (Bhattacharya Sur, 2003; Dutta et al., 2003; Kotloff et al., 1999; Sur et al., 2004). Albeit, achieving the goal to eliminate or reduce shigellosis in developing countries is highly demanding, however concerted efforts need to be continued by international agencies and local health care institutions to address the issue. Higher prevalence of Campylobacteriosis is con- firmed in Thailand which is predominantly ascribed to drug resistance. Similarly, Bangladesh, India and Pakistan are considered to be the regions in South Asia with relatively higher frequency of Campylobacter infec- tions. C. jejuni is the most common milk borne pathogen known to be prevalent in Pakistan, India and Bangladesh and implicates a significant portion of the population in various community settings (Haq Rahman, 1991; Serichantalergs et al., 2007). Like other foodborne patho- gens, drug resistance of Campylobacter is an important cause of increased prevalence of Campylobacteriosis. Imperfect and unsatisfactory surveillance and moni- toring system in developing countries are some of the potential determinants, leading to failure in controlling Campylobacteriosis (Gibreel Taylor, 2006). Enterotoxigenic E. coli (ETEC) are known to be the most common cause of diarrhea, affecting infants, chil- dren and adolescents in countries with limited resources. Morbidity rate due to ETEC in five developing countries demonstrated a continual trend in diarrheal cases during thefirstthreeyearsoflife(Huilanetal.,1991).Breastfeed- ing is reported to be a preventive measure for diarrhea Table 2.  Study population, disease episodes, and shigellosis incidence at six study sites (all ages). Characteristic China Thailand Indonesia Vietnam Pakistan Bangladesh TotalZhengding Saraburi North Jakarta Nha Trang Karachi Dhaka Total population 75,630 80,141 160,257 200,410 59,584 29,309 605,331 Surveillance period 1/2002– 5/2000– 8/2001– 1/2001– 1/2002– 6/2002– – 12/2002 4/2003 7/2003 12/2003 12/2003 5/2004 Presentations 11,342 8,612 16,872 11,419 10,540 3,481 62,266 DE included in analysis 10,104 6,536 16,225 10,258 10,371 3,464 56,958 (% of presentations)a –89% –76% –96% –90% –98% –100% –91% DE Shigella spp. isolated 330 146 1,203 390 394 464 2,927 (% of included episodes) –3% –2% –7% –4% –4% –13% –5% S. flexneri episodes (% of SE) 305 (92%) 22 (15%) 866 (72%) 282 (72%) 242 (62%) 259 (58%) 1,976 (68%) S. sonnei episodes (% of SE) 25 (8%) 124(85%) 277 (23%) 101 (26%) 72 (18%) 53 (10%) 652 (22%) S. dysenteriae episodes (% of SE) 0 0 21(2%) 6(2%) 37(9%) 46(9%) 110 (4%) S. boydii episodes (% of SE) 0 0 39(3%) 1(0%) 43 (11%) 106 (23%) 189 (6%) SE hospitalized (% of SE) 5 (2%) 2 (1%) 76 (6%) 71(18%) 0 (0%) NA 154 (6%) IR diarrhea, per 100 per year 13.4 2.7 5.1 1.7 8.7 5.9 4 IR shigellosis, per 1,000 per year 4.4 0.6 3.8 0.6 3.3 7.9 2.1 DE, diarrhea episodes; IR, incidence rate; NA, not available; SE, Shigellosis episodes. a To be included in the analysis patients had to have diarrhea, defined as three or more loose bowel movements within 1 day or one or more loose bowel movements with visible blood, and to consent to participate in the study. Source: von Seidlein et al. (2006) CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
6  S. Akhtar et al. Critical Reviews in Microbiology among infants in Bangladesh (Merson et al., 1980) and Mexico (Spencer et al., 1980), however the control did not last over the first 2 to 3 years of life (Kotloff et al., 1999). Likewise, milk based indigenous sweet products were found to be a substantial source of E.coli contami- nation causing infection in India as E. coli was frequently isolated from milk products like Mawa, Gulabjamun, Rasgulla (indigenous sweet products), cream, yoghurt, cheese and butter (Kumar Prasad, 2010) (Table 3). World has seen a considerable vigilance among coun- tries of the European Union after the deadly outbreak of shiga toxin-producing enterohaemorrhagic E coli O104:H4 in Northern Germany which resulted in numer- ous deaths and infected over 1,700 people (Greinacher et al., 2011). Developing countries including India, Pakistan and Bangladesh seem much cautious about the deadly strain of shiga toxin-producing E coli. Haemolytic uremic syndrome (HUS) causing kidney failure is the common outcome of the infection by these bacteria (Sinha, 2011). Staphylococcus aureus food poisoning is less recog- nized in developing countries as compared to the devel- oped nations where it is prioritized as a public-health agenda. South Asian countries are more likely to suffer from staphylococcal food poisoning for being resource- limited and poorer economies (Nickerson et al., 2009). Staphylococcal food poisoning is more prevalent among infants in different community reservoirs in South Asian countries. The mortality rate due to this type of food infection is much higher i.e. ~50%. Methicillin- resistant S. aureus is a threat for being highly prevalent in South Asian developing countries (Hiramatsu et al., 1997; Nickerson et al., 2006). Epidemiological surveillance and studies from Asian countriesillustratedanannualincidenceofS.typhipreva- lencetobemuchhigherinPakistan(451.7cases/100,000) as compared to neighboring countries like India (214.2 cases/100,000), Vietnam (21.3 cases/100,000), and China (15.3 cases/100,000) (Ochiai et al., 2008; 2010). A few reports from Pakistan indicate S. enteritidis to be more devastating for the population at risk. Out of a total of 58 isolates of Salmonella spp., from poultry eggs, poultry meat, poultry droppings and stool from human diarrhea cases in Faisalabad city of Pakistan, 75.86% of the isolates were S. enteritidis (Akhtar et al., 2010). Earlier, listeriosis was thought to occur sporadically in Asia but it is currently much widespread across the region. These sporadic infections in subcontinent are normally attributed to raw and heated food samples, milk, and vegetables. Human listeriosis appears among individuals having suppressed T-cell immunity (Farber Peterkin, 1991; Kohler et al., 1991). Pregnant women and neonates generally become a target of listeriosis (Holbach et al., 1988; Zaidman et al., 1990). Sanitation and hygienic conditions in Indian subcon- tinent are life threatening and are likely to jeopardize the entire food supply chain. Reported cases of listeriosis confirmed 17.5% food samples to be contaminated in Mangalore, South India, indicating the magnitude of the prevalence of the disease in the region. Seafood, beef, raw milk, vegetables were found to be implicated with Listeria spp. Similarly, several other studies demonstrated the presence of Listeria spp., in a variety of foods tested in India such as meat and their products. L. innocua, L. murrayi, L. seeligeri, and L. ivanovii were identified as the principle strains involved (Kamat Nair, 2007). Cholerae epidemics in third world countries are gener- ally linked with unsanitary conditions that often exist in this region. South Asian countries also witnessed many cholerae outbreaks in the documented history and in addition to six pandemics of V. cholerae, El Tor biotype was found to be responsible for seventh cholerae pandemic (Sacketal.,2004).Similarly,newlydescribednon-O1sero- group of V. cholerae caused unusual cholerae outbreaks in India and Bangladesh in 1992 (Cholera Working Group, 1993; Ramamurthy et al., 1993).V. cholerae serogroup O139 was reported in Karachi, Pakistan (Fisher-Hoch et al., 1993). Among 689 V. cholerae isolates from a tertiary care hospital in Karachi, 144 (21%) were detected to be of serogroup O139 in 2001(Jabeen Hasan, 2003). V. cholerae O139 is shown to be a potential cause of major epidemic in populations with compromised immune systems. V. cholerae non-O1 serogroups were also identified as a cause of diarrhea epidemics in 1992. Larger part of India and Bangladesh was inflicted with V. cholerae O139 outbreak which reached Pakistan in a few months in 1993 (Fisher-Hoch et al., 1993). Similarly, two consecutive V. cholerae epidemics were observed in a peri-urban village in Karachi, Pakistan in 2006 resulting in high morbidity (Siddiqui et al., 2006) (Table 4). Food safety in Central and South American developing countries Recent episodes of foodborne illness and substan- dard food safety status in countries of Latin America Table 3.  Estimated incidence of foodborne Salmonellosis in some developing countries. Product Egypt Brazil Zimbabwe India Poultry (Raw) 14,800 728,000 49,300 28,300 Eggs 572,000 3,270,000 53,100 2,830,000 (Raw) Beef 0 256,000 13,900 405,000 (Raw) Pork 201 129,000 0 584,000 (Raw) Milk dairy products 5,230 51,000 1,200 241,000 (Ready-to-eat) Fish seafood 34,200 135,000 2,030 1,410,000 (Ready-to-eat) Fruit vegetables 332 1,240 46 12,600 (Ready-to-eat) Total 627,000 4,570,000 120,000 5,510,000 Source: WHO (2002). CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
Food safety in the developing world  7 © 2012 Informa Healthcare USA, Inc. necessitate improved hygiene, sanitation, and awareness for the availability of safe food. According to an estimate, 6000 outbreaks of a number of different foodborne dis- eases were reported in Latin America and the Caribbean between 1993 and 2002. The economic loss incurred through these outbreaks and several single cases of food- borne disease is enormous (Anon, 2012). Microbiological contamination of a plenty of foods has been identified as a potential cause of foodborne illness in Latin American countries e.g. 90 samples of ready-to-eat foods were evaluated to ascertain their microbiological safety in Costa Rica, taking Salmonella, L. monocytogenes, C. perfringens, C. botulinum, and B. cereus as indicators of quality and safety of these foods. High fecal contamination in these foods explicitly sug- gested application of GMP, better sanitation and hygiene withafocusoncriticalcontrolpoints(Rodríguez-Cavallini et al., 2010). Another study confirmed the prevalence of L. monocytogenes in Costa Rican soft cheese samples, an identified source of Listeriosis in the region and is considered a potential source of pathogenic strains for humans (Chaves Arias 2009).C. perfringens type A food poisoning is the third most commonly reported food- borne illness in the United States (McClane, 2007; Olsen et al., 2000). Costa Rican foods, particularly meat is prone to contamination by this microorganism. Rodríguez et al. (2002) evaluated raw and cooked meats for C. perfrin- gens in relation to environment in Costa Rica. The results showed that 88% of the soil samples collected from the slaughter house environment, were contaminated with C. perfringens. Bacterial isolates were also evaluated for enterotoxin production and the researchers suggested to adopt sanitation and hygiene to prevent the risk of food- borne intoxication by these bacteria. Guatemala’sfoodexportwasbannedfortwooutbreaks occurring in 1996 and 1997 which sickened the people on consuming Guatemalan raspberries contaminated with a parasite called cyclospora. Florida outbreak of typhoid fever inflicting 16 people in 1998–1999 was traced to the consumption of fruit shakes prepared by using frozen mamey, contaminated with fecal coliforms and exported from Guatemala and Honduras (Katz et al., 2002). Similarly, the documented epidemic in humans with S. enteritidis in Uruguay demonstrated that the organ- ism was associated with foodborne illness in Central American developing countries. The microorganism is particularly prevalent in inappropriately handled poultry products. A nationwide survey to analyze sera from 5,751 birds and 12,400 eggs in Guatemala concluded 24.4% and 6.3% of the birds infected with Salmonella group O:9 and S. enteritidis, respectively (Betancor et al., 2010). The reported shiga toxin-producing E. coli (STEC) out- break in July 2011 in Germany, distressing 852 patients with HUS and 32 deaths associated with HUS has alerted the international community to exercise very special cautions to avoid such incidence. STEC proliferate through cattle’s feces and hides in the slaughterhouses. A study evaluated the carcasses for STEC in Argentina and reported 12.34% and 18.64% of STEC at the slaughter house and sanitary control cabin. Argentina has the high- est incidence of HUS in the world therefore, an extensive survey to assess non-O157 STEC contamination in car- casses and feces of bovines from nine beef abattoirs in Argentina was carried out. The results reported that 4.8% (39 of 811) of the bovine carcasses were found contami- nated with non-O157 STEC strains. The outcome of the survey revealed that these levels of contamination are a public health issues and need immediate attention (Masana et al., 2011; Etcheverría et al., 2010). Outbreaks of botulism reported in Argentina since 1992 are the corollary of inappropriate processing of meats and vegetables and other homemade foods. Moreover, ham, red, and green chili peppers have also been implicated in such outbreaks (Rebagliati et al., 2009). Yersinia enterocolitica, a species of Gram-negative coccobacillus-shaped bacterium is able to cause acute Table 4.  Comparison of demographic and clinical characteristics of 29 Vibrio cholerae O139 patients in 2002 and Vibrio cholerae O1 patients in 2003 in Rehri Goth, Pakistan. Characteristic V. cholera O139 [n (%)] V. cholera O1 [n (%)] p value OR (95% CI)b Under 2 years old 6 (21) 18 (49) 0.02 — Male 16 (55) 23 (62) 0.16 — Sick for 2 days prior to presentation 3 (10) 10 (27) 0.09 0.5 (0.1—2.0) Dysentery 2 (7) 2 (5) 0.80 0.8 (0.1—6.3) Watery diarrhea 16 (55) 31(84) 0.01 0.2 (0.1—0.6) Increased thirst 26 (90) 21(57) 0.00 5.9 (1.5—23) Dehydrated 2 (7) 5 (14) 0.38 0.5 (0.1—2.9) Abdominal pain 2 (7) 0 (0) 0.11 — Vomiting 5 (17) 8 (22) 0.66 1.0 (0.3—3.7) History of fever 16 (55) 2 (5) 0.00 38(6.9—208) Fever (37.5°C) on presentation 11(38) 1(3) 0.00 23 (2.7—195) Intravenous fluids required 4(14) 9 (24) 0.28 0.4 (0.1—1.7) a Case report forms were completed for 29 of 30 patients in the 2002 outbreak. b Odds ratio (OR) and 95% CI adjusted for age. Source: Siddiqui et al. (2006). CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
8  S. Akhtar et al. Critical Reviews in Microbiology gastroenteritis in humans. The prevalence of Y. entero- colitica in meat products has also been widely reported (Estrada et al., 2012; Siriken, 2004; Laganà et al., 2008) in the literature. An attempt to improve food safety conditions and health system as a part of Brazilian National Program, was made to monitor antibacterial resistance in chicken in the year 2004–2006, covering 15 Brazilian cities in the five geographic regions, Salmonella spp., were isolated and serotyping was carried out and Salmonella strains were tested against 18 antimicrobials. The results pre- sented S. enteritidis, to be the most prevalent strain (48.8%) followed by S. infantis (7.6%). The researchers reported high multidrug-resistant among these strains (Medeiros et al., 2011). In Chile, a total of 171 samples of salmon, shrimp, and tilapia imported from 12 countries in three retail stores in Baton Rouge, LA were analyzed for Campylobacter, E. coli, Listeria, Salmonella, Shigella, and Vibrio. The highest prevalence of L.monocytogenes (9.4%) was noticed in this study. Intermediate bacterial resistance against ampicillin was seen for V. parahaemolyticus. The results were suggestive of the potential food safety hazards associated with imported seafood in Chile. Besides, frequency of diarrhoeal episodes was attributed to seafood consumption (shellfish) and prevalence of V. parahaemolyticus in the environment of Puerto Montt, Chile was also reported (Wang et al., 2011). Similarly, Campylobacter contamination of poultry slaughter houses indicated high counts in Chile attributing the contamination with limited effect of chilling process and improper cooking practices (Figueroa et al., 2009; Fuenzalida et al., 2006). Around 9000 people died in 2 years and 1 million were affected by epidemic of cholerae in Latin America during 1991–1993. Drinking water was linked as the cause of this outbreak in Peru. Moreover, unwashed fruits and veg- etables in addition to the consumption of street vended foods were associated with Cholerae outbreak. This epi- demic, crossing the Peruvian borders reached Ecuador, then Colombia and afflicted millions of people in the adjoining states. The author concluded that state of food safety is distressing in most of the Latin American coun- tries, especially the rural areas thus requiring immediate intervention. Lacking sanitation and hygiene and avail- ability of clean potable water were suggested to be the major determinants for such epidemics in these regions (Guthmann, 1995). Foodborne illness is an important public health issue and the consumers around the globe are concerned with the safety of the foods. Venezuela, as a developing coun- try has a week food safety system in place. Several studies have demonstrated perilous food supply system espe- cially the seafood in this region. The fecal contamination of raw seafood (oysters) was investigated for the presence of enteric bacteria in Venezuela. The oysters were found to be heavily contaminated with Proteus mirabilis sug- gesting a potential human health risk associated with the consumption of raw seafood (Fernández-Delgado etal.,2007).MilksamplesinVenezuelawerealsoobserved to carry heavy contamination such as Staphylococcus, Streptococcus, Enterococcus Bacilli (Faría Reyes et al., 2002). Food safety in African developing countries Literacy, access to basic necessities of life, food secu- rity, standards of living and policies and legislation are some of the primary drivers leading to food safety and economic growth. Food safety is an issue of paramount importance and has been identified as an instrumental determinant for huge disease burden, leading to desta- bilized and weak economy of developing countries of Africa. Most of the cases of foodborne illness in Sub- Saharan African countries emanate from poor food sup- ply system and microbiological contamination during production, processing, storage, and handling of several foods. Unsatisfactory conditions of hygiene and sanita- tion are highly prevalent and are linked with extreme poverty and resourcelessness in this region. Several studies have reported unhygienic food supply and extensive contamination of commonly consumed foods, leading to high prevalence of foodborne illness in these areas e.g. bovine meat procured from slaughter house and tested for E. coli in Algeria indicated 7% of the total (230) samples contaminated with the pathogenic E. coli including E. coli O157, suggesting poor hygienic conditions of slaughterhouses (Chahed et al., 2006). Likewise L. monocytogenes have been implicated in raw milk, and raw milk products, posing a potential risk for consumers. Another study in Algeria confirmed that 2.61% of 153 and 7.50% 80 tested samples of farm milk and tankers’ milk, respectively were found contaminated with L. innocua (Hamdi et al., 2007). Like other developing countries of South Asia and Latin America, Salmonellosis prevails in South African regions where broiler farms and slaughterhouses have been regarded as major sources of contamina- tion. Elgroud et al. (2009) reported high prevalence of Salmonella contamination of broiler farms (37%) and slaughterhouse (53%) in Constantine-Algeria. High prevalence of salmonella contamination in these regions highlights unsatisfactory hygiene practices throughout the supply chain. Causative microorganism for Typhoid- paratyphoid fever was 98% S. typhi in Algeria (Guechi Hamza, 1992). Foodborne illnesses of microbial origin are a major health problem associated with street foods (Mensah et al., 2002). Several studies have demonstrated high preva- lence of various pathogenic microorganisms in a variety of street vended foods. Higher levels of enterotoxigenic B. cereus were observed in tested vegetable samples pro- cured from streets of Gaborone, Botswana, suggesting risks associated with the consumption of street vended foods in South African regions. A similar study in Kumasi, GhanarevealedhighprevalenceofStaphylococci(23.7%), CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
Food safety in the developing world  9 © 2012 Informa Healthcare USA, Inc. Bacillus spp. (21.5), and S. aureus (3.7%) in most of the tested foods. Contamination of 60 food samples with enteric bacteria and food poisoning organisms virtually represented a potential risk for local residents and was also a proxy for the poor hygiene and sanitation in the entire food chain in this area (Murindamombe et al., 2005; Feglo Saky, 2012). E. coli contamination in meat samples was assessed in 400 samples, collected from 15 supermarkets and butch- eries in Gaborone, Botswana. Microbiological analysis manifested high prevalence of E. coli O157 i.e. 5.22% in meat cube samples, 3.76% in minced meat samples, and 2.26% in fresh sausages. Likewise, personal hygiene and the level of contamination through food handlers were evaluated among a total of 200 food handlers in Gaborone, Botswana for S. aureus contamination by sampling at various anatomical sites i.e. hand, nasal cavity, and face. The upshots of the study confirmed 115 handlers (57.5%) to be positive for S. aureus. The authors suggested training of vendors and improvement in envi- ronmental hygiene in this area (Magwira et al., 2005; Loeto et al., 2007). Shiga toxin-producing E. coli and enteropathogenic E. coli isolated from mastitis milk in Egypt represented a greater risk for human health as these potentially patho- genic microorganisms belonged to serogroups associated with diarrhea and hemolytic-uremic syndrome (Osman et al., 2012). Consumption of raw or undercooked meat of bovine origin has been the most common means of transmitting this organism (Hiko et al., 2008). A group of researchers investigated the occurrence of Salmonella in foods in Morocco. The Salmonella prevalence lev- els observed were 71% for slaughterhouses and 9% for seafood (Beneduce et al., 2008). Similarly, presence of Staphylococcal strains in Morocco indicated another potential risk for foodborne illness in South African ter- ritories (Bendahou et al., 2008). Moreover, presence of Alicyclobacillus spp., a thermoacidophilic, nonpatho- genic, spore-forming bacteria, in juices is now an impor- tantconcernforbeverageindustryinSouthAfricabecause these bacteria have been found to contaminate high-acid concentrated fruit products (Steyn et al., 2011; Abdelgadir et al., 2008). Selected meat and meat products sold in the Amathole District Municipality of the Eastern Cape ProvinceofSouthAfricawereevaluatedforE.coliO157:H7 and microbiological quality of these types of foods was found highly questionable (Abong’o Momba, 2009). Microbiological quality of Sudanese cultural foods was determined to gauge food safety and hygiene in this area. Traditional Sudanese fermented camel’s milk product Gariss collected from nine different regions of Sudan and Gergoush, a naturally fermented Sudanese bread snack, were microbiologically evaluated. The results showed the presence of S. infantarius, a potential human pathogen, in these samples (Thorsen et al., 2011; Abdelgadir et al., 2008). Zimbabwe is located in southern region of Africa and has a diverse food culture. Food safety status of Zimbabwean foods is highly hazardous and the indica- tors for such conditions resemble with adjoining states. Presence of high counts of E. coli, S. aureus and total viable bacteria in raw and processed milk indicated food safety to be an issue of public health significance (Mhone et al., 2011). Similarly, prepared food and drink tested for E. coli exhibited high contamination, suggesting a need for education to prevent cross contamination of foods (Simango Mwakurudza, 2008). Economic impact of foodborne illness Considerable prevalence of foodborne illness has been well recognized in the developing nations; however, there is no statistical data available to assess the eco- nomic implications of this issue. This situation not only amplifies the existing economic losses due to foodborne illness but also hinders the overall national economic growth. Developed nations have a precise data to esti- mate such losses thus these data would indicate the extent of economic costs associated with foodborne ill- ness. The Economic Research Service–USDA took the initiative to publish economic costs of foodborne illness in terms of medical costs, productivity losses and pre- mature deaths resulting from various infections such Campylobacteriosis, non-typhi Salmonella, E. coli O157, E. coli non-O157 STEC and L. monocytogene in 2000 (Henson, 2003). Estimated economic cost of foodborne illness by spe- cific pathogens in the US only amounts to US $6.5 bil- lion to $34.9 billion while £300–700 million were spent as medical cost in addition to value of lives in United Kingdom in 1996. A recent review on economic losses of foodborne illness in the United States presents the most comprehensive report to precisely depict the volume of economic loss incurred in US (Scharff, 2012). The statis- tics provided in this review could be a clear manifestation of the relative economic losses in countries of underde- veloped world due to foodborne infection. Little efforts were directed to compute economic losses linked with foodborne illness in India and Peru in 1988 and 1997 after an outbreak of S. aureus and cholerae outbreak, respectively. The economic loss seemed to occur in the form of loss of wages and medical cost in India while in Peru the same was indicated in the shape of a massive cholerae epidemic (Buzby Roberts, 1997; Sudhakar et al., 1988). The author remained unsuccessful to grasp any detailed data indicating the economic cost of foodborne diseases in South Asian and Latin American develop- ing countries. This situation is a clear delineation of the complete absence of any mechanism to document food safety and related issues and to devise policies to fight against the challenging task of reducing foodborne ill- ness in the region. However, WHO took the initiative to collect data on foodborne illness (Salmonellosis) in some developing countries by devising a systematic and risk assessment-based approach involving number of total CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
10  S. Akhtar et al. Critical Reviews in Microbiology estimated incidences caused by non-typhi and paratyphi Salmonella as a marker of the total diarrheal incidences (WHO, 2002). Sub-Saharan Africa and India underwent the huge economic losses due to diarrheal disease i.e. 32% and 30%, respectively, suggesting foodborne illness and food safety issues to be the most potential barriers to national economic growth in these regions. Studies on the assessment of the economic loss of foodborne illness in numerical terms in the developing countries have been scarce (Henson, 2003). Precise data on economic loss of foodborne illness emanating from the developed world especially the United States constitute a very strong basis to assume that such losses could be quite massive in South Asian and African and Latin American develop- ing countries. Infant diarrhea is one of the predominant indicators to multiply disease burden. Probably no sig- nificant fluxes elucidating any visible change in the last few decades in diarrhea incidence has been witnessed in these developing countries (Käferstein, 2003). The cost of foodborne illness is calculated in terms of the economic loss born by the individual as cost of health care, absence from work and low productiv- ity which subsequently mounts up national economic loss. South Asian, African and Latin American devel- oping countries lack surveillance, reporting and docu- mentation system for the incidence of microbiological outbreaks and individual cases of foodborne illness therefore figurative assessment can be made in terms of DALYs (Henson, 2003). Contrarily, this system is quite efficient and functional in developed world where every single case is generally recorded thereby provid- ing evidence based statistical data to calculate such losses. Moreover, economic cost is reportedly higher in developing countries on the basis of percentage of per capita income as compared to the developed nations (Sudhakar et al., 1988). Conclusions Developing countries lack any integrated food safety frameworkwhichconsequentlyposesadamagingimpact throughout the food supply chain. Microbiological con- tamination of food and resulting foodborne illness are therefore, a routine incidence in underdeveloped nations especially the countries of South Asia, Latin America and Africa, though majority of the foodborne illness cases go unreported and unrecognized. Botulism, campylobacte- riosis, E. coli infection, Staphylococcus aureus infection, salmonellosis, listeriosis and Cholerae are of particular concern with food safety standpoint in these poorer economies. Assuring food safety in different food chains like industries, hotels and restaurants may be achieved through strict monitoring and surveillance in the coun- tries of third world. Moreover, street vending of foods is believed to be a potential cause of illness and thus needs to be precisely focused. Assessment of the burden of foodborne infections and identification of foodborne illness outbreaks obviously are not possible without monitoring and surveillance. This target to strengthen- ing surveillance and disease control is hard to achieve in the absence of political commitment, intervention of international agencies, awareness and strict legislation in the developing world. Implementation of HACCP and food safety management systems (ISO 22000) is scant. The food industries and allied entrepreneurs are often inclined to get them certified in the developing countries as a strategy to promote business and often evade apply- ing the systems with a professional spirit. Conclusively, the prevailing food safety situation is highly precarious in the developing countries and the recent challenges like antibiotic resistance, emergence of new and more stub- born bacterial strains and increasing demand for food to feed the rapidly growing population among the nations of developing world need to be sagaciously addressed for wellness and prosperity in these regions. Declaration of interest TheauthorsaregratefultoHigherEducationCommission of Pakistan for providing funds to Dr Saeed Akhtar to undertake post doctorate at Oregon State University, Corvallis, OR, USA and to carry out various Projects on Food Safety in Pakistan which paved the way to construct this manuscript with the coauthors. The authors report no declaration of interest. References Abdelgadir W, Nielsen DS, Hamad S, Jakobsen M. (2008). A traditional Sudanese fermented camel’s milk product, Gariss, as a habitat of Streptococcus infantarius subsp. infantarius. Int J Food Microbiol, 127, 215–219. 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Micro Biology Food Safety

  • 1. 1 Introduction Food safety has emerged as a global challenge and most of the developing countries are the victims of the dev- astating perils of foodborne illness. Since, microbes are developing resistance and are able to survive many food production and processing operations thus they pose a potential threat to human health and are regarded as the major sources of foodborne illness. Food safety is well recognized as a primary indicator of economic growth in the developing world therefore, a wave of realization has spurred both at public and government levels for safe food supply.However,the situationstill remains much depress- ing in the developing countries. International organiza- tions are inclined to help developing nations combat food safety issues; hence, numerous NGOs and local consumer groups are teeming in these states to work for food safety. In spite of the recent advancement in the domain of Food Science and Technology and a growing concern raised by various international working groups on food safety, prevalence of foodborne illness still remains a substantial cause of morbidity and preventable death. Developed economies are no exception to the risk of foodborne illness as one-third of the population undergoes this type of illness annually. Moreover, outbreaks in the United States, Australia, Germany, and India are clear indicative of the severity of the problem because30%ofthepopulationinthesecountriessuffered from foodborne illness each year (Tauxe, 1997), and 9.4 million in the United Kingdom (Walker et al., 2003). Similarly, 1200 million cases of diarrheal illness in the US are reported annually involving E. coli, Salmonella spp., Shigella spp., Cyclospora spp., Cryptosporidium spp., Campylobacter jejuni, Clostridium difficile, and other enteric viruses (Guerrant et al., 2001). Prevalence of foodborne illness though not well docu- mented on account of poor monitoring and surveillance REVIEW ARTICLE Microbiological food safety: a dilemma of developing societies Saeed Akhtar1 , Mahfuzur R. Sarker2 , and Ashfaque Hossain3 1 Bahauddin Zakariya University Multan, Department of Food Science and Technology, Multan, Pakistan, 2 Oregon Sate University, Department of Microbiology, Corvallis, Oregon, USA, and 3 University of Hail, College of Health Sciences, Hail, Saudi Arabia Abstract Current food safety issues are deleteriously reshaping the life style of the population in the developing world. Socioeconomic status of the population in poorer economies is one of the major determinants to delineate the availability of safe food to the vulnerable population. Assessment of the prevalence of foodborne illness in developing world is the most neglected area to control disease. Botulism, Shigellosis, Campylobacteriosis, Escherichia coli infection, Staphylococcus aureus infection, Salmonellosis, Listeriosis and Cholerae are extensively prevalent and pose a major threat to human health in underdeveloped communities. The existing food safety status of many African, South Asian, Central, and South American developing countries is distressing therefore; it seems much timely to highlight the areas for the improvement to ensure the supply of safe food to the population in these regions. Extensive literature search at PubMed, Science Direct and Medline was carried out during the current year to catch on relevant data from 1976 to date, using selective terms like food safety, South East Asia, Africa, Central and South America, and foodborne illness etc. Efforts were made to restrict the search to low income countries of these regions with reference to specific foodborne pathogens. This report briefly discusses the present food safety situation in these developing countries and associated consequences as prime issues, suggesting foodborne illness to be the most distressing threat for human health and economic growth. Keywords:  Botulism, Campylobacteriosis, Escherichia coli infection, Staphylococcus aureus infection, Salmonellosis Address for Correspondence: Dr Saeed Akhtar, Bahauddin Zakariya University Multan, Department of Food Science and Technology, Bosan Road, Multan, Pakistan. E-mail: [email protected] (Received 25 April 2012; revised 06 October 2012; accepted 17 October 2012) Critical Reviews in Microbiology, 2012; Early Online: 1–13 © 2012 Informa Healthcare USA, Inc. ISSN 1040-841X print/ISSN 1549-7828 online DOI: 10.3109/1040841X.2012.742036 CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
  • 2. 2  S. Akhtar et al. Critical Reviews in Microbiology is recognized as a potential determinant for rapidly declining economic growth in underdeveloped countries. Paucity of literature and statistical data to estimate the economic loss associated with foodborne illness in devel- oping regions is existent and this scarcity of information implies poor surveillance systems that hinder the nations to achieve higher food safety standards. Experience shows that infection control requires plenty of expertise in related fields such as food microbiology, chemistry, and epidemiology etc. Possibly, these skills are available in developing countries but there is no systematic approach available so far to undermine the fast growing incidence of foodborne illness. For example, no significant food- borne illness outbreak has been documented systemati- cally in South Asian or African developing economies so far, though very small epidemiological studies were car- ried out in the past which undeniably could not suffice to estimate the real economic loss. Most of the countries of developing world have no precise foodborne illness mon- itoring and surveillance system to compute economic losses incurred as non-productivity, cost of medication and Disability Adjusted Life Years (DALYs). Extent of mortality among children in developing countries due to diarrhea estimates 1.8 million deaths annually, suggesting a massive economic burden as a result of foodborne illness (WHO, 2005). Economic constraints, political instability, nonexistence of infra- structure and nonadherence with the existing food laws are the significant markers of unsafe food supply. This is further intensified by scantiness of public awareness on health and economic consequences of foodborne illness, illiteracy, poverty, malpractices, and corruption and on top of that legislation that needs to be compatible with the local beliefs and principals in the low income coun- tries. It is particularly important to understand what eco- nomic consequences are ahead if corrective measures are not taken (Henson, 2003). Hardly any developing country would have acquired precise estimates of the burden of foodborne disease because numerous instru- mental reasons deter the correct estimation, for example a majority of the cases especially for diarrheal illness are not reported (Flint et al., 2005). Extensive body of literature confirms number of food- borne disease outbreaks worldwide. Several recent food- borne disease outbreaks are reported in the United States where hygiene and sanitation is much better and the gov- ernmental agencies like local health departments, Center for Disease Control and Prevention (CDC), Federal Regulatory Agencies, Food and Drug Administration (FDA), USDA’s Food Safety and Inspection Service (FSIS), and the Environmental Protection Agency (EPA) are effi- ciently functioning to control foodborne illness. Twenty nine people died in Colorado within a time span of 3 months only i.e. July-September owing to the consump- tion of Del Monte cantaloupe infected with Salmonella spp. (CDC, 2011). FoodborneillnessintheUScausedbyCampylobacter, non-typhi Salmonella spp., E. coli O157, E. coli non-O157 shiga toxin E. coli (STEC) and Listeria mono- cytogenes resulted in a loss of $6.9 billion in terms of medical costs, productivity losses and value of prema- ture deaths in 2000. Correspondingly, an expected loss of $7.2 million is endured for each death of a child dying before the first birthday comparing with one dying at an age of 85 or more (Henson, 2003). These statistics might be virtuously exploited to make a comparison of the economic losses born by the US government with all those services and resources available which practi- cally do not exist in the developing countries of South Asia, Africa, and Central and South America. Therefore, understanding the emerging food safety challenge is rather demanding and requires public health workers and all stakeholders to strive with improved methods to overcome foodborne illness in developing countries (WHO, 2005). Thepresentreviewisanattempttoassimilatefactsand figures with particular emphasis on South Asian, Central and South American and African developing countries to assist governments to develop a food safety roadmap to combat foodborne illness. Bacterial agents and foodborne illness Botulism Four main species of Clostridium produce disease in humans i.e. C. botulinum, C. difficile, C. perfringens, and C. tetani. Foodborne botulism is caused by ingesting minimally processed foods such as canned foods espe- cially prepared at home because heat resistant spores survive in these erroneously handled foods. A potent neurotoxin, found in seven different forms is produced during the growth of C. botulinum resulting in severe neuroparalytic syndrome (Arnon et al., 2001; Skarin et al., 2011). Paralysis begins with blocking motor nerve terminals at the myoneural junction and the resulting conditions lead to death. Nevertheless, the illness is rare and uncommon because the organism thrives in specific conditions of temperature, oxygen, acidity, and water activity. These conditions generally do not exist simul- taneously in a food system to favor the bacterial growth but usually involve health risks with higher mortality rate (Cengiz et al., 2006; Dobbs Austin 1997). Shigellosis Shigellosis, primarily a disease of children and young adults, kills 600,000 children under 5 years of age annu- ally worldwide. The symptoms of shigellosis include fever, abdominal cramps and tenesmus coupled with loose stools containing blood and mucus, eventually resulting in hemolytic uraemic syndrome. S. sonnei, S. boydii, S. flexneri, and S. dysenteriae are the four sero- groups mostly responsible for shigellosis. Thus, shig- ellosis is considered a major public health problem worldwide and is recognized as a global problem (Frost et al., 1981; Hossain et al., 1990; Rosenberg et al., 1976; Sur et al., 2004). CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
  • 3. Food safety in the developing world  3 © 2012 Informa Healthcare USA, Inc. Campylobacteriosis Campylobacter jejuni is reported as the major cause of gastroenteritis worldwide. Developing countries how- ever, are more prone to campylobacteriosis owing to mishandling of foods, unhygienic water supply, and poor sanitary conditions. Campylobacteriosis is aggravated due to the lack of treatment facilities and health care services in developing countries subsequently distress- ing the impoverished people. The victims generally do not have access to safe drinking water and live in proper sanitary conditions (Coker et al., 2002; Oberhelman Taylor, 1999; Soofi et al., 2011; WHO, 2002). Development of post infection neurological complications due to Campylobacter is another intimidating feature of this organism. Patients suffering from Campylobacter enteri- tis are at increased risk of developing Gullien Barre syndrome (GBS), a serious life-threatening neurological disease (Tam et al., 2007). Escherichia coli infection E. coli is mainly found in the gut of humans, mam- mals, and birds and infection is considered as a reli- able marker of fecal contamination. Enteropathogenic and/or toxigenic microorganisms of intestinal tract of mammalian species are well represented by the presence of E. coli. Majority of the E. coli strains may not be hazardous however,a few of them cause severe intestinal disease in man. Classification of harmful E. coli is generally made on the basis of the production of virulence factors and clinical manifestations (Kaper et al., 2004). Staphylococcus aureus infection Staphylococcus aureus, a most frequent pathogen, is known to be a major cause of foodborne illness (gas- troenteritis). Food poisoning occurs on absorption of staphylococcal enterotoxins and is indicated as abdomi- nal cramps, nausea, vomiting following diarrhea (Le Loir et al., 2003). S aureus is an inhabitant of nostrils, skin and hair of warm-blooded animals and is carried by 30–50% of the human population. The microorganism is capable of growing under a wide range of temperature i.e. 7–48.5°C (Schmitt et al., 1990). Salmonellosis Salmonella spp., a group of Gram-negative enteric bac- teria, is important human food poisoning pathogens in the developed and developing world. Salmonella mainly reside in chicken products however, a wide range of foods have been identified for being contami- nated with these bacteria which subsequently transmit disease in humans particularly children (Flor et al., 2011; Rajashekara et al., 2000). Last decade witnessed increased worldwide incidence of gastrointestinal infections by Salmonella, transmitted through infected poultry flocks, meat, and eggs (Holt et al., 1994). S. enteritidis is known to be the most prevalent and the major cause of human salmonellosis. Approximately, 380 salmonellosis outbreaks resulted in around fifty deaths in United States from 1985 to 1991 (Mishu et al., 1994). Salmonellosis, as a major public health problem, is shown to severely impact socioeconomic status of the sufferers and is also a primary concern for developing countries (Hassan et al., 2008; Razzaque et al., 2009) (Table 1). S. typhi and S. paratyphi, are much more dangerous in developing societies. The bacteria stay within human and are transmitted through consumption of foods infected with patient’s and carrier’s feces. Street vended cultural foods, a commonplace in developing economies, are considered to be the route of S. paratyphi transmission. S. typhi and S. paratyphi, though less prevalent, con- tributed 50% of salmonellosis in the last decade among South-Central Asia and South-East Asian countries (Crump Mintz, 2010; Fangtham Wilde, 2008; Hardy, 2004; Linam Gerber, 2007). Table 1.  Annual burden of diarrhea due to ETEC among children aged up to 4 years in different settings in the developing world. Setting Age group 0–11 month(s) 1–4 year(s) Total 0–4 year(s) Domicile  Total no. of diarrheal cases 429,975,000 868,455,000 1,298,430,000  % of ETEC episodes 14.5 22.5 19.8  No. of diarrheal cases due to ETEC 62,346,375 195,402,380 257,748,755 Outpatient  Total no. of diarrheal cases 50,212,500 74,655,000 124,867,500  % of ETEC episodes 10.9 19.7* 16.2  No. of diarrheal cases due to ETEC 5,473,162 14,707,035 20,180,197 Hospital  Total no. of diarrheal cases 7,312,500 1,890,000 9,202,500  % of ETEC episodes 13.7* 12.9 13.5  No. of diarrheal cases due to ETEC 1,001,812 243,810 1,245,622 All settings  Total no. of diar- rheal cases 487,500,000 945,000,000 1,432,500,000  % of ETEC episodes 14.1 22.2 19.4  No. of diarrheal cases due to ETEC 68,821,349 210,353,225 279,174,574  No. of diarrheal episodes due to ETEC/person/year 0.54 0.47 ND *ETEC was not significantly more often isolated from individuals with diarrhea than from controls. ETEC, enterotoxigenic Escherichia coli; ND, not done. Source: Wennerås and Erling (2004). CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
  • 4. 4  S. Akhtar et al. Critical Reviews in Microbiology Listeriosis Listeria monocytogene, a potentially opportunistic food- borne pathogen, is responsible for infection in popula- tion especially with immunosuppression. High mortality rate is recorded for this pathogen among neonates and adults. Although, infection caused by L. monocyto- gene is rare, even then numerous outbreaks resulting from this pathogen are recorded in the history involv- ing milk, cheese, vegetables, and meat products as the vehicles of transmission. These food commodities are generally considered a source of Listeriosis in 99% cases. Septicemia, meningitis, and loss of fetus are common outcomes of L. monocytogene infection and mortality rate due to Listeriosis accounts for 25% (Slutsker et al., 2000). The organism is unique for its ability to grow at refrigeration temperatures and at a wide range of pH thus poses a threat in food industries producing products with extended shelf life and kept at low temperature (Moretro Langsrud, 2004; WHO, 1988) Vibrio cholerae infection According to World Health Organization, global preva- lence of cholera has amplified resulting in 100,000– 130,000 deaths and covering a dominating part from the developing world in 2010 (Reidl Klose, 2002; WHO, 2010). Cholerae has been identified both epidemic and endemic in many parts of the world especially the coun- tries of the third world where a majority of the cases are not reported. Therefore, it is hard to figure out the correct incidence rate of cholerae in the developing world (Sack et al., 2004). Food safety in South Asian developing countries Food processing and marketing in South Asian coun- tries undergo several stages involving quite a large number of handlers in the market chain. Moreover, modern technologies for processing and storage are lacking and the awareness on food safety for human health among the stakeholders is still missing. Amongst several potential determinants, absence of food safety management systems, good agricultural practices (GAP) and good manufacturing practices (GMP) espe- cially at small scale production and processing has been a known reason for the development of foodborne illness in this region. The street vending of a wide range of food products in most of the resource constrained South Asian countries magnifies the issue manifold and calls for serious efforts to tackle the unique chal- lenge of food safety. The situation of botulism outbreaks in different parts of the world is sufficiently terrifying. Magnitude of the global prevalence of foodborne outbreaks of botulism is increasing especially in the developing economies owing to changing life styles and poor sanitation and hygiene (Rebagliati et al., 2009). Ecological studies show massive botulism outbreaks associated with the consumption of inappropriately prepared indigenous cultural foods. Botulism cases reported in the last few decades e.g. 33 cases with three deaths between 1989 and 2005 in United Kingdom (McLauchlin et al., 2006), 160 foodborne botu- lism outbreaks between 1990 and 2000 in United States (Sobel et al., 2004) and a total of 91 botulism cases in Alaska between 1990 and 2000 (Chiou et al., 2002), clearly indicate that the developed nations with improved deliv- ery of health services and a substantial level of food safety surveillance system are no exception to this issue. Various reports on the prevalence of botulism in India (Agarwal et al., 2004; Dhaked et al., 2002; Lalitha Gopakumar, 2000), implicating several communities consuming canned meat products and fish, demon- strated consequential dominance of the disease in the region. Another massive botulism outbreak afflicting 310 students of a residential school in rural Gujrat, India for consuming ladoo (a local sweet product), curd, but- termilk, sevu (crisp made of gram flour), resulted in 14 deaths (Chaudhry et al., 1998). A total of 209 people in a village in Thailand suffered from ingestion of botulinum toxin through contaminated home-canned bamboo shoots in 2006. Among these, 134 persons were seriously distressed and 42 were placed on mechanical ventilation. That episode of food poisoning was considered to be a massive outbreak of botulism in Northern Thailand and serious concern was raised on international capacity to urgently address the issue (Ungchusak et al., 2007). Similarly, occurrence of botu- lism in China resulted in 421 deaths through 1989 from 15 provinces reporting 2861 cases involved in 745 out- breaks and 986 outbreaks of botulism were reported in Xinjiang, province of China during 1958–1983 sickening 4,377 people of which 548 died (Gao et al., 1990; Shih Chao, 1986). Epidemiological studies demonstrated botulism as a potential human health risk in various parts of Iran. Likewise, occurrence of botulism was reported in the northern province of Iran in 1997 affecting 27 patients withonedeath(Aminzadehetal.,2007;BarariKalantar, 2010; Vahdani et al., 2006). No significant study on outbreaks of botulism has been documented in Bangladesh so far. Unidentified and unreported cases are likely to go unnoticed owing to the absence of any surveillance and reporting mechanism. Data pertaining to C. botulinum incidences in Pakistan are also scant; the cases relating to botulinum outbreaks are hardly diagnosed and recorded. Children under five are the most vulnerable popula- tion fraction severely affected by shigellosis in the devel- oping countries. A substantial number of reports from developing countries including, Pakistan, Bangladesh, Sri Lanka, Maldives, Nepal, Bhutan, Thailand and India evidently indicate shigellosis as the most perilous infec- tion resulting in high morbidity and mortality throughout the year. The high prevalence of shigellosis in developing countries is associated with inappropriate sanitation, hygiene, hot, humid and rainy season and particularly flies ubiquitous in these regions (Agtini et al., 2005; Levine Levine, 1991). Shigellosis affects around 163.2 CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
  • 5. Food safety in the developing world  5 © 2012 Informa Healthcare USA, Inc. million people in developing countries each year (Kotloff et al., 1999; Sur et al., 2004; WHO, 2005). Other estimates show 414,000 deaths, occurring due to shigellosis in Asia (Legros, 2004) and 1.1 million deaths in developing countries (Niyogi, 2005). Despitethefactthathigherstandardsofsanitationand hygiene are in place in Thailand, 19–37% children under various age groups during 1993–2006 were affected by shigellosis. Population in Bangkok was mainly affected by S. flexneri while S. sonnei clustered around in southern Thailand in 2006 (Bangtrakulnonth et al., 2008) (Table 2). Shigellosis appears to be widely pervasive in Indian subcontinent with S. flexneri to be a common serogroup. Bangladesh is one of the most affected regions in South Asia with regard to foodborne illness. Poverty and natu- ral calamities specifically cyclones are a commonplace and badly affect the socioeconomic status of the popu- lation. Incidence of foodborne illness is a usual event in Bangladesh. Diarrheal episodes in Bangladesh are at the rise particularly during the rainy season (Lobitz et al., 2000; Sack et al., 2004). Prevalence of shigellosis in community settings of Pakistan is alarming and has shown to deleteriously impact the health and wellbeing of the masses. Estimates show 576 000 deaths among children per year in north- ern regions of Pakistan (Bennish, 1991; Soofi et al., 2011; WHO, 1988). In addition to several other contributory factors, ratio- nalreductioninshigellosisincidencesinunderdeveloped countries may be achieved through the improvement of living standards, developing awareness on the compli- cations of foodborne illness and specifically supplying safe water. Moreover, availability of diagnostic facilities at the onset of disease, surveillance and monitoring, implementation of health care policies, awareness on the benefits of hand washing practices to stop transmission of disease from one person to other and introduction of an effective vaccine against Shigella seem to be the effective approaches to reduce shigellosis in the region (Bhattacharya Sur, 2003; Dutta et al., 2003; Kotloff et al., 1999; Sur et al., 2004). Albeit, achieving the goal to eliminate or reduce shigellosis in developing countries is highly demanding, however concerted efforts need to be continued by international agencies and local health care institutions to address the issue. Higher prevalence of Campylobacteriosis is con- firmed in Thailand which is predominantly ascribed to drug resistance. Similarly, Bangladesh, India and Pakistan are considered to be the regions in South Asia with relatively higher frequency of Campylobacter infec- tions. C. jejuni is the most common milk borne pathogen known to be prevalent in Pakistan, India and Bangladesh and implicates a significant portion of the population in various community settings (Haq Rahman, 1991; Serichantalergs et al., 2007). Like other foodborne patho- gens, drug resistance of Campylobacter is an important cause of increased prevalence of Campylobacteriosis. Imperfect and unsatisfactory surveillance and moni- toring system in developing countries are some of the potential determinants, leading to failure in controlling Campylobacteriosis (Gibreel Taylor, 2006). Enterotoxigenic E. coli (ETEC) are known to be the most common cause of diarrhea, affecting infants, chil- dren and adolescents in countries with limited resources. Morbidity rate due to ETEC in five developing countries demonstrated a continual trend in diarrheal cases during thefirstthreeyearsoflife(Huilanetal.,1991).Breastfeed- ing is reported to be a preventive measure for diarrhea Table 2.  Study population, disease episodes, and shigellosis incidence at six study sites (all ages). Characteristic China Thailand Indonesia Vietnam Pakistan Bangladesh TotalZhengding Saraburi North Jakarta Nha Trang Karachi Dhaka Total population 75,630 80,141 160,257 200,410 59,584 29,309 605,331 Surveillance period 1/2002– 5/2000– 8/2001– 1/2001– 1/2002– 6/2002– – 12/2002 4/2003 7/2003 12/2003 12/2003 5/2004 Presentations 11,342 8,612 16,872 11,419 10,540 3,481 62,266 DE included in analysis 10,104 6,536 16,225 10,258 10,371 3,464 56,958 (% of presentations)a –89% –76% –96% –90% –98% –100% –91% DE Shigella spp. isolated 330 146 1,203 390 394 464 2,927 (% of included episodes) –3% –2% –7% –4% –4% –13% –5% S. flexneri episodes (% of SE) 305 (92%) 22 (15%) 866 (72%) 282 (72%) 242 (62%) 259 (58%) 1,976 (68%) S. sonnei episodes (% of SE) 25 (8%) 124(85%) 277 (23%) 101 (26%) 72 (18%) 53 (10%) 652 (22%) S. dysenteriae episodes (% of SE) 0 0 21(2%) 6(2%) 37(9%) 46(9%) 110 (4%) S. boydii episodes (% of SE) 0 0 39(3%) 1(0%) 43 (11%) 106 (23%) 189 (6%) SE hospitalized (% of SE) 5 (2%) 2 (1%) 76 (6%) 71(18%) 0 (0%) NA 154 (6%) IR diarrhea, per 100 per year 13.4 2.7 5.1 1.7 8.7 5.9 4 IR shigellosis, per 1,000 per year 4.4 0.6 3.8 0.6 3.3 7.9 2.1 DE, diarrhea episodes; IR, incidence rate; NA, not available; SE, Shigellosis episodes. a To be included in the analysis patients had to have diarrhea, defined as three or more loose bowel movements within 1 day or one or more loose bowel movements with visible blood, and to consent to participate in the study. Source: von Seidlein et al. (2006) CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
  • 6. 6  S. Akhtar et al. Critical Reviews in Microbiology among infants in Bangladesh (Merson et al., 1980) and Mexico (Spencer et al., 1980), however the control did not last over the first 2 to 3 years of life (Kotloff et al., 1999). Likewise, milk based indigenous sweet products were found to be a substantial source of E.coli contami- nation causing infection in India as E. coli was frequently isolated from milk products like Mawa, Gulabjamun, Rasgulla (indigenous sweet products), cream, yoghurt, cheese and butter (Kumar Prasad, 2010) (Table 3). World has seen a considerable vigilance among coun- tries of the European Union after the deadly outbreak of shiga toxin-producing enterohaemorrhagic E coli O104:H4 in Northern Germany which resulted in numer- ous deaths and infected over 1,700 people (Greinacher et al., 2011). Developing countries including India, Pakistan and Bangladesh seem much cautious about the deadly strain of shiga toxin-producing E coli. Haemolytic uremic syndrome (HUS) causing kidney failure is the common outcome of the infection by these bacteria (Sinha, 2011). Staphylococcus aureus food poisoning is less recog- nized in developing countries as compared to the devel- oped nations where it is prioritized as a public-health agenda. South Asian countries are more likely to suffer from staphylococcal food poisoning for being resource- limited and poorer economies (Nickerson et al., 2009). Staphylococcal food poisoning is more prevalent among infants in different community reservoirs in South Asian countries. The mortality rate due to this type of food infection is much higher i.e. ~50%. Methicillin- resistant S. aureus is a threat for being highly prevalent in South Asian developing countries (Hiramatsu et al., 1997; Nickerson et al., 2006). Epidemiological surveillance and studies from Asian countriesillustratedanannualincidenceofS.typhipreva- lencetobemuchhigherinPakistan(451.7cases/100,000) as compared to neighboring countries like India (214.2 cases/100,000), Vietnam (21.3 cases/100,000), and China (15.3 cases/100,000) (Ochiai et al., 2008; 2010). A few reports from Pakistan indicate S. enteritidis to be more devastating for the population at risk. Out of a total of 58 isolates of Salmonella spp., from poultry eggs, poultry meat, poultry droppings and stool from human diarrhea cases in Faisalabad city of Pakistan, 75.86% of the isolates were S. enteritidis (Akhtar et al., 2010). Earlier, listeriosis was thought to occur sporadically in Asia but it is currently much widespread across the region. These sporadic infections in subcontinent are normally attributed to raw and heated food samples, milk, and vegetables. Human listeriosis appears among individuals having suppressed T-cell immunity (Farber Peterkin, 1991; Kohler et al., 1991). Pregnant women and neonates generally become a target of listeriosis (Holbach et al., 1988; Zaidman et al., 1990). Sanitation and hygienic conditions in Indian subcon- tinent are life threatening and are likely to jeopardize the entire food supply chain. Reported cases of listeriosis confirmed 17.5% food samples to be contaminated in Mangalore, South India, indicating the magnitude of the prevalence of the disease in the region. Seafood, beef, raw milk, vegetables were found to be implicated with Listeria spp. Similarly, several other studies demonstrated the presence of Listeria spp., in a variety of foods tested in India such as meat and their products. L. innocua, L. murrayi, L. seeligeri, and L. ivanovii were identified as the principle strains involved (Kamat Nair, 2007). Cholerae epidemics in third world countries are gener- ally linked with unsanitary conditions that often exist in this region. South Asian countries also witnessed many cholerae outbreaks in the documented history and in addition to six pandemics of V. cholerae, El Tor biotype was found to be responsible for seventh cholerae pandemic (Sacketal.,2004).Similarly,newlydescribednon-O1sero- group of V. cholerae caused unusual cholerae outbreaks in India and Bangladesh in 1992 (Cholera Working Group, 1993; Ramamurthy et al., 1993).V. cholerae serogroup O139 was reported in Karachi, Pakistan (Fisher-Hoch et al., 1993). Among 689 V. cholerae isolates from a tertiary care hospital in Karachi, 144 (21%) were detected to be of serogroup O139 in 2001(Jabeen Hasan, 2003). V. cholerae O139 is shown to be a potential cause of major epidemic in populations with compromised immune systems. V. cholerae non-O1 serogroups were also identified as a cause of diarrhea epidemics in 1992. Larger part of India and Bangladesh was inflicted with V. cholerae O139 outbreak which reached Pakistan in a few months in 1993 (Fisher-Hoch et al., 1993). Similarly, two consecutive V. cholerae epidemics were observed in a peri-urban village in Karachi, Pakistan in 2006 resulting in high morbidity (Siddiqui et al., 2006) (Table 4). Food safety in Central and South American developing countries Recent episodes of foodborne illness and substan- dard food safety status in countries of Latin America Table 3.  Estimated incidence of foodborne Salmonellosis in some developing countries. Product Egypt Brazil Zimbabwe India Poultry (Raw) 14,800 728,000 49,300 28,300 Eggs 572,000 3,270,000 53,100 2,830,000 (Raw) Beef 0 256,000 13,900 405,000 (Raw) Pork 201 129,000 0 584,000 (Raw) Milk dairy products 5,230 51,000 1,200 241,000 (Ready-to-eat) Fish seafood 34,200 135,000 2,030 1,410,000 (Ready-to-eat) Fruit vegetables 332 1,240 46 12,600 (Ready-to-eat) Total 627,000 4,570,000 120,000 5,510,000 Source: WHO (2002). CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
  • 7. Food safety in the developing world  7 © 2012 Informa Healthcare USA, Inc. necessitate improved hygiene, sanitation, and awareness for the availability of safe food. According to an estimate, 6000 outbreaks of a number of different foodborne dis- eases were reported in Latin America and the Caribbean between 1993 and 2002. The economic loss incurred through these outbreaks and several single cases of food- borne disease is enormous (Anon, 2012). Microbiological contamination of a plenty of foods has been identified as a potential cause of foodborne illness in Latin American countries e.g. 90 samples of ready-to-eat foods were evaluated to ascertain their microbiological safety in Costa Rica, taking Salmonella, L. monocytogenes, C. perfringens, C. botulinum, and B. cereus as indicators of quality and safety of these foods. High fecal contamination in these foods explicitly sug- gested application of GMP, better sanitation and hygiene withafocusoncriticalcontrolpoints(Rodríguez-Cavallini et al., 2010). Another study confirmed the prevalence of L. monocytogenes in Costa Rican soft cheese samples, an identified source of Listeriosis in the region and is considered a potential source of pathogenic strains for humans (Chaves Arias 2009).C. perfringens type A food poisoning is the third most commonly reported food- borne illness in the United States (McClane, 2007; Olsen et al., 2000). Costa Rican foods, particularly meat is prone to contamination by this microorganism. Rodríguez et al. (2002) evaluated raw and cooked meats for C. perfrin- gens in relation to environment in Costa Rica. The results showed that 88% of the soil samples collected from the slaughter house environment, were contaminated with C. perfringens. Bacterial isolates were also evaluated for enterotoxin production and the researchers suggested to adopt sanitation and hygiene to prevent the risk of food- borne intoxication by these bacteria. Guatemala’sfoodexportwasbannedfortwooutbreaks occurring in 1996 and 1997 which sickened the people on consuming Guatemalan raspberries contaminated with a parasite called cyclospora. Florida outbreak of typhoid fever inflicting 16 people in 1998–1999 was traced to the consumption of fruit shakes prepared by using frozen mamey, contaminated with fecal coliforms and exported from Guatemala and Honduras (Katz et al., 2002). Similarly, the documented epidemic in humans with S. enteritidis in Uruguay demonstrated that the organ- ism was associated with foodborne illness in Central American developing countries. The microorganism is particularly prevalent in inappropriately handled poultry products. A nationwide survey to analyze sera from 5,751 birds and 12,400 eggs in Guatemala concluded 24.4% and 6.3% of the birds infected with Salmonella group O:9 and S. enteritidis, respectively (Betancor et al., 2010). The reported shiga toxin-producing E. coli (STEC) out- break in July 2011 in Germany, distressing 852 patients with HUS and 32 deaths associated with HUS has alerted the international community to exercise very special cautions to avoid such incidence. STEC proliferate through cattle’s feces and hides in the slaughterhouses. A study evaluated the carcasses for STEC in Argentina and reported 12.34% and 18.64% of STEC at the slaughter house and sanitary control cabin. Argentina has the high- est incidence of HUS in the world therefore, an extensive survey to assess non-O157 STEC contamination in car- casses and feces of bovines from nine beef abattoirs in Argentina was carried out. The results reported that 4.8% (39 of 811) of the bovine carcasses were found contami- nated with non-O157 STEC strains. The outcome of the survey revealed that these levels of contamination are a public health issues and need immediate attention (Masana et al., 2011; Etcheverría et al., 2010). Outbreaks of botulism reported in Argentina since 1992 are the corollary of inappropriate processing of meats and vegetables and other homemade foods. Moreover, ham, red, and green chili peppers have also been implicated in such outbreaks (Rebagliati et al., 2009). Yersinia enterocolitica, a species of Gram-negative coccobacillus-shaped bacterium is able to cause acute Table 4.  Comparison of demographic and clinical characteristics of 29 Vibrio cholerae O139 patients in 2002 and Vibrio cholerae O1 patients in 2003 in Rehri Goth, Pakistan. Characteristic V. cholera O139 [n (%)] V. cholera O1 [n (%)] p value OR (95% CI)b Under 2 years old 6 (21) 18 (49) 0.02 — Male 16 (55) 23 (62) 0.16 — Sick for 2 days prior to presentation 3 (10) 10 (27) 0.09 0.5 (0.1—2.0) Dysentery 2 (7) 2 (5) 0.80 0.8 (0.1—6.3) Watery diarrhea 16 (55) 31(84) 0.01 0.2 (0.1—0.6) Increased thirst 26 (90) 21(57) 0.00 5.9 (1.5—23) Dehydrated 2 (7) 5 (14) 0.38 0.5 (0.1—2.9) Abdominal pain 2 (7) 0 (0) 0.11 — Vomiting 5 (17) 8 (22) 0.66 1.0 (0.3—3.7) History of fever 16 (55) 2 (5) 0.00 38(6.9—208) Fever (37.5°C) on presentation 11(38) 1(3) 0.00 23 (2.7—195) Intravenous fluids required 4(14) 9 (24) 0.28 0.4 (0.1—1.7) a Case report forms were completed for 29 of 30 patients in the 2002 outbreak. b Odds ratio (OR) and 95% CI adjusted for age. Source: Siddiqui et al. (2006). CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
  • 8. 8  S. Akhtar et al. Critical Reviews in Microbiology gastroenteritis in humans. The prevalence of Y. entero- colitica in meat products has also been widely reported (Estrada et al., 2012; Siriken, 2004; Laganà et al., 2008) in the literature. An attempt to improve food safety conditions and health system as a part of Brazilian National Program, was made to monitor antibacterial resistance in chicken in the year 2004–2006, covering 15 Brazilian cities in the five geographic regions, Salmonella spp., were isolated and serotyping was carried out and Salmonella strains were tested against 18 antimicrobials. The results pre- sented S. enteritidis, to be the most prevalent strain (48.8%) followed by S. infantis (7.6%). The researchers reported high multidrug-resistant among these strains (Medeiros et al., 2011). In Chile, a total of 171 samples of salmon, shrimp, and tilapia imported from 12 countries in three retail stores in Baton Rouge, LA were analyzed for Campylobacter, E. coli, Listeria, Salmonella, Shigella, and Vibrio. The highest prevalence of L.monocytogenes (9.4%) was noticed in this study. Intermediate bacterial resistance against ampicillin was seen for V. parahaemolyticus. The results were suggestive of the potential food safety hazards associated with imported seafood in Chile. Besides, frequency of diarrhoeal episodes was attributed to seafood consumption (shellfish) and prevalence of V. parahaemolyticus in the environment of Puerto Montt, Chile was also reported (Wang et al., 2011). Similarly, Campylobacter contamination of poultry slaughter houses indicated high counts in Chile attributing the contamination with limited effect of chilling process and improper cooking practices (Figueroa et al., 2009; Fuenzalida et al., 2006). Around 9000 people died in 2 years and 1 million were affected by epidemic of cholerae in Latin America during 1991–1993. Drinking water was linked as the cause of this outbreak in Peru. Moreover, unwashed fruits and veg- etables in addition to the consumption of street vended foods were associated with Cholerae outbreak. This epi- demic, crossing the Peruvian borders reached Ecuador, then Colombia and afflicted millions of people in the adjoining states. The author concluded that state of food safety is distressing in most of the Latin American coun- tries, especially the rural areas thus requiring immediate intervention. Lacking sanitation and hygiene and avail- ability of clean potable water were suggested to be the major determinants for such epidemics in these regions (Guthmann, 1995). Foodborne illness is an important public health issue and the consumers around the globe are concerned with the safety of the foods. Venezuela, as a developing coun- try has a week food safety system in place. Several studies have demonstrated perilous food supply system espe- cially the seafood in this region. The fecal contamination of raw seafood (oysters) was investigated for the presence of enteric bacteria in Venezuela. The oysters were found to be heavily contaminated with Proteus mirabilis sug- gesting a potential human health risk associated with the consumption of raw seafood (Fernández-Delgado etal.,2007).MilksamplesinVenezuelawerealsoobserved to carry heavy contamination such as Staphylococcus, Streptococcus, Enterococcus Bacilli (Faría Reyes et al., 2002). Food safety in African developing countries Literacy, access to basic necessities of life, food secu- rity, standards of living and policies and legislation are some of the primary drivers leading to food safety and economic growth. Food safety is an issue of paramount importance and has been identified as an instrumental determinant for huge disease burden, leading to desta- bilized and weak economy of developing countries of Africa. Most of the cases of foodborne illness in Sub- Saharan African countries emanate from poor food sup- ply system and microbiological contamination during production, processing, storage, and handling of several foods. Unsatisfactory conditions of hygiene and sanita- tion are highly prevalent and are linked with extreme poverty and resourcelessness in this region. Several studies have reported unhygienic food supply and extensive contamination of commonly consumed foods, leading to high prevalence of foodborne illness in these areas e.g. bovine meat procured from slaughter house and tested for E. coli in Algeria indicated 7% of the total (230) samples contaminated with the pathogenic E. coli including E. coli O157, suggesting poor hygienic conditions of slaughterhouses (Chahed et al., 2006). Likewise L. monocytogenes have been implicated in raw milk, and raw milk products, posing a potential risk for consumers. Another study in Algeria confirmed that 2.61% of 153 and 7.50% 80 tested samples of farm milk and tankers’ milk, respectively were found contaminated with L. innocua (Hamdi et al., 2007). Like other developing countries of South Asia and Latin America, Salmonellosis prevails in South African regions where broiler farms and slaughterhouses have been regarded as major sources of contamina- tion. Elgroud et al. (2009) reported high prevalence of Salmonella contamination of broiler farms (37%) and slaughterhouse (53%) in Constantine-Algeria. High prevalence of salmonella contamination in these regions highlights unsatisfactory hygiene practices throughout the supply chain. Causative microorganism for Typhoid- paratyphoid fever was 98% S. typhi in Algeria (Guechi Hamza, 1992). Foodborne illnesses of microbial origin are a major health problem associated with street foods (Mensah et al., 2002). Several studies have demonstrated high preva- lence of various pathogenic microorganisms in a variety of street vended foods. Higher levels of enterotoxigenic B. cereus were observed in tested vegetable samples pro- cured from streets of Gaborone, Botswana, suggesting risks associated with the consumption of street vended foods in South African regions. A similar study in Kumasi, GhanarevealedhighprevalenceofStaphylococci(23.7%), CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
  • 9. Food safety in the developing world  9 © 2012 Informa Healthcare USA, Inc. Bacillus spp. (21.5), and S. aureus (3.7%) in most of the tested foods. Contamination of 60 food samples with enteric bacteria and food poisoning organisms virtually represented a potential risk for local residents and was also a proxy for the poor hygiene and sanitation in the entire food chain in this area (Murindamombe et al., 2005; Feglo Saky, 2012). E. coli contamination in meat samples was assessed in 400 samples, collected from 15 supermarkets and butch- eries in Gaborone, Botswana. Microbiological analysis manifested high prevalence of E. coli O157 i.e. 5.22% in meat cube samples, 3.76% in minced meat samples, and 2.26% in fresh sausages. Likewise, personal hygiene and the level of contamination through food handlers were evaluated among a total of 200 food handlers in Gaborone, Botswana for S. aureus contamination by sampling at various anatomical sites i.e. hand, nasal cavity, and face. The upshots of the study confirmed 115 handlers (57.5%) to be positive for S. aureus. The authors suggested training of vendors and improvement in envi- ronmental hygiene in this area (Magwira et al., 2005; Loeto et al., 2007). Shiga toxin-producing E. coli and enteropathogenic E. coli isolated from mastitis milk in Egypt represented a greater risk for human health as these potentially patho- genic microorganisms belonged to serogroups associated with diarrhea and hemolytic-uremic syndrome (Osman et al., 2012). Consumption of raw or undercooked meat of bovine origin has been the most common means of transmitting this organism (Hiko et al., 2008). A group of researchers investigated the occurrence of Salmonella in foods in Morocco. The Salmonella prevalence lev- els observed were 71% for slaughterhouses and 9% for seafood (Beneduce et al., 2008). Similarly, presence of Staphylococcal strains in Morocco indicated another potential risk for foodborne illness in South African ter- ritories (Bendahou et al., 2008). Moreover, presence of Alicyclobacillus spp., a thermoacidophilic, nonpatho- genic, spore-forming bacteria, in juices is now an impor- tantconcernforbeverageindustryinSouthAfricabecause these bacteria have been found to contaminate high-acid concentrated fruit products (Steyn et al., 2011; Abdelgadir et al., 2008). Selected meat and meat products sold in the Amathole District Municipality of the Eastern Cape ProvinceofSouthAfricawereevaluatedforE.coliO157:H7 and microbiological quality of these types of foods was found highly questionable (Abong’o Momba, 2009). Microbiological quality of Sudanese cultural foods was determined to gauge food safety and hygiene in this area. Traditional Sudanese fermented camel’s milk product Gariss collected from nine different regions of Sudan and Gergoush, a naturally fermented Sudanese bread snack, were microbiologically evaluated. The results showed the presence of S. infantarius, a potential human pathogen, in these samples (Thorsen et al., 2011; Abdelgadir et al., 2008). Zimbabwe is located in southern region of Africa and has a diverse food culture. Food safety status of Zimbabwean foods is highly hazardous and the indica- tors for such conditions resemble with adjoining states. Presence of high counts of E. coli, S. aureus and total viable bacteria in raw and processed milk indicated food safety to be an issue of public health significance (Mhone et al., 2011). Similarly, prepared food and drink tested for E. coli exhibited high contamination, suggesting a need for education to prevent cross contamination of foods (Simango Mwakurudza, 2008). Economic impact of foodborne illness Considerable prevalence of foodborne illness has been well recognized in the developing nations; however, there is no statistical data available to assess the eco- nomic implications of this issue. This situation not only amplifies the existing economic losses due to foodborne illness but also hinders the overall national economic growth. Developed nations have a precise data to esti- mate such losses thus these data would indicate the extent of economic costs associated with foodborne ill- ness. The Economic Research Service–USDA took the initiative to publish economic costs of foodborne illness in terms of medical costs, productivity losses and pre- mature deaths resulting from various infections such Campylobacteriosis, non-typhi Salmonella, E. coli O157, E. coli non-O157 STEC and L. monocytogene in 2000 (Henson, 2003). Estimated economic cost of foodborne illness by spe- cific pathogens in the US only amounts to US $6.5 bil- lion to $34.9 billion while £300–700 million were spent as medical cost in addition to value of lives in United Kingdom in 1996. A recent review on economic losses of foodborne illness in the United States presents the most comprehensive report to precisely depict the volume of economic loss incurred in US (Scharff, 2012). The statis- tics provided in this review could be a clear manifestation of the relative economic losses in countries of underde- veloped world due to foodborne infection. Little efforts were directed to compute economic losses linked with foodborne illness in India and Peru in 1988 and 1997 after an outbreak of S. aureus and cholerae outbreak, respectively. The economic loss seemed to occur in the form of loss of wages and medical cost in India while in Peru the same was indicated in the shape of a massive cholerae epidemic (Buzby Roberts, 1997; Sudhakar et al., 1988). The author remained unsuccessful to grasp any detailed data indicating the economic cost of foodborne diseases in South Asian and Latin American develop- ing countries. This situation is a clear delineation of the complete absence of any mechanism to document food safety and related issues and to devise policies to fight against the challenging task of reducing foodborne ill- ness in the region. However, WHO took the initiative to collect data on foodborne illness (Salmonellosis) in some developing countries by devising a systematic and risk assessment-based approach involving number of total CriticalReviewsinMicrobiologyDownloadedfrominformahealthcare.comby182.186.117.100on11/23/12 Forpersonaluseonly.
  • 10. 10  S. Akhtar et al. Critical Reviews in Microbiology estimated incidences caused by non-typhi and paratyphi Salmonella as a marker of the total diarrheal incidences (WHO, 2002). Sub-Saharan Africa and India underwent the huge economic losses due to diarrheal disease i.e. 32% and 30%, respectively, suggesting foodborne illness and food safety issues to be the most potential barriers to national economic growth in these regions. Studies on the assessment of the economic loss of foodborne illness in numerical terms in the developing countries have been scarce (Henson, 2003). Precise data on economic loss of foodborne illness emanating from the developed world especially the United States constitute a very strong basis to assume that such losses could be quite massive in South Asian and African and Latin American develop- ing countries. Infant diarrhea is one of the predominant indicators to multiply disease burden. Probably no sig- nificant fluxes elucidating any visible change in the last few decades in diarrhea incidence has been witnessed in these developing countries (Käferstein, 2003). The cost of foodborne illness is calculated in terms of the economic loss born by the individual as cost of health care, absence from work and low productiv- ity which subsequently mounts up national economic loss. South Asian, African and Latin American devel- oping countries lack surveillance, reporting and docu- mentation system for the incidence of microbiological outbreaks and individual cases of foodborne illness therefore figurative assessment can be made in terms of DALYs (Henson, 2003). Contrarily, this system is quite efficient and functional in developed world where every single case is generally recorded thereby provid- ing evidence based statistical data to calculate such losses. Moreover, economic cost is reportedly higher in developing countries on the basis of percentage of per capita income as compared to the developed nations (Sudhakar et al., 1988). Conclusions Developing countries lack any integrated food safety frameworkwhichconsequentlyposesadamagingimpact throughout the food supply chain. Microbiological con- tamination of food and resulting foodborne illness are therefore, a routine incidence in underdeveloped nations especially the countries of South Asia, Latin America and Africa, though majority of the foodborne illness cases go unreported and unrecognized. Botulism, campylobacte- riosis, E. coli infection, Staphylococcus aureus infection, salmonellosis, listeriosis and Cholerae are of particular concern with food safety standpoint in these poorer economies. Assuring food safety in different food chains like industries, hotels and restaurants may be achieved through strict monitoring and surveillance in the coun- tries of third world. Moreover, street vending of foods is believed to be a potential cause of illness and thus needs to be precisely focused. Assessment of the burden of foodborne infections and identification of foodborne illness outbreaks obviously are not possible without monitoring and surveillance. This target to strengthen- ing surveillance and disease control is hard to achieve in the absence of political commitment, intervention of international agencies, awareness and strict legislation in the developing world. Implementation of HACCP and food safety management systems (ISO 22000) is scant. The food industries and allied entrepreneurs are often inclined to get them certified in the developing countries as a strategy to promote business and often evade apply- ing the systems with a professional spirit. Conclusively, the prevailing food safety situation is highly precarious in the developing countries and the recent challenges like antibiotic resistance, emergence of new and more stub- born bacterial strains and increasing demand for food to feed the rapidly growing population among the nations of developing world need to be sagaciously addressed for wellness and prosperity in these regions. Declaration of interest TheauthorsaregratefultoHigherEducationCommission of Pakistan for providing funds to Dr Saeed Akhtar to undertake post doctorate at Oregon State University, Corvallis, OR, USA and to carry out various Projects on Food Safety in Pakistan which paved the way to construct this manuscript with the coauthors. The authors report no declaration of interest. References Abdelgadir W, Nielsen DS, Hamad S, Jakobsen M. (2008). A traditional Sudanese fermented camel’s milk product, Gariss, as a habitat of Streptococcus infantarius subsp. infantarius. Int J Food Microbiol, 127, 215–219. 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