biosensors

Review
Application of Biosensors for Detection of Pathogenic
Food Bacteria: A Review
Athmar A. Ali 1 , Ammar B. Altemimi 1 , Nawfal Alhelfi 1 and Salam A. Ibrahim 2, *
1 Department of Food Science, College of Agriculture, University of Basrah, Basrah 61001, Iraq;
athmar.ali93@gmail.com (A.A.A.); ammaragr@siu.edu (A.B.A.); nawfalalhelfi@gmail.com (N.A.)
2 Food and Nutritional Science Program, North Carolina A & T State University, Greensboro, NC 27411, USA
* Correspondence: ibrah001@ncat.edu




Received: 28 April 2020; Accepted: 27 May 2020; Published: 30 May 2020


Abstract: The use of biosensors is considered a novel approach for the rapid detection of foodborne
pathogens in food products. Biosensors, which can convert biological, chemical, or biochemical
signals into measurable electrical signals, are systems containing a biological detection material
combined with a chemical or physical transducer. The objective of this review was to present the
effectiveness of various forms of sensing technologies for the detection of foodborne pathogens in
food products, as well as the criteria for industrial use of this technology. In this article, the principle
components and requirements for an ideal biosensor, types, and their applications in the food industry
are summarized. This review also focuses in detail on the application of the most widely used
biosensor types in food safety.

Keywords: biosensors; pathogenic bacteria; bioluminescence; ATP; foodborne

1. Introduction
Many people around the world become ill each year by consuming food pathogens. These foodborne
illnesses are highly correlated to both physical and chemical contamination of foods in addition
to the presence of pathogenic microorganisms [1,2]. A number of authors have reported that food
contamination caused by microorganisms could be attributed to the natural contamination that occurs
in raw materials [3] or the cross-contamination of foods due to different contaminated sources such as
air, water, hair, dirt, animal feces, humans, infected wounds, etc. [4].
Microbial pathogens can contaminate foods and cause foodborne diseases [5]. The Centers
for Disease Control and Prevention (CDC) in the United States has stated that either foodborne or
waterborne pathogens are considered to be the primary causative factors in 76 million cases each year
for foodborne illnesses in the United States alone [6]. The percentage of pathogenic bacteria, parasites,
and viruses was five million cases, two million cases, and thirty million cases, respectively [7,8].
Multiple conventional tests were applied to detect microbial contaminants in foods, surfaces,
utensils, and equipment. These tests included the following: viable cell counting [9], staining [10],
carbohydrate fermentation assay, enzyme linked immunosorbent assay [11], polymerase chain
reaction [12], ultraviolet detection [13], and fluorescence techniques [14]. Despite the development
of many analytical techniques using automated and complex instrumentation for monitoring and
detecting the biological contaminants in foods, there are still several drawbacks and limitations to using
these traditional approaches [8]. For example, these traditional approaches require large numbers of
samples, high skill levels, and are time consuming and costly [15,16]. In addition, most traditional
methods require a long time to obtain accurate microbiological results [17]. Consequently, in the past
few years, a lot of developed and rapid in situ methods were investigated as an alternative to the

Biosensors 2020, 10, 58; doi:10.3390/bios10060058 www.mdpi.com/journal/biosensors

Biosensors 2020, 10, 58 2 of 22

existing microbiological approaches. These methods were highly sensitive to count and evaluate food
contamination as well as the degree of cleaning and sanitizing of food contact surfaces [18].
Biosensors represent one such innovative method that has been developed to overcome some major
problems regarding food sample analysis. Moreover, the use of biosensors to monitor and provide
rapid real-time information will be superior compared to traditional microbiological approaches [19].
Adenosine triphosphate (ATP) bioluminescence, a highly effective biosensor, can be used for food
process manufacture monitoring such as HACCP (hazard analysis and critical control points) [20,21].
Bioluminescence is the mechanism of light emission from organisms and thereby reflects the chemical
conversion of energy into light. The ATP bioluminescence test is since ATP is a significant biological
source of energy found in various microbes and thus represents the presence of a living microbe [22].
Biosensor technology was developed to be a useful indicator of bacterial contamination on food
and food contact surfaces. In this review, we present the effectiveness of various forms of sensing
technologies for the detection of foodborne pathogens in food products, as well as the criteria for
industrial use of this technology. This review will also focus in detail on the application of the most
widely used biosensor types in food safety.

2. Foodborne Pathogens
In recent years, the demand for enhanced food security has gradually increased. As reported in
the media and other sources, diseases caused by bacterial contamination represent about 40% in all
infections, and the diseases due to foodborne pathogenic have a significant effect on the health of the
population as a whole as well as the economy [23].
Foodborne illnesses thus represent an enormous challenge to worldwide health care systems [24].
For example, in the US, about 48 million individuals suffer from foodborne illnesses each year resulting
in around 128,000 hospitalizations, 3000 deaths, and $15.6 billion in economic losses [25]. Because
human food and water sources can be easily contaminated by a broad spectrum of microbial pathogens,
serious illness results if these microbial pathogens or their toxins are consumed [26]. Bacteria, viruses,
and parasites are the most prevalent pathogens that cause foodborne diseases [27,28], but fungal
foodborne diseases are also identified [29]. Bacteria are the most well-known foodborne pathogen,
and cause the greatest number of foodborne illnesses, including the most hospitalizations (63.9%) and
deaths (63.7%) [25]. Bacterial contamination can cause repeating intestinal irritation, kidney disease,
mental incapacity, receptive joint inflammation, visual impairment, and even death [30]. In addition,
foodborne diseases can occur because of toxins produced either from bacteria or fungi, which may
survive even after food processing. Foods that are raw, including meat and poultry or vegetables,
fruits, eggs, dairy products, and even cooked seafood, can be contaminated with both foodborne
pathogens and their toxins [31–33]. Examples of foodborne diseases caused by pathogens in the food
matrix are shown in Table 1.

Table 1. Examples of Foodborne Diseases Caused by Microorganisms in the Food Matrix.

Symptoms and
Pathogenic Sources Food Matrix References
Illnesses
Unpasteurized Milk and Khare et al. [34]
Staphylococcus aureus Food Poisoning
Cheese Products Mostafa et al. [35]
Dairy Products, Dry
Grutsch et al. [36]
Bacillus cereus Foods, Rice, Egg Diarrhea, Vomiting
Griffiths and Schraft [37]
Products
Diarrheal Diseases and
Xu et al. [38]
E. coli O157:H7 Meat Products and Milk Producing of
Kramarenko et al. [39]
Shiga Toxins
Letchumanan et al. [40]
Vibrio parahaemolyticus Seafood Diarrhea
Jiang et al. [41]
Biosensors 2020, 10, 58 3 of 22

Table 1. Cont.

Symptoms and
Pathogenic Sources Food Matrix References
Illnesses
Stomach Cramps, Bloody
Ma et al. [42]
E. coli O26 Ground Beef Diarrhea, Vomiting and
Amagliani et al. [43]
High Fever
Meats, Eggs, Fruits, Vomiting, Diarrhea, Sharma [44]
Salmonella enteritidis
Vegetables Cramps, Fever Paramithiotis et al. [45]
Vibrio parahaemolyticus Freshwater Fish Li et al. [46]
Severe Diarrhea, Cholera
Vibrio cholerae and Shellfish Baron et al. [47]
Fresh Fruits and Mesbah Zekar et al. [48]
Klebsiella pneumoniae Pneumonia
Vegetables Ghafur et al. [49]
Postinfectious Reactive Riley [50]
Campylobacter jejuni Meat, Poultry
Arthritis Skarp et al. [51]
Human Gastrointestinal Hamad et al. [52]
Clostridium perfringens Poultry Meat
Diseases Rouger et al. [53]
Uncooked Food, Aston and Beeching [54]
Clostridium botulinum Botulism
Canned Foods Yadav et al. [55]
Gastroenteritis and Drali et al. [56]
Listeria monocytogenes Lentil Salad
Invasive Infection Vojkovska et al. [57]
Watery Diarrhea Mixed Nisa et al. [58]
Shigella sp. Poor Water Supply
with Blood and Mucous Shafqat et al. [59]
Bigoraj et al. [60]
hepatitis E virus Rabbit Meat Liver Disease
Kaiser et al. [61]
Yang et al. [62]
Salmonella Fresh Vegetables Gastroenteritis
Saw et al. [63]

3. Monitoring of Microorganism Activities in the Food Matrix

A successful microbiological environmental surveillance system can provide early warning of
possible microbiological hazards in food items, detect problems, and thereby support comprehensive
microbiological safety. Thus, for several decades, the microbiological aspects of food safety have been
intensively examined. For example, maintaining food protection has always been a very critical aspect
of government policies in some countries. Management systems have been set up to prevent harmful
contaminants from being introduced into the food chain [8]. According to the Centers for Disease
Control and Prevention (CDC), the influence of microorganisms such as bacteria, viruses, and fungi on
human life is worthy of significant attention [22]. The implementation and monitoring of microbial
food safety contributes to enhanced productivity, higher wages, sustainable development, and better
livelihoods, which is why it has been suggested that policy makers implement appropriate food safety
policies in order to enhance global nutrition and improved food security [64].
Microbial food safety is radically different from chemical food safety. Although chemical
contaminants and additives usually join the food chain at predetermined levels, microbes may join
at any point [65]. Consequently, food regulations everywhere are very straightforward on this level.
For instance, the EU General Food Law [66] states: “a high level of protection of human life and health
should be assured in the pursuit of community policies”. The microbiological safety of consumer
products is also closely linked to the hygienic properties of the manufacturing system. Under these
conditions, the implementation of adequate sanitation methods is essential for the protection of the
final product. Evaluation of the efficacy of such methods is important for the assurance of these
procedures [67]. In fact, all food safety regulations require these inspection activities. Researchers are
therefore making considerable efforts to establish rapid and effective methods to meet the requirements
of daily investigation and monitoring of food production [67].
Biosensors 2020, 10, 58 4 of 22

The requirement of monitoring contamination in the food chain involves several analytical
methods and the use of sophisticated and automated instrumentation that has been recently developed
for detection of contaminants in food [68]. However, there are still many drawbacks and limitations to
using these traditional approaches [8]. Furthermore, diagnostic tools must be capable of assessing
feasibility and flexible enough to identify the pathogen of concern. Table 2 shows a list of some
microbiological analysis approaches used to monitor food safety.

Table 2. Examples of Microbiological Analysis Approaches for Monitoring Food Safety.

Microbiological Detection Limit

Time Consumed References
Approaches (Log CFU/mL)
Rajapaksha et al. [9]
Viable Cell Counting Unlimited days
González-Ferrero et al. [69]
Sakamoto et al. [70]
Microscopy Unlimited min
Mobed et al. [71]
Hazan et al. [72]
Absorbance 8–9 Immediate
Ikonen et al. [73]
Enzyme Linked Shen et al. [74]
2.83–3 3h
Immunosorbence Preechakasedkit et al. [75]
Staining with Guo et al. [76]
3–4 26 min
Fluorescence Dyes Annenkov et al. [77]
Start Growth Time 1.60–2.60 h Hazan et al. [72]
Ou et al. [78]
Flow Cytometry 4–8 h
Adan et al. [79]
Methylene Blue Dye Bapat et al. [80]
7 h
Reduction Test Pawar et al. [81]
Isothermal Fricke et al. [82]
>2 5–7 h
Microcalorimeters Broga et al. [83]
Laser-Induced Breakdown Multari et al. [84]
1 3 min
Spectroscopy (LIBS) Moncayo et al. [85]
Fourier Transform Infrared Ellis et al. [86]
5.3 60 s
(FT-IR) Spectroscopy Johler et al. [87]
Nanoprobe-ATP 2–6 20 min Xu et al. [88]

4. Biosensors
Leland Charles Clark Jr. designed the first biosensor research instrument in 1956 using an electrode
to measure the oxygen concentration in blood. After that, scientists from different fields, such as
physics, chemistry, and material science, have come together to build more sophisticated, reliable, and
mature biosensing devices for applications in the field of medicine [89]. Several approaches using
innovative techniques for pathogen enumeration and identification in perishable and semi-perishable
foods have been identified in the last few years. In most microbiological research, quantification of
bacterial cells is necessary. Therefore, seeking cost-effective techniques with several properties is
required, namely high sensitivity, specificity, and fast responses [70,90].
The word biosensor refers to an effective and creative analytical device that has a biological
sensing function with a broad variety of applications such as food safety, environmental monitoring,
biomedicine, and drug discovery [91]. More specifically, biosensors are widely used in the identification
and detection of bacteria and have attracted great interest as one of the most efficient and accurate
methods of food analysis and food safety monitoring [92–94]. In addition, biosensors typically deliver
fast, on-site tracking and thus provide real-time details throughout the production process [95,96].
Biosensors are thus another broad class of bacteria detection method. For example, conductometric
measurements provide fast and simple bacterial detection [97].
sensing function with a broad variety of applications such as food safety, environmental
monitoring, biomedicine, and drug discovery [91]. More specifically, biosensors are widely used in
the identification and detection of bacteria and have attracted great interest as one of the most
efficient and accurate methods of food analysis and food safety monitoring [92–94]. In addition,
biosensors
Biosensors 2020,typically
10, 58 deliver fast, on-site tracking and thus provide real-time details throughout 5 ofthe
22
production process [95,96]. Biosensors are thus another broad class of bacteria detection method.
For example, conductometric measurements provide fast and simple bacterial detection [97].
Because
Because biosensors
biosensors are are analytical
analytical devices
devices forfor the
the detection
detection ofof microbial
microbial contamination,
contamination, their
their
function
function depends on the interaction between biologically active agents, the transducer, and
depends on the interaction between biologically active agents, the transducer, and aa signal
signal
conversion
conversion unit unit [98,99]. Mayer and
[98,99]. Mayer and Baeumner
Baeumner [100]
[100] clarified
clarified that
that biosensors
biosensors typically
typically contain
contain two
two
main components: a target recognition component such as receptors, nucleic
main components: a target recognition component such as receptors, nucleic acids, or antibodies acids, or antibodies and a
signal transducer that transforms target recognition into physically detectable
and a signal transducer that transforms target recognition into physically detectable signals. The signals. The internal
reflection, fluorescencefluorescence
internal reflection, resonance energy transfer (FRET),
resonance energy chemiluminescence,
transfer (FRET), bioluminescence,
chemiluminescence, and
surface plasmon resonance (SPR) have been employed as manufacturing
bioluminescence, and surface plasmon resonance (SPR) have been employed as manufacturing optical transducers in the
fabrication of biosensors
optical transducers in the[8]. In general,
fabrication biosensors[8].
of biosensors may Inbe divided
general, into threemay
biosensors basic
begroups
dividedbased
into
on the type of transduction element: optical biosensors, mechanical biosensors,
three basic groups based on the type of transduction element: optical biosensors, mechanical and electrochemical
sensors
biosensors,[22].andAn electrochemical
example of different components
sensors of biosensors
[22]. An example used incomponents
of different food analysisofisbiosensors
shown in
Figure
used in1.foodMany compounds,
analysis is shownsuchinasFigure
bacterial antigens,
1. Many toxins, microbial
compounds, such ascontaminated by-products,
bacterial antigens, toxins,
or spoilage precursors, could be easily detected using biosensors for
microbial contaminated by-products, or spoilage precursors, could be easily detected using the rapid analysis of food
deterioration and food quality [101].
biosensors for the rapid analysis of food deterioration and food quality [101].

Diagram showing the different components of a biosensor used in food analysis.

Figure 1. Diagram analysis.

4.1. Types of Biosensors

Biosensors are categorized into various groups depending on their working principles (Figure 2).
Examples of biosensors include electrochemical, mechanical, biological, acoustic sensors, surface
plasmon resonance (SPR), and optical biosensors. Three of the most important biosensors are
discussed below.
 Biosensors 2020, 10, x FOR PEER REVIEW 6 of 23

4.1. Types of Biosensors

Biosensors are categorized into various groups depending on their working principles (Figure
2). Examples of biosensors include electrochemical, mechanical, biological, acoustic sensors, surface
Biosensors 2020, 10,plasmon
58 resonance (SPR), and optical biosensors. Three of the most important biosensors are 6 of 22
discussed below.

Figure 2. Schematic
Figure 2. Schematic representation
representation ofofvarious
various combinations of physical
combinations ofand biological and
physical elements of
biological elements
biosensors.
of biosensors.
4.1.1. Optical Biosensors
4.1.1. Optical Biosensors
Optical biosensor methods characterized by high sensitivity, simple handling, and rapid
detection have been used extensively to identify very large numbers of bacteria [102]. Optical
Optical biosensor methods characterized by high sensitivity, simple handling, and rapid detection
biosensors enable visualization of microbial activities in food with the naked eye. The alteration in
have been used theextensively to identify
transduction surface very
due to cell largebynumbers
connection of bacteria
means of direct binding or[102]. Optical biosensors enable
ligand identification
assists in active analyte detection. Ivnitski et al.[103] demonstrated that optical biosensors may
visualization of microbial activities in food with the naked eye. The alteration in the transduction
distinguish microbes in food through either in situ detection in the refractive index or by means of
surface due to the
cellthickness
connection by means
that develops of direct
as bacterial binding
cells attach or ligand
to receptors identification
on the transducer assists
surface [103]. The in active analyte
opticalet
detection. Ivnitski biological
al. [103] sensor contains a biodegradable
demonstrated that optical polymer by analytical
biosensors mayenzymes secreted bymicrobes in food
distinguish
microorganisms during the deterioration of the natural product. As the number of bacteria
through eitherincreases,
in situthere
detection insecretion
is increased the refractive
of enzymesindex orfood
that cause by degradation,
means ofwhich the thickness
will be visiblethat develops as
bacterial cells attach to receptors on the transducer surface [103]. The optical biological
with the degradation of the polymer [104]. Colorimetric, fluorescence, chemiluminescence, and sensor contains
surface plasmon resonance (SPR) are the principal optical techniques employed [105]. Newly
a biodegradable polymer by analytical enzymes secreted by microorganisms during the deterioration
created biosensors for the identification of microbial contamination in food items are shown in
of the natural product.
Table 3. As the number of bacteria increases, there is increased secretion of enzymes that
cause food degradation, which will be visible with the degradation of the polymer [104]. Colorimetric,
fluorescence, chemiluminescence, and surface plasmon resonance (SPR) are the principal optical
techniques employed [105]. Newly created biosensors for the identification of microbial contamination
in food items are shown in Table 3.
Alamer et al. [105] developed an immunoassay with sandwich to diagnose pathogenic bacteria in
poultry such as Salmonella Typhimurium, Staphylococcus aureus, Salmonella enteritidis, and Campylobacter
jejuni. Immobilized lactoferrin on a cotton swab was employed to pick up the bacterial contamination on
the surface of the chicken, accompanied by a sandwich immunoassay formulated with a different antibody
coupled with colored nano-beads. The form and concentration of the present microorganism defined
the color and strength of the cotton swab [105]. Several plant pathogens including the cucumber mosaic
virus [106], Pantoea stewartii [107], plum pox virus [108], Prunus necrotic ringspot virus [109], citrus tristeza
virus [110], and potato virus [111] have already been detected using various optical biosensors. SPR
biosensors have been used to successfully identify and detect cowpea mosaic virus, tobacco mosaic
virus, lettuce mosaic virus, Fusarium culmorum, Phytophthora infestans, and Puccinia striiformis [112].

4.1.2. Electrochemical Biosensors

Electrochemical biosensing techniques are among the most employed platforms for detection of
foodborne pathogens [113]. Electrochemical biosensors have been reported to be successful techniques
for bacterial detection due to their low cost, accuracy, miniaturization capacity and ability to detect
changes directly based on the interaction between the sensor and sample. However, the time required
Biosensors 2020, 10, 58 7 of 22

to detect food contamination using electrochemical biosensors has significantly decreased with the
advancement of new methods, some of which require as little as 10 min [19]. Electrochemical
biosensors are categorized according to the various electrical signals produced by the existence of
targets into impedimetric, potentiometric, amperometric, electrochemiluminescent, voltammetric, and
conductometric methods [114].
During the last decade, exponential development in electrochemical biosensors has been observed
for analysis of food and beverages and to identify genetically modified organisms (GMOs) in
food [19]. Chen and colleagues recently established and developed polyaniline- carbon nanotubes
(CNTs) as a redox nanoprobe connected to a signal probe to enhance the electrochemical signal for
Mycobacterium tuberculosis detection [115]. A single-walled carbon nanotube (SWCNT) biosensor
was successfully immobilized with a polyclonal antibody to detect Yersinia enterocolitica in Kimchi
solutions with a low detection of 4 log CFU/mL [116]. The disposable potentiometric paper-based
biosensor was designed to detect of Salmonella Typhimurium. In the first step, the combination from
ethylenedioxythiophene:polystyrene sulfonate was coated on filter paper. Next, antibodies to the
target bacteria were covalently attached to filter paper. A linear range of 4.07 log CFU/mL was
recorded, with a detection limit of 0.698 log CFU/mL. Less than 5 min was sufficient to perform the
analysis and obtain the results [117]. Similarly, Silva and coworkers developed another approach for
Salmonella Typhimurium detection in apple juice using a potentiometric biosensor conjugating on a gold
nanoparticle polymer inclusion membrane, and a detection limit of 6 cells/mL was achieved [118].

4.1.3. Mechanical Biosensors

Mechanical biosensors can measure a mass sensitive sensor surface deflection because the target
analytes will be bonded on the functionalized surface [119]. Mechanical biosensors are typically
classified into four broad groups according to the sensor-analyte chemical interactions: affinity-based
assays, fingerprint assays, separation-based assays, and spectrometric assays [120]. Quartz crystal
microbalance (QCM) is a mechanical biosensor that is widely used due to its capacity to track shifts
in mass in sub-nanogram amounts. The change in mass using QCM biosensors is recognized by the
resonant frequency of quartz crystal, and this technique is commonly used with extreme sensitivity
for quantification of the whole cell of microorganisms [121]. Bayramoglu et al. [122] designed A
QCM-aptasensor to isolate and rapid detect Brucella melitensis in milk and milk products. The aptamer
was immobilized on magnetic nanoparticles and the QCM chip for the quantitative detection of
B. melitensis with high specificity. The QCM biosensor detection limit for determination of B. melitensis
was 3 log CFU/mL [122].
Lectins were employed and immobilized as a recognition element on the surface of the QCM
chip to detect the foodborne pathogen Campylobacter jejuni. The limit of detection was 3 log CFU/mL.
A modified strategy was utilized to improve the sensitivity of the assay by Masdor et al. [123] who
detected E. Campylobacter jejuni based on the inclusion of antibody conjugated gold nanoparticles.
The limit of detection was enhanced and found to be 2.17 log CFU/mL because the gold nanoparticles
exhibited mass amplification effects. Several other studies were successfully employed to develop
a novel sensor based on a quartz crystal microbalance with dissipation to detect the most widely
spread mycotoxins in red wine called ochratoxin A. The method described here was fast, sensitive, and
cost effective, and the analysis time was less than one hour. A limit of detection of 0.16 ng/ml was
attained with an excellent linear range between 0.2 and 40 ng/ml [124]. The most advanced mechanical
biosensors for the identification of microbial contamination in food items are shown in Table 3.
Biosensors 2020, 10, 58 8 of 22

Table 3. Newly Created Biosensors for the Identification of Various Contaminants in Food Items.

Consuming
Type of Sensor Contaminant Food Items Detection Limit Reference
Times
Optical Biosensor
Listeria
Chemiluminescence Milk 1.1 log CFU/mL 40 min Shang et al. [125]
monocytogenes
Cronobacter Powdered Kim et al. [126]
Colorimetric 3.85 log CFU/mL 30 min
sakazakii Infant Shukla et al. [127]
localized Surface Plasmon Salmonella
Pork Meat 4 log CFU/mL 30–35 min Oh et al. [128]
Resonance (LSPR) typhimurium
Zaraee et al. [129]
Interferometric Escherichia coli Buffer 0.34 log CFU/mL 2h
Janik [130]
Surface Plasmon Mudgal et al. [131]
Pseudomonas Water 7.09 log CFU/mL 25 min
Resonance (SPR) Zhang et al. [132]
Mechanical Biosensor
Multi-Channel Series
Mycobacterium Ren et al. [133]
Piezoelectric Guartz Buffer 1 log CFU/mL 1 day
tuberculosis He et al. [134]
Crystal (MSPQC)
Quartz Crystal Ozalp et al. [135]
Salmonella Milk 2 log CFU/mL 10 min
Microbalance (QCM) Farka et al. [136]
Campylobacter Wang et al. [137]
QCM Poultry 1.30 log CFU/mL 30 min
jejuni Masdor et al. [138]
Staphylococcus Pohanka [139]
QCM Buffer 7.41 log CFU/mL 1 day
aureus Noi et al. [140]
Electrochemical
Staphylococcus Zelada-Guillén et al. [141]
Potentiometric Pig skin 2.90 log CFU/mL 2 min
aureus Arora et al. [142]
Salmonella Sheikhzadeh et al. [143]
Impedimetric Apple Juice 0.47 log CFU/mL 45 min
Typhimurium Bagheryan et al. [144]
Streptococcus Vásquez et al. [145]
Amperometric Fish 1–7 log CFU/mL 90 min
agalactiae Arachchillaya [146]
Electrochemical Chemiluminescence (ELC) Biosensors
Aptamer-Based ECL Luria–Bertani
Escherichia coli 0.17 CFU/mL 40 min Hao et al. [147]
Sensors Broth
Vibrio
ECL Immunosensor Seafood 0.69 log CFU/mL 1h Sha et al. [148]
parahaemolyticus
Paper-Based Bipolar Listeria
Buffer 10 copies/µL 10 s Liu and Zhou [149]
electrode ECL monocytogenes
Photoelectrochemical Biosensors
label-Free
Photoelectrochemical Bisphenol Milk 0.5 nM 90 s Qiao et al. [150]
Aptasensor
Tungsten Disulfide (WS2)
Nanosheet-Based Chloramphenicol Milk Powder 3.6 pM 105 min Zhou et al. [151]
Photoelectrochemical
Visible-Light
Photoelectrochemical Sulfadimethoxine Milk 0.55 nM 50 s Okoth et al. [152]
Aptasensing

5. Bioluminescence Methods for Detection of Food Contamination

The overall number of microbes is normally calculated using colony plate counts, dilution methods,
methods of contact plate and swab, or techniques of membrane filtering. These methods produce
repeatable findings that reflect the microbiological contamination. However, the long incubation time
of the sample (up to 72 h for bacteria; up to 5 days for fungi) does not allow for rapid correction
within one technical process, so for this purpose, tests to estimate the amount of bacteria need to be
added quickly [153]. Consequently, Sharpe et al. [154] proposed utilizing the ATP test dependent on
bioluminescence. This approach is becoming increasingly common in HACCP program in situ hygiene
monitoring. Its principal benefit is the identification of microbial and chemical pollutants within a
few minutes.
Biosensors 2020, 10, 58 9 of 22

Recent developments in bio-analytical instruments have allowed for using the capacity of certain
enzymes to release photons as a by-product of the enzymes’ reactions. This effect is known as
“bioluminescence”, which can be used to identify the cells’ activity. This technique provides results in a
short time and is among the latest technologies for rapid microbiological results [155]. Bioluminescence
plays an important role in real-time process monitoring due to the emission of bright light by living
microorganisms. Some study results also demonstrated that metal ions, heavy metals, phosphorus,
naphthalene, genotoxicants and chlorophenols were detected by employing bioluminescence-based
biosensors [156]. The bioluminescent organisms in nature are broadly distributed and include a wide
remarkably different of species. Among the organisms that emit light are bacteria, dinoflagellates,
fungi, fish, insects, shrimp, and squid. The enzyme luciferase is responsible for catalyzing the
bioluminescence reactions that occur in these organisms, and in certain instances the substrates are
referred to as luciferins. Bioluminescence is very effective when used for fast spot tracking because
tests are obtained in less than 15 minutes [157]. This procedure has been used on several food items
including fresh and pasteurized dairy products [158], meat and poultry products [159], beer [160], and
fruit products [161].
Sanitizing programs and hazard analysis and critical control point (HACCP) programs can be
achieved in the food processing industry by using the common bioluminescence method of adenosine
triphosphate (ATP). Bioluminescence assays and the identification of bacterial adenosine triphosphate
(ATP) are strong predictors of the occurrence of food contamination in meat, poultry and dairy products
and the cross-contamination of surfaces [162]. All living organisms use ATP to store energy. ATP acts
as a chemical energy storage unit for free energy that is emitted through catabolism and thereafter
used for anabolic processes [163]. The amount of ATP specifically reflects the presence of metabolic
cells and can be used to count viable living cells in samples. This is because there is a linear association
between the total number of available ATP molecules and the total number of colony-forming units,
especially in bacteria and yeast [164].
The relationship between microbial biomass and intercellular ATP can be used to quantify the
total number of microorganisms in food items. Recent studies have shown that the amount of ATP
present in a cell differs based on the species and growth states of microorganisms. For instance, the
extracellular ATP present in Acinetobacter junii and Pseudomonas aeruginosa at an incubation time of
6 h was 255.2 ± 56.8 nM/OD and 25.5 ± 1.1 nM/OD, respectively [165]. Xu et al. [88] developed the
traditional ATP fluorescence detection system by using a rapid detection system based on a nanoprobe
and graphite electrode coupled with ATP bioluminescence technology for Escherichia coli detection
in food. With this new approach, the researchers were not only able to use the probe to capture and
enrich Escherichia coli via an antibody–antigen reaction, they were also able to enrich ATP using an
electric field generated by the graphene transparent electrode (GTE) in order to improve the accuracy
of the system. This method resulted in the successful generation of a linear correlation coefficient
of up to 0.972 compared to other traditional methods and satisfied the design criteria. The analysis
was obtained within 20 min. The system was able to detect the total bacteria count in the range of
2–6 log CFU/mL, and its precision has a CV of 4.2%, indicating good reliability and repeatability [88].
Moreover, Fan and colleagues confirmed the possibility of developing a bioluminescence-based
ATP assay using antibacterial peptide-coated magnetic spheres to distinguish Gram-positive G+ bacteria
from Gram-negative G− bacteria. The authors obviously found the conventional bioluminescence-based
ATP cannot distinguish G+ bacteria from G− ones since ATP can be released from both bacterial cells.
The results exhibited a linear range for G+ bacteria between 3.36 and 7.07 log CFU/mL, and the limit of
detection was 2.34 log CFU/mL within 33 min [166].

6. Principle of Bioluminescence Based-ATP Determination

Adenosine triphosphate is the main activated energy carrier of all living cells in nature, including
bacteria, mold, yeast, and algae [167]. ATP levels can also be used as a criterion for microbial activity
measurement. ATP bioluminescence is based on a biochemical reaction catalyzed by the enzyme [168].
Biosensors 2020, 10, 58 10 of 22

The reaction is catalyzed by the luciferase enzyme conversion of luciferin to oxyluciferin in the
presence of oxygen (O2 ) and magnesium cation (Mg++ ), and ATP adenosine triphosphate is converted
to adenosine monophosphate (AMP) with the emission of light [169]. The intensity of light in the
luminescence reaction is expressed in relative light units (RLU). The reaction between ATP and luciferin
and luciferase complex is described according to the following equation:
.
luci f erase, Mg+2
Luciferin + ATP + O2 −−−−−−−−−−−−−→ Oxyluciferin + AMP + prodcuts + light (1)

This light output from the breakdown of cellular ATP by the bioluminescence reaction can be
measured using sensitive photons of light meters in an instrument called a luminometer. The greater the
amount of ATP will present, the higher amount of light produced by the APP assay test; consequently,
the greater the RLU level produced. ATP bioluminescence has often been used for the investigation
of microbial contamination of food contact surfaces and for measuring the efficiency of cleaning
procedures. It is a simple and rapid method that provides results within minutes compared to
conventional methods, which typically take 24–48 h. Libudzisz and Kowal and [170] stated that on the
bacterial cell possesses approximately 1 ATP femtogram. Based on the species, physiological status or
metabolic function of microorganisms, the concentration will vary from 0.1 to 5.5 fg/cell. Luo et al. [171]
claimed that the average concentration of ATP in a cell is approximately 0.47 Cell fg. To determine the
number of microbes in each sample, it is presumed that 1 pg of ATP is equal to 1000 bacterial cells.
Table 4 below shows the content of ATP (fg/cell) in some bacterial, mold, and yeast cells.

Table 4. The Content of ATP (fg/cell) in Some Bacterial, mold and Yeast Cells.

Microorganisms ATP (fg/Cell) References

Campylobacter jejuni 1.7 Ng et al. [172]
Yeast 100 Miller and Galston [173]
Lactobacillus sp. 2.0–2.2 Libudzisz and Kowal [170]
Pseudomonas fluorescens 0.6 Pistelok et al. [174]
Escherichia coli 1 Libudzisz and Kowal [170]
Bacteria Mixture 1 Miller and Galston [173]
Lactobacillus acidophilus 0.33 Nelson [175]
Campylobacter coli 2.1 Ng et al. [172]

7. Applications of Bioluminescence Based ATP in the Food Industry

7.1. Hygiene Monitor

The efficacy of ATP-based bioluminescent assays is enhanced due to their ability to provide rapid
results that indicate the existence or absence of certain biological contaminants in real time [176].
ATP bioluminesce assays are widely used in the food industry for estimating the cross-contamination of
surfaces and products through swabbing. This type of application enables results within 5 min
that are just as accurate as those obtained using traditional techniques. The levels of overall
surface contamination can be indicated successfully because ATP from all microbial sources will
be detected [177]. The time of bacterial viability on certain kitchen surfaces ranges between four and
24 h. Therefore, during food preparation it is necessary to design appropriate hygienic protocols such as
proper washing and disinfection to control and avoid microbial risks. The ATP test thus helps to quickly
verify that surfaces are clean and properly disinfected. In addition, this method does not pose a threat
to humans [178]. However, because raw materials of plant or animal origin increase ATPs, the test
results can be overstated. About cleanliness and hygiene, it is not known yet whether microorganisms
or traces of biological content are found throughout the work and the production equipment by
Biosensors 2020, 10, 58 11 of 22

measuring only the ATP [179]. In this case, the values are usually dependent on the relative light units
(RLU) rather than the concentration of ATP collected. The findings are correlated with the previously
defined baseline levels for the industry and the individual measurement points. Low RLU rates would
mean that the measurement point is safe and clear of chemical and microbiological contaminants,
while high RLU levels would be indicative of points of contamination [179]. In a study conducted
by Rodrigues et al. [180], the relationship between the values of ATP-bioluminescence and the extent
of microbial contamination was estimated according to traditional methods in order to evaluate the
cleanliness of the cutting surfaces in the poultry slaughterhouse [180]. Their findings confirmed
that that there was a linear relationship between the microbial content using conventional methods
and the bioluminescent ATP approach. Using the bioluminescent ATP detection system, extremely
low contamination rates can be identified in seconds, enabling a rapid assessment of the surface
hygiene [180].
Despite rapid hygiene monitoring using ATP tests, recent studies by Bakke and Suzuki [181] who
reported that ATP could be hydrolyzed by heat treatment, acidic factors or alkaline conditions to ADP
and AMP. Consequently, the values of collected RLU will not be accurate. Bakke and Suzuki [181] have
developed a novel hygiene monitoring based on the detection of total adenylate (A3) in a wide variety
of foods such as fermented foods, dairy, vegetables, meat, nuts, seafood, and fruits. After thorough
washing with detergent and rinsing the stainless steel, the amount of collected RLU of A3 was 200.
In contrast, less than 200 RLU was seen on a traditional ATP system. In conclusion, the A3 assay seems
to be a successful approach and more sensitive for detecting adenylates from food residues that are not
identified by traditional ATP assays [181].

7.2. Milk and Dairy Products

The shelf life of milk depends on its initial microbial load, the form and distribution of microbes,
and how well such microbes grow under different storage conditions. Conventional qualitative and
quantitative methods were applied in microbiological analysis of food to detect microbial contamination
using a selective media, non-selective media and biochemical screening [182]. These approaches
are time-consuming and require additional confirmation and interpretation by qualified technicians,
which can take several days. Therefore, an alternate, fast, efficient, and lower cost method for
real-time identification of milk spoilage is warranted [183]. Recently, the bioluminescence-based
ATP technique has been developed to monitor the presence of microorganisms and can easily be
applied to determine both somatic cell counts (SCC) and microbial counts for controlling raw milk
production quality [178,184]. After treatment with a non-ionic detergent, an indication of the somatic
cell concentration in milk can be obtained from the ATP concentration level. This result can be
considered as an indicator for infection with mastitis [178]. Indeed, Moore et al. [185] reported that
ATP bioluminescence procedures were performed in 5–10 min to detect as few as 4 log CFU/mL of
milk bacteria which undoubtedly resulted in faster and better-informed decisions regarding the status
of incoming milk tankers the milk processing industries.
Other studies have examined the use of the bioluminescence -based ATP technique compared
to total bacterial count (TBC) cultivation for rapid microbial identification to monitor ultra-high
temperature (UHT) milk quality [186]. ATP bioluminescence was suitable for detecting very low
concentrations of microbial content compared to results for conventional total bacterial counts,
and the analysis time was only 20 min. Similarly, Lomakina and others used a bioluminescence
ATP assay to ascertain the quality of milk within 20 min with a detection limit of approximately
1.11 log CFU/mL [168].

7.3. Meat and Meat Products

Meat and meat products can be used effectively as rich media for growing several microflora
(bacteria, yeasts, and molds), some of which are pathogens [187]. The ATP bioluminescence method
was used to monitor the microbial content of meat. The study reported that there was a significant
Biosensors 2020, 10, 58 12 of 22

correlation between the content of ATP and total bacteria counts of vacuum-packed cooked cured meat
products, and a detection limit of 5–6 log CFU/g was sufficient for screening purposes [188]. Similarly,
Siragusa and colleagues established a quick ATP assay to quantify total bacteria counts in beef and
pork carcasses in commercial food industries and to compare findings with the standard method
of viable plate counts using correlation analysis [189]. The results of this research showed that the
correlation coefficient between the conventional microbiological assay and the ATP method was 0.91
for beef and 0.93 for pork carcass samples. The ATP test applied linearly to microbial contamination
rates > log 2.0 aerobic CFU/cm2 in carcasses of beef and > log 3.2 aerobic CFU/cm2 in carcasses of pork.
The ATP test including sampling took approximately 5 min [190].
However, one concern with this approach is the presence of ATP in meat and in all living cells.
Therefore, ATP must be destroyed before an ATP bioluminescence method can be performed to measure
only the microbial ATP produced [190,191]. Hence, Cheng et al. [190] conducted an experiment to
combine an ATP bioluminescence assay with functional magnetic nanoparticles (FMNPs) for rapid
isolation and detection of Escherichia coli from artificially contaminated ground beef. To release the
target bacterial ATP in the presence of luciferin–luciferase mechanism, immune particles were used to
precisely capture and separate the bacteria to generate the luminescence signal. E. coli bacteria can be
calculated with a detection limit of 1.30 log CFU/mL in the range of 1.30–6.30 log CFU/mL. The whole
process used to identify E. coli took approximately 1 h. The range of identification and assay time
obtained in this study has been shown to be superior to that of other techniques [190].

7.4. Fish and Fish Products

For more than 50 years, ATP and associated compounds have been used for the quality evaluation
of fish and shellfish [192]. Bioluminescence is the production and release of light by a living entity
and exists commonly in aquatic vertebrates and invertebrates. Shim et al. [193] measured the ATP
content in the muscle of olive flounder (Paralichthys olivaceus) by calculating the intensity of light
released using luciferase provided by American fireflies. The findings of bioluminescence were nearly
equal to high-performance liquid chromatography (HPLC). Indeed, the results of the study showed
a high correlation of r2 = 0.98 between luminometer-measured RLU and HPLC-based ATP content.
Tanaka et al. [194] have established a bioluminescence system for the identification of AMP in the
Atlantic bonito (Sarda sarda). Polyphosphate (polyP)-AMP phosphotransferase (PPT) and adenylate
kinase (ADK) were utilized from the Acinetobacter johnsonii strain conjugated with firefly luciferase.
With this approach, the researchers were able to identify high-sensitivity AMP in food residues [194].
Regarding the evaluation of different microbiological methods, Gram [195] found that the correlation
between bacterial ATP levels and plate counts was 0.97–0.99 for four fish species. During storage
trials, the ratio of bacterial ATP to total count bacteria remained constant and did not vary significantly
among fish species [195]. As the amount of ATP per cell varies based on nutritional conditions, stress,
etc., it is advised that a standard curve for each specific product be generated [196].
Other experiments conducted by Miettinen et al. [197] reported the presence of Listeria in 28 fish
processing factories and the extent of surface contamination utilizing specific approaches such as total
aerobic heterotrophic and enterobacteria, yeast and mold tests and ATP levels. ATP tests and the
total bacteria contact agar slide methods were negatively associated (r = 0.21). However, for both
methods, 68 percent of the samples were rated as decent to fair or unacceptable. The microbiological
limit of 1 RLU using an ATP assay was exceeded in 43.3% of the samples. The results of this study
confirmed that the ATP system recognized 18.1% of the samples that were considered contaminated
per the results of the contact agar slide process, and 13.6% of the samples allowed by the contact agar
slide system were rejected by the ATP process [197].

8. Advantages and Disadvantages of ATP Bioluminescence

ATP bioluminescence provides a better image of the reaction to the contaminant by presenting
physiologically relevant data. Bioluminescence is fast and simple to calculate, resulting in the in-situ
Biosensors 2020, 10, 58 13 of 22

detection of a wide range of microorganisms. The bioluminescent sensors of whole cells have
benefits over conventional approaches by being faster, more cost effective, easy to carry out and less
labor-intensive [198]. While not an alternative to traditional approaches, an ATP-bioluminescence-assay
can also be a valuable tool for determining the efficacy of environmental cleanliness procedures even
with very low microbial counts [199]. Moreover, bioluminescent techniques often possess several
benefits compared to fluorometric techniques mainly because no wavelength of excitation is required
for the representation of light. In addition, unlike the fluorescent labeling of bacterial species, there is a
total energy reliance on the emission of bioluminescents, which enables the capability to distinguish
between living and dead cells. Consequently, bioluminescence is a highly valuable instrument for
regulating in situ microbial deterioration and is thus a desirable tool for hygiene efficacy [200].
Luminescent approaches often pose some general disadvantages. The most significant
disadvantage is the quenching of released light, which negatively influences measurements. The sum
of light determined photometrically may be greatly decreased by molecules from the biological samples.
However, the biological samples produce certain luminescent non-microbial substances that increase
the intensity of the measured light. Bacterial bioluminescent assays are thus capable of being a liability
in the food microbiology industry. For example, the results of bacterial bioluminescent assays can be
false negatives or false positives by using phage or plasmid host ranges that are either too specific
or too extensive [177]. Another disadvantage of bacterial bioluminescent assays is their unreliability
about efficiently identifying gram-negative bacteria due to the incomplete lysis of the cells [201].

9. Conclusions and Future Directions

Developing biosensors with the necessary properties for reliable and effective use in routine
applications is challenging. Despite the great effort spent on the development of various types of
biosensors over the past few years, only a few for bacterial detection are commercially available or are
approaching commercialization. Requirements for ideal sensors include the specificity to distinguish
the target bacteria in a complex food product, sensitivity to detect bacteria directly, and the ability to
provide real-time results within a reasonable time. Detection of pathogen or toxic chemicals in food
matrix is not a simple and rapid approach. Indeed, it requires additional preparation steps before
detection. This includes sample preparation and harvesting the target microbial cells or chemical.
The development of any rapid biosensors for detection of pathogens also relies on the type of food
products and the nutrients present in these products, such as fat, proteins, and fibers. Hence, there
might be a need to develop a specific sensor for each food product or specific analytical tools and
sampling methods.
This review highlights potentially reliable biosensor methods to expand research in this area and
to address the need for the development of more economical and cost-effective methods. In addition,
there is a need to develop a portable bioluminescence-based ATP unit that can be utilized on farms to
detect pathogens on the surface of fresh produce. Moreover, such biosensors should provide reliable
results in addition to being easy and simple to use without the need for consumer training.

Funding: This research received no external funding.

Acknowledgments: The authors are thankful to the Department of Food Science, College of Agriculture, University
of Basrah for providing all assistance to complete this review.
Conflicts of Interest: The authors declare no conflict of interest.

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