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Biosensor in smart food traceability system for

food safety and security

Catarina Meliana, Jingjing Liu, Pau Loke Show & Sze Shin Low

To cite this article: Catarina Meliana, Jingjing Liu, Pau Loke Show & Sze Shin Low (2024)
Biosensor in smart food traceability system for food safety and security, Bioengineered, 15:1,
2310908, DOI: 10.1080/21655979.2024.2310908

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BIOENGINEERED
2024, VOL. 15, NO. 1, 2310908
https://doi.org/10.1080/21655979.2024.2310908

Biosensor in smart food traceability system for food safety and security
Catarina Melianaa, Jingjing Liub, Pau Loke Showc,d, and Sze Shin Low a

a
Nottingham Ningbo China Beacons of Excellence Research and Innovation Institute, University of Nottingham Ningbo China, Ningbo,
Zhejiang Province, China; bCollege of Automation Engineering, Northeast Electric Power University, Jilin, Jilin Province, China; cDepartment
of Chemical Engineering, Khalifa University, Abu Dhabi, Abu Dhabi Municipality, United Arab Emirates; dDepartment of Chemical and
Environmental Engineering, Faculty of Science and Engineering, University of Nottingham Malaysia, Semenyih, Selangor Darul Ehsan,
Malaysia

ABSTRACT ARTICLE HISTORY

The burden of food contamination and food wastage has significantly contributed to the Received 12 November 2023
increased prevalence of foodborne disease and food insecurity all over the world. Due to this, Revised 15 January 2024
there is an urgent need to develop a smarter food traceability system. Recent advancements Accepted 23 January 2024
in biosensors that are easy-to-use, rapid yet selective, sensitive, and cost-effective have shown KEYWORDS
great promise to meet the critical demand for onsite and immediate diagnosis and treatment Biosensors; traceability tools;
of food safety and quality control (i.e. point-of-care technology). This review article focuses on food safety; food analysis;
the recent development of different biosensors for food safety and quality monitoring. In smart packaging; food
general, the application of biosensors in agriculture (i.e. pre-harvest stage) for early detection contaminants
and routine control of plant infections or stress is discussed. Afterward, a more detailed
advancement of biosensors in the past five years within the food supply chain (i.e. post-
harvest stage) to detect different types of food contaminants and smart food packaging is
highlighted. A section that discusses perspectives for the development of biosensors in the
future is also mentioned.

1. Introduction
foodborne diseases has contributed significantly to
Ensuring access to sufficient amount of safe and the global burden of disease and mortality. This
nutritious food yet environmentally friendly have results in public health problems as well as economic
been a growing attention since the last decades. It is and social concerns worldwide. According to the
notorious that the increasing prevalence of World Health Organization (WHO), there are

CONTACT Sze Shin Low [email protected] Nottingham Ningbo China Beacons of Excellence Research and Innovation Institute,
University of Nottingham Ningbo China, Ningbo, Zhejiang Province 315100, China
© 2024 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted
use, distribution, and reproduction in any medium, provided the original work is properly cited. The terms on which this article has been published allow the posting of the
Accepted Manuscript in a repository by the author(s) or with their consent.
2 C. MELIANA ET AL.

600 million (i.e. about 1 in 10 people in the world) security) [8]. Biosensors have been known to be
cases of people becoming ill after eating contami­ reusable and able to replace conventional analyti­
nated food. This number contributes to the global cal techniques by giving rapid, accurate, reliable,
deaths of 420,000 and the loss of 33 million healthy and multiple analyses [9,10]. Many significant
years of life in 2010 [1]. Data from the annual report advancements of biosensors for food safety and
on food security and nutrition further stated that analysis have been explored, including portable
nearly 8.9% of the total population, or 690 million detections of foodborne disease agents in contami­
people, in the world are hungry, although there is nated food. The main principle of detection by
sufficient food to feed the world’s population [2,3]. biosensors is the combination of a bioreceptor
The burden of foodborne diseases and food (i.e. biological recognition element) with
insecurity as part of food sustainability issues a transducer (i.e. sensing element), generating
have influenced both developed and developing a measurable signal proportional to the concentra­
countries. However, the highest burden occurs in tion of analytes. Different types of biosensors have
low- and middle-income countries (i.e. developing been discovered based on the bioreceptor type (e.g.
countries) that have a high level of poverty and enzymes, antibodies, microbes, etc.), yet the sig­
pollution. Rapid urbanization, changes in consu­ nificance is usually based on the interaction with
mer habits, globalization, and climate change have analytes (i.e. the need to be highly specific) [9].
been known to underpin greater challenges to Alternately, the most common type of biosensor
ensuring food safety and security [4]. According based on its transducer type is electrochemical,
to the global estimates, there are 31 foodborne while others include optical and mass-sensitive
hazards causing 32 diseases, with the most promi­ biosensors [11].
nent cases being caused by bacteria, viruses, para­ Although there are many review articles dis­
sites, or chemical substances through cussing recent developments of biosensor in food
contaminated food [4]. Meanwhile, food waste system [12–17], yet it is still limited to found one
and loss are strongly linked to food insecurity that discuss applications of biosensor in a whole
and a high carbon footprint [5]. complex system of food supply chain. The pre­
Contamination of food, along with food loss sence review article aims to combine previous
and waste, may occur at any stage throughout studies of biosensors in food safety and analysis
the food supply chain (i.e. the process from farm from pre-harvest to post-harvest stage. Highlights
to fork, including manufacturing, packaging, dis­ on the advantages of different biosensors devel­
tribution, storing, and further processing or cook­ oped within the past 5 years in correlation with
ing for consumption). This is because the process smart traceability system are discussed. In general,
inherently deals with the uncertainty of safety and there are three sections in this review. In the first
quality aspects [6,7]. Due to this, traceability section, general concepts and the development of
across the supply chain must be maintained and food traceability systems and application of bio­
continually developed by all sectors (i.e. govern­ sensors as traceability tools from pre-harvest to
ment, researchers, food industry, and consumers). post-harvest are discussed. In the second section,
For instance, government should strengthen the information regarding mechanisms and applica­
requirement of legislation and certification in the tions of biosensors in food safety and security is
food industry. Meanwhile scientific and industry mentioned. Lastly, the challenges and future per­
sectors should cooperate in developing better food spectives of recent developments are mentioned.
traceability system for ensuring food safety and
quality. Consumers, at the end, should demanding
more food information. 2. Food traceability and biosensor
Smart food traceability has been known to sig­
2.1. Food traceability
nificantly help overcome the global challenges
related to food omics (i.e. the food fingerprint, The International Organization for Standardization
which covers the nutritional values, quality, and (ISO) and Codex Alimentarius Commission (CAC)
authenticity of foods, as well as their safety and define food traceability as the ability to follow or
 BIOENGINEERED 3

track the movement or progress of a product (i.e. for consumption [23]. As a result, more people
feed or food) through the food chain, including are becoming more knowledgeable about food
production, processing, and distribution [18]. and demand food credibility or food supply
Another extent to which the definition of food trace­ chain transparency.
ability relates to assurance of food safety is made by Food traceability enables whole process moni­
the American Production and Inventory Control toring of the uncertainty and complexity of the
Society (APICS) [18]. The drivers or motivating food supply chain. Thus, ensuring food safety
factors determining the necessity of food traceability and quality that prevent food waste and the possi­
often differ depending on the specific information bility of food contamination, causing foodborne
needed along the supply chain. A review by Islam & illness [24]. With rapid technological advance­
Cullen [19] classified the drivers into five categories, ments, traceability systems have progressed to
including (1) legislation and certification, (2) safety a smarter or more intelligent system (Figure 1).
and quality, (3) customer satisfaction, (4) sustain­ The main principles of smart food traceability are
ability, and (5) value and efficiency. to leverage portable sensors and indicators to col­
It is notable that the urgency for assurance and lect more comprehensive, traceable, and timely
transparency of food safety within the food supply data about food products. The leading group of
chain underlined those five driver categories. For technologies developed includes portable detection
instance, certain legislation and certification of devices, smart indicators and sensors incorporated
a reliable traceability system are required to ensure into food packages, data-assisted whole genome
fair practices in food trade and facilitate the free sequencing, and other new digital technologies
movement of safe food products within the region (e.g. Internet-of-Things (IoT) and cloud comput­
[20]. Study by [21] and [22] to assess consumer ing) [8]. Table 1 summarizes the advantages and
preferences and willingness to pay for traceable disadvantages of current portable technologies.
food further proves the statement that food trace­
ability can provide customer satisfaction. The
2.2. Biosensors in supporting smart food
rationale behind this is the significant number of
traceability
potentially substantial disruptions (e.g. food
pathogens, climate, etc.) during the supply chain 7In a similar direction with the development of
and the occurrence of food fraud for economic smart food traceability, research surrounding bio­
gain that results in unsafe and unsuitable food sensors has attracted researchers’ attention. In fact,

Figure 1. Development stages of food traceability system. Reprinted from [18] with permission from Elsevier.
4 C. MELIANA ET AL.

Table 1. Advantages and disadvantages of portable traceability technologies.

Technology Advantage Disadvantage Ref
Vibrational Simple, low cost, portable, no or minimum sample Unrealistic measurement due to low resolution, [25,26]
spectroscopy preparation, robust, rapid narrow wave number, and interference from
environmental and food intrinsic factors
Array sensors Simple, low cost and no need of chemical reagents, Unstable sensor due to environmental factors [27]
multi analysis (temperature, humidity) and other gases in the air.
Microfluidic system Simple, rapid, minimum sample consumption, multi- Disposable leading to high detection cost, [28, 29]
functional integration, small size, multiplex require high technology (e.g. antibody
detection and portability immobilization), difficult integration of
microfluidic chips and peripheral devices
IoT, blockchain, and Simple, decentralized data management, guaranteed Unable to eliminate the use of unauthorized or [30, 31, 32]
radio frequency data security, simultaneous data integration, wide fraudulent foodstuffs itself
identification application, and lower communication cost
(RFID)
Smartphone-based Feasible, low cost, records organization, and practical Still dependent or semi-dependent on laboratory [33]
analysis

the current development of biosensors has further high specificity within 1.5 hours. Figure 2 presents
surpassed the disadvantages of different portable the mechanisms of the developed biosensor for
traceability technologies. Biosensors are well- rapid detection of P. infestans [36].
known in the food supply chain for meeting the Other biosensors were developed to minimize
critical demand for onsite and immediate diagnosis abiotic stress-mediated crop loss based on phyto­
and treatment of food quality control. This is hormone responses, the production of small mole­
because biosensors enable rapid yet selective, sensi­ cules, free radicals, etc. An electrochemical
tive, and cost-effective detection of targeted analytes. biosensor to monitor phytohormones, such as sal­
Its ability to be easy-to-use without the need for icylic acid, was developed by utilizing micronee­
complicated and expensive sample preparation has dle-based electrodes. The electrodes are known to
been one of the key features to be applied to point-of be functionalized with a layer of salicylic acid-
-care (POC) technology [34]. POC in the food sup­ selective magnetic molecularly imprinted poly­
ply chain usually revolves around the concerns of mers. The biosensor showed a detection limit of
nutrient monitoring, food safety and security, and 2.74 μM in both in vitro and in vivo [37]. More
food production environment control [35]. examples of biosensor application and comparison
Within the pre-harvest stage, food crops might with conventional techniques within the pre-
be exposed to microbial infestation due to afla­ harvest stage (i.e. in the agriculture) are summar­
toxin contamination, deficiency of nutrients, ized in Table 2 as well as elaborately described
extreme weather conditions (drought and floods), elsewhere [58–60].
and others. Thus, early detection and routine con­ On the other side, the post-harvest stage usually
trol (i.e. traceability) are urgently needed to pre­ consists of a more aggregate and complex process,
vent pre-harvest loss and further contamination in including harvesting, sorting, storage, processing,
the supply chain. Many of the biosensors devel­ packaging, distribution, and consumption.
oped have been focusing on the detection of crop Application of biosensor in the post-harvest stage
pathogens. For instance, a gold nanoparticle generally deals with food safety and authentication
(AuNP)-based lateral flow biosensor integrated analysis which are mainly done during production
with universal primer-mediated asymmetric poly­ and processing to ensure the food’s suitability. The
merase chain reaction (UP-APCR) was developed analysis might include internal (e.g. nutrients, taste,
for rapid visual detection of Phytophthora infes­ pH, acidity, enzymes, etc.) and external (e.g. color,
tans, the casual late blight disease in potatoes and odor, texture, etc.) qualities [58]. As food is still con­
tomatoes [36]. The visual detection was done stantly moved from one process to another until it is
using sandwich-type hybridization assays with bought by consumers, the need for smart traceability
a detection limit of 0.1 pg/μL genomic DNA and is still urgent. This is because, after being packaged,
 BIOENGINEERED 5

Figure 2. Mechanism of AuNP-based biosensor based on UP-APCR for rapid detection of P. infestans. A region of P. infestans-specific
repetitive DNA sequence was amplified to generate large amounts of ssDNA using APCR. The ssDNA was then applied to the lateral
flow biosensor, giving a characteristic red band when there is AuNPs accumulation. Reprinted from [36] with permission from
Elsevier.

the food is still prone to contamination and deteriora­ organoleptic quality, inhibit microbial contamina­
tion due to changes in the surrounding environment. tion or growth, and prevent the contaminants’
While biosensors are known for their great ability to migration is known through the interaction of
conduct onsite food safety and analysis, the recent the product, package, and environment through
development of biosensors as part of smart food the absorption of oxygen, ethylene, moisture, car­
packaging has further shown the great potency of bon dioxide (CO2), and odors, as well as the
biosensors in food traceability systems. As an active release of CO2, ethanol, flavor, and antimicrobial
and intelligent system, smart food packaging enables agents [61]. Meanwhile, intelligent packaging sys­
manufacturers and consumers to trace the product’s tems play roles to detect, record, trace, or commu­
conditions during storage and distribution while nicate information about the food products within
extending and maintaining the shelf-life and quality the food chain by perceiving information concern­
of the food [61,62]. This smart packaging has been ing the initial food composition and storage con­
incorporated into perishable products such as dairy, dition, headspace composition, and microbial
meat, seafood, fruits and vegetables, as well as bakery growth through three principal systems: indica­
and confectionery products in recent years. The sche­ tors, sensors, and radio frequency identification
matic mechanism of active and intelligent food packa­ systems (i.e. data carriers) [64].
ging is shown in Figure 3 [63]. A biosensor incorporated with nanomaterials (i.e.
The underlying mechanism of active packaging nanosensors) has been extensively researched for their
to prolong shelf-life, maintain nutritional and excellent prospects in food safety analysis and smart
6 C. MELIANA ET AL.

Table 2. Recent advancement of biosensors as smart food traceability system.

Category Advancement Advantage Future direction References
Agriculture Monitor dissolved oxygen in In-situ, continuous, and autonomous Stable over long-term performance [38]
water
Detect antibiotics in soil Simultaneous, easily parallelizable, cost- Specifically measure the concentration of [39]
effective a particular tetracycline type
Monitor soil contamination Simple, reliable, safe, inexpensive, Real time application in soil [40, 41]
portable, highly responsive, ambient
light blocked, temperature controlled,
and water jacketed
Detect plant infections, abiotic On-site, in-vivo, online, and fast detection More research and development [42, 43]
stress, metabolic content, and reproducibility
phytohormones, miRNAs,
genetically modified (GM)
plants
Food Determine polyphenols Easy sample preparation, selective and Simple optimization method to limit [44]
quality sensitive, reproducible, low cost, interference of electrodeposition of
portable, wide linear range, and nanoparticles
accurate with excellent limit of
detection (LOD)
Assess antioxidant capacities Sensitive and precise, fast response time, Integration of intelligent devices, [45]
and ease of miniaturization functional material application and
model diversification, and explicit
mechanism
Assess food authenticity and Highly selective and sensitive, facile, Modification of nanoparticles with [46, 47]
detect illegal food additives robust, portable, cost effective, higher specific ligands to improve selectivity,
detectability, universal simple sample pretreatment
Detect food freshness Highly sensitive, low cost, robust, and Increase rate of reusability with simple [48]
portable cleaning process
Quantify ethanol in beverages Simple, fast, and highly sensible with Usage of nanomaterials to enhance [49]
elevated stability and biocompatibility sensibility and applied for monitoring
fermentation stage
Monitor survival and freshness of Simple, rapid, and accurate Longer lifespan, stable over [50]
fish environmental factors, multiple
freshness marker measured, and low
cost
Food Detect allergens sensitive, selective, low-cost, and time- Associations of different transducer [51]
safety efficient systems and nanomaterials with novel
immobilization methods
Detect antibiotics Simple, low price, rapid response, real- Improvement in electrode materials (e.g. [52], 53]
time, good selectivity and sensitivity, improve electrical conductivity and
easy miniaturization catalytic activity, amplifies
biorecognition events), usage of
different kind of nanomaterials,
development of aptamers and
molecularly imprinted polymers (MIPs)
for multi-target analysis
Detect pathogenic Rapid, real-time, easy to carry out, and More sensitive and specific portable [54]
microorganisms less labor-intensive biosensor for utilization on farms to
detect pathogens of fresh produce
surface
Detect fungal and bacterial High specific affinity, good chemical Sunlight powered and self-powered [55]
toxins stability, low cost, easy to synthesis and biosensor, split-type PEC biosensors
modification and integrating PEC biosensing with
arrays, microfluidics and chips for high-
throughput and automation analysis
Detect chemical contaminants Low cost, continuous, specific, real-time, Lower production cost to promote [56, 57]
(e.g. heavy metals, pesticides) rapid, multiple analysis commercialization, modular assembly
for real-time POC analysis,
incorporation with nanotechnology
and CRISPR-Cas-based diagnosis
 BIOENGINEERED 7

Figure 3. General schematic diagram of active and intelligent food packaging. Reprinted from [63] with permission from frontiers
(CC-BY 4.0 license).

packaging. Nanomaterials have been explored for 3. Biosensors in food safety and security
their great antimicrobial, mechanical, optical, and Increased food demand because of exponential
thermal properties to indicate the freshness, period population growth have prompted the need to
for safe consumption, storage temperature, and others frame the food security challenge and solution
of food [65]. Current discoveries of the combined through food system transformation. The food sys­
integration of biosensors with nanomaterials include tem should adopt a multidimensional approach at all
the development of a microfluidic colorimetric bio­ stages of the food supply chain (from production to
sensor using gold nanoparticles (AuNPs) for rapid consumption) to be environmentally, economically,
detection of Escherichia coli O157:H7 concentrations and socially sustainable, resilient, and efficient
in chicken samples with color change output [66]. [68,69]. As mentioned by [70], technologies such as
This combined integrated biosensor and nanomater­ remote sensing, tracing and tracking, active packa­
ials have shown a breakthrough in the challenges of ging, etc. are promising tools to tackle food security
smart food packaging, where gold nanoparticles pro­ issues. This is because it could reduce the demand
vide an excellent platform for fast, low-cost, portable, trajectory, fill the production gap, and avoid produc­
and on-site food safety biosensors through their tion losses. Biosensors represent a cutting-edge fron­
hydrogen bonding, nucleic acid hybridization, apta­ tier in food traceability systems, enabling smart food
mer-target binding, antigen-antibody recognition, safety and quality management tools. Thus, food
enzyme inhibition, and enzyme mimicking activity security issues due to food contamination and the
[67]. Another great bio-based material employed as deterioration of nutrients and qualities could also be
biosensors for food packaging is chitosan-based easily traced and prevented.
hydrogels that have antimicrobial, antioxidant, and There have been many types of biosensors devel­
biodegradability qualities [67]. Table 2 summarizes oped around food safety and quality tools, yet the
the present development of biosensors in smart food main classification of biosensors in foodborne appli­
traceability system from pre-harvest stage (i.e. agricul­ cations is based on their transducers. Optical biosen­
ture) to post-harvest stage (i.e. to determine food sors, whose output signal is light emission, usually
quality and safety). allow direct (label-free) detection of foodborne
8 C. MELIANA ET AL.

pathogens. The basic detection principle is usually principle of detection lies in the self-calibration
found when cells bind to receptors or become immo­ of ratiometric electrochemical measurement to
bilized on the transducer surface, causing changes reduce internal or external disturbances, along
that can be detected by the sensors. Electrochemical with specific signal amplification using rapid
biosensor detection, on the other hand, is primarily SRCA amplification technology and the trans-
relate to the ability to detect specific molecules (e.g. cleavage capabilities of Cas12a. The biosensor dis­
DNA-binding drugs, glucose, hybridized DNA). The played a detection limit as low as 2.08 fg/μL of
principle is based on the measurable electrons or Salmonella in pure culture and 100% sensitivity,
ions that are produced or suppressed by different 97.8% specificity, and 98% accuracy in the actual
types of chemical reactions [71]. sample [122]. Another low-field NMR (Nuclear
The applications of biosensors within food Magnetic Resonance) biosensor based on a high-
safety and security include the detection of food­ density carboxyl polyacrylate targeting gadolinium
borne pathogens, toxins, veterinary drugs, pesti­ (Gd) probe was developed to rapidly detect
cides, and other chemical contaminants (i.e. food Salmonella in milk. Figure 4 presents the sche­
allergen, heavy metals, etc.) as described next. matic diagram of the principle of the NMR bio­
Table 3 summarizes the development of biosensors sensor for detecting Salmonella in milk samples.
to detect contaminants that concern food safety At first, the target probe was obtained through an
and quality. amide reaction resulting in activated polyacrylic
acid and streptavidinylated polyacrylic acid (SA-
PAA), which further undergoes a chelating
3.1. Detection of foodborne pathogens
adsorption reaction for gadolinium. The target
The majority of foodborne disease outbreaks are probe of SA-PAA-Gd was then used to capture
caused by various forms of pathogenic bacteria, Salmonella through antigen-antibody interaction.
viruses, and parasites. Among the severe and fatal This biosensor has shown a detection limit of
bacterial infections, Salmonella, Campylobacter, 3.3 × 103 CFU/mL within 1.5 hours [123].
and enterohaemorrhagic E. coli are the most com­ E. coli O157:H7, as part of the Shiga-toxin-
mon pathogens, affecting millions of people producing E. coli (STEC), and C. jejuni infections
annually. The symptoms might include fever, have also presented an alarming challenge in food
headache, nausea, vomiting, abdominal pain, and safety. [124] developed a microfluidic chemilumi­
diarrhea. Outbreaks of salmonellosis are usually nescence biosensor based on multiple signal
linked with eggs, poultry, and other products of amplification of a combined CHA with H2-Au
animal origin, while foodborne cases caused by NP-catalyzed CL reaction for rapid and ultrasensi­
Campylobacter are mainly caused by raw milk, tive detection of E. coli O157:H7. A label-free,
raw or undercooked poultry, and drinking water. specific, rapid, and cost-effective electrochemical
Enterohaemorrhagic E. coli, on the other hand, is biosensor has also been successfully developed
usually associated with unpasteurized milk, under­ using phage EP01 as the recognition agent for
cooked meat, and contaminated fresh fruits and detection of E. coli O157:H7 GXEC-N07 in fresh
vegetables. Other bacteria that have caused food­ milk and raw pork [125]. For Campylobacter
borne diseases are Listeria infections from unpas­ detection, a whole-cell V. harveyi-based biosensor
teurized dairy products and various ready-to-eat assay developed to accurately quantify and observe
foods, and V. cholerae, which mainly contaminate the interspecies signaling molecule of C. jejuni
rice, vegetables, millet gruel, and various types of called autoinducer-2 (AI-2) has shown great pro­
seafood [4]. spect in complex food matrices of food production
Recently, a ratiometric electrochemical biosen­ [126]. A paper-based DNA biosensor based on an
sor based on the combination of SRCA (Saltatory enhanced chemiluminescence signal on a DNA
Rolling Circle Amplification) and the CRISPR/ dot blot and a silica nanoparticle was also devel­
Cas12a (CRISPR associated with system 12a) sys­ oped to monitor Campylobacter in naturally con­
tem for ultrasensitive and specific detection of taminated chicken meat without pre-amplification
Salmonella in food was developed. The basic [127].
 BIOENGINEERED 9

Table 3. Recent development of biosensors in food safety and quality field.

Category Analyte Type Bioreceptor Food sample LOD Linear range References
Pathogen Salmonella sp. Magnetic Phage Orange juice 5 CFU/mL 102 to 108 CFU/mL [72]
Salmonella sp. Electrochemical Phage Chicken 1.3 × 102 2 × 102 to 2 × 105 CFU/ [73]
CFU/mL mL
Salmonella sp. Calorimetric Aptamer Fresh-cut 6.0 × 101 6.0 × 101 to 6.0 × 105 [74]
vegetable CFU/mL CFU/mL
Salmonella Electrochemical DNA Egg, milk 1 CFU/mL 1.8 × 105 to 1.8 CFU/mL [75]
typhimurium
Campylobacter Fluorescence Antibody Poultry liver 10 CFU/mL 10 to 106 CFU/mL [76]
jejuni
Campylobacter Fluorescence Aptamer Livestock and 3 CFU/mL 10 to 107 CFU/mL [77]
jejuni dairy
E. coli O157:H7 Chemiluminescence DNA - 130 CFU/mL 2 × 102 to 108 CFU/mL [78]
E. coli O157:H7 Electrochemical Phage Fresh milk and 11.8 CFU/ 102 to 107 CFU/mL [79]
raw pork mL
E. coli Magnetic Aptamer - 1 × 102 CFU 100 to 400 μg/mL [80]
Yersinia Single walled carbon Antibody Kimchi 104 CFU/mL 106 to 104 CFU/mL [81]
enterocolitica nanotube
Vibrio Electrochemiluminescence Aptamer - 1 CFU/mL 1 to 106 CFU/mL [82]
parahaemolyticus
Shigella flexneri Electrochemical DNA - 7.4 × 10−22 8 × 1010 to 80 cells/ml [83]
mol/L
Staphylococcus Fluorescence Aptamer Pork and beef 25 CFU/mL 63 to 6.3 × 106 CFU/mL [84]
aureus
Vibrio cholerae Electrochemical DNA - 7.41 × 10−8 to 10−14 and 10−14 [85]
−30
10 to 10−27 mol/L
mol/L
Norovirus Electrochemical Antibody - 60 ag/mL 1 fg/mL to 1 ng/mL [86]
Rotavirus Electrochemical Phage - 5 copies/mL 101 to 105 copies/mL [87]
Veterinary Ampicillin Optical Antibody Milk 7.4 × 10−10 4 × 10−5 to 4 × 10−9 g/mL [88]
drug g/mL
Ampicillin Electrochemical Aptamer - 1.33 fg/mL 1.0 × 10−5 to 5.0 ng/mL [89]
Penicillin sodium Electrochemical Enzyme Milk 0.64 ng/mL 0.1 to 10 ng/mL [90]
Kanamycin Electrochemical Enzyme - 0.5 pM 1 pM to 1 μM [91]
Oxytetracycline Electrochemical Aptamer Milk 30.0 pM 1.00 to 540 nM [92]
Oxytetracycline Electrochemical Antibody - 0.33 ng/mL 1 to 200 ng/mL [93]
Tetracycline Electrochemical Aptamer Milk 3 × 10−17 M 1 × 10−16 to 1 × 10−6 M [94]
Sulfameter Fluorescence Aptamer - 1.57 ng/mL 2 to 250 ng/mL [95]
Mycotoxin Aflatoxin B1 Electrochemical Aptamer Wine and soy 0.016 pg/ 0.1 to 10 pg/mL [96]
sauce mL
Aflatoxin B1 Electrochemical Antibody Corn 0.54 pg/mL 1 pg/mL to 10 µg/mL [97]
Aflatoxin B1 Fluorescence DNA Peanut 0.92 pg/mL 0.001 to 80 ng/mL [98]
Ochratoxin A Optical Enzyme Maize 54 pg/mL 0.1 to 50 ng/mL [99]
Ochratoxin A Electrochemiluminescence Enzyme - 3 pg/mL 0.01 to 5 ng/mL and 5 to [100]
100 ng/mL.
Ochratoxin A Fluorescence Aptamer Rice 0.005 ng/ 0.01 to 10 ng/mL [101]
mL
Ochratoxin A Fluorescence Aptamer - 0.36 nmol/L 0.69 to 8.0 nmol/L [102]
Pesticide Carbendazim Fluorescence Aptamer - 0.05 ng/mL 0.1 to 5000 ng/mL [103]
Carbaryl Colorimetric Enzyme - 0.008 ng/ 0.01 to 0.25 ng/mL [104]
mL
Carbaryl Electrochemical Enzyme Apple 4.5 nmol/L 5.0 to 30.0 nmol/L [105]
Food Ara h1 Fluorescence Aptamer - 0.04 ng/mL 0.1 to 100 ng/mL [106]
allergen Ara h1 Electrochemical Aptamer Cookie dough 21.6 ng/mL 50 to 1000 ng/mL [107]
Tropomyosin Magnetic Aptamer Seafood 30.76 ng/ 0.1 to 2.5 μg/mL [108]
mL
Tropomyosin Fluorescence Antibody Fish fillet and 0.01 μg/mL 0.005 to 1 μg/mL [109]
meatball
Ovomucoid Electrochemical Phage - 0.12 μg/mL 1.55 to 12.38 μg/mL [110]
Arginine kinase Fluorescence Aptamer Shellfish 0.298 μg/ 0 to 2.5 μg/mL [111]
mL
Beta-lactoglobulin Fluorescence Aptamer - 0.048 mg/L 0.39 to 1000 mg/L [112]
Beta-lactoglobulin Fluorescence Aptamer Infant food 96.91 μg/L 0.36 to 500 mg/L [113]
products
(Continued )
10 C. MELIANA ET AL.

Table 3. (Continued).
Category Analyte Type Bioreceptor Food sample LOD Linear range References
Heavy Mercury Colorimetric Whole-cell - 0.1 ppm 0.1 to 0.75 ppm [114]
metal Cadmium 0.2 ppm 0.2 to 0.75 ppm
Copper 2 ppm 2 to 7.5 ppm
Lead (II) Electrochemiluminescence Aptamer Water 0.059 ng/L 0.1 to 1 × 106 ng/L [115]
Arsenic (III) Electrochemical Whole-cell Water 1.5 ppb 2.5 to 50 ppb [116]
Copper (II) Bioluminescence Enzyme Water 2.5 mg/L - [117]
Others Acrylamide Fluorescence DNA Bread crust 2.41 × 10−8 5 × 10−3 to 1 × 10−7 M [118]
M
Hypoxanthine Colorimetric Enzyme Fish 8.22 μmol/L 0.01 to 0.16 mmol/L [119]
Hypoxanthine Electrochemical Enzyme Fish 15 μM 50 to 800 μM [120]
Xanthine Electrochemical Enzyme Fish 0.35 nM 0.001 to 0.004 μM and [121]
0.005 to 50.0 μM

In viral pathogens, norovirus (NoV) is one of human health, portable chemiluminescence optical
the most common foodborne infections, causing fiber aptamer-based biosensors for ultrasensitive
nausea, explosive vomiting, watery diarrhea, and onsite assay of multiplex mycotoxins in food are devel­
abdominal pain [4]. Given that NoV causes over oped [132]). With a LOD of 0.015–0.423 pg/mL, the
200,000 deaths each year, [128] created biosensor demonstrated sensitive and multiple analy­
a photoelectrochemical biosensor coupled with sis of mycotoxins in infant cereals. The selective and
a novel custom-made monoclonal antibody as multiple analysis of the biosensor is mainly based on
a convenient POC system for diagnosing NoV optical fibers that have specific recognition of single-
infection and detecting NoV-contaminated food stranded binding proteins (SSB) and mycotoxin apta­
samples. An electrochemical biosensor based on mers (Jia et al., 2022).
specific binding peptides coated onto the gold Another portable chemiluminescence biosensor
electrode has also exhibited highly specific detec­ for rapid on-field screening and quantification of
tion of NoV from oysters [129]. The schematic OTA in wine and coffee samples was developed
illustration of the biosensor to detect NoV is [133]. The user-friendly smartphone-based biosen­
shown in Figure 5 [129]. Similarly, [130] also sor was developed using the combination of low-
developed a 3D electrochemical aptasensor for cost, disposable analytical cartridges that contain
NoV detection in spiked oysters based on phos­ a lateral flow immunoassay (LFIA) strip with the
phorene-gold nanocomposites. chemiluminescence detection system of the smart­
phone camera as a light detector. The biosensor
showed a LOD of 0.3 and 0.1 μg/L for wine and
3.2. Detection of mycotoxins
coffee, respectively. On the other hand, [6] success­
Mycotoxins, the secondary metabolites produced by fully developed an electrochemical biosensor based
fungi, have been known to have a significant toxicity on E. coli as the signal recognition element, p-ben­
effect on human and animal health, economies, and zoquinone as the mediator, and a two-step reaction
international trade. Mycotoxin contamination might procedure. The biosensor showed detection limits
occur on crops either during harvesting or storage. of 1 and 6 ng/mL for Aflatoxin B1 (AFB1) and ZEN,
There have been about 300 mycotoxins identified and enabling a promising tool for toxicity evaluation in
reported to contaminate 30 to 100% of food and feed corn and peanut oils. Moreover, a colorimetric bio­
samples in the world. Five major mycotoxin groups sensor with a wide detection range for dual myco­
that are commonly found are aflatoxins (AF), ochra­ toxins detection was developed using a Fe3O4/GO-
toxins (OTA), fumonisins, zearalenone (ZEN), and based platform for AFB1 detection and a Fe3O4
deoxynivalenol/nivalenol (DON) [131]. As multiple @Au based platform for OTA detection [134]. The
mycotoxin contamination in foodstuffs poses syner­ detection principle of a colorimetric biosensor is
gistic effects that cause a more significant threat to shown in Figure 6 [134].
 BIOENGINEERED 11

Figure 4. Schematic diagram of NMR biosensor to detect salmonella in milk. Firstly, the target probe was prepared (a) followed with
detection of salmonella in milk (b). Reprinted from [123] with permission from Elsevier.

3.3. Detection of veterinary drug drugs (i.e. antibiotics) often leads to the deposition
of drug residues in the tissues and organs of food
Antibiotics, such as chloramphenicol, sulfadiazine,
neomycin, and kanamycin, are the major group of animals. This will then induce serious health hazards
veterinary drugs used in food-producing animals to (e.g. allergies, antimicrobial resistance) when accu­
prevent or cure disease. The misuse of veterinary mulated in the human body. [109] have successfully
12 C. MELIANA ET AL.

Figure 5. Detection of Norovirus using peptide-coated electrochemical biosensor. Reprinted from [129] with permission from
Elsevier.

fabricated an ultrasensitive label-free biosensor a LOD of 0.6 pM to detect kanamycin in milk was
based on aptamer-functionalized 2D photonic crys­ also manufactured based on exonuclease III-assisted
tal (SiO2-Au-ssDNA 2D PC) to detect kanamycin in dual-recycling amplification [136]. The ultrasensi­
milk. With the combination of the negatively tive and catalytic signal amplification of the biosen­
charged AuNPs and sulfhydryl-modified ssDNA, sor were constructed using high-conductive
the biosensor has resulted in excellent performance MXene/VS2 and high-activity CeCu2O4 bimetallic
with a LOD of 1.10 pg/mL [135]. A more recent nanoparticles as the electrode surface and nanozyme,
development of an electrochemical biosensor with respectively. Meanwhile, the accurate detection of

Figure 6. Detection principle of a colorimetric biosensor to detect AFB1 and OTA. Formerly, the two platforms of Fe3O4/GO and TP-
GO and Fe3O4@Au and Au NPs were formed through the combination of an AFB1 aptamer and the complementary strands of an
OTA aptamer and probe, respectively. The absence and presence of both AFB1 and OTA will result in platform separation and
a colorless supernatant. The addition of an alkaline solution to magnetically separated solids and the usage of Au NPs in the
supernatant, on the other hand, results in a dark blue-colored solution. Reprinted from [134] with permission from Elsevier.
 BIOENGINEERED 13

the biosensor was fabricated from the dual supple­ antibiotics was constructed with a LOD of 0.333
mentary recycling of primer DNA and hairpin DNA ng/mL [139].
(Figure 7). Furthermore, ampicillin (AMP), as one of the
Another ultrasensitive and selective colorimetric most used β-lactam antibiotics with antibacterial
biosensor based on G-quadruplex DNAzyme was activity against gram-negative and positive bac­
also developed to detect residues of tetracyclines in teria, is also extensively used in agriculture, live­
foods [137]. Tetracycline antibiotics (e.g. tetracy­ stock, poultry, aquaculture, etc. There have been
cline (TET), oxytetracycline (OTC), chlortetracy­ a number of severe environmental and food safety
cline (CTC), and doxycycline (DOX)) are widely concerns recorded due to the overdose of this
used in the field of livestock husbandry, and when antibiotic, including endocarditis, membranitis,
they are misused, their residues are often found in intestinal infection, and irritability. Yadav et al.
animal-derived foods such as milk, honey, and [140] have successfully fabricated a label-free elec­
pork [138]. The buildup in the human body can trochemical immunosensor based on molybdenum
lead to serious diseases such as liver damage, tooth disulfide nanoparticles modified disposable
yellowing, allergic disorders, intestinal flora disor­ indium tin oxide (ITO) with a LOD of 0.028 µg/
ders, and bacterial resistance. The underlying mL in different food samples (milk, orange juice,
mechanism of the biosensor to give results of and tap water). Detection of sulfamethazine, which
tetracycline detection that could be determined is the most widely used and detected sulfonamide
even by the naked eye is based on the reaction in animal-derived foods, was also studied with an
between tetracycline and DNAzyme, which is antibody-antigen-aptamer sandwich electrochemi­
composed of hemin and G-quadruplex and has cal biosensor [141].
peroxidase-like activity to form a stable complex
and reduce catalytic activity. This reaction will
then cause the solution’s color to change from 3.4. Detection of pesticides
yellow to green [137]. A more recent similar col­ Organophosphate (OPP) and carbamate pesti­
orimetric biosensor to detect tetracycline cides have had a positive impact on insect pest

Figure 7. Schematic diagram of electrochemical biosensor based on exonuclease-III-assisted dual-recycling amplification for rapid,
sensitive, and accurate detection of kanamycin in milk. Reprinted from [136] with permission from Elsevier.
14 C. MELIANA ET AL.

control and crop production globally. However, principle of the biosensor is known to rely on
the indiscriminate and widespread use may result AChE-catalyzed hydrolytic product-triggered dis­
in impending toxicity to the environment and integration of MnO2 nanosheets. Another type of
human health [142]. The progressive research biosensor, which is voltametric with confirmed
on the development of various biosensors has reusability after 90 days, was also executed based
ranged from the use of conventional immobiliz­ on enzyme activity inhibition of fungal laccase and
ing supports to more advanced hybrid or com­ bacterial catalase [150].
posite nanomaterials [143]. Previous reviews by
[144] and [145] have summarized different enzy­
matic electrochemical biosensors for pesticide
3.5. Detection of other contaminants
detection in foods. In particular, the inhibition-
based biosensors that utilize the acetylcholines­ Although it is not a common food allergen, there
terase (AChE) enzyme are shown to be mostly has been a growing incidence of mustard allergies.
preferred. This is because the toxicity of organo­ Therefore, a disposable electrochemical PCR-free
phosphorus pesticides will result in the formation biosensor was generated for the selective detection
of covalent bonding and the permanent inactivity of protein Sin a 1, the most potent allergen in
of the AChE enzyme (Figure 8a). yellow mustard [151]. The detection principle
For instance, a low cost and highly sensitive was done through the formation of DNA/RNA
biosensor which immobilized the AChE enzyme heterohybrid-specific antibodies by sandwich
on zinc oxide (ZnO) demonstrated excellent per­ hybridization, resulting in simple and fast detec­
formance with the detection limit range from 0.5 tion with a LOD of 3 pM. In a similar direction,
nM–5 µM [147] (Figure 8b). A graphene/chitosan/ [152] have successfully fabricated an aptameric
parathion multi-residue electrochemical biosensor biosensor using graphene oxide to detect the
was also fabricated to detect 11 types of OP pesti­ alarming shrimp allergy due to tropomyosin. The
cides through an indirect competitive method advancement of biosensors that allow allergen
[148]. The biosensor was prepared by combining detection and evaluation of allergy drugs was also
the formation of phosphorylated AChE between studied. Jeong et al. [153] constructed
organophosphorus molecules and AChE as well a bioelectronic sensor based on nanovesicles com­
as the excellent conductivity of graphene. bined with anti-immunoglobulin E (anti-IgE) anti­
Likewise, a portable electrochemical biosensor body receptors for signal amplification. The
was constructed by integrating a laser-induced sensing system showed that it was sensitive and
graphene (LIG) electrode on polyimide (PI) foil selectively able to detect the peanut allergen
and MnO2 nanosheets loaded on the paper [149]. Arachis hypogaea 2 (Ara h 2) with a LOD of 0.1
With a ‘sign-on’ electrochemical response of OPs fM in real food samples such as peanut and egg
determination in vegetables, the detection white.

Figure 8. (a) inhibition activity of AChE by OP and carbamate pesticides. Reprinted from [146] with permission from hibiscus
Publisher (CC by 4.0 license); (b) schematic diagram of zinc oxide (ZnO)-based biosensor to detect OP. Reprinted from [147] with
permission from MDPI (CC by 4.0 license).
 BIOENGINEERED 15

Heavy metals (e.g. mercury, lead, cadmium, result in significant health hazards, Vasconcelos
and arsenic) are known to pose a serious threat et al. [157] developed a chemiluminescence bio­
to food safety if consumed above the weekly sensor using a hydroxyethylcellulose-based mem­
allowable intake. [154] developed a cell-free brane to detect hydrogen peroxide (H2O2) in
paper-based biosensor for on-site detection of different types of milk (i.e. fresh-raw, whole, semi-
Hg2+ and Pb2+ in water using a combination of skimmed, and skimmed milk). The biosensor
in vitro transcription (IVT) technology with proved to be a quick, environmentally friendly,
allosteric transcription factors (aTFs). The detec­ and low-cost method for detecting H2O2 in milk,
tion principle mainly relied on the aTFs specific with a LOD of 1.0 × 10−3 % w/w for fresh, raw,
affinity characteristic toward metal ions that skim, and whole milk, and 2.0 × 10−3 % w/w for
cause dissociation from DNA and result in semi-skimmed milk. Moreover, synthetic colorants
a measurable signal of transcribed fluorescent that are often used to enhance the sensory proper­
RNA (Figure 9). Copper is a heavy metal that ties of foods are known to contain azo compounds,
is also classified as an essential micronutrient for which pose hazards to human health. A study by
performing various bodily functions for plant, Manjunatha [158] developed a sensitive and selec­
animal, and human health (e.g. production of tive cyclic voltammetric sensing system that uti­
red blood cells, collagen, energy, etc.). Copper lized a poly (glycine) modified carbon paste
should be monitored on a regular basis to avoid electrode to determine tartrazine with a LOD of
toxicity and health problems caused by over- 2.83 × 10−7 mol/L.
and underconsumption [155]. Žunar et al.
[156] have successfully transformed the native
copper response of yeast S. cerevisiae into 4. Challenges and future perspective
a whole-cell eukaryotic whole-cell copper bio­ Despite the necessity of traceability system within
sensor to evaluate copper bioavailability. the complex food supply chain, not all food com­
Food additives, in particular hydrogen peroxide panies have sufficient economic value or scale to
(H2O2), are strong oxidizing agents that are often invest in. It is claimed by many studies that bio­
used in food processing as a bleaching agent in sensors are cost-effective, yet the cost to manufac­
wheat flour, an antimicrobial agent in milk, or ture biosensors still needs to be reduced as
a sterilizing agent for food packaging materials. commercial applications are still lacking.
As high ingestion of hydrogen peroxide could Currently, self-powered biosensors based on

Figure 9. Schematic diagram of a cell-free paper-based biosensor for on-site detection of heavy metals Hg2+ and Pb2+ in water
based on aTfs. Reprinted from [154] with permission from Elsevier.
16 C. MELIANA ET AL.

biofuel cells have attracted great interest as they to the automation and cloud-data saving from
could advance the cost-efficiency of biosensors to smartphone. With the current globalization
another extent while being user-friendly and where smartphones are being used by almost all
highly suitable for miniaturization, portability, people, smartphone-assisted biosensors will give
and wearability [159]. Lack of uniformity in the enormous potential for onsite detection of food
systems, coordination, allocation of costs and ben­ contaminants. For instance, Abdelbasset et al.
efits for research and development, as well as glo­ [165] discussed that smartphone-based aptasensor
balization pace, climate, geographical location, and offers a semi-automated user interface that can be
natural resources between each country have pose exploited by an inexpert person, along with fast
further challenges for implementing efficient and wireless data transferability. It could then be
application of biosensor for food system. [160] a breaking stone for onsite, portable, and simple
have successfully developed a highly thermal and monitoring in the smart food traceability system.
storage stable electrochemical biosensor for facil­ As for sensor array, it can improve the specificity
itating rapid pesticide detection of fruits and vege­ of biosensor due to its ability to accurately identify
tables in a variety of climates. Another biosensor very similar and wide range of analytes in mixtures
developed with long shelf life after 40 days also for fingerprint identification. This then can be
further supported the advancement of biosensor used for detecting any food adulteration. Lastly,
to tackle challenges in food safety and analysis biosensor and IoT technologies could lead in the
technologies [161]. wireless transmission technology [154,166].
Furthermore, as nanomaterials could be toxic,
the fabrication of biosensor using this material
might rise other challenges related to health. 5. Conclusion
Therefore, further study on green synthesis and The increased prevalence of foodborne illness and
incorporation of biocompatible materials have food insecurity have shown great urgency in devel­
grasped the insurgencies along with enhancing oping smart food traceability systems that are rapid,
the sustainability value of biosensors in the food accurate, reliable, low cost, and able to conduct
system (i.e. repurpose, reuse, degradable, or recycl­ multiple analyses. Many advancements in biosen­
able material) [162]. Development of biosensors sors over the years have shown great promise in
using microorganisms as the bioreceptor also enabling whole process monitoring to tackle the
have attracted many researchers’ attention. This uncertainty and complexity of the food supply
is because the regulatory genes and proteins of chain. The present review highlights different fabri­
microorganisms possess various responsive cations of biosensors within the pre- and post-
mechanisms to cope with environmental stress, harvest stages of food (e.g. agriculture, detecting
pollutants, and heavy metals [163,164]. This then biological and chemical food contaminants, smart
could be useful for the development of biosensor food packaging). Based on the current trends, many
in agriculture as well as environmental monitor­ biosensors associated with nanoparticles have more
ing. By having minimum requirements of electri­ advantages, such as a lower detection limit, higher
city, water, gas, and energy from biosensor, sensitivity, selectivity, and stability over long-term
minimal generation of carbon footprints could usage. However, there are still, many challenges to
also be achieved. be tackled and improved in the future.
As food system has become more complex, it is
also urgently needed nowadays to have a more
integrated food detection system. Biosensor com­ Disclosure statement
bined with emerging technologies, such as smart­ No potential conflict of interest was reported by the author(s).
phones, 3D printing, IoT, AI, and blockchain,
could lead biosensor into another extend of
advancement. For instance, combining biosensor Funding
and smartphone could significantly improve detec­ This work was supported by the Ningbo Yongjiang Talent
tion accuracy and shorten the detection time due Introduction Program (2023A-140- G), Ningbo Natural
 BIOENGINEERED 17

Science Foundation Program (2023J247) and Nottingham [11] Mishra GK, Barfidokht A, Tehrani F, et al. Food safety
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