sensors

Review
Applications of Nanotechnology in Sensor-Based
Detection of Foodborne Pathogens
Harsh Kumar 1 , Kamil Kuča 2, * , Shashi Kant Bhatia 3 , Kritika Saini 1 , Ankur Kaushal 4 ,
Rachna Verma 5 , Tek Chand Bhalla 6 and Dinesh Kumar 1, *
1 School of Bioengineering & Food Technology, Shoolini University of Biotechnology and Management
Sciences, Solan 173229, H.P., India; microharshs@[Link] (H.K.); sainikritika@[Link] (K.S.)
2 Center for Basic and Applied Research, Faculty of Informatics and Management, University of Hradec
Kralove, Hradec Kralove 50003, Czech Republic
3 Department of Biological Engineering, College of Engineering, Konkuk University, Seoul 143-701, Korea;
shashikonkukuni@[Link]
4 Centre of Nanotechnology, Amity University, Manesar, Gurugram, Haryana 122413, India;
ankur.biotech85@[Link]
5 School of Biological and Environmental Sciences, Shoolini University of Biotechnology and Management
Sciences, Solan 173229, H.P., India; rachnaverma@[Link]
6 Department of Biotechnology, Himachal Pradesh University, Summer Hill, Shimla 171005, H.P., India;
bhallatc@[Link]
* Correspondence: [Link]@[Link] (K.K.); dineshkumar@[Link] (D.K.)




Received: 11 March 2020; Accepted: 30 March 2020; Published: 1 April 2020


Abstract: The intake of microbial-contaminated food poses severe health issues due to the outbreaks
of stern food-borne diseases. Therefore, there is a need for precise detection and identification of
pathogenic microbes and toxins in food to prevent these concerns. Thus, understanding the concept
of biosensing has enabled researchers to develop nanobiosensors with different nanomaterials and
composites to improve the sensitivity as well as the specificity of pathogen detection. The application
of nanomaterials has enabled researchers to use advanced technologies in biosensors for the transfer of
signals to enhance their efficiency and sensitivity. Nanomaterials like carbon nanotubes, magnetic and
gold, dendrimers, graphene nanomaterials and quantum dots are predominantly used for developing
biosensors with improved specificity and sensitivity of detection due to their exclusive chemical,
magnetic, mechanical, optical and physical properties. All nanoparticles and new composites used in
biosensors need to be classified and categorized for their enhanced performance, quick detection, and
unobtrusive and effective use in foodborne analysis. Hence, this review intends to summarize the
different sensing methods used in foodborne pathogen detection, their design, working principle and
advances in sensing systems.

Keywords: nanotechnology; nanomaterials; safety; sensor; foodborne pathogens

1. Introduction
Nanotechnology is the science to understand the matter at a nanoscale dimension, generally
ranging between 1 and 100 nm. This technology involves the fabrication, manipulation, study of
technique, material, modes and use of nano-devices in various applications. Nowadays, nanotechnology
is extensively used in developing biosensors using different types of nanocomposite [1–3]. The different
nanomaterials used in nanotechnology display unique features including chemical, physical and
surface effects because of their dimensions and tolerances to sizes less than 100 nanometers.

Sensors 2020, 20, 1966; doi:10.3390/s20071966 [Link]/journal/sensors

Sensors 2020, 20, 1966 2 of 19

Every year globally, contaminated food is responsible for 420 000 deaths and 600 million cases of
food-borne infection. According to WHO, approximately 30% of death occurs among children (≤5 years)
due to foodborne disease [4]. The established microbial culture methods may help in the detection of a
single specific bacterium, but this procedure takes a few days for results, and in many instances these
methods do not produce considerable data. By using nanotechnology-based methods, the pathogenic
bacteria present in complex food products can be detected with high sensitivity and specificity as
compared to the conventional methods [5–7]. A biosensor is a device in which a biological element
(i.e., an antibody, receptor, nucleic acid, or other biorecognition element) interacts with an analyte and
the response thus generated is transformed into an electrical signal by a transducer. The response of
biosensors is highly specific, quick, free from interference, and has low limits for detection, but still the
non-targeted microorganisms can interfere with the operations of biosensors.
The development of many signal transduction technologies using nanomaterials in biosensor is
transforming the field of biological and chemical analysis to empower in vivo studies. In microbial
detection, highly fascinating and promising outcomes have been produced in research using
nanotechnology. The characteristics of nanomaterials with high surface permeability, higher surface to
volume ratio, reactivity, and high penetrability allow less material and substrate usage and as compared
to large size materials, they work more efficiently in physical and chemical reactions [8]. A high
advantage of establishing a small automated system was worked out for the use in field with rapid and
cost-effective microbial detection, and sensitive stick tests were developed by using gold nanoparticles
with high specificities for the same [9–11]. This review highlights the effectiveness of nanomaterials for
developing biosensors, especially for detecting the microbial pathogens present in contaminated food.
The first section of this review describes the various properties of the nanomaterials used for sensing
applications, and the safety issues and guidelines issued by various organizations for use at workplace
or in laboratories. The other section discusses the utilization of nanomaterials and present status of
sensors used for the detection of foodborne pathogens in various food matrixes.

2. Criteria for Selection of Nanomaterials for use in Biosensors

Nanosensors are generally used for the measurement of biological response output quantity as
well as for conversion of biological response into output signals for further interpretation and analysis.
The selection of nanomaterial used in various biosensing applications is dependent on its properties
(Table 1).
Sensors 2020, 20, 1966 3 of 19

Table 1. Properties, and synthesis of different types of nanomaterials used in sensors fabrication and other applications.
Nanomaterials Physical Properties Synthesis Applications Ref
Redox activity
Sensing: electronic devices and electrochemical sensing
Surface-enhanced Raman scattering (SERS)
Gold Solution-based approaches Therapeutics: drugs delivery [12]
Surface Plasmon resonance (SPR)
Imaging: cell imaging, target tumor specific antigens
Fluorescence quenching
Biomedical applications: artificial implants, tissue engineering,
Equilibrium structure cancer cell identification and drugs and genes delivery
Lattice constant viz lattice parameter, density, Electrochemical devices: supercapacitors and electromechanical
interlayer spacing Chemical vapour deposition technique actuators used in robots and hybrid electric vehicles
Carbon Nanostructures Optical properties viz fundamental gap Laser- ablation technique Hydrogen storage: fuel cells that powers electric vehicles and [13,14]
Electrical transport Carbon arc-discharge technique laptop computers
Thermal transport Field emission devices: lamps, gas discharge tubes, microwave
Elastic behaviour generators
Sensors and Probes
Co-precipitation
Microemulsion Industrial applications: used as synthetic pigments in ceramics,
Magnetic effect due to spinning electric- charged Thermal decomposition paints and porcelain
particle Solvothermal Biomedical applications: used in vivo to destroy the pathological
Critical size depends on magnetic saturation, Sonochemic cells by hyperthermia, drugs delivery, NMR imaging,
Magnetic Nanoparticles [15]
strength of crystal, exchange forces, surface energy, Microwave assisted bioseparation of specific biological entities from their native
and shape of the particles Chemical vapour deposition environment
Zero coercivity Combustion synthesis Environmental applications: removal of organic and inorganic
Carbon arc pollutants
Laser pyrolysis
Optical properties viz bright emission, Light- emitting applications: multicolour silicon-based light
Pulsed laser ablation
photostability, size dependent and wavelength emission diodes
Heating degradation
tuneable luminescence and long fluorescence Energy and Electronic fields: lithium battery, solar cell battery,
Silicon Nanomaterials Ball milling [16]
Electronic properties viz quantum confinement, Microwave assisted
Chemical synthesis
type of dopant, composition of material, surface filed-effect transistor
Electrochemical etching
functionalization and post treatment Photocatalysts
Membranes and Coatings: gas transport, water treatment
Mechanical properties to enhance the strength Stimuli-responsive materials: humidity actuation, thermal/light
Electrical properties include high electron mobility Bottom-up approach responsive actuation, electrochemical actuation, multi-stimuli
Graphene oxide [17]
and electrical conductivity Top-down approach actuation
Thermal properties Corrosion resistance
Energy storage: lithium ions batteries, supercapacitors
Low viscosity
High solubility and miscibility due to many chain Biomedical field: drugs and genes delivery, photodynamic
ends Divergent method therapy, enhancing drug solubility
Dendrimers [18,19]
High surface areas in relation to volume Convergent method Water purification
Encapsulate guest molecule in the macromolecular Analytical devices
interior due to their globular shape
Chemical method
High conductivity viz. reversible redox Electronic devices: light emitting diodes, solar cells
Electrochemical method
Nonlinear optical properties Electromagnetic shielding materials
Photochemical method
Electric properties Microwave absorbing materials
Conducting polymers Concentrated emulsion method [20]
Microwave absorbing properties Rechargeable batteries
Inclusion method
Wettability Sensors
Plasma polymerization
Pyrolysis method
 Sensors 2020, 20, 1966 4 of 19

Nanomaterial-based sensors are highly sensitive and specific in their nature as compared to the
traditional material-based
Nanomaterial-based sensors.
sensors Somesensitive
are highly commonandnanomaterials usednature
specific in their in sensor technology
as compared to are
theshown
in Figure
traditional 1.
material-based sensors. Some common nanomaterials used in sensor technology are shown
in Figure 1.

Figure 1. Commonly
Figure used used
1. Commonly nanomaterials in various
nanomaterials kind of
in various sensors
kind fabrication
of sensors with their
fabrication withsizes.
theirL:sizes. L:
length; D: Diameter.
length; D: Diameter.

The The
nanosensors
nanosensors are operated at a at
are operated scale similar
a scale to thetobiological
similar processes
the biological to increase
processes the
to increase the
specificity of biological response. One of the important steps of experimental design before
specificity of biological response. One of the important steps of experimental design before addition of addition of
a nanomaterial
a nanomaterial into into
the sensing application
the sensing is “Nanofabrication”.
application is “Nanofabrication”.This step
Thisleads
step to twotoimportant
leads two important
actions, i.e., first,the manufacturing and designing of nanoscale adhesive through the use
actions, i.e., first, the manufacturing and designing of nanoscale adhesive through the use of integratedof integrated
circuits and and
circuits second, the use
second, theof micromachining
use of micromachiningprocesses for thefor
processes engineering of nanomaterial
the engineering surfaces.
of nanomaterial surfaces.
FourFour basic processes involved in biosensing by nanofabrication are chemical
basic processes involved in biosensing by nanofabrication are chemical bonding, photolithography, bonding,
photolithography, surface etching strategies and thin film etching/growth. With the rise of chronic
surface etching strategies and thin film etching/growth. With the rise of chronic diseases, e.g., diabetes
diseases, e.g., diabetes and cancer, there is a need for awareness among the masses for the early-stage
and cancer, there is a need for awareness among the masses for the early-stage identification of
identification of these diseases, as biosensors provide a quick response and high sensitivity at the
these diseases, as biosensors provide a quick response and high sensitivity at the initial stages.
initial stages. Nanoscale electrodes are produced from the lithography technique, which is one of the
Nanoscale electrodes are produced from the lithography technique, which is one of the basic process
basic process of nanofabrication. The use of nanomaterials in biosensing provides better and greater
of nanofabrication.
surface The use of
area for immobilization nanomaterials
with in biosensing
better precision provides
[21]. Glucose better and
biosensors weregreater surface area for
first developed
usingimmobilization
this techniquewith better
by the use precision [21]. Glucose
of the enzyme biosensors
glucose oxidase andwere first developed
the detection using
of analytic this technique
materials
was improved by the addition of platinum nanoparticles above the sheets of carbon nanotubes. These by the
by the use of the enzyme glucose oxidase and the detection of analytic materials was improved
additionenable
biosensors of platinum nanoparticles
the recognition of above
glucosethefrom
sheetsseveral
of carbon nanotubes.
sources other These
than biosensors
blood. Theenable
the recognition
antigen–antibody of glucose
complexes fromin
formed several sources
the reaction canother than
also be blood. by
identified The antigen–antibody
immune-sensors complexes
in which
thinformed
films are incoated
the reaction cansensing
above the also be surface
identified by immune-sensors
to allow for quick and betterin which thin films
recognition areanalytes
of the coated above
[22].the sensing surface to allow for quick and better recognition of the analytes [22].

5
Sensors 2020, 20, 1966 5 of 19

Nanoelectromechanical systems (NEMS) are other highly sensitive devices with nanoscale
functions. This technology, when engineered with nanomaterials, provides novel properties from
nanoscale to nanometer level in energy harvesting, sensing display, imaging, portable power generation
and also in drug delivery. NEMS, along with micro-electrochemical systems (MEMS) devices, result
in better performance with mechanical materials when attached to biological systems and lead to
improvement of bio-adhesion features and response to a widespread range of stimuli. This technology
enables the demonstration of the biochemical interactions with the help of biomarkers for the rapid
diagnosis of new diseases [23]. Flurophores are other important components of biosensors which can
absorb and emit light within wavelengths of excitation and emission spectra and make use of total
internal reflection. These are commonly used as recognition reagents in flow cytometry in conjugation
with the antibody critical angle of reflection.
In nanomaterials, the sensing materials should have sharp and precise scale optical response with
the incident light surface plasmon resonance (SPR) [24]. The SPR furnishes the nano-biosensor in a
better way and allows the estimation of biological interactions through the detection of the minutest
interaction phenomenon. The plasmonic peak of nanoparticles with sizes smaller than 10 nm can be
described in a better way by the modified dielectric function as compared to the other models [25–27].
The safety of the environment and human health is of prime concern and many reports have highlighted
the toxicity associated with various nanomaterials (Table 2).

Table 2. Toxicity studies of various used in sensor development under in vitro and in vivo conditions.

Nanomaterials Toxic Effects Dosage Level Ref

Damage to micronucleus, macronucleus, and membrane
was observed in Stylonychiamytilus
1 mg/ml
Decrease in maternal, fetal weight and skeletal
Multiwalled Carbon 100.8–162.5 µg/mouse
malformation in mouse model [28–31]
nanotubes 4–20 mg/kg
Increased abortion rate in mouse model
45 µg/m3
Increase in C-C motif ligand 20, basic fibroblast growth
factor, and soluble IL-1 receptor II in human subjects
Singlewalled Carbon Fetal morphological abnormalities in mouse model 0.1–30 µg/mouse
[32,33]
nanotubes Increased resorption rate in mouse model 10 mg/kg
Reduction in phagocytic activity and hemocyte viability in
Quantum dots 8 mg/L
the hemolymph of Elliptio complanata [34,35]
(Cadmium telluride) 20–125 µg/mouse
Reduced survival rate in mouse model
Induced decreases in body weight, red blood cells, and
Gold NPs 550–2200 µg/kg [36]
hematocrit in mouse model
Cytotoxic for human jurkat cell line, mouse embryonic
Polypyrrole >19.4 µg/mL [37]
fibroblasts and mouse hepatoma cell line (MH-22A)
Toxic for the liver, kidney, spleen, lung, intestine, and
Graphene oxide 500 mg/kg [38]
brain in rat model
Acute inflammation in the liver and tarsal joints, induced
Magnetite the vaginal secretion IgA, Bcl-2 reactivity in the 45 mg/mouse [39]
hepatocytes in mice model
Increases in lysosomal activity of HaCaT cells, an
Dendrimers (PAMAM) 1.5–1.8 µM [40]
immortal non-cancerous human keratinocyte cell line

Many organizations across world have given recommendations regarding the safety of researchers
and employees dealing with nanomaterials at the workplace (Table 3).
Sensors 2020, 20, 1966 6 of 19

Table 3. Guidelines/recommendations to address the safety of nanomaterials used in sensor fabrication.

Country/Agency Key Guidelines/Recommendations Applicable Sector Ref

Eliminating worker exposure to nanomaterials wherever
possible throughout the manufacturing and handling of
nanomaterials
Substitution is unlikely to be an applicable hazard
reduction method because the unique properties of
Australia/University of nanomaterials are the key to their potential and are
Small scale laboratory [41]
Wollongong essentially driving their development
In addition to taking into account the regulatory
requirements and production imperatives, safe layouts
must be designed to eliminate situations involving risks
for the process and for the workers

Nanoparticles are to be handled in a form that is not easily

airborne, such as in solution or on a substrate. Use of
respiratory air filters N100 or N95 is recommended Research laboratories
India/DST [42]
Wear safety glasses, goggles, full facepiece respirator Industries
(Recommended when there is exposure to solvent or hot
material)
Awareness or safety training for students, staff, employees
or anyone involved working with nanoparticles
Canada/Concordia Development and application of standard operating
Laboratory facilities [43]
University procedures (SOPs) when working with specific
nanoparticles

Operations which involve the likely release of Agriculture

manufactured nanomaterials (MNMs) into the air should Electronic
be performed in contained installations or in facilities that Medicines
can be operated remotely from a protected area Medical technology
European Commission Processes where there is a potential for creating dusts or Construction [44]
aerosols of MNMs should be carried out in areas with Automotive production
efficient local exhaust or extraction ventilation Textiles
Adequate training and information should be provided to Food processing
individual workers Cosmetics
The Guideline Development Group (GDG) recommends
assigning hazard classes to all MNMs according to the
Globally Harmonized System (GHS) of Classification and
Labelling of Chemicals for use in safety data sheets
WHO Industries [45]
The GDG recommends updating safety data sheets with
MNM-specific hazard information, or indicating which
toxicological end-points did not have adequate testing
available
Agglomeration and size distribution of nanomaterials
under the conditions of toxicity testing and as expected in
the final product
FDA In vitro and in vivo toxicological data on nanomaterial Cosmetic industries [46]
ingredients and their impurities, dermal penetration,
potential inhalation, irritation (skin and eye) and
sensitization studies, mutagenicity/genotoxicity studies.

3. Various Nanomaterials used for Sensor Fabrication with Special Reference to Food
Borne Pathogens

3.1. Carbon Nanotubes

In the last decade, carbon nanotubes (CNTs) have emerged as one of the most extensively used
nanomaterials in drug delivery and in biomolecular techniques. CNTs are cylindrical hollow tubes
containing one or more concentric layers of graphite enclosed by fullerenic hemispheres, referred to as
single- to multi-walled CNTs, respectively. They have unique structures, high electrical and mechanical
properties, chemical stability, light weight, high thermal conductivity, unique electrocatalytic action,
minimal surface fouling and high surface to volume ratio [47].
The key challenge for developing effective biosensors is their specificity, sensitivity and detection
time to assess the presence of food-borne pathogens in normal and toxin-supplemented samples.
Single-wall surface carbon nanotubes (SWCNTs) were employed in a DNA sensor application for
the detection of Salmonella using N-ethyl-N’-(3-dimethylaminopropyl) carbodiimide hydrochloride
(3-dimethylaminopropyl) covalently bonded to the nanotubes [48]. For this, an electrode along with
ssDNA probe solution (Salmonella specific) was incubated at room temperature for 2 h. The sensor
Sensors 2020, 20, 1966 7 of 19

showed sensitivity at the target concentration of 1 × 10−9 mol/L DNA. Moreover, no fluctuation was
noted in the signal via the ssDNA probe on the mismatching of the single nucleotide. An amino-modified
aptasensor was developed using indium tin oxide (ITO) deposited on a multi-walled carbon nanotube
(MWCNTs) electrode and assessed for the detection of Salmonella enteritidis and Salmonella typhimurium
with detection limits of 5.5 ×101 and 6.7 × 101 cfu mL−1 , respectively [49]. Additionally, the sensitivity
of an aptasensor was validated via the PCR technique, by detecting the 148bp invA gene, which is also
present in S. enteritidis and S. typhimurium. The sensitivity limit of PCR was found to be 102 cfu mL−1 for
both the strains of [Link], the sensitivity limit of the aptasensor was found to be 101 cfu
mL−1 when assessed on raw chicken samples which were spiked with Salmonella. Hence, this confirms
that the ssDNA/MWCNTs/ITO electrode coupled to an aptamer is more effective in comparison
to PCR detection approach on the basis of its detection limit. Furthermore, the developed sensor
shows no specificity against non-Salmonella bacteria. In 2014, the group of researchers immobilized
anti-Escherichia coli antibodies on SWCNT-based joint biosensor developed to detect the E. coli K-12
strain. The developed sensor showed the detection limit of 102 cfu mL−1 in less than 5 min. Moreover,
minute fluctuation in the electric current was detected, when checked with Staphylococcus aureus, which
confirms its specificity and sensitivity to E. coli [50].

3.2. Gold Nanoparticles

Gold nanoparticles are frequently used in nanotechnology-based applications. Gold nanoparticle
(AuNPs) synthesis in organic or aqueous solvents requires a stabilizing mediator (surfactant) for its
stability and can be achieved by chemical binding or by adsorption of the appropriate mediator on
the gold NPs. Usually, to avoid the aggregation of loaded NPs, the surfactant need to be loaded and
different gold NP properties can be adjusted by choosing separate surfactants [51].
The biological compatibility, exceptional conducting capability, and high surface-to-volume ratio
are the few characteristics of AuNPs, which makes it the nanoparticle of interest [52]. The redox
activity is an interesting characteristic of gold NPs, which enhances the sensitivity of electrochemical
biosensors in the analysis of foodborne pathogens. The use of gold NPs onto electrochemical biosensors
in conjugation with ssDNA complementary to the microbial DNA under evaluation improves their
binding with DNA-gold NPs on the transducer surface and enhances the sensitivity of the developed
biosensor [53]. In another example, gold NPs were used in conjugation with redox enzymes that
precisely oxidize/reduce the analyte as the substrate in the reaction. On binding to the analyte,
the immobilized enzyme-gold NPs eventually increase the current signal and confirm detection [51].
The AuNPs conjugated with E. coli O157: H7 antibodies were also used for detection of E. coli
O157: H7 in milk. In this study, screen-printed carbon electrodes (SPCE) were fabricated with
AuNPscontaining E. coli O157: H7-specific antibodies conjugated with horseradish peroxidase with a
detection limit of 102 –107 cfu mL−1 using hydrogen peroxide and ferrocene dicarboxylic acid (FeDC)
as a substrate [54]. This analysis confirmed that immunosensing strips of AuNPs/FeDC–SPCE shows
no specificity towards other bacteria like E. coli K12, Listeria monocytogens, S. choleraesuis and Vibrio
parahaemolyticus. Hong et al. developed a selective and quick electrochemical biosensor for the
detection of Norovirus (NoV) [55]. This biosensor is fabricated with a nanostructured gold electrode
containing concanavalin A (ConA) as a recognition element that selectively detects NoV. In this study,
the sample solution extracted from lettuce was used to measure the concentration of NoV in a realistic
atmosphere for its validation with a detection limit of LoD=60 copies mL−1 . The sensor was found to
be non-targeted against hepatitis A viruses (HAV) as well as hepatitis E viruses (HEV). It also showed
effective thermal stability at both 4 and 25 ◦ C, respectively.
Davis et al. developed a modified electrode-AuNPs biosensor for assessing the presence of
L. monocytogenes in spiked blueberries and the detection limit was found to be 2 log cfu/g after
1 h of assay [56], whereas, another group of researchers developed an enhanced AuNP aptasensor
via Surface-enhanced Raman spectroscopy (SERS) for instantaneous detection of S. aureus and
S. typhimurium in a spiked sample of pork [57]. In this study, the intensities of the signals for other
Sensors 2020, 20, 1966 8 of 19

bacteria like Bacillus cereus, E. coli, Shigella dysenteriae and V. parahaemolyticus were found to be very low.
The outcome of this aptasensor was similar to the plate counting method exhibiting recovery between
108.33% for S. aureus and 94.12% for S. typhimurium.

3.3. Quantum Dots

Carbon quantum dots (CDs) are very small artificial semiconductor particles with sizes normally
less than 10 nanometers. These nanoparticles are extensively used in research due to their high
luminescence properties, high solubility and biocompatibility [58,59]. Carbon quantum dots (CDs)
are quasi-sphere nanoparticles (diameter less than 10 nm) formed from crystalline sp2 hybridization
graphite cores and amorphous aggregations used in bioanalytics and biolabeling. On the other
hand, graphene quantum dots (GDs) consist of single or very few graphene lattices (<10). Due to
bigger conjugated domains and periodic structure, the GDs are generally more crystalline than CDs.
These nanostructures based on carbon are actually two distinct allotropes and both the allotropes
are functionalized with oxygen-related complex surface group molecules such as carboxylates or
hydroxylate derivatives that improve optical features and particle solubility [60,61]. The variability
in fabrication of these materials gives rise to diverse surface functionalization and more complex
hybridization in biosensor applications.
CDs have been used to detect harmful microbial culture and toxins, together with S. typhimurium
and aflatoxin B1 (AFB1) [62,63]. Wang et al. fabricated carbon dot aptamer complexes (CD-apt) for the
quantitative identification of S. typhimurium in eggshell and tap water solutions at a test range of 103 to
105 cfu mL−1 and a LOD of 50 cfu mL−1 , for which the detection time was found to be 2 h without
interference from E. coli O157:H7 and S. aureus [62]. The developed sensor exhibited unvaried results in
comparison to the standard plate count method in the egg sample as well as in tap water the standard
plate count showed 3.6 × 104 and 5.9 × 104 results whereas for the developed sensor the readings were
3.27 × 104 and 5.51 × 104 cfu mL−1 , respectively. Various trials have verified the specificity of microbial
identification using biosensors in simple or complex food settings using CDs, GQDs, carbon nanotubes
and semiconductors [63–65]. Wang et al. assembled CDs and AuNPs for specific AFB1 detection with
the help of an aptamer and achieved a 5 pg/mL LOD (16 pM) [63]. This method was employed with
actual samples like corn and peanuts, which were supplemented with varied concentrations of AFB1 in
which average recovery was found to be in range of 92%–105%. This recovery enhanced on changing
the aptamer, such as ochratoxin aptamers (designed to assess fungal toxins only).

3.4. Magnetic NPs beads as Label in Biosensor-based Detection

Magnetic NPs are another class of nanomaterials used in biosensors which can be amended by
changing the magnetic field. These NPs are clusters of magnetic beads of 50–500 nm diameters [66–68].
Magnetic NPs have emerged as one of important fabricating material to develop a flow assay as they
have strong color and can separate the target material from the complex matrix. These NPs have
additional benefits as it provides robust magnetic and visual signals. Various researchers have used
magnetic beads to develop flow assays for detecting pathogenic bacteria [69,70]. Wang et al. developed
antibody-covered magnetic beads of 300nm and used them as indicators for spore detection of Bacillus
anthracis with a detection limit of 6 × 104 spores/g of milk powder, 2 × 105 spores/g of starch, and
5× 105 spores/g of baking soda, respectively [71]. The designed sensor did not show any specificity
towards other Bacillus species like B. cereus, B. thuringiensis and B. mycoides. In contrast to traditional
lateral-flow method, this process does not require the pre-treatment of the sample and it provides
instant results for magnetic, naked-eye and optical detection within 20 min. Suaifan et al. established a
biological assay with magnetic beads for robust recognition of E. coli O157:H7 in food with detection
limits of 12 cfu mL−1 of broth and 30–300 cfu mL−1 of other food matrices [72]. In this study, peptides
of E. coli O157:H7 (e.g., protease) were used asa substrate and conjugated with magnetic nanoparticles
(MNPs). Furthermore, the crude protease synthesized by E. coli O157:H7 was down-streamed onto
immobilized sensing platform and during enzymatic reaction a magnet attached on the back of sensor
Sensors 2020, 20, 1966 9 of 19

stripe, magnetizingthe cleaved MNP-peptide moieties, and generating the visual signals for qualitative
assessment of the test sample within 30 seconds. The developed biosensor exhibited long-term stability,
i.e., six months, and showed no specificity towards L. monocytogenes, Pseudomonas aeruginosa and
S. aureus protease. On the other hand, Xia et al. developed gold magnetic nanobeads for the rapid
recognition of S. choleraesuis with a detection limit of 5 × 105 cfu mL−1 and detection time of 20 h in
whole milk as compared to colloid gold-based lateral flow assay with a limit of 5 × 106 cfu mL−1 , thus
confirming the superiority of magnetic beads to the colloidal gold [73].

3.5. Dendrimers
Dendrimers (DEN) are complex globular shaped-branched structures of 2–20 nm in size.
The structural properties like monodispersity, manageable size, easily amendable surface functionalities,
hydrophilicity, high mechanical and chemical strength makes them the preferred synthetic nanoparticle
for developing biosensors [74]. The polyamidoamine (PAMAM) dendrimer is one of these which
hasgained significant attention as it provides large surface areas with high number of functional groups
to allow the easy binding of biological entities. It also contains mono-disperse as well as hyper-branched
polymers with active functional groups present at end of dendrimer structure. These functional
groups aid in immobilizing the bio-recognizing molecules, by acting as a bio-conjugating moiety
and play diverse roles in biosensor technology. Electrochemical techniques like amperometric,
electrochemiluminescence, impedimetric and potentiometric are generally used for estimating specific
molecules using dendrimers with high selectivity and sensitivity [74].
Shiddiky et al. developed the competitive and sandwich-based bioassays for assessing
DNA and protein using H2 O2 reduction activity using a conducting polymer based on
poly-5,20 :50 ,2”-terthiophene-30 -carboxylic acid (pTTCA) [75,76]. Another biosensor, made up of the
monolayer of 3G PAMAM (poly amido amine) dendrimer covalently linked by chemisorption to
AuNPs/CdS nanoparticles was also developed using immobilized AuNPs on bioreceptor molecule and
showed a detection limit of 450 aM and 4 fg mL−1 , respectively, for DNA and protein. This biosensor
was 70 times more sensitive as compared to plain pTTCA layer due to AuNPsbeing attached
on the pTTCA/DEN layer, which allows the binding of different proteins, avidin and hydrazine.
Competitive immune interaction-based sensors have also been developed for detecting anti-microbial
agents and biomarkers. The detection of AFB1, a food contaminant, was done using an aptamer-based
biosensor [77]. In this study, the fourth generation polyamidoamine dendrimers were immobilized on
a cystamine-covered gold electrode with further attachment with AFB1-specific DNA aptamers and
showed a detection limit of LOD = 0.40 ± 0.03 nM at 4 ◦ C without losing its stability for up to 60 hours.
The developed sensor did not exhibit any specificity towards ochratoxin A (OTA) and was effective in
detecting the AFB1 in contaminated peanuts sample.

3.6. Silicon Nanomaterials

Silicon nanostructure-based sensors have been developed with high specificity for use in rational
fabrication biosensing and bioimaging applications [78–80]. Silicon nanomaterials can be converted
into molecules knows for renal clearance as these are biodegradable in nature and are excreted from the
body without any toxicity evidence [81,82]. Silicon nanoparticles (SiNPs), with a diameter of 3–10 nm,
have been permitted by the Food and Drug Administration for use in human clinical trials [83].
A variety of silicon surface-enhanced Raman scattering (SERS) sensors are used in selective and
sensitive detection of reproducible chemical and biological species. Pathogens with colony forming
units of E. coli can be detected using biosensors based on porous silicon using chemiluminescence
assay [84]. The sensitivity of this biosensor chip for E. coli was determined to be 101 and 102 cells for
40 and 30 min, respectively. In another study, porous silicon was fabricated using an anodization
process in an electrochemical Teflon cell [85]. In this study, platinum wire was used as a cathode and
the silicon chip was used as the anode and ssDNA of S. enteritidis strain was used as a probe, for
functionalized porous silicon platform. It was further observed that biosensors with porous silicon
Sensors 2020, 20, 1966 10 of 19

were highly sensitive and have more active surface area as compared to the biosensors based on
planner silicon and probes specific to the targeted DNA.

3.7. Graphene-based Nanomaterials

Graphene-based nanomaterials are another type of material used as transducers of biosensors.
These nanomaterials are generally used for the conversion of targeted and receptor molecules for
detectable measurement using EDC/NHS chemistry [86]. On the other hand, graphene is the most
commonly used nanomaterial for different biosensors designs with different transduction modes as
it contains a large surface area, capacity to immobilize with different molecules with high electron
transmission rate and electrical conductivity [87]. Graphene-based nanomaterials can also be used as
a quencher to generate fluorescent transducer-based biosensors, as reduced graphene oxide (rGO),
graphene (G), and graphene oxide (GO) possess a very high fluorescent quenching efficiency [88–90].
During sensor design, the detection limit of targeted molecules is affected by graphene and the
sensitivity and selectivity of biosensors can also be affected by bioreceptors and G, GO or rGO sheet
orientation. Differences can be observed in the sensing performance of biosensors by functional groups,
graphene oxidation state, and number of layers as well as by different derivatives used.
A GO-modified iron oxid-chitosan hybrid nanocomposite-based electrochemical sensor was
also used for E. coli O157:H7 detection using a specific probe oligonucleotide sequence covalently
immobilized on nanocomposite films [91]. This sensor showed a detection limit of 1 × 10−14 M
with a linear response to the complementary DNA in 10−6 to 10−14 M. Meanwhile, the specificity
of the pDNA/GIOCh/ITO bioelectrode against various target DNA sequences (complementary,
non-complementary and one base mismatch) and with the samples of E. coli, S. typhimurium, Neisseria
meningitidis and Klebsiella pneumonia showed insignificant signal. This confirms that the fabricated
biosensor has high selectivity, sensitivity and reserved significant activity (i.e., 90% of the initial
activity) even after the usage of up to sixcycles. In another study involving a graphene-based biosensor
designed specifically for detection by E. coli O157:H7-specific antibodies showed sensitivity in range of
10–100 cells ml−1 and did not display any specificity towards E. coli DH5α strain [92]. The shelf-life
of functionalized chips of this biosensor when stored at 4 ◦ C lasted for 4 weeks. Srivastava et al.
developed an electrochemical sensor for the food toxin detection by binding the monoclonal antibodies
on rGO surface to AFB1 with a sensitivity of 68 uA ng−1 ml cm−2 , and a limit of detection of 0.12 ng
mL−1 [93]. The storage stability of this immune-electrode was determined by passing the current at
regular interval of 5 days for 45 days along with 25ng dL−1 AFB1 and showed no substantial variation in
the current, even after 45 days. In another study, a BSA/anti-AFB1/AuNPs/rGO nanocomposite-based
immunosensor showed a high sensitivity of 182.4 µA ng−1 mL−1 cm−2 for the recognition of AFB1
with a limit of detection of 0.1–12 ng−1 mL−1 and consistency up to 56 days [94].

3.8. Conducting Polymers

Conducting polymers withdistinctive characteristics have made these an effective alternative
for some materials currently used in the biosensor fabrication. Polymers are good insulators and
some polymers are found to have good conducting properties due to their combination of metallic
and semiconductor characteristics. There are varieties of conducting polymers used in different
applications [95]. Out of these, polyaniline, polythiophene, and polypyrrole are used as nanomaterials
and show biocompatibility and can reduce the leading disturbances affecting the working environment
and these also help in preventing the electrodes from fouling [96,97]. Only polyaniline and polypyrrole
are extensively used for the detection of foodborne pathogens. Conducting polymers are used as an
excellent immobilizing platform with biomolecules at electrodes to deliver better signal transduction,
high sensitivity, selectivity, durability, biocompatibility and flexibility [98,99].
Tully et al. reported direct immunosensor use for the identification of a cell-surface protein on
L. monocytogenes with label-free immunosensing of Internalin B (InlB) with a limit of detection for
InlB at 4.1 pg mL−1 [99]. Muhammad-Tahir and Alocilja reported the performance of a biosensor
Sensors 2020, 20, 1966 11 of 19

based on electrochemical transducer using polyaniline in measuring an immune reaction for detecting
7.8 × 101 cfu/mL of E. coli O157:H7 in 10 min [100]. Polyaniline was also reported as an identifier
for the electrochemical sandwich immunoassay of E. coli O157:H7 detection in fresh produce such
as lettuce, alfalfa sprouts, and straw-berries and with an average of 81 cfu mL−1 in nine samples
in 6 mins [101]. Sheikhzadeh et al. used a label-free impedimetric biosensor for the detection of S.
typhimurium based on the effect of the aptamer/target response to the central conjugation of poly
[pyrrole-co-3-carboxyl-pyrrole] copolymer-based aptamer to its electrical characteristics [102]. In this
study, the S. typhimurium was detected with high selectivity over other pathogens at a concentration
range of 102 –108 cfu mL−1 with a limit of detection of 3 cfu mL−1 . The developed aptasensor showed
high selectivity towards S. typhimurium on comparing its detection value with other potential model
strains viz. E. coli 375, E. coli 797, E. coli 3274, Enterobacter, and Citrobacter. Moreover, the developed
aptasensor showed robust detection of S. typhimurium in 45 min in spiked apple juice.

4. Current Status and Future Prospects

Various developments in nanotechnology have shown its proficiency in detecting pathogenic
microbes and resulted in an answer to different problems related to biotransformation and metabolism
of ingested NPs (Table 4).
Sensors 2020, 20, 1966 12 of 19

Table 4. Types of nanomaterials used in sensor fabrication for foodborne pathogens and their toxins detection.

Nanomaterials used in
Biosensors Sensing Platform Food Matrix Pathogens/Toxins Detection Limit Analysis Time Ref
Biosensor Fabrication
PLA-AuNPs (polylactic
Electrochemical
Screen printed carbon electrode acid-stabilized gold Shellfish Standard Vibrio parahemolyticus 2.16 × 10−6 µM NS [103]
biosensor
nanoparticles)
Electrochemical DNA biosensor Screen printed carbon electrode PLA-AuNPs Cockle Standard Vibrio parahemolyticus 5.3 × 10−12 10 min [104]
Ground beef,
Paper-based biosensor Gold electrode Magnetic beads Turkey sausage, Standard Staphylococcus aureus 40 cfu/mL 1 min [105]
Lettuce and Milk
Cys-PAMAM
Aptamer-based biosensor Gold electrode (cystamine-poly(amido-amine) Peanuts Aflatoxin B1 0.40 nM 10 min [77]
dendrimers)
Electrochemical Carboxylic acid-MWCNT Standard Salmonella, Campylobacter
Graphite electrode Milk 400–800 cfu/mL 30 min [106]
immunosensor (multiwalled carbon nanotubes) and Escherichia coli
Electrochemical impedance
Glassy carbon electrode AuNPs-MWCNT-PAMAM Milk Standard Salmonella typhimurium 5.0 × 102 cfu/mL NS [107]
Immunosensor
Lytic phage-based Iron-Nickel Base Magnetic Standard Staphylococcus aureus 1.76 log cfu/25 mm2
Cr-Au layer (Chromium) Spinach Leaves 30 min [108]
magnetoelastic biosensors ribbon (MRSA) surface of spinach
Amperometric immunosensing
Screen printed carbon electrode AuNPs Milk Standard Escherichia coli O157:H7 50 cfu/strip in milk 1h [54]
strips
Impedimetric biosensor Gold disk electrodes Pyrrole-3-carboxylic acid Apple Juice Standard Salmonellatyphimurium 3 cfu/mL 45 min [102]
Laboratory isolates of Listeria
Amperometry biosensor Glassy carbon disc electrode Polypyrrole NA 105 cfu/mL 30 min [109]
monocytogenes
Colorimetric aptasensor Magnetic beads NA (not applicable) Salmon Standard Vibrio parahemolyticus 102 –107 cfu/mL NS [110]
CdTe quantum dots (Cadmium
Fluorescence immunoassay NA Whole milk Standard Escherichia coli O157:H7 5 × 102 –107 cfu/mL NS [111]
telluride)
Lateral flow biosensor AuNPs (Gold nanoparticles) NA Milk Standard Salmonella enteriditis 101 cfu/mL 10 min [112]
Mid-Infrared pathogen sensor Magnetic nanoparticles NA Spinach and Milk Standard bacterial cultures 104 –105 cfu/mL 30 min [113]
Laboratory isolates of Escherichia coli
Aptamer-based biosensor AuNPs NA Milk powder 10 cfu/mL 30 min [114]
O157:H7
Electrochemical biosensor Gold electrode NA Lettuce Laboratory isolates of Norovirus 60 copies/mL 1h [55]
Laboratory isolates of
Staphylococcus aureus,
Gold nanoprobe AuNPs NA NS (not specified) 123 fg/µL 30 min [115]
Listeria monocytogenes,
Salmonella spp.
Fluorometric graphene
Graphene oxide NA NA Standard Salmonella enteriditis 25 cfu/mL NS [116]
oxide-based assay
Fe3 O4 GO NPs (Graphene Standard pre killed Escherichia coli
Chemiluminescent aptasensor NA NA 4.5 × 103 cfu/mL 1h [117]
oxide/iron nanoparticles) O157:H7
Magnetoresistive-based Fe2 O3 superparamagnetic
NA NA Standard Aflatoxins B1, Zearalenone 50 pg/mL 10 min [118]
immunoassay particles
Goldnanoprobe-nucleic acid
Au colloid NA NA Standard Salmonella strains 5 cfu/mL 80 min [119]
sequence-based amplification
8.1 × 105 cfu/ml and 2.6 ×
Bioconjugate nanocapsules AuNPs NA NA Listeria monocytogenes 5 min [120]
107 cfu/mL
Silicon-based DNA Laboratory isolates of Salmonella
Silicon wafer NA NS 1 ng/mL NS [85]
biosensor enteritidis
Sensors 2020, 20, 1966 13 of 19

5. Conclusions
The application of sensors in food processing industries has also changed the current trend
as these can identify the various contaminants formed within the food chain with high sensitivity.
The advancements in diagnostics have increased the demand for portable devices for robust and precise
detection in food industries. Nano-sensors have the potential to meet both the demand of miniaturization
and low-cost analytical devices. In the past few years, applications of e-nose technologies have come
through advances in sensor design, material improvements, software innovations and progress in
micro-circuitry design and systems integration. There is significant interest in methods for the early
detection of quality changes in food products. The development of electronic nose technology has
stimulated interest in the use of characteristic volatiles and odors as a rapid, early indication of
deterioration in food quality [121,122]. The research on nanotechnology has progressed so much that
it has encouraged the expansion of nanosensors for the detection of foodborne pathogens with high
improvements overthe conventional methods. Ultrasensitive transglutaminase-based nanosensors
used for early diagnosis of celiac diseases in human and identification of foodborne pathogens
and food-related disorders using biosensor are some specific examples of biosensor use [123–125].
The extensive research progress in nanotechnology for nanomaterial exploration and the development
of new mechanisms in the future will enable researchers to develop highly sensitive, specific and
unobtrusive nanosensors for analyzing food-borne microbes at an affordable cost.

Author Contributions: H.K., S.K.B., K.S., D.K. and K.K. conceptualized the manuscript. H.K., K.S. wrote the
manuscript. K.K., S.K.B., T.C.B. and R.V. assisted in writing, updated information and edited the manuscript. K.K.,
A.K., T.C.B., R.V., and D.K. contributed in critically revising the draft and updating the manuscript for publication.
All authors have read and agreed to the published version of the manuscript.
Funding: Supported by Excellence project FIM UHK.
Conflicts of Interest: The authors declare no conflicts of interest.

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