key: cord-0965312-3iaxlolh
authors: Misra, Ranjita; Acharya, Sarbari; Sushmitha, Nehru
title: Nanobiosensor‐based diagnostic tools in viral infections: Special emphasis on Covid‐19
date: 2021-06-23
journal: Rev Med Virol
DOI: 10.1002/rmv.2267
sha: f6073ccf8f1a63e59f10ae7152e9f724ca90b8b9
doc_id: 965312
cord_uid: 3iaxlolh

The rapid propagation of novel human coronavirus 2019 and its emergence as a pandemic raising morbidity calls for taking more appropriate measures for rapid improvement of present diagnostic techniques which are time‐consuming, labour‐intensive and non‐portable. In this scenario, biosensors can be considered as a means to outmatch customary techniques and deliver point‐of‐care diagnostics for many diseases in a much better way owing to their speed, cost‐effectiveness, accuracy, sensitivity and selectivity. Besides this, these biosensors have been aptly used to detect a wide spectrum of viruses thus facilitating timely delivery of correct therapy. The present review is an attempt to analyse such different kinds of biosensors that have been implemented for virus detection. Recently, the field of nanotechnology has given a great push to diagnostic techniques by the development of smart and miniaturised nanobiosensors which have enhanced the diagnostic procedure and taken it to a new level. The portability, hardiness and affordability of nanobiosensor make them an apt diagnostic agent for different kinds of viruses including SARS‐CoV‐2. The role of such novel nanobiosensors in the diagnosis of SARS‐CoV‐2 has also been addressed comprehensively in the present review. Along with this, the challenges and future position of developing such ultrasensitive nanobiosensors which should be taken into consideration before declaring these nano‐weapons as the ideal futuristic gold standard of diagnosis has also been accounted for here.

From the wide palate of viruses posing a threat to mankind, respiratory viruses are the deadliest affecting infants, children, elderly people, immunocompromised or patients with co-morbidity. 2 Despite significant progress in the prevention, diagnosis and treatment over the past 100 years, the recovery rate for these viral diseases is far from satisfactory where over 95% of these deaths are due to the deficiency of correct diagnosis and treatment. Concerning treatment, major hindrances include imprudent use of antimicrobials, the emergence of multidrug resistance in pathogens, the appearance of novel variants of pathogenic viruses and so forth. 3 Similarly, traditional diagnostic methods such as microscopy, immunology and the polymerase chain reaction (PCR) approaches although effective are plagued by issues like inaccuracy and ineptness. 2 Although both diagnosis and treatment go hand in hand, early prognosis gives the treatment of these infections an upper edge, so the development of rapid and sensitive identification methods is paramount for better dissemination of therapeutics in these challenging times. 4, 5 In the current scenario, the main strategy to control the Covid-19 pandemic depends on testing and diagnosis of the disease at early stages. Reverse transcription PCR (RT-PCR) testing remains the primary method for diagnosing SARS-CoV-2 although some clinicians may utilise chest computed tomography (CT) scans as a more reliable way to assess the stage of the disease. 6 However, while the former is quite a time taking process the latter cannot detect the early onset of the disease. Besides, CT scans cannot distinguish between Covid-19 and viral pneumonia patients. It can be said that the present diagnostic modalities are the rate-limiting factors in terms of the number of persons that can be tested. Thus, for better management of Covid-19, more reliable, sensitive and quick diagnostic methods are paramount.

Biosensors are deductive devices where biological identification entities such as enzymes, antibodies or nucleic acids are bound with another component called transducer and detector which identify the analyte and give a digitised output. 7 Viral biosensors offer an elating secondary means to conventional diagnostic analyses owing to their pocket-friendly, delicate, speedy, miniaturised and portable nature, which are critical parameters of efficient diagnostic agents. 8 In this regard, electrochemical (EC)-based DNA-sensing biosensors were successfully employed for diagnosing the Ebola virus while a paper-based biosensor was used for the identification of the chikungunya virus. 9, 10 Recently, the field of nanotechnology has given a great push to imaging and diagnosis technologies. In this context, comprehending the biosensing concept is the basic groundwork required for developing nanobiosensors for uninterrupted monitoring of human wellness. Several nanomaterials like nanowires, nanorods, nanoparticles and thin films made up of nanocrystalline matter have been preferably used in nanobiosensors owing to their superlative electronic and mechanical properties which help in reinforcing better biological signalling and transduction mechanisms. 11 High sensitivity and better amplification of signals owing to the intrinsic properties of nanomaterials like tunnelling and quantum effects, the high surfaceto-volume ratio for the better surface area makes these nanobiosensors unique for point-of-care tests. 12 The portability, hardiness and affordability of nanobiosensor make them an apt diagnostic agent for the prognosis of a wide array of diseases like cancer, diabetes, malaria, HIV and bilharzia. Recently, a membrane-based EC sensitive nanobiosensor was designed for the detection of West Nile viral particles. 13 It is already known that nanobiosensor-based approaches provide a more meticulous and targeted method for the detection of infections are being considered for early diagnosis of the disease. Nanomaterials such as gold and carbon have garnered a lot of attention in this context for detecting the virus and its biomolecule. 15 These nanomaterials when attached with analyte-like complementary single-stranded nucleic acid aptamer could be a novel approach for sensing SARS-CoV-2 by identifying spike protein S1 in clinical samples. 16 The present review is an elaborate compilation of such kind of nanobiosensors which are futuristic devices which can be tailor-made and modulated to become indispensable diagnostics tools for correct authentication of Covid-19 or any such viral antigens with ease.

Infectious diseases caused by viruses have been discovered at a speedy pace lately and have been the root cause of many epidemics, endemics and pandemics for every demographic region. These obligate parasites upon entry inside a host cell utilising receptor-ligand interaction chemistry are responsible for causing many diseases.

Illustrious representation of human viruses that cause evidential 2 of 13health problems comprise HIV, hepatitis B virus (HBV) and hepatitis C virus (HCV). Similarly, other viruses like rotavirus, astroviruses, Zika virus (ZKV), West Nile virus, influenza, respiratory syncytial virus cause significant damage to the organs they affect posing as great threats to human health, consequently leading to morbidity and mortality. 1 The year 2014-2016 witnessed the outbreak of Ebola in West Africa which took the world by surprise with its unexplainable magnitude and aggressiveness and raised questions about the readiness of public health systems. 17 In February 2016, the public failed to comprehend the implications of the ZKV after the World Health Organization (WHO) stated it as an international civic health emergency owing to its relationship in cases of a rare congenital condition called microcephaly in Brazil. 18 The first report of human virus infection such as yellow fever was first reported in the US army at the starting of the 20th century and found its way into Brazil as an outbreak in 2017. Another outbreak in 2018 of an unusual viruslike the Lassa virus in Nigeria resulted in 100 deaths due to haemorrhagic fever. The transition of the ZKV, from an unknown pathogen to a deadly one was swift and quick. The western hemisphere which was devoid of this virus till 2015 reported about 800,000 cases in pen and paper. Moreover, the Asian descent of ZKV, accountable for the 2015-2016 epidemic, caused severe congenital defects in children known as congenital Zika syndrome if the women contracted it during pregnancy. 19 The Nipah virus made its first registered appearance in Malaysia in 1998 where the virus is believed to be transferred from fruit bats to domestic pigs. It is believed to be a major reason for two epidemic outbreaks that occurred in 2001 and 2007 in Bangladesh. The outbreak of this exotic virus was first reported in Kerala, India, which caused severe inflammation of the brain claiming 14 lives. 20 In the contemporary world, three extremely pathogenic influenza viruses, CoVs, SARS-CoV-1 the Middle East respiratory syndrome CoV (MERS-CoV), and the recently emerged SARS-CoV-2 are the major viruses that have resulted in different respiratory diseases throughout the world. 21 The first influenza viruses which are believed to have come from birds and then to horses before spreading to humans was the root cause of the first pandemic in 1918 which killed around 50 million people in 2 years around the globe.

Similarly, the Asian flu and the Hong Kong flu of the 1950s and 1970s killed roughly 2 million people. 22 The delayed spectre of the 1918 flu, along with more recent rounds of avian flu, had led a galore of experts to fear the emergence of another deadly strain of influenza which became true recently with the outbreak of the Covid-19 pandemic. As the present SARS-CoV-2 has emerged as the deadliest virus in the past 100 years affecting millions, worldwide research presently is going on to decipher this mysterious pathogen.

The focus of the entire scientific fraternity is now to find a definite therapeutic intervention and diagnostic tool which will help to rein this devastating virus. Before designing an implementing diagnostics technique for the identification of the pathogen which is the need of the hour, we need first to know about Covid-19 which is summarised below. coughing or sneezing and it can be transmitted from the contaminated objects as well. RNA trace was detected in rectal swabs suggesting that the transmission is possible through fecal-oral. 25 The clinical presentation of Covid-19 includes fever, sore throat, cough, headache, myalgia, shortness of breath, pneumonia, conjunctivitis, ORFs covering one third of the RNA genome code the main structural proteins that are spike glycoprotein (S), an envelope protein (E), nucleocapsid protein (N) and membrane glycoprotein (M). Apart from these main four structural proteins, several accessory proteins are also present whose functions are not known. They do not take part in the viral replication process.

Numerous scientists discovered that SARS-CoV-2 needs angiotensin-converting enzyme 2 (ACE 2) as the receptor for entering the host cells, just like SARS-CoV. For the pathogenesis of contamination, the binding of the virus to the cell receptors is significant. 28 The virus binds to the ACE 2 receptor through the spike protein, following the entry of cells through endosomes. Once inside the cell, the viral genome is released and translated into viral polyproteins. 29 The RNA and capsid protein of the virus are getting replicated and transcribed in the cytoplasm. All the other structural proteins are getting transcribed and translated in the endoplasmic reticulum and are transported to the golgi complex.

They are further assembled and released from the host cells ( Figure 1 ). 30 The natural host for SARS-CoV-2 are bats, however not much is known about their intermediate host and this knowledge is pressing to prevent further spread of this pandemic. In this regard, a recent study was done to anticipate the potential intermediate hosts of SARS-CoV-2 by assessing the composition and variations of coronavirus spike proteins and host ACE2 receptors. 31 Thus, owing to its unique features and aggressive nature, designing treatment and detection strategies of the Covid-19 pathogen has been the dilemma of researchers worldwide. 36 Most of the testing methods used for the diagnosis of SARS-CoV-2 are listed out in Table 1 .

Despite all the above-mentioned techniques, what the need of the hour is to devise diagnostic methods which are portable, sensitive, pocket friendly and do not require skilled technicians or extensive laboratory facilities. In this area, innovative methods like biosensors can be enforced to improve prognosis and can decide the outcome of the treatment.

The first biosensor was created in 1956 although the biosensors concept came in 1903. 37 Biosensors are devices that involve in transforming biological responses into electrical signals. The purpose of a biosensor is to detect or sense a specific biological material which may be proteins, antibodies, immunological molecules, enzymes ans so forth. 38 Biosensors are user-friendly to operate and provide exceptional performance, rapid response, high specificity and sensitivity, compact size, portability and real-time analysis. Since the 1980s, the number of publications regarding biosensors has come into the limelight which has increased exponentially and today, for example, over 55,000 related items on the PubMed database can be found on this topic. 39 Biosensors are used in detecting various biological materials like nucleic acids, proteins, cancer biomarkers, explosives, microorganisms like bacteria, viruses. It is also used in food processing for the detection of toxins, environmental screening, diagnosis in the clinical field and bioterrorism. Researchers are focusing on fabrication quality and biosensor development, nowadays, to enhance the sensitivity and specificity of various techniques. Also, to enhance them, researchers are expanding affinity between creative surface chemistries and using nanomaterials like 

Different types of nanomaterials are used in biosensors in recent years to increase their selectivity and accuracy. Some of the important types of nanobiosensors are discussed in the following sections.

Spherical carbon nanoparticles are used in medicine because of their simple geometry, uniform surface chemistry, non-immunogenicity and biocompatibility. However, their importance is low because of fewer biomedical applications. 60 In this context, carbon in the form 

This is another well-known carbon-based nanomaterial that has unique physical properties. The graphene oxide (GO) reduction method is used to produce graphene-based nanobiosensors. Graphene from GO reduction is also called functionalised graphene sheets or chemically reduced GO and has advantages to be used in nanobiosensors like intrinsically high surface-to-volume ratio and high electron transferability. However, its optical properties are not explored to date. The main application of graphene is the EC detection of small biomolecules. Like CNTs, graphite is also decorated with metallic nanoparticles for the detection of viruses which is more accurate than conventional methods. Optical biosensing techniques have been employed for the detection of many special viruses. 64 As an example, Afsagi et al. developed a portable graphenebased biosensor for detecting the ZKV. Zika antigens in human serum were measured using field effect biosensing with monoclonal antibodies which were covalently linked to graphene nanoparticles. 65 

AuNPs have unique properties like simple and rapid synthesis, large surface area, strong adsorption ability and facile conjugation to biomolecules. Because of these properties, they are studied on EC and optical techniques based on nanobiosensors for various viral detection. AuNPs act as electroactive and catalytic tags for the detection of viruses in EC assays. 67 

Semiconductor-based nanobiosensors have wide application in the detection of analytes because of their surface potential and tunable fluorescence properties. 73 They also have unique photophysical, optical, catalytic and electronic properties which help in biorecognition processes. The most commonly used semiconductors in the application of nanobiosensors include zinc oxide (ZnO) and titanium dioxide.

Nanostructures such as nanorods, nanobelts, nanodisks, nanoparticles, nanosheets, nanoporous and radial nanowire assay were synthesised from these semiconductors. 74 Also, QDs, having intrinsic electronic and optical properties, are 

Electrospinning is a widely used technique in nanotechnology in which energy is applied in the form of electrostatic field force to any To overcome all these shortcomings, nanotechnology-based sensors can be preferred for the detection of Covid-19. It can enable high interactions between target and receptor because of their extremely large surface-to-volume ratios and so, they are rapid and produce more reliable results. 79 In this regard, scientists at the National Institute of Animal Biotechnology, India, had devised an indigenous nanobiosensor device (eCovSens) using fluorine-doped tin oxide electrode (FTO) and AuNPs which were immobilised with nCovid-19 monoclonal antibody for the detecting spike antigen in saliva samples. The advantage of such a system was its ability to detect the said protein in very low concentrations in the human saliva. Besides portability, the nanobiosensor boasted of its ease of collection of data which was done by either connecting to a computer or a cell phone via bluetooth. 81 Many such nanobiosensors which are being studied to be implemented for SARS-CoV-2 detection are described in Figure 4 and discussed below.

Paper 

An extremely precise RT-LAMP-based test mediated with nanoparticles-based biosensor has been developed for the detection of SARS-CoV-2. In this method, LAMP primer sets, F1ab (opening reading frame 1a/b) and nucleoprotein genes of the virus are amplified and detected simultaneously in one step. A nanoparticlebased biosensor is used to interpret the detection results. This assay is more accurate and highly sensitive as the sensitivity was 12 copies per reaction. Also, they produce low false-positive results. The detection method was very fast and was completed within an hour. 83 

The entire world is plagued by the menace of SARS-CoV-2 which has infiltrated every nook and corner. Both treatment and diagnosis of the virus remain challenging even though researchers have deciphered many facts about the virus. Correct diagnosis is the first step to initiate the treatment procedures in Covid-19 patients. The standard procedure adopted for SARS-CoV-2 identification involves CT scan, RT-qPCR and LFICS along with the rapid diagnostic kit and strips implemented in many places. Unfortunately, due to the intense and grim situation in many places, these techniques are not sufficient and adequate to meet the demands of the teeming millions. Hence, designing more dependable, fast, affordable and widely accessible diagnostic tools or sensing strategies is the call of the hour and a challenge to be met by every scientist and researcher.

In this context, ultrasensitive biosensors targeting virus antigen detection have garnered a lot of impetus. Besides being user-friendly, the ability of combined detection of different biomarkers has helped the biosensors to smoothly make their way into clinics for diagnosis of many diseases. These biosensors are aptly designed and implemented in the early diagnosis of Covid-19 infection via detecting 10 of 13various virus antigens to appraise the severity of infection. In this context, special emphasis has been levied on EC biosensors, SERSbased biosensors, FET-based biosensors and SPR-based biosensors.

Another important issue, that is, a prerequisite of any biosensor is that it should be portable and reusable besides being highly selective so that it can distinguish viral targets from other elements with ease. The advent of nanotechnology has infused new potentiality for betterment in this arena. 90, 91 In this regard, the concept of nano-biosensor has germinated which is based on the binding of a biological species to perturb electrical properties thereby detecting analytes with high speed, fantabulous sensitivity and precision. The attention is principally to harness various nano-effects like quantum size effect, macro quantum tunnel effect and surface effect which is unique to nanomaterials. The high mutation rates in coronavirus affect the viral detection process. Ultra-sensitive nanobiosensors owing to specific physicochemical characteristics can detect low viral load thus paving roadmaps towards impending insights in diagnosis.

Besides, the dependability and reproducibility of nanobiosensors can be boosted by developing podiums that aid machine learning-based signal processing and direct readout of results. It is soon anticipated that these nanobiosensors will be incorporated into miniature biochips to make probes which we can carry in our pockets for onsite detection. For asymptomatic patients, such nanobiosensors will be readily available that can substantiate the presence or absence of SARS-CoV-2 anywhere. Similarly, smartphone-based biosensors also have the potential to become the point-of-care treatment strategies in the future.

Nevertheless, frequent use of such platforms is hindered owing to some drawbacks. Sometimes the nanobiosensor designed is not able to amplify the signals owing to improper biochemical reactions between the analyte and biological component of the biosensor.

This can be due to a lack of detailed knowledge about validated markers which hinders the specificity of nanobiosensors. Even the long-term safety and efficiency of such platforms need to be assessed impartially before recommending it as the gold standard of diagnosis. False exaggerated optimism regarding such nanobiosensors can harm its use. Thus, due to the unique characteristics of Covid-19 pathogen, designing portable and smart one-size-fits-all nanobiosensors may revolutionise the field of diagnostics making it much easier for identifying the pathogen even if it is present at a minimum amount.

Technology and Sarbari Acharya is thankful to KIIT University for the support provided.

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None to declare.

The text has been written and edited by RM, SA, and SN.

Data sharing not applicable to this article as no datasets were generated or analysed during the current study.

https://orcid.org/0000-0002-3812-3669