Immuno-Colorimetric Neutralization Test: A Surrogate for Widely Used Plaque Reduction Neutralization Tests in Public Health Virology
Abstract
:1. Developments in Detection of Viral Plaques
2. Plaque- and Focus-Based Neutralization Tests
3. Measurement of Neutralizing Antibodies to Public Health-Important Viruses
4. Sero-Epidemiological Investigations, Vaccine Trials, and Cross-Neutralization Studies
5. Recent Developments and Automations
6. Important Unresolved Issues and Way Forward
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Dulbecco, R. Production of Plaques in Monolayer Tissue Cultures by Single Particles of an Animal Virus. Proc. Natl. Acad. Sci. USA 1952, 38, 747–752. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dulbecco, R.; Vogt, M. Plaque formation and isolation of pure lines with poliomyelitis viruses. J. Exp. Med. 1954, 99, 167–182. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hotchin, J.E. Use of methyl cellulose gel as a substitute for agar in tissue-culture overlays. Nature 1955, 175, 352. [Google Scholar] [CrossRef] [PubMed]
- Schulze, I.T.; Schlesinger, R.W. Plaque assay of dengue and other group B arthropod-borne viruses under methyl cellulose overlay media. Virology 1963, 19, 40–48. [Google Scholar] [CrossRef]
- Rapp, F. Variants of herpes simplex virus: Isolation, characterization, and factors influencing plaque formation. J. Bacteriol. 1963, 86, 985–991. [Google Scholar] [CrossRef] [Green Version]
- Ennis, F.A. Immunity to mumps in an institutional epidemic. Correlation of insusceptibility to mumps with serum plaque neutralizing and hemagglutination-inhibiting antibodies. J. Infect. Dis. 1969, 119, 654–657. [Google Scholar] [CrossRef]
- Albrecht, P.; Herrmann, K.; Burns, G.R. Role of virus strain in conventional and enhanced measles plaque neutralization test. J. Virol. Methods 1981, 3, 251–260. [Google Scholar] [CrossRef]
- Morens, D.M.; Halstead, S.B.; Repik, P.M.; Putvatana, R.; Raybourne, N. Simplified plaque reduction neutralization assay for dengue viruses by semimicro methods in BHK-21 cells: Comparison of the BHK suspension test with standard plaque reduction neutralization. J. Clin. Microbiol. 1985, 22, 250–254. [Google Scholar] [CrossRef] [Green Version]
- Matrosovich, M.; Matrosovich, T.; Garten, W.; Klenk, H.D. New low-viscosity overlay medium for viral plaque assays. Virol. J. 2006, 3, 63. [Google Scholar] [CrossRef] [Green Version]
- Cohen, B.J.; Audet, S.; Andrews, N.; Beeler, J.; WHO working group on measles plaque reduction neutralization test. Plaque reduction neutralization test for measles antibodies: Description of a standardised laboratory method for use in immunogenicity studies of aerosol vaccination. Vaccine 2007, 26, 59–66. [Google Scholar] [CrossRef]
- Weldon, W.C.; Oberste, M.S.; Pallansch, M.A. Standardized Methods for Detection of Poliovirus Antibodies. Methods Mol. Biol. 2016, 1387, 145–176. [Google Scholar] [CrossRef]
- Tomori, O.; Johnson, K.M.; Kiley, M.P.; Elliott, L.H. Standardization of a plaque assay for Lassa virus. J. Med. Virol. 1987, 22, 77–89. [Google Scholar] [CrossRef]
- Mauldin, J.; Carbone, K.; Hsu, H.; Yolken, R.; Rubin, S. Mumps virus-specific antibody titers from pre-vaccine era sera: Comparison of the plaque reduction neutralization assay and enzyme immunoassays. J. Clin. Microbiol. 2005, 43, 4847–4851. [Google Scholar] [CrossRef] [Green Version]
- Okuno, Y.; Igarashi, A.; Fukai, K. Neutralization tests for dengue and Japanese encephalitis viruses by the focus reduction method using peroxidase-anti-peroxidase staining. Biken J. 1978, 21, 137–147. [Google Scholar]
- Okuno, Y.; Fukunaga, T.; Tadano, M.; Okamoto, Y.; Ohnishi, T.; Takagi, M. Rapid focus reduction neutralization test of Japanese encephalitis virus in microtiter system. Brief report. Arch. Virol. 1985, 86, 129–135. [Google Scholar] [CrossRef]
- Okuno, Y.; Yamanishi, K.; Lwin, S.; Takahashi, M. Micro-neutralization test for mumps virus using the 96-well tissue culture plate and PAP (peroxidase-antiperoxidase) staining technique. Microbiol. Immunol. 1985, 29, 327–335. [Google Scholar] [CrossRef] [Green Version]
- Raharjo, E.; Tadano, M.; Okamoto, Y.; Okuno, Y. Development of a micro-neutralization test for chikungunya virus. Biken J. 1986, 29, 27–30. [Google Scholar]
- Okuno, Y.; Tanaka, K.; Baba, K.; Maeda, A.; Kunita, N.; Ueda, S. Rapid focus reduction neutralization test of influenza A and B viruses in microtiter system. J. Clin. Microbiol. 1990, 28, 1308–1313. [Google Scholar] [CrossRef] [Green Version]
- Samuel, D.; Megson, B.; Strang, M.; Appleton, H. A microtitre plate method for isolation and typing of poliovirus using a blue-cell ELISA. J. Virol. Methods 2000, 90, 125–133. [Google Scholar] [CrossRef]
- Chen, M.H.; Zhu, Z.; Zhang, Y.; Favors, S.; Xu, W.B.; Featherstone, D.A.; Icenogle, J.P. An indirect immunocolorimetric assay to detect rubella virus infected cells. J. Virol. Methods 2007, 146, 414–418. [Google Scholar] [CrossRef]
- Vaidya, S.R.; Brown, D.W.; Jin, L.; Samuel, D.; Andrews, N.; Brown, K.E. Development of a focus reduction neutralization test (FRNT) for detection of mumps virus neutralizing antibodies. J. Virol. Methods 2010, 163, 153–156. [Google Scholar] [CrossRef] [PubMed]
- Vaidya, S.R.; Kumbhar, N.S.; Bhide, V.S. Detection of measles, mumps and rubella viruses by immuno-colorimetric assay and its application in focus reduction neutralization tests. Microbiol. Immunol. 2014, 58, 666–674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zielinska, E.; Liu, D.; Wu, H.Y.; Quiroz, J.; Rappaport, R.; Yang, D.P. Development of an improved microneutralization assay for respiratory syncytial virus by automated plaque counting using imaging analysis. Virol. J. 2005, 2, 84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, L.; He, D.; Tang, M.; Li, Z.; Liu, C.; Xu, L.; Chen, Y.; Du, H.; Zhao, Q.; Zhang, J.; et al. Development of an enzyme-linked immunosorbent spot assay to measure serum-neutralizing antibodies against coxsackievirus B3. Clin. Vaccine Immunol. 2014, 21, 312–320. [Google Scholar] [CrossRef] [Green Version]
- Whiteman, M.C.; Bogardus, L.; Giacone, D.G.; Rubinstein, L.J.; Antonello, J.M.; Sun, D.; Daijogo, S.; Gurney, K.B. Virus Reduction Neutralization Test: A Single-Cell Imaging High-Throughput Virus Neutralization Assay for Dengue. Am. J. Trop. Med. Hyg. 2018, 99, 1430–1439. [Google Scholar] [CrossRef]
- Lopez, A.L.; Adams, C.; Ylade, M.; Jadi, R.; Daag, J.V.; Molloy, C.T.; Agrupis, K.A.; Kim, D.R.; Silva, M.W.; Yoon, I.K.; et al. Determining dengue virus serostatus by indirect IgG ELISA compared with focus reduction neutralization test in children in Cebu, Philippines: A prospective population-based study. Lancet Glob. Health 2021, 9, e44–e51. [Google Scholar] [CrossRef]
- Jirakanjanakit, N.; Sanohsomneing, T.; Yoksan, S.; Bhamarapravati, N. The micro-focus reduction neutralization test for determining dengue and Japanese encephalitis neutralizing antibodies in volunteers vaccinated against dengue. Trans. R. Soc. Trop. Med. Hyg. 1997, 91, 614–617. [Google Scholar] [CrossRef]
- Watanabe, K.; Hirokawa, C.; Kon, M.; Tamura, T.; Nishikawa, M. Estimation of focus reduction neutralization test for measurement of neutralizing antibody titer against Japanese encephalitis virus. Jpn. J. Infect. Dis. 2008, 61, 424–425. [Google Scholar] [CrossRef]
- Park, Y.; Kim, A.R.; Hwang, Y.H.; Yang, H.; Lee, J.W.; Kim, M.Y.; Kim, H.S.; Chung, G.T.; Yoo, J.S.; Kim, Y.J.; et al. Comparison of plaque reduction and focus reduction neutralization tests for the measurement of neutralizing antibody titers against japanese encephalitis virus. J. Virol. Methods 2022, 306, 114540. [Google Scholar] [CrossRef]
- Murata, R.; Hashiguchi, K.; Yoshii, K.; Kariwa, H.; Nakajima, K.; Ivanov, L.I.; Leonova, G.N.; Takashima, I. Seroprevalence of West Nile virus in wild birds in far eastern Russia using a focus reduction neutralization test. Am. J. Trop. Med. Hyg. 2011, 84, 461–465. [Google Scholar] [CrossRef]
- Friedrich, B.M.; Beasley, D.W. ELISA and Neutralization Methods to Measure Anti-West Nile Virus Antibody Responses. Methods Mol. Biol. 2016, 1435, 129–141. [Google Scholar] [CrossRef]
- Ngwe Tun, M.M.; Inoue, S.; Thant, K.Z.; Talemaitoga, N.; Aryati, A.; Dimaano, E.M.; Matias, R.R.; Buerano, C.C.; Natividad, F.F.; Abeyewickreme, W.; et al. Retrospective seroepidemiological study of chikungunya infection in South Asia, Southeast Asia and the Pacific region. Epidemiol. Infect. 2016, 144, 2268–2275. [Google Scholar] [CrossRef] [Green Version]
- Vanderheiden, A.; Edara, V.V.; Floyd, K.; Kauffman, R.C.; Mantus, G.; Anderson, E.; Rouphael, N.; Edupuganti, S.; Shi, P.Y.; Menachery, V.D.; et al. Development of a Rapid Focus Reduction Neutralization Test Assay for Measuring SARS-CoV-2 Neutralizing Antibodies. Curr. Protoc. Immunol. 2020, 131, e116. [Google Scholar] [CrossRef]
- Chang, A.; Akhtar, A.; Linderman, S.L.; Lai, L.; Orellana-Noia, V.M.; Valanparambil, R.; Ahmed, H.; Zarnitsyna, V.I.; McCook-Veal, A.A.; Switchenko, J.M.; et al. Humoral Responses Against SARS-CoV-2 and Variants of Concern After mRNA Vaccines in Patients With Non-Hodgkin Lymphoma and Chronic Lymphocytic Leukemia. J. Clin. Oncol. 2022, 40, 3020–3031. [Google Scholar] [CrossRef]
- Medigeshi, G.R.; Batra, G.; Murugesan, D.R.; Thiruvengadam, R.; Chattopadhyay, S.; Das, B.; Gosain, M.; Ayushi Singh, J.; Anbalagan, A.; Shaman, H.; et al. Sub-optimal neutralisation of omicron (B.1.1.529) variant by antibodies induced by vaccine alone or SARS-CoV-2 Infection plus vaccine (hybrid immunity) post 6-months. EBioMedicine 2022, 78, 103938. [Google Scholar] [CrossRef]
- Khan, K.; Karim, F.; Cele, S.; Reedoy, K.; San, J.E.; Lustig, G.; Tegally, H.; Rosenberg, Y.; Bernstein, M.; Jule, Z.; et al. Omicron infection enhances Delta antibody immunity in vaccinated persons. Nature 2022, 607, 356–359. [Google Scholar] [CrossRef]
- Hassert, M.; Geerling, E.; Stone, E.T.; Steffen, T.L.; Feldman, M.S.; Dickson, A.L.; Class, J.; Richner, J.M.; Brien, J.D.; Pinto, A.K. mRNA induced expression of human angiotensin-converting enzyme 2 in mice for the study of the adaptive immune response to severe acute respiratory syndrome coronavirus 2. PLoS Pathog. 2020, 16, e1009163. [Google Scholar] [CrossRef]
- Won, H.; Kim, A.R.; Yoo, J.S.; Chung, G.T.; Kang, H.J.; Kim, S.J.; Kim, S.S.; Lee, J.W. Cross-neutralization between vaccine and circulating wild-type mumps viruses in Korea. Vaccine 2021, 39, 1870–1876. [Google Scholar] [CrossRef]
- Gouma, S.; Ten Hulscher, H.I.; Schurink-van ‘t Klooster, T.M.; de Melker, H.E.; Boland, G.J.; Kaaijk, P.; van Els, C.A.C.M.; Koopmans, M.P.G.; van Binnendijk, R.S. Mumps-specific cross-neutralization by MMR vaccine-induced antibodies predicts protection against mumps virus infection. Vaccine 2016, 34, 4166–4171. [Google Scholar] [CrossRef]
- Vaidya, S.R.; Kamble, M.B.; Chowdhury, D.T.; Kumbhar, N.S. Measles & rubella outbreaks in Maharashtra State, India. Indian J. Med. Res. 2016, 143, 227–231. [Google Scholar] [CrossRef] [Green Version]
- Vaidya, S.R.; Dvivedi, G.M.; Jadhav, S.M. Cross-neutralization between three mumps viruses & mapping of haemagglutinin-neuraminidase (HN) epitopes. Indian J. Med. Res. 2016, 143, 37–42. [Google Scholar] [CrossRef] [PubMed]
- Vaidya, S.R.; Hamde, V.S.; Kumbhar, N.S.; Walimbe, A.M. Utility of neutralization test for laboratory diagnosis of suspected mumps. Microbiol. Immunol. 2018, 62, 243–247. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vaidya, S.R.; Kasibhatla, S.M.; Kamble, M.B.; Munivenkatappa, A.; Kumbhar, N.S.; Jayaswamy, M.M.; Ramtirthkar, M.R.; Kale, M.M.; Kulkarni-Kale, U. Genetic and antigenic characterization of wild type rubella viruses isolated from India. Vaccine 2021, 39, 876–881. [Google Scholar] [CrossRef] [PubMed]
- Vaidya, S.R.; Kumbhar, N.S.; Kamble, S.S.; Walimbe, A.M.; Ashok, M. Usefulness of diverse serological tests in the laboratory diagnosis of fever with skin-rash cases in children. J. Clin. Virol. Plus 2022, 2, 100071. [Google Scholar] [CrossRef]
- Terletskaia-Ladwig, E.; Enders, G.; Meier, S.; Dietz, K.; Enders, M. Development and evaluation of an automatable focus reduction neutralisation test for the detection of measles virus antibodies using imaging analysis. J. Virol. Methods 2011, 178, 124–128. [Google Scholar] [CrossRef]
- Terletskaia-Ladwig, E.; Meier, S.; Enders, M. Improved high-throughput virus neutralisation assay for antibody estimation against pandemic and seasonal influenza strains from 2009 to 2011. J. Virol. Methods 2013, 189, 341–347. [Google Scholar] [CrossRef]
- Lin, Y.; Gu, Y.; McCauley, J.W. Optimization of a Quantitative Micro-neutralization Assay. J. Vis. Exp. 2016, 118, 54897. [Google Scholar] [CrossRef] [Green Version]
- Smith, J.L.; Hirsch, A.J. Analysis of Serum Anti-Zika Virus Antibodies by Focus Reduction Neutralization Test. Methods Mol. Biol. 2020, 2142, 73–80. [Google Scholar] [CrossRef]
- Scheck, M.K.; Lehmann, L.; Zaucha, M.; Schwarzlmueller, P.; Huber, K.; Pritsch, M.; Barba-Spaeth, G.; Thorn-Seshold, O.; Krug, A.B.; Endres, S.; et al. FluoRNT: A robust, efficient assay for the detection of neutralising antibodies against yellow fever virus 17D. PLoS ONE 2022, 17, e0262149. [Google Scholar] [CrossRef]
- Luo, Y.; Xiong, D.; Li, H.H.; Qiu, S.P.; Lin, C.L.; Chen, Q.; Huang, C.H.; Yuan, Q.; Zhang, J.; Xia, N.S. Development of an HSV-1 neutralization test with a glycoprotein D specific antibody for measurement of neutralizing antibody titer in human sera. Virol. J. 2016, 13, 44. [Google Scholar] [CrossRef] [Green Version]
- Lundkvist, A.; Hukic, M.; Hörling, J.; Gilljam, M.; Nichol, S.; Niklasson, B. Puumala and Dobrava viruses cause hemorrhagic fever with renal syndrome in Bosnia-Herzegovina: Evidence of highly cross-neutralizing antibody responses in early patient sera. J. Med. Virol. 1997, 53, 51–59. [Google Scholar] [CrossRef]
- Lundkvist, A.; Vapalahti, O.; Henttonen, H.; Vaheri, A.; Plyusnin, A. Hantavirus infections among mammalogists studied by focus reduction neutralisation test. Eur. J. Clin. Microbiol. Infect. Dis. 2000, 19, 802–803. [Google Scholar] [CrossRef] [PubMed]
- Lundkvist, A.; Lindegren, G.; Brus Sjölander, K.; Mavtchoutko, V.; Vene, S.; Plyusnin, A.; Kalnina, V. Hantavirus infections in Latvia. Eur. J. Clin. Microbiol. Infect. Dis. 2002, 21, 626–629. [Google Scholar] [CrossRef] [PubMed]
- Goeijenbier, M.; Hartskeerl, R.A.; Reimerink, J.; Verner-Carlsson, J.; Wagenaar, J.F.; Goris, M.G.; Martina, B.E.; Lundkvist, Å.; Koopmans, M.; Osterhaus, A.D.; et al. The hanta hunting study: Underdiagnosis of Puumala hantavirus infections in symptomatic non-travelling leptospirosis-suspected patients in the Netherlands, in 2010 and April to November 2011. Eurosurveillance 2014, 19, 20878. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gerna, G.; Chambers, R.W. Varicella-zoster plaque assay and plaque reduction neutralization test by the immunoperoxidase technique. J. Clin. Microbiol. 1976, 4, 437–442. [Google Scholar] [CrossRef]
- Chen, L.; Liu, J.; Wang, W.; Ye, J.; Wen, L.; Zhao, Q.; Zhu, H.; Cheng, T.; Xia, N. Development of a varicella-zoster virus neutralization assay using a glycoprotein K antibody enzyme-linked immunosorbent spot assay. J. Virol. Methods 2014, 200, 10–14. [Google Scholar] [CrossRef]
- Fournier, C.; Duverlie, G.; François, C.; Schnuriger, A.; Dedeurwaerder, S.; Brochot, E.; Capron, D.; Wychowski, C.; Thibault, V.; Castelain, S. A focus reduction neutralization assay for hepatitis C virus neutralizing antibodies. Virol. J. 2007, 4, 35. [Google Scholar] [CrossRef] [Green Version]
- Flaegstad, T.; Traavik, T.; Christie, K.E.; Joergensen, J. Neutralization test for BK virus: Plaque reduction detected by immunoperoxidase staining. J. Med. Virol. 1986, 19, 287–296. [Google Scholar] [CrossRef]
- Falsey, A.R.; Formica, M.A.; Walsh, E.E. Microneutralization assay for the measurement of neutralizing antibodies to human metapneumovirus. J. Clin. Virol. 2009, 46, 314–317. [Google Scholar] [CrossRef] [Green Version]
- Craigo, J.K.; Ezzelarab, C.; Montelaro, R.C. Development of a high throughput, semi-automated, infectious center cell-based ELISA for equine infectious anemia virus. J. Virol. Methods 2012, 185, 221–227. [Google Scholar] [CrossRef] [Green Version]
- Bannai, H.; Nemoto, M.; Tsujimura, K.; Yamanaka, T.; Kondo, T.; Matsumura, T. Development of a focus-reduction neutralizing test for detecting equine herpesvirus type-1-neutralizing antibodies. J. Vet. Med. Sci. 2013, 75, 1209–1212. [Google Scholar] [CrossRef] [Green Version]
- Canakoglu, N.; Berber, E.; Ertek, M.; Yoruk, M.D.; Tonbak, S.; Bolat, Y.; Aktas, M.; Kalkan, A.; Ozdarendeli, A. Pseudo-plaque reduction neutralization test (PPRNT) for the measurement of neutralizing antibodies to Crimean-Congo hemorrhagic fever virus. Virol. J. 2013, 10, 6. [Google Scholar] [CrossRef] [Green Version]
- Bamunuarachchi, G.; Harastani, H.; Rothlauf, P.W.; Dai, Y.N.; Ellebedy, A.; Fremont, D.; Whelan, S.P.J.; Wang, D.; Boon, A.C.M. Detection of Bourbon Virus-Specific Serum Neutralizing Antibodies in Human Serum in Missouri, USA. mSphere 2022, 7, e0016422. [Google Scholar] [CrossRef]
- Abai, A.M.; Smith, L.R.; Wloch, M.K. Novel microneutralization assay for HCMV using automated data collection and analysis. J. Immunol. Methods 2007, 322, 82–93. [Google Scholar] [CrossRef]
- Chen, R.T.; Markowitz, L.E.; Albrecht, P.; Stewart, J.A.; Mofenson, L.M.; Preblud, S.R.; Orenstein, W.A. Measles antibody: Reevaluation of protective titers. J. Infect. Dis. 1990, 162, 1036–1042. [Google Scholar] [CrossRef]
- Karger, A.B.; Brien, J.D.; Christen, J.M.; Dhakal, S.; Kemp, T.J.; Klein, S.L.; Pinto, L.A.; Premkumar, L.; Roback, J.D.; Binder, R.A.; et al. The Serological Sciences Network (SeroNet) for COVID-19: Depth and Breadth of Serology Assays and Plans for Assay Harmonization. mSphere 2022, 7, e0019322. [Google Scholar] [CrossRef]
- Simões, M.; Camacho, L.A.; Yamamura, A.M.; Miranda, E.H.; Cajaraville, A.C.; da Silva Freire, M. Evaluation of accuracy and reliability of the plaque reduction neutralization test (micro-PRNT) in detection of yellow fever virus antibodies. Biologicals 2012, 40, 399–404. [Google Scholar] [CrossRef] [Green Version]
- Fatemi Nasab, G.S.; Salimi, V.; Abbasi, S.; Adjami Nezhad Fard, F.; Mokhtari Azad, T. Comparison of neutralizing antibody titers against outbreak-associated measles genotypes (D4, H1 and B3) in Iran. Pathog. Dis. 2016, 74, ftw089. [Google Scholar] [CrossRef] [Green Version]
- Moon, S.S.; Wang, Y.; Shane, A.L.; Nguyen, T.; Ray, P.; Dennehy, P.; Baek, L.J.; Parashar, U.; Glass, R.I.; Jiang, B. Inhibitory effect of breast milk on infectivity of live oral rotavirus vaccines. Pediatr. Infect. Dis. J. 2010, 29, 919–923. [Google Scholar] [CrossRef] [Green Version]
- Moon, S.S.; Groome, M.J.; Velasquez, D.E.; Parashar, U.D.; Jones, S.; Koen, A.; van Niekerk, N.; Jiang, B.; Madhi, S.A. Prevaccination Rotavirus Serum IgG and IgA Are Associated With Lower Immunogenicity of Live, Oral Human Rotavirus Vaccine in South African Infants. Clin. Infect. Dis. 2016, 62, 157–165. [Google Scholar] [CrossRef] [Green Version]
- Taketa-Graham, M.; Powell Pereira, J.L.; Baylis, E.; Cossen, C.; Oceguera, L.; Patiris, P.; Chiles, R.; Hanson, C.V.; Forghani, B. High throughput quantitative colorimetric microneutralization assay for the confirmation and differentiation of West Nile Virus and St. Louis encephalitis virus. Am. J. Trop. Med. Hyg. 2010, 82, 501–504. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Katzelnick, L.C.; Coello Escoto, A.; McElvany, B.D.; Chávez, C.; Salje, H.; Luo, W.; Rodriguez-Barraquer, I.; Jarman, R.; Durbin, A.P.; Diehl, S.A.; et al. Viridot: An automated virus plaque (immunofocus) counter for the measurement of serological neutralizing responses with application to dengue virus. PLoS Negl. Trop. Dis. 2018, 12, e0006862. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yu, P.; Ma, C.; Nawaz, M.; Han, L.; Zhang, J.; Du, Q.; Zhang, L.; Feng, Q.; Wang, J.; Xu, J. Outbreak of acute respiratory disease caused by human adenovirus type 7 in a military training camp in Shaanxi, China. Microbiol. Immunol. 2013, 57, 553–560. [Google Scholar] [CrossRef] [PubMed]
- Coelho, I.C.B.; Haguinet, F.; Colares, J.K.B.; Coelho, Z.C.B.; Araújo, F.M.C.; Schwarcz, W.D.; Duarte, A.C.; Borges, B.; Minguet, C.; Guignard, A. Dengue Infection in Children in Fortaleza, Brazil: A 3-Year School-Based Prospective Cohort Study. Am. J. Trop. Med. Hyg. 2020, 103, 100–111. [Google Scholar] [CrossRef] [PubMed]
- Tigoi, C.; Lwande, O.; Orindi, B.; Irura, Z.; Ongus, J.; Sang, R. Seroepidemiology of selected arboviruses in febrile patients visiting selected health facilities in the lake/river basin areas of Lake Baringo, Lake Naivasha, and Tana River, Kenya. Vector Borne Zoonotic Dis. 2015, 15, 124–132. [Google Scholar] [CrossRef] [Green Version]
- Vilibic-Cavlek, T.; Savic, V.; Sabadi, D.; Peric, L.; Barbic, L.; Klobucar, A.; Miklausic, B.; Tabain, I.; Santini, M.; Vucelja, M.; et al. Prevalence and molecular epidemiology of West Nile and Usutu virus infections in Croatia in the ‘One health’ context, 2018. Transbound. Emerg. Dis. 2019, 66, 1946–1957. [Google Scholar] [CrossRef]
- Nguyen, C.T.; Moi, M.L.; Le, T.Q.M.; Nguyen, T.T.T.; Vu, T.B.H.; Nguyen, H.T.; Pham, T.T.H.; Le, T.H.T.; Nguyen, L.M.H.; Phu Ly, M.H.; et al. Prevalence of Zika virus neutralizing antibodies in healthy adults in Vietnam during and after the Zika virus epidemic season: A longitudinal population-based survey. BMC Infect. Dis. 2020, 20, 332. [Google Scholar] [CrossRef]
- Luvai, E.A.C.; Kyaw, A.K.; Sabin, N.S.; Yu, F.; Hmone, S.W.; Thant, K.Z.; Inoue, S.; Morita, K.; Ngwe Tun, M.M. Evidence of Chikungunya virus seroprevalence in Myanmar among dengue-suspected patients and healthy volunteers in 2013, 2015, and 2018. PLoS Negl. Trop. Dis. 2021, 15, e0009961. [Google Scholar] [CrossRef]
- Jackson, K.C.; Gidlewski, T.; Root, J.J.; Bosco-Lauth, A.M.; Lash, R.R.; Harmon, J.R.; Brault, A.C.; Panella, N.A.; Nicholson, W.L.; Komar, N. Bourbon Virus in Wild and Domestic Animals, Missouri, USA, 2012–2013. Emerg. Infect. Dis. 2019, 25, 1752–1753. [Google Scholar] [CrossRef]
- Kaduskar, O.; Gurav, Y.K.; Deshpande, K.; Desphande, G.R.; Yadav, P.; Rakhe, A.; Tilekar, B.N.; Gomade, P.; Salunke, A.; Patil, C.; et al. Understanding the dynamics of IgM & IgG antibodies in COVID-19-positive patients. Indian J. Med. Res. 2022, 155, 565–569. [Google Scholar] [CrossRef]
- Furuya, A.K.M.; Hunt, D.; George, K.S.; Dupuis, A.P., 2nd; Kramer, L.D.; Shi, P.Y.; Wong, S. Use of the immunoglobulin G avidity assay to differentiate between recent Zika and past dengue virus infections. Clin. Sci. 2019, 133, 859–867. [Google Scholar] [CrossRef]
- Nguyen, T.H.T.; Clapham, H.E.; Phung, K.L.; Nguyen, T.K.; DInh, T.T.; Nguyen, T.H.Q.; Tran, V.N.; Whitehead, S.; Simmons, C.; Wolbers, M.; et al. Methods to discriminate primary from secondary dengue during acute symptomatic infection. BMC Infect. Dis. 2018, 18, 375. [Google Scholar] [CrossRef] [Green Version]
- Medialdea-Carrera, R.; Levy, F.; Castanha, P.; Carvalho de Sequeira, P.; Brasil, P.; Lewis-Ximenez, L.L.; Turtle, L.; Solomon, T.; Bispo de Filippis, A.M.; Brown, D.W.; et al. A Systematic Evaluation of IgM and IgG Antibody Assay Accuracy in Diagnosing Acute Zika Virus Infection in Brazil: Lessons Relevant to Emerging Infections. J. Clin. Microbiol. 2021, 59, e0289320. [Google Scholar] [CrossRef]
- Sevencan, F.; Gözalan, A.; Uyar, Y.; Kavakli, I.; Türkyilmaz, B.; Ertek, M.; Lundkvist, A. Serologic Investigation of Hantavirus Infection in Patients with Previous Thrombocytopenia, and Elevated Urea and Creatinine Levels in an Epidemic Region of Turkey. Jpn. J. Infect. Dis. 2015, 68, 488–493. [Google Scholar] [CrossRef] [Green Version]
- Theel, E.S.; Sorenson, M.; Rahman, C.; Granger, D.; Vaughn, A.; Breeher, L. Performance Characteristics of a Multiplex Flow Immunoassay for Detection of IgG-Class Antibodies to Measles, Mumps, Rubella, and Varicella-Zoster Viruses in Presumptively Immune Health Care Workers. J. Clin. Microbiol. 2020, 58, e00136-20. [Google Scholar] [CrossRef]
- Xie, X.; Nielsen, M.C.; Muruato, A.E.; Fontes-Garfias, C.R.; Ren, P. Evaluation of a SARS-CoV-2 lateral flow assay using the plaque reduction neutralization test. Diagn. Microbiol. Infect. Dis. 2021, 99, 115248. [Google Scholar] [CrossRef]
- González, A.M.; Nguyen, T.V.; Azevedo, M.S.; Jeong, K.; Agarib, F.; Iosef, C.; Chang, K.; Lovgren-Bengtsson, K.; Morein, B.; Saif, L.J. Antibody responses to human rotavirus (HRV) in gnotobiotic pigs following a new prime/boost vaccine strategy using oral attenuated HRV priming and intranasal VP2/6 rotavirus-like particle (VLP) boosting with ISCOM. Clin. Exp. Immunol. 2004, 135, 361–372. [Google Scholar] [CrossRef]
- Zhang, W.; Azevedo, M.S.; Wen, K.; Gonzalez, A.; Saif, L.J.; Li, G.; Yousef, A.E.; Yuan, L. Probiotic Lactobacillus acidophilus enhances the immunogenicity of an oral rotavirus vaccine in gnotobiotic pigs. Vaccine 2008, 26, 3655–3661. [Google Scholar] [CrossRef] [Green Version]
- Azevedo, M.S.; Yuan, L.; Iosef, C.; Chang, K.O.; Kim, Y.; Nguyen, T.V.; Saif, L.J. Magnitude of serum and intestinal antibody responses induced by sequential replicating and nonreplicating rotavirus vaccines in gnotobiotic pigs and correlation with protection. Clin. Diagn. Lab. Immunol. 2004, 11, 12–20. [Google Scholar] [CrossRef] [Green Version]
- Maha, M.M.; Ali, M.A.; Abdel-Rehim, S.E.; Abu-Shady, E.A.; El-Naggar, B.M.; Maha, Y.Z. The role of coxsackieviruses infection in the children of insulin dependent diabetes mellitus. J. Egypt. Public Health Assoc. 2003, 78, 305–318. [Google Scholar]
- Çelebi, G.; Öztoprak, N.; Öktem, İ.M.A.; Heyman, P.; Lundkvist, Å.; Wahlström, M.; Köktürk, F.; Pişkin, N. Dynamics of Puumala hantavirus outbreak in Black Sea Region, Turkey. Zoonoses Public Health 2019, 66, 783–797. [Google Scholar] [CrossRef] [PubMed]
- Saipin, K.; Thaisomboonsuk, B.; Siridechadilok, B.; Chaitaveep, N.; Ramasoota, P.; Puttikhunt, C.; Sangiambut, S.; Jones, A.; Kraivong, R.; Sriburi, R.; et al. A replication competent luciferase-secreting DENV2 reporter for sero-epidemiological surveillance of neutralizing and enhancing antibodies. J. Virol. Methods 2022, 308, 114577. [Google Scholar] [CrossRef] [PubMed]
- Kramps, J.A.; Magdalena, J.; Quak, J.; Weerdmeester, K.; Kaashoek, M.J.; Maris-Veldhuis, M.A.; Rijsewijk, F.A.; Keil, G.; van Oirschot, J.T. A simple, specific, and highly sensitive blocking enzyme-linked immunosorbent assay for detection of antibodies to bovine herpesvirus 1. J. Clin. Microbiol. 1994, 32, 2175–2181. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kramps, J.A.; Perrin, B.; Edwards, S.; van Oirschot, J.T. A European inter-laboratory trial to evaluate the reliability of serological diagnosis of bovine herpesvirus 1 infections. Vet. Microbiol. 1996, 53, 153–161. [Google Scholar] [CrossRef]
- Nzietchueng, S.; Kitua, A.; Nyatanyi, T.; Rwego, I.B. Facilitating implementation of the one health approach: A definition of a one health intervention. One Health 2023, 16, 100491. [Google Scholar] [CrossRef]
Virus/Strain | Virus Detection Automation/Manual | FRNT or Similar Modified Protocol | Cell Substrate | Assay Time | Samples Tested EPD/Vaccine | Reference |
---|---|---|---|---|---|---|
Respiratory Syncytial virus (A2 strain) | Immunospot analyzer | FRNT | Vero CCL-34 | 3 days | Pooled serum panel | [23] |
Coxsackievirus B3(XM08-2035) | Immunospot analyzer | Nt-ELISPOT/ FRNT | RD | 12 h | Suspected HFMD cases | [24] |
Dengue Virus (DENV) | Imaging cytometer | FRNT | Vero CCL-81 | 1 day | Sera of 81 DEN-4 cases | [25] |
DENV (serotype 1, 2, 3, 4) | Immunospot analyzer | FRNT | Vero-81 | 48 h | Longitudinal seroprevalence | [26] |
Dengue (1–4) Japanese Encephalitis Virus (JEV) (Nakayama, Beijing) | Manual | Micro FRNT | C6/36 | Not Available | Dengue negative & vaccinated 102-sera | [27] |
JEV | Manual | FRNT | Vero Osaka | 46 h | 133 JEV PRNT positive sera | [28] |
JEV (Nakayama, Beijing vaccine) | Immunospot analyzer | FRNT | Vero-E6 | 48 h | 39-sera (Unvaccinated) 53-sera (JE vaccinated) | [29] |
JEV | Manual/Microscope | FRNT | BHK-21 | 24–28 h | 20 sera (healthy adults) | [15] |
West Nile (NY99-6922)JE (Genotype-1) | Microscope/ Manual | FRNT | BHK-21 CCL-10 | 24 h | 145-wild birds sera | [30] |
West Nile virus | Manual | FRNT | Vero CCL-81 | 2-days | Not Available | [31] |
Chikungunya virus (S-27 Africa, RRV T48) | Stereomicroscope | FRNT | Vero | 30 h | 800-sera from suspected dengue cases | [32] |
Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2) | Immunospot analyzer | FRNT | Vero-E6 | 3 days | Plasma samples 9-healthy controls 10-convalescent | [33,34] |
SARS-CoV-2 (ancestral B.1, delta, omicron) | AID iSPOT reader | FRNT | Vero-E6 | 24/ 32 h | 80-sera (immunized with different vaccines) | [35] |
SARS-CoV-2 (ancestral B.1, delta, omicron) | Immunospot analyzer | FRNT | Vero-E6 H1299-E3 | 18 h | 39-sera (vaccinated with different vaccines) | [36] |
SARS-CoV-2 | Immunospot analyzer | FRNT | Vero WHO | 24 h | Methodology (basic study) | [37] |
Mumps virus (MuV) | Immunospot analyzer | FRNT | Vero hSLAM | 48 h | 50 MMR (1 dose) Vaccinated sera | [38] |
MuV | Manual | FRNT | Vero | 40 h | 105-serum samples (pre/post-outbreak) with two doses of MMR | [39] |
MuV (Enders, Miyake, Urabe) | Manual | FRNT | Vero | 2 days | 17-sera (lab confirmed mumps) | [16] |
Measles virus (MeV) MuV Rubella virus (RuV) | Manual | ICA/ FRNT | Vero hSLAM Vero Vero hSLAM | 2 days 2 days 3 days | Serum/ throat swabs from suspected MMR cases | [21,22,40,41,42,43,44] |
MeV | EliSopt Reader Image Analyzer | FRNT | Vero (ECCC UK) | 28 h | 90-serum samples 38 IV-Ig-products | [45] |
Influenza virus (5 Strains) NYMC X-179A (H1N1) A/California/7/2/2009) | EliSopt Reader Image Analyzer | FRNTELISA-TCID50 | MDCK | 18–20 h | 108 serum samples (Immunized subjects, Laboratory workers & Clinically suspected) | [46] |
Influenza A and B virus | Microscope | FRNT | MDCK | 24 h | 60-serum samples | [18] |
Influenza A and B viruses | Flatbed scanner | FRNT | MDCK MDCK-SIAT | Overnight | Methodology | [47] |
Zika virus | ELISPOT Reader | FRNT | Vero WHO C6/36 | 40 h | Serum panel | [48] |
Yellow fever virus (YF-17-D) | ELISPOT Reader | FRNT | BHK-21 | 4 days | 15-sera (vaccinated healthy volunteers) | [49] |
Poliovirus | Manual | CPE Blue-Cell ELISA/ICA | Hep-2C RD L20B, Vero | 24 h 48 h 7 days | 97 poliovirus isolates 43-isolation positive specimens | [19] |
Herpes Simplex Virus 1 (KOS strain) | Immunospot analyzer | ELISOPT-NT PRNT | U-2 OS | 14 h 3 days | 269-Sera (healthy individuals) | [50] |
Hantavirus (7 strains) | Manual | FRNT | Vero-E6 | 9–12 days | 190-sera 17-Mammalogists sera Seroepidemiology (Lativa, n = 333) | [51,52,53] |
Hantavirus (DOBV Slovenia, SEOV 80-39, PUUV Kazaan) | Manual | FRNT | Vero-E6 | 7–13 days | 22-serum samples | [54] |
Varicella-zoster (VR 841) | Manual | Immuno Peroxidase technique based PRNT | WI-38 | 72 h | 8-serum samples | [55] |
Varicella zoster virus | Immunospot analyzer | FRNT | ARPE-19 | 3-days | Mouse serum (53-immunized & 16-non-immunized) | [56] |
Hepatitis C virus (JFH-1 HCV 2a) | Manual | FRNT | Huh-7 | 3-days | 77-sera (57-chronic HCV patients) | [57] |
Human polyomavirus BK (BKV, prototype Gardner) | Microscope/ Manual | Immunoperoxidase-NT | Vero | 6-days | 64-serum samples | [58] |
Human Metapneumovirus (CAN 97-83, group-A & CAN 98-75, group-B) | Manual | FRNT | LLC-MK2 | 5-days | 20-serum samples | [59] |
Equine Infectious Anemia virus (PV & D9 strains) | Immunospot analyzer | FRNT | Fetal Equine Kidney | 72–96 h | Serum panel (n = 6) | [60] |
Equine Herpesvirus type-1 (EHV-1 strain 89C25p) | Manual | FRNT | MDBK | 24–48 h | Foal serum (n = 30) Infected Horse sera (n = 16) | [61] |
Crimean-Congo hemorrhagic fever virus (Turkey-Kelkit06) | Microscope/ Manual | FRNT (both ICA/IFA) | Vero-E6 | 3-days | 69-serum samples (20-acute & 49-convalescent) | [62] |
Bourbon virus | Immunospot analyzer | FRNT (both ICA/IFA) | Vero-E6 CCL81 | 24 h | 440-serum samples | [63] |
Human cytomegalovirus (HCMV AD169) | Immunospot analyzer | FRNT | MRC-5 HEL-299 WI-38 | 14–20 h | Serum panel (n = 57) | [64] |
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Vaidya, S.R. Immuno-Colorimetric Neutralization Test: A Surrogate for Widely Used Plaque Reduction Neutralization Tests in Public Health Virology. Viruses 2023, 15, 939. https://doi.org/10.3390/v15040939
Vaidya SR. Immuno-Colorimetric Neutralization Test: A Surrogate for Widely Used Plaque Reduction Neutralization Tests in Public Health Virology. Viruses. 2023; 15(4):939. https://doi.org/10.3390/v15040939
Chicago/Turabian StyleVaidya, Sunil R. 2023. "Immuno-Colorimetric Neutralization Test: A Surrogate for Widely Used Plaque Reduction Neutralization Tests in Public Health Virology" Viruses 15, no. 4: 939. https://doi.org/10.3390/v15040939
APA StyleVaidya, S. R. (2023). Immuno-Colorimetric Neutralization Test: A Surrogate for Widely Used Plaque Reduction Neutralization Tests in Public Health Virology. Viruses, 15(4), 939. https://doi.org/10.3390/v15040939