Evaluation of Three Commercially Available Japanese Encephalitis Virus IgM Enzyme-Linked Immunosorbent Assays

Jaimie S. Robinson Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Fort Collins, Colorado; Expanded Programme on Immunization/Immunization, Vaccines and Biologicals Department/Family and Child Health Cluster/World Health Organization, Geneva, Switzerland; Department of Neurovirology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Bangalore, India; Immunization and Vaccine Development, World Health Organization–South-East Asia Regional Office (WHO–SEARO), New Delhi, India; National Polio and Measles Laboratory, IPH, Dhaka, Bangladesh; Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Global Immunization Division, Atlanta, Georgia

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David Featherstone Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Fort Collins, Colorado; Expanded Programme on Immunization/Immunization, Vaccines and Biologicals Department/Family and Child Health Cluster/World Health Organization, Geneva, Switzerland; Department of Neurovirology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Bangalore, India; Immunization and Vaccine Development, World Health Organization–South-East Asia Regional Office (WHO–SEARO), New Delhi, India; National Polio and Measles Laboratory, IPH, Dhaka, Bangladesh; Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Global Immunization Division, Atlanta, Georgia

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Ravi Vasanthapuram Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Fort Collins, Colorado; Expanded Programme on Immunization/Immunization, Vaccines and Biologicals Department/Family and Child Health Cluster/World Health Organization, Geneva, Switzerland; Department of Neurovirology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Bangalore, India; Immunization and Vaccine Development, World Health Organization–South-East Asia Regional Office (WHO–SEARO), New Delhi, India; National Polio and Measles Laboratory, IPH, Dhaka, Bangladesh; Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Global Immunization Division, Atlanta, Georgia

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Brad J. Biggerstaff Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Fort Collins, Colorado; Expanded Programme on Immunization/Immunization, Vaccines and Biologicals Department/Family and Child Health Cluster/World Health Organization, Geneva, Switzerland; Department of Neurovirology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Bangalore, India; Immunization and Vaccine Development, World Health Organization–South-East Asia Regional Office (WHO–SEARO), New Delhi, India; National Polio and Measles Laboratory, IPH, Dhaka, Bangladesh; Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Global Immunization Division, Atlanta, Georgia

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Anita Desai Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Fort Collins, Colorado; Expanded Programme on Immunization/Immunization, Vaccines and Biologicals Department/Family and Child Health Cluster/World Health Organization, Geneva, Switzerland; Department of Neurovirology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Bangalore, India; Immunization and Vaccine Development, World Health Organization–South-East Asia Regional Office (WHO–SEARO), New Delhi, India; National Polio and Measles Laboratory, IPH, Dhaka, Bangladesh; Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Global Immunization Division, Atlanta, Georgia

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Nalini Ramamurty Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Fort Collins, Colorado; Expanded Programme on Immunization/Immunization, Vaccines and Biologicals Department/Family and Child Health Cluster/World Health Organization, Geneva, Switzerland; Department of Neurovirology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Bangalore, India; Immunization and Vaccine Development, World Health Organization–South-East Asia Regional Office (WHO–SEARO), New Delhi, India; National Polio and Measles Laboratory, IPH, Dhaka, Bangladesh; Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Global Immunization Division, Atlanta, Georgia

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Anwarul Haque Chowdhury Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Fort Collins, Colorado; Expanded Programme on Immunization/Immunization, Vaccines and Biologicals Department/Family and Child Health Cluster/World Health Organization, Geneva, Switzerland; Department of Neurovirology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Bangalore, India; Immunization and Vaccine Development, World Health Organization–South-East Asia Regional Office (WHO–SEARO), New Delhi, India; National Polio and Measles Laboratory, IPH, Dhaka, Bangladesh; Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Global Immunization Division, Atlanta, Georgia

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Hardeep S. Sandhu Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Fort Collins, Colorado; Expanded Programme on Immunization/Immunization, Vaccines and Biologicals Department/Family and Child Health Cluster/World Health Organization, Geneva, Switzerland; Department of Neurovirology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Bangalore, India; Immunization and Vaccine Development, World Health Organization–South-East Asia Regional Office (WHO–SEARO), New Delhi, India; National Polio and Measles Laboratory, IPH, Dhaka, Bangladesh; Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Global Immunization Division, Atlanta, Georgia

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Kathleen F. Cavallaro Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Fort Collins, Colorado; Expanded Programme on Immunization/Immunization, Vaccines and Biologicals Department/Family and Child Health Cluster/World Health Organization, Geneva, Switzerland; Department of Neurovirology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Bangalore, India; Immunization and Vaccine Development, World Health Organization–South-East Asia Regional Office (WHO–SEARO), New Delhi, India; National Polio and Measles Laboratory, IPH, Dhaka, Bangladesh; Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Global Immunization Division, Atlanta, Georgia

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Barbara W. Johnson Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Fort Collins, Colorado; Expanded Programme on Immunization/Immunization, Vaccines and Biologicals Department/Family and Child Health Cluster/World Health Organization, Geneva, Switzerland; Department of Neurovirology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Bangalore, India; Immunization and Vaccine Development, World Health Organization–South-East Asia Regional Office (WHO–SEARO), New Delhi, India; National Polio and Measles Laboratory, IPH, Dhaka, Bangladesh; Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Global Immunization Division, Atlanta, Georgia

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We evaluated performance of three commercial Japanese encephalitis virus (JEV) IgM antibody capture enzyme-linked immunosorbent assay (MAC ELISA) kits with a panel of serological specimens collected during a surveillance project of acute encephalitis syndrome in India and acute meningitis and encephalitis syndrome in Bangladesh. The serum and cerebral spinal fluid specimens had been referred to the Centers for Disease Control and Prevention (CDC) for confirmatory testing. The CDC results and specimen classifications were considered the reference standard. All three commercial kits had high specificity (95–99.5%), but low sensitivities, ranging from 17–57%, with both serum and cerebrospinal fluid samples. Specific factors contributing to low sensitivity compared with the CDC ELISA could not be determined through further analysis of the limits and dilution end points of IgM detection.

Author Notes

*Address correspondence to Jaimie S. Robinson, 3150 Rampart Rd., Fort Collins, CO 80521. E-mail: fxa3@cdc.gov

Authors' addresses: Jaimie S. Robinson, Brad J. Biggerstaff, and Barbara W. Johnson, Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Fort Collins, CO, E-mails: fxa3@cdc.gov, BBiggerstaff@cdc.gov, and bfj9@cdc.gov. David Featherstone, Expanded Programme on Immunization/Immunization, Vaccines and Biologicals Department/Family and Child Health Cluster/World Health Organization, Geneva, Switzerland, E-mail: featherstoned@who.int. Ravi Vasanthapuram and Anita Desai, Department of Neurovirology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Bangalore, India, E-mails: virusravi@gmail.com and adesai@gmail.com. Nalini Ramamurty, World Health Organization - South-East Asia Regional Office I.P. Estate, New Delhi, India, E-mail: Ramamurtyn@SEARO.WHO.INT. Anwarul Haque Chowdhury, National Polio and Measles Laboratory, IPH, Dhaka, Bangladesh, E-mail: banplab@gmail.com. Hardeep S. Sandhu and Kathleen F. Cavallaro, CORP Bldg, Atlanta, GA, E-mails: hsandhu@cdc.gov and kfc1@cdc.gov.

  • 1.

    Vaughn DW, Hoke CH Jr, 1992. The epidemiology of Japanese encephalitis: prospects for prevention. Epidemiol Rev 14: 197221.

  • 2.

    Burke DS, Nisalak A, Ussery MA, Laorakpongse T, Chantavibul S, 1985. Kinetics of IgM and IgG responses to Japanese encephalitis virus in human serum and cerebrospinal fluid. J Infect Dis 151: 10931099.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Chanama S, Sukprasert W, Sa-ngasang A, An A, Sangkitporn S, Kurane I, Anantapreecha S, 2005. Detection of Japanese encephalitis (JE) virus-specific IgM in cerebrospinal fluid and serum samples from JE patients. Jpn J Infect Dis 58: 294296.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Solomon T, Ooi MH, Beasley DW, Mallewa M, 2003. West Nile encephalitis. BMJ 326: 865869.

  • 5.

    WHO, 2007. Manual for the Laboratory Diagnosis of Japanese Encephalitis Virus Infection. Geneva: World Health Organization.

  • 6.

    Jacobson JA, Hills SL, Winkler JL, Mammen M, Thaisomboonsuk B, Marfin AA, Gibbons RV, 2007. Evaluation of three immunoglobulin M antibody capture enzyme-linked immunosorbent assays for diagnosis of Japanese encephalitis. Am J Trop Med Hyg 77: 164168.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Ravi V, Desai A, Balaji M, Apte MP, Lakshman L, Subbakrishna DK, Sridharan G, Dhole TN, Ravikumar BV, 2006. Development and evaluation of a rapid IgM capture ELISA (JEV-Chex) for the diagnosis of Japanese encephalitis. J Clin Virol 35: 429434.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Cuzzubbo AJ, Endy TP, Vaughn DW, Solomon T, Nisalak A, Kalayanarooj S, Dung NM, Warrilow D, Aaskov J, Devine PL, 1999. Evaluation of a new commercially available immunoglobulin M capture enzyme-linked immunosorbent assay for diagnosis of Japanese encephalitis infections. J Clin Microbiol 37: 37383741.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Shrivastva A, Tripathi NK, Parida M, Dash PK, Jana AM, Lakshmana Rao PV, 2008. Comparison of a dipstick enzyme-linked immunosorbent assay with commercial assays for detection of Japanese encephalitis virus-specific IgM antibodies. J Postgrad Med 54: 181185.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    WHO 2006. WHO-recommended standards for surveillance of selected vaccine preventable diseases. Geneva: WHO.

  • 11.

    Martin DA, Biggerstaff BJ, Allen B, Johnson AJ, Lanciotti RS, Roehrig JT, 2002. Use of immunoglobulin M cross-reactions in differential diagnosis of human flaviviral encephalitis infections in the United States. Clin Diagn Lab Immunol 9: 544549.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Martin DA, Muth DA, Brown T, Johnson AJ, Karabatsos N, Roehrig JT, 2000. Standardization of immunoglobulin M capture enzyme-linked immunosorbent assays for routine diagnosis of arboviral infections. J Clin Microbiol 38: 18231826.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Lanciotti RS, Tsai TF, 2007. Arboviruses. Murray PR, Baron EJ, Jorgensen JH, Landry ML, Pfaller MA, eds. Manual of Clinical Microbiology. Washington, DC: ASM Press, 14861500.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Chang GJ, Hunt AR, Holmes DA, Springfield T, Chiueh TS, Roehrig JT, Gubler DJ, 2003. Enhancing biosynthesis and secretion of premembrane and envelope proteins by the chimeric plasmid of dengue virus type 2 and Japanese encephalitis virus. Virology 306: 170180.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Purdy DE, Chang GJ, 2005. Secretion of noninfectious dengue virus-like particles and identification of amino acids in the stem region involved in intracellular retention of envelope protein. Virology 333: 239250.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Lindsey HS, Calisher CH, Mathews JH, 1976. Serum dilution neutralization test for California group virus identification and serology. J Clin Microbiol 4: 503510.

  • 17.

    Beaty BJ, Calisher CH, Shope RE, 1995. Diganostic procedures for viral, rickettsial and chlamydial infections. Lennette EH, Lennette DL, Lennette ET, eds. Arboviruses. Washington, DC: American Public Health Association, 465478.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Chambers TJ, Nestorowicz A, Mason PW, Rice CM, 1999. Yellow fever/Japanese encephalitis chimeric viruses: construction and biological properties. J Virol 73: 30953101.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Guirakhoo F, Arroyo J, Pugachev KV, Miller C, Zhang ZX, Weltzin R, Georgakopoulos K, Catalan J, Ocran S, Soike K, Ratterree M, Monath TP, 2001. Construction, safety, and immunogenicity in nonhuman primates of a chimeric yellow fever-dengue virus tetravalent vaccine. J Virol 75: 72907304.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Pugachev KV, Guirakhoo F, Mitchell F, Ocran SW, Parsons M, Johnson BW, Kosoy OL, Lanciotti RS, Roehrig JT, Trent DW, Monath TP, 2004. Construction of yellow fever/St. Louis encephalitis chimeric virus and the use of chimeras as a diagnostic tool. Am J Trop Med Hyg 71: 639645.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Johnson BW, Kosoy O, Hunsperger E, Beltran M, Delorey M, Guirakhoo F, Monath T, 2009. Evaluation of chimeric Japanese encephalitis and dengue viruses for use in diagnostic plaque reduction neutralization tests. Clin Vaccine Immunol 16: 10521059.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Calisher CH, Karabatsos N, Dalrymple JM, Shope RE, Porterfield JS, Westaway EG, Brandt WE, 1989. Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. J Gen Virol 70: 3743.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    WHO, 2007. Guidelines for Plaque Reduction Neutralizing Testing of Human Antibodies to Dengue Viruses. Geneva: WHO.

  • 24.

    Ravi V, Robinson JS, Russell BJ, Desai A, Ramamurty N, Featherstone D, Johnson BW, 2009. Evaluation of IgM antibody capture enzyme-linked immunosorbent assay kits for detection of IgM against Japanese encephalitis virus in cerebrospinal fluid samples. Am J Trop Med Hyg 81: 11441150.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Wilson EB, 1927. Probable inference the law of succession and statistical inference. J Am Stat Assoc 22: 209212.

  • 26.

    May WL, Johnson WD, 1997. Confidence intervals for differences in correlated binary proportions. Stat Med 16: 21272136.

  • 27.

    May WL, Johnson WD, 1998. Hypothesis testing and confidence interval construction in 2 × 2 tables of correlated proportions. J Biopharm Stat 8: 115130.

  • 28.

    Mabey D, Peeling RW, Ustianowski A, Perkins MD, 2004. Diagnostics for the developing world. Nat Rev Microbiol 2: 231240.

  • 29.

    Burke DS, Nisalak A, Ussery MA, Laorakpongse T, Chantavibul S, 1985. Kinetics of IgM and IgG responses to Japanese encephalitis virus in human serum and cerebrospinal fluid. J Infect Dis 151: 10931099.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    A-Nuegoonpipat A, Panthuyosri N, Anantapreecha S, Chanama S, Sa-Ngasang A, Sawanpanyalert P, Kurane I, 2008. Cross-reactive IgM responses in patients with dengue or Japanese encephalitis. J Clin Virol 42: 7577.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Burke DS, Nisalak A, Ussery MA, 1982. Antibody capture immunoassay detection of Japanese encephalitis virus immunoglobulin M and G antibodies in cerebrospinal fluid. J Clin Microbiol 16: 10341042.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Roehrig JT, Johnson AJ, Hunt AR, Bolin RA, Chu MC, 1990. Antibodies to dengue 2 virus E-glycoprotein synthetic peptides identify antigenic conformation. Virology 177: 668675.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Martin DA, Biggerstaff BJ, Allen B, Johnson AJ, Lanciotti RS, Roehrig JT, 2002. Use of immunoglobulin M cross-reactions in differential diagnosis of human flaviviral encephalitis infections in the United States. Clin Diagn Lab Immunol 9: 544549.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Roehrig JT, 2003. Antigenic structure of flavivirus proteins. Adv Virus Res 59: 141175.

  • 35.

    Roehrig JT, Mathews JH, Trent DW, 1983. Identification of epitopes on the E glycoprotein of Saint Louis encephalitis virus using monoclonal antibodies. Virology 128: 118126.

    • PubMed
    • Search Google Scholar
    • Export Citation
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