Development of gold nanoparticles-lateral flow test as a novel field diagnostic assay for detecting foot-and-mouth disease and lumpy skin disease viruses
Abstract
Background and Objectives: Rapid diagnosis is a cornerstone for controlling and preventing viral disease outbreaks. The present study is aimed to develop a rapid field diagnostic test based on gold nanoparticles for the detection of lumpy skin diseases (LSD), and foot and mouth diseases (FMD) in animals with high sensitivity and specificity.
Materials and Methods: FMD and LSD vaccines were used as a source of viruses' antigens for preparing monoclonal antibodies and conjugated with gold nanoparticles that characterized using various techniques such as UV-visible spectrometry, and transmission electron microscopy (TEM). Monoclonal antibodies (mAbs) for each serotype produced in experimental rats and used to capture antibodies for FMDV and /or LSDV. ELISA was used to screen 469 milk samples and 1165 serum samples from naturally infected cattle, buffaloes, sheep, and goats for validation of the lateral flow test (LFT). LSDV DNA was extracted from 117 blood and skin biopsy samples collected from naturally infected cattle during the 2019 outbreak.
Results: The specificity and sensitivity of GNP-LFT were evaluated and compared to Ag-ELISA, Western blot tests (WB), and PCR. A total of 95 FMDV positives out of 469 (20.25%) milk samples and 268 FMDV positives out of 1165 (23.3%) serum samples from natural infected cattle, buffaloes, sheep, and goats examined by ELISA to valid GNPS-LFT Viral LSDV DNA was detected in 60/117 (51.5%) and 31/60 (52.9%). While the GNPS-LFT assay results were 49/117 (41.9%) and 29/60 (48.3%) blood and skin biopsy samples, respectively. The diagnostic sensitivity and specificity of the GNP-LFT test were 72% and 82%, respectively. All vesicular fluid and epithelium samples collected from infected animals were identified as positive by the GNP- LFT and Ag-ELISA. Ag-ELISA, on the other hand, was 90% and 100%. While the developed GNP-LFT used LSDV polyclonal antibodies were similar to ELISA and IgG-WB with a sensitivity of 72.8% and a specificity of 88.8%, respectively.
Conclusion: The GNPS-LFT is a novel immunoassay based on mono or polyclonal antibodies conjugated with gold nanoparticles that provides an accurate, rapid, specific, and sensitive tool for field rapid diagnosis of FMDV and LSDV.
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15. Singh S, Dhawan A, Karhana S, Bhat M, Dinda AK. Quantum dots: an emerging tool for point-of-care testing. Micromachines (Basel) 2020; 11: 1058.
16. Kim J, Mohamed MAA, Zagorovsky K, Chan WCW. State of diagnosing infectious pathogens using colloidal nanomaterials. Biomaterials 2017; 146: 97-114.
17. Tian W, Xie HQ, Fu H, Pei X, Zhao B. Immunoanalysis methods for the detection of dioxins and related chemicals. Sensors (Basel) 2012; 12: 16710-16731.
18. Abdalhamed AM, Ghazy AA, Ibrahim ES, Arafa AA, Zeedan GSG. Therapeutic effect of biosynthetic gold nanoparticles on multidrug-resistant Escherichia coli and Salmonella species isolated from ruminants. Vet World 2021; 14: 3200-3210.
19. Abdalhamed AM, Hassanain MA, Zeedan GSG, Shaapan RM. Evaluation of Toxoplasma gondii propagated in specific pathogen free embryonated chicken egg, for diagnosis of toxoplasmosis in equids and human. J
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22. Sun B, Bosch A, Myrmel M. Extended direct lysis method for virus detection on berries including droplet digital RT-PCR or real time RT-PCR with reduced influence from inhibitors. J Virol Methods 2019; 271: 113638.
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25. Mahapatra M, Parida S. Foot and mouth disease vaccine strain selection: current approaches and future perspectives. Expert Rev Vaccines 2018; 17: 577-591.
26. Seki C, Robiolo B, Periolo O, Iglesias M, D'Antuono A, Maradei E, et al. Rapid methodology for antigenic profiling of FMDV field strains and for the control of identity, purity and viral integrity in commercial virus vaccines using monoclonal antibodies. Vet Microbiol 2009; 133: 239-251.
27. Li K, Wang S, Cao Y, Bao H, Li P, Sun P, et al. Development of foot-and-mouth disease virus-neutralizing monoclonal antibodies derived from plasmablasts of infected cattle and their germline gene usage. Front Immunol 2019; 10: 2870.
28. Huang HS, Tsai CL, Chang J, Hsu TC, Lin S, Lee CC. Multiplex PCR system for the rapid diagnosis of respiratory virus infection: systematic review and meta-analysis. Clin Microbiol Infect 2018; 24: 1055-1063.
29. Poonsuk K, Giménez-Lirola L, Zimmerman JJ. A review of foot-and-mouth disease virus (FMDV) testing in livestock with an emphasis on the use of alternative diagnostic specimens. Anim Health Res Rev 2018; 19: 100-112.
30. Nelson N, Paton DJ, Gubbins S, Colenutt C, Brown E, Hodgson S, et al. Predicting the ability of preclinical diagnosis to improve control of farm-to-farm foot-and-mouth disease transmission in cattle. J Clin Microbiol 2017; 55: 1671-1681.
31. He Y, Li K, Cao Y, Sun Z, Li P, Bao H, et al. Structures of foot-and-mouth disease virus with neutralizing antibodies derived from recovered natural host reveal a mechanism for cross-serotype neutralization. PLoS Pathog 2021; 17(4):e1009507.
32. Chen H, Liu K, Li Z, Wang P. Point of care testing for infectious diseases. Clin Chim Acta 2019; 493: 138-147.
33. Wang C, Liu M, Wang Z, Li S, Deng Y, He N. Point-of-care diagnostics for infectious diseases: from methods to devices. Nano Today 2021; 37: 101092.
34. Wang HM, Zhao GM, Hou PL, Yu L, He CQ, He HB. Rapid detection of foot-and-mouth disease virus using reverse transcription recombinase polymerase amplification combined with a lateral flow dipstick. J Virol Methods 2018; 261: 46-50.
35. Cao Y, Li K, Xing X, Zhu G, Fu Y, Bao H, et al. Development and validation of a competitive ELISA based on bovine monoclonal antibodies for the detection of neutralizing antibodies against foot-and-mouth disease virus serotype A. J Clin Microbiol 2022; 60(4): e0214221.
36. Paton DJ, Di Nardo A, Knowles NJ, Wadsworth J, Pituco EM, Cosivi O, et al. The history of foot-and-mouth disease virus serotype C: the first known extinct serotype? Virus Evol 2021; 7: veab009.
37. Salem R, El-Kholy AA, Ibrahim M. Eight novel single chain antibody fragments recognising VP2 of foot-and-mouth disease virus serotypes A, O, and SAT 2. Virology 2019; 533: 145-154.
38. Ahmed NH, Osman NA, Alfouz W, Saeed HM, Raouf YA. Serological detection and genetic characterization of foot-and-mouth disease virus from cattle in northern sudan, 2016 2018. Vet Anim Sci 2021; 13: 100188.
39. Mwiine FN, Velazquez‐Salinas L, Ahmed Z, Ochwo S, Munsey A, Kenney M, et al. Serological and phylogenetic characterization of foot and mouth disease viruses from Uganda during cross‐sectional surveillance study in cattle between 2014 and 2017. Transbound Emerg Dis 2019; 66: 2011-2024.
40. Chellapandian C, Ramkumar B, Puja P, Shanmuganathan R, Pugazhendhi A, Kumar P. Gold nanoparticles using red seaweed Gracilaria verrucosa: green synthesis, characterization and biocompatibility studies. Process Biochem 2019; 80: 58-63.
2. Zeedan GSG, Mahmoud AH, Abdalhamed AM, El-Razik KAEA, Khafagi MH, Zeina HAAA. Detection of lumpy skin disease virus in cattle using real-time polymerase chain reaction and serological diagnostic assays in different governorates in Egypt in 2017. Vet World 2019; 12:1093-1100.
3. Kang J, Tahir A, Wang H, Chang J. Applications of nanotechnology in virus detection, tracking, and infection mechanisms. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2021; 13(4): e1700.
4. Haegeman A, De Leeuw I, Saduakassova M, Van Campe W, Aerts L, Philips W, et al. The Importance of Quality Control of LSDV Live Attenuated Vaccines for Its Safe Application in the Field. Vaccines (Basel) 2021; 9: 1019.
5. Nielsen SS, Alvarez J, Bicout DJ, Calistri P, Canali E, Drewe JA, et al. Assessment of the control measures for category A diseases of animal health law: lumpy skin disease. EFSA J 2022; 20 (1): e07121.
6. Krotova A, Byadovskaya O, Shumilova I, van Schalkwyk A, Sprygin A. An in-depth bioinformatic analysis of the novel recombinant lumpy skin disease virus strains: from unique patterns to established lineage. BMC Genomics 2022; 23: 396.
7. Longjam N, Deb R, Sarmah AK, Tayo T, Awachat VB, Saxena VK. A brief review on diagnosis of foot-and-mouth disease of livestock: conventional to molecular tools. Vet Med Int 2011; 2011: 905768.
8. Rémond M, Kaiser C, Lebreton F. Diagnosis and screening of foot-and-mouth disease. Comp Immunol Microbiol Infect Dis 2002; 25: 309-320.
9. Hoelzer K, Bielke L, Blake DP, Cox E, Cutting SM, Devriendt B, et al. Vaccines as alternatives to antibiotics for food producing animals. Part 2: new approaches and potential solutions. Vet Res 2018; 49: 70.
10. Shehata AA, Elsheikh HA, Abd-Elfatah EB. Molecular detection and characterization of Orf virus from goats in Egypt. Open Vet J 2022; 12: 273-280.
11. Wang Y, Yu L, Kong X, Sun L. Application of nanodiagnostics in point-of-care tests for infectious diseases. Int J Nanomedicine 2017; 12: 4789-4803.
12. Chen Y, Wang Z, Liu Y, Wang X, Li Y, Ma P, et al. Recent advances in rapid pathogen detection method based on biosensors. Eur J Clin Microbiol Infect Dis 2018; 37: 1021-1037.
13. Tram DTN, Wang H, Sugiarto S, Li T, Ang WH, Lee C, et al. Advances in nanomaterials and their applications in point of care (POC) devices for the diagnosis of infectious diseases. Biotechnol Adv 2016; 34: 1275-1288.
14. De Paz HD, Brotons P, Muñoz-Almagro C. Molecular isothermal techniques for combating infectious diseases: towards low-cost point-of-care diagnostics. Expert Rev Mol Diagn 2014; 14: 827-843.
15. Singh S, Dhawan A, Karhana S, Bhat M, Dinda AK. Quantum dots: an emerging tool for point-of-care testing. Micromachines (Basel) 2020; 11: 1058.
16. Kim J, Mohamed MAA, Zagorovsky K, Chan WCW. State of diagnosing infectious pathogens using colloidal nanomaterials. Biomaterials 2017; 146: 97-114.
17. Tian W, Xie HQ, Fu H, Pei X, Zhao B. Immunoanalysis methods for the detection of dioxins and related chemicals. Sensors (Basel) 2012; 12: 16710-16731.
18. Abdalhamed AM, Ghazy AA, Ibrahim ES, Arafa AA, Zeedan GSG. Therapeutic effect of biosynthetic gold nanoparticles on multidrug-resistant Escherichia coli and Salmonella species isolated from ruminants. Vet World 2021; 14: 3200-3210.
19. Abdalhamed AM, Hassanain MA, Zeedan GSG, Shaapan RM. Evaluation of Toxoplasma gondii propagated in specific pathogen free embryonated chicken egg, for diagnosis of toxoplasmosis in equids and human. J
Parasit Dis 2019; 43: 498-505.
20. Andersson AM, Aspán A, Wisselink HJ, Smid B, Ridley A, Pelkonen S, et al. European inter-laboratory trial to evaluate the performance of three serological methods for diagnosis of Mycoplasma bovis infection in cattle using latent class analysis. BMC Vet Res 2019; 15: 369.
21. Maw MT, Khin MM, Hadrill D, Meki IK, Settypalli TBK, Kyin MM, et al. First Report of lumpy skin disease in myanmar and molecular analysis of the field virus isolates. Microorganisms 2022; 10: 897.
22. Sun B, Bosch A, Myrmel M. Extended direct lysis method for virus detection on berries including droplet digital RT-PCR or real time RT-PCR with reduced influence from inhibitors. J Virol Methods 2019; 271: 113638.
23. Oem JK, Kye SJ, Lee KN, Kim YJ, Park JY, Park JH, et al. Development of a Lightcycler-based reverse transcription polymerase chain reaction for the detection of foot-and-mouth disease virus. J Vet Sci 2005; 6:207-212.
24. Rajko-Nenow P, Flannery J, Arnold H, Howson ELA, Darpel K, Stedman A, et al. A rapid RT-LAMP assay for the detection of all four lineages of Peste des Petits Ruminants Virus. J Virol Methods 2019; 274: 113730.
25. Mahapatra M, Parida S. Foot and mouth disease vaccine strain selection: current approaches and future perspectives. Expert Rev Vaccines 2018; 17: 577-591.
26. Seki C, Robiolo B, Periolo O, Iglesias M, D'Antuono A, Maradei E, et al. Rapid methodology for antigenic profiling of FMDV field strains and for the control of identity, purity and viral integrity in commercial virus vaccines using monoclonal antibodies. Vet Microbiol 2009; 133: 239-251.
27. Li K, Wang S, Cao Y, Bao H, Li P, Sun P, et al. Development of foot-and-mouth disease virus-neutralizing monoclonal antibodies derived from plasmablasts of infected cattle and their germline gene usage. Front Immunol 2019; 10: 2870.
28. Huang HS, Tsai CL, Chang J, Hsu TC, Lin S, Lee CC. Multiplex PCR system for the rapid diagnosis of respiratory virus infection: systematic review and meta-analysis. Clin Microbiol Infect 2018; 24: 1055-1063.
29. Poonsuk K, Giménez-Lirola L, Zimmerman JJ. A review of foot-and-mouth disease virus (FMDV) testing in livestock with an emphasis on the use of alternative diagnostic specimens. Anim Health Res Rev 2018; 19: 100-112.
30. Nelson N, Paton DJ, Gubbins S, Colenutt C, Brown E, Hodgson S, et al. Predicting the ability of preclinical diagnosis to improve control of farm-to-farm foot-and-mouth disease transmission in cattle. J Clin Microbiol 2017; 55: 1671-1681.
31. He Y, Li K, Cao Y, Sun Z, Li P, Bao H, et al. Structures of foot-and-mouth disease virus with neutralizing antibodies derived from recovered natural host reveal a mechanism for cross-serotype neutralization. PLoS Pathog 2021; 17(4):e1009507.
32. Chen H, Liu K, Li Z, Wang P. Point of care testing for infectious diseases. Clin Chim Acta 2019; 493: 138-147.
33. Wang C, Liu M, Wang Z, Li S, Deng Y, He N. Point-of-care diagnostics for infectious diseases: from methods to devices. Nano Today 2021; 37: 101092.
34. Wang HM, Zhao GM, Hou PL, Yu L, He CQ, He HB. Rapid detection of foot-and-mouth disease virus using reverse transcription recombinase polymerase amplification combined with a lateral flow dipstick. J Virol Methods 2018; 261: 46-50.
35. Cao Y, Li K, Xing X, Zhu G, Fu Y, Bao H, et al. Development and validation of a competitive ELISA based on bovine monoclonal antibodies for the detection of neutralizing antibodies against foot-and-mouth disease virus serotype A. J Clin Microbiol 2022; 60(4): e0214221.
36. Paton DJ, Di Nardo A, Knowles NJ, Wadsworth J, Pituco EM, Cosivi O, et al. The history of foot-and-mouth disease virus serotype C: the first known extinct serotype? Virus Evol 2021; 7: veab009.
37. Salem R, El-Kholy AA, Ibrahim M. Eight novel single chain antibody fragments recognising VP2 of foot-and-mouth disease virus serotypes A, O, and SAT 2. Virology 2019; 533: 145-154.
38. Ahmed NH, Osman NA, Alfouz W, Saeed HM, Raouf YA. Serological detection and genetic characterization of foot-and-mouth disease virus from cattle in northern sudan, 2016 2018. Vet Anim Sci 2021; 13: 100188.
39. Mwiine FN, Velazquez‐Salinas L, Ahmed Z, Ochwo S, Munsey A, Kenney M, et al. Serological and phylogenetic characterization of foot and mouth disease viruses from Uganda during cross‐sectional surveillance study in cattle between 2014 and 2017. Transbound Emerg Dis 2019; 66: 2011-2024.
40. Chellapandian C, Ramkumar B, Puja P, Shanmuganathan R, Pugazhendhi A, Kumar P. Gold nanoparticles using red seaweed Gracilaria verrucosa: green synthesis, characterization and biocompatibility studies. Process Biochem 2019; 80: 58-63.
| Files | ||
| Issue | Vol 14 No 4 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i4.10245 | |
| Keywords | ||
| Foot-mouth disease; Gold nanoparticles; Lateral flow test; Lumpy skin disease virus; Rapid diagnostic tests; Skin lesion biopsy | ||
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How to Cite
1.
Abdalhamed A, Mohammed Naser S, Mohamed A, Zeedan G. Development of gold nanoparticles-lateral flow test as a novel field diagnostic assay for detecting foot-and-mouth disease and lumpy skin disease viruses. Iran J Microbiol. 2022;14(4):574-586.
