Advertisement
Research Article| Volume 78, ISSUE 6, P476-483, June 2019

SV40 seroprevalence in two Latin American countries involved in field trials of candidate oral poliovaccines

Published:April 15, 2019DOI:https://doi.org/10.1016/j.jinf.2019.04.007

      Highlights

      • Polyomavirus SV40 was an unrecognized contaminant of early poliovaccines administered to millions.
      • People in Latin America where vaccine trials took place often have SV40 neutralizing antibodies.
      • Evidence indicates that SV40 is causing human infections today.
      • Results of studies of SV40 infections in humans depend on the populations analyzed.

      Summary

      Objectives

      This study sought to determine SV40 seroprevalence in residents of two Latin American countries, Colombia and Nicaragua, which were sites of prelicensure oral poliovaccine (OPV) trials.

      Methods

      Archival sera were tested for SV40 neutralizing antibody using a virus-specific plaque-reduction assay. Samples included 517 sera from Colombia and 149 sera from Nicaragua.

      Results

      Overall SV40 seroprevalence was 22.8% for Colombian subjects and 12.8% for Nicaraguans. Subgroups of Colombian subjects ranged in frequency of SV40 seropositivity from 10.0% to 38.6%. Birth cohorts both older and younger than the age cohort that contained potential OPV vaccinees from both countries had SV40 antibodies. Gender and ethnicity had no significant effects on SV40 seropositivity.

      Conclusions

      Inhabitants of both Colombia and Nicaragua had detectable SV40 neutralizing antibody, including those of ages presumably not recipients of potentially SV40-contaminated OPV. This observation provides support for the concept that transmission of SV40 human infections can occur. Frequency of SV40 antibody positivity was elevated over that reported for the US where there was limited use of contaminated OPV. This investigation indicates also that study results of SV40 infections in humans will reflect whether subject populations had probable exposures to contaminated poliovaccines and to environmental conditions favoring cycles of viral transmission.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Infection
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Butel J.S.
        Polyomavirus SV40: model infectious agent of cancer.
        in: Robertson E. Cancer associated viruses. Springer Science, 2012: 377-417
        • Shah K.
        • Nathanson N.
        Human exposure to SV40: review and comment.
        Am J Epidemiol. 1976; 103: 1-12
        • Butel J.S.
        Patterns of polyomavirus SV40 infections and associated cancers in humans: a model.
        Curr Opin Virol. 2012; 2: 508-514
        • Melnick J.L.
        • Stinebaugh S.
        Excretion of vacuolating SV-40 virus (papova virus group) after ingestion as a contaminant of oral poliovaccine.
        Proc Soc Exp Biol Med. 1962; 109: 965-968
        • Li R.M.
        • Branton M.H.
        • Tanawattanacharoen S.
        • Falk R.A.
        • Jennette J.C.
        • Kopp J.B.
        Molecular identification of SV40 infection in human subjects and possible association with kidney disease.
        J Am Soc Nephrol. 2002; 13: 2320-2330
        • Vanchiere J.A.
        • Nicome R.K.
        • Greer J.M.
        • Demmler G.J.
        • Butel J.S.
        Frequent detection of polyomaviruses in stool samples from hospitalized children.
        J Infect Dis. 2005; 192: 658-664
        • Vanchiere J.A.
        • White Z.S.
        • Butel J.S.
        Detection of BK virus and simian virus 40 in the urine of healthy children.
        J Med Virol. 2005; 75: 447-454
        • Vanchiere J.A.
        • Abudayyeh S.
        • Copeland C.M.
        • Lu L.B.
        • Graham D.Y.
        • Butel J.S.
        Polyomavirus shedding in the stool of healthy adults.
        J Clin Microbiol. 2009; 47: 2388-2391
        • Vanchiere J.A.
        • Carillo B.
        • Morrow A.L.
        • Jiang X.
        • Ruiz-Palacios G.M.
        • Butel J.S.
        Fecal polyomavirus excretion in infancy.
        J Pediatr Infect Dis Soc. 2016; 5: 210-213
        • Bofill-Mas S.
        • Albiñana-Giménez N.
        • Pipkin P.A.
        • Minor P.D.
        • Girones R.
        Isolation of SV40 from the environment of a colony of cynomolgus monkeys naturally infected with the virus.
        Virology. 2004; 330: 1-7
        • Bofill-Mas S.
        • Formiga-Cruz M.
        • Clemente-Casares P.
        • Calafell F.
        • Girones R.
        Potential transmission of human polyomaviruses through the gastrointestinal tract after exposure to virions or viral DNA.
        J Virol. 2001; 75: 10290-10299
        • McQuaig S.M.
        • Scott T.M.
        • Harwood V.J.
        • Farrah S.R.
        • Lukasik J.O.
        Detection of human-derived fecal pollution in environmental waters by use of a PCR-based human polyomavirus assay.
        Appl Environ Microbiol. 2006; 72: 7567-7574
        • Bofill-Mas S.
        • Rodriguez-Manzano J.
        • Calgua B.
        • Carratala A.
        • Girones R.
        Newly described human polyomaviruses Merkel cell, KI and WU are present in urban sewage and may represent potential environmental contaminants.
        Virol J. 2010; 7: e141
        • Sabin A.B.
        Perspectives on rapid elimination and ultimate global eradication of paralytic poliomyelitis caused by polioviruses.
        Eur J Epidemiol. 1991; 7: 95-120
        • Graham D.Y.
        Helicobacter pylori in human populations: the present and predictions of the future based on the epidemiology of polio.
        (Helicobacter pylori 1990)in: Menge H. Gregor M. Tytgat G.N.J. Proceedings of the second international symposium on Helicobacter pylori, Bad Nauheim, August 25–26, 1989. Springer-Verlag, Berlin1991: 97-102
        • Feinstone S.M.
        • Gust I.D.
        Hepatitis A virus.
        in: Richman D.D. Whitley R.J. Hayden F.G. Clinical virology. ASM Press, Washington, D.C.2002: 1019-1039
        • Wong C.
        • Vilchez R.A.
        • Quiroz J.
        • Adam E.
        • Butel J.S.
        Ethnic differences in polyomavirus simian virus 40 seroprevalence among women in Houston, Texas.
        J Infect. 2013; 66: 67-74
        • Butel J.S.
        • Jafar S.
        • Wong C.
        • Arrington A.S.
        • Opekun A.R.
        • Finegold M.J.
        • et al.
        Evidence of SV40 infections in hospitalized children.
        Hum Pathol. 1999; 30: 1496-1502
        • Minor P.
        • Pipkin P.
        • Jarzebek Z.
        • Knowles W.
        Studies of neutralising antibodies to SV40 in human sera.
        J Med Virol. 2003; 70: 490-495
        • Kean J.M.
        • Rao S.
        • Wang M.
        • Garcea R.L.
        Seroepidemiology of human polyomaviruses.
        PLoS Pathogens. 2009; 5e1000363
        • Abad-Gómez H.
        • Piedrahita F.
        • Solórzano R.
        • da Silva M.M.
        Communitywide vaccination program with attenuated poliovirus in Andes, Colombia.
        J Am Med Assoc. 1959; 170: 906-913
        • Abad Gómez H.
        • Gaviria D.
        • Piedrahita F.
        • Galdós M.
        • da Silva M.M.
        Vaccination of 133,000 children under 10 years of age with live attenuated poliovirus in Medellin, Colombia—preliminary report.
        in: Proceedings of the first international conference on live poliovirus vaccines (Washington, D.C., 22–26 June 1959). Papers presented and discussions held. Pan American Sanitary Bureau, Washington, DC1959: 458-463 (Scientific Publication No. 44)
        • Serpa-Florez F.
        • Maldonado-Romero D.
        • Arguello-Pinzon A.
        • Bahamon-Soto A.
        • Pineros-Bernal H.
        Mass immunization of children with oral, trivalent poliovirus vaccine (Lederle strains).
        Pediatrics. 1964; 33: 878-886
        • da Silva M.M.
        • Berrios M.L.
        • Alcocer J.J.
        The use of attenuated poliovirus in an epidemic area.
        in: Proceedings of the first international conference on live poliovirus Vaccines (Washington, D. C., 22–26 June 1959). Papers presented and discussions held. Pan American Sanitary Bureau, Washington, DC1959: 464-482 (Scientific Publication No. 44)
        • Alcocer J.J.
        • Armijo R.
        • da Silva M.M.
        Vaccination and challenge—poliomyelitis in Nicaragua, 1959–1960.
        in: Proceedings of the second international conference on live poliovirus vaccines (Washington, D.C., 6–10 June 1960). Papers presented and discussions held. Pan American Health Organization, Washington, DC1960: 547-560 (Scientific Publication No. 50)
        • Cabasso V.J.
        • Jervis G.A.
        • Moyer A.W.
        • Roca-Garcia M.
        • Orsi E.V.
        • Cox H.R.
        Cumulative testing experience with consecutive lots of oral poliomyelitis vaccine.
        Br Med J. 1960; 1: 373-387
        • Dueñas A.
        • Adam E.
        • Melnick J.L.
        • Rawls W.E.
        Herpesvirus type 2 in a prostitute population.
        Am J Epidemiol. 1972; 95: 483-489
        • Adam E.
        • Hollinger F.B.
        • Melnick J.L.
        • Dueñas A.
        • Rawls W.E.
        Type B hepatitis antigen and antibody among prostitutes and nuns: a study of possible venereal transmission.
        J Infect Dis. 1974; 129: 317-321
        • Thorell K.
        • Bengtsson-Palme J.
        • Liu O.H.
        • Gonzales R.V.P.
        • Nookaew I.
        • Rabeneck L.
        • et al.
        In vivo analysis of the viable microbiota and Helicobacter pylori transcriptome in gastric infection and early stages of carcinogenesis.
        Infect Immun. 2017; 85: e00031-17
        • Thorell K.
        • Hosseini S.
        • Gonzáles R.V.P.
        • Chaotham C.
        • Graham D.Y.
        • Paszat L.
        • et al.
        Identification of a Latin American-specific BabA adhesin variant through whole genome sequencing of Helicobacter pylori patient isolates from Nicaragua.
        BMC Evol Biol. 2016; 16: 53
        • Jafar S.
        • Rodriguez-Barradas M.
        • Graham D.Y.
        • Butel J.S.
        Serological evidence of SV40 infections in HIV-infected and HIV-negative adults.
        J Med Virol. 1998; 54: 276-284
        • Nurgalieva Z.Z.
        • Wong C.
        • Zhangabylov A.K.
        • Omarbekova Z.E.
        • Graham D.Y.
        • Vilchez R.A.
        • et al.
        Polyomavirus SV40 infections in Kazakhstan.
        J Infect. 2005; 50: 142-148
        • Butel J.S.
        • Wong C.
        • Vilchez R.A.
        • Szücs G.
        • Dömök I.
        • Kriz B.
        • et al.
        Detection of antibodies to polyomavirus SV40 in two central European countries.
        Cent Eur J Publ Health. 2003; 11: 3-8
        • Meneses A.
        • Lopez-Terrada D.
        • Zanwar P.
        • Killen D.E.
        • Monterroso V.
        • Butel J.S.
        • et al.
        Lymphoproliferative disorders in Costa Rica and simian virus 40.
        Haematologica. 2005; 90: 1635-1642
        • Quirce J.M.
        • Méndez O.V.
        • Núñez J.
        • Montoya J.A.
        • Brody J.
        • Henderson D.A.
        • et al.
        Vaccination with attenuated polioviruses in Costa Rica.
        in: Proceedings of the first international conference on live poliovirus vaccines (Washington, D.C., June 22–26, 1959). Papers presented and discussions held. Pan American Sanitary Bureau, Washington, D.C.1959: 510-513 (Scientific Publication No. 44)
        • Núñez J.
        • Vargas-Méndez O.
        • Guevara E.C.
        • Quirce J.M.
        • Montoya J.A.
        • Doany H.
        • et al.
        Vaccination with attenuated polioviruses in Costa Rica. Second progress report. Section I. Vaccination program. Section II. Surveillance program.
        in: Proceedings of the second international conference on live poliovirus vaccines (Washington, D.C., June 6–10, 1960). Papers presented and discussions held. Pan American Health Organization, Washington, D.C.1960: 561-568 (Scientific Publication No. 50)
        • Meinzen-Derr J.K.
        • Guerrero M.L.
        • Altaye M.
        • Ortega-Gallegos H.
        • Ruiz-Palacios G.M.
        • Morrow A.L.
        Risk of infant anemia is associated with exclusive breast-feeding and maternal anemia in a Mexican cohort.
        J Nutr. 2006; 136: 452-458
        • Alvarez M.R.
        • Santos F.G.
        • Rivera L.R.
        • Mayes O.
        Viral and serological studies in children immunized with live poliovirus vaccine—preliminary report of a large trial conducted in Mexico.
        in: Proceedings of the first international conference on live poliovirus vaccines (Washington, D.C., 22–26 June 1959). Papers presented and discussions held. Pan American Sanitary Bureau, Washington, D.C.1959: 483-494 (Scientific Publication No. 44)
        • Alvarez M.R.
        • Bustamante M.E.
        • Alba R.A.
        Use of Sabin's live poliovirus vaccine in Mexico. Results of a large-scale trial.
        in: Proceedings of the second international conference on live poliovirus vaccines (Washington, D.C., 6–10 June 1960). Papers presented and discussions held. Pan American Health Organization, Washington, D.C.1960: 386-409 (Scientific Publication No. 50)
        • Morris J.A.
        • Johnson K.M.
        • Aulisio C.G.
        • Chanock R.M.
        • Knight V.
        Clinical and serologic responses in volunteers given vacuolating virus (SV40) by respiratory route.
        Proc Soc Exp Biol Med. 1961; 108: 56-59
        • Horváth L.B.
        SV40 neutralizing antibodies in the sera of man and experimental animals.
        Acta Virol. 1972; 16: 141-146
        • Engels E.A.
        • Switzer W.M.
        • Heneine W.
        • Viscidi R.P.
        Serologic evidence for exposure to simian virus 40 in North American zoo workers.
        J Infect Dis. 2004; 190: 2065-2069
        • Carter J.J.
        • Madeleine M.M.
        • Wipf G.C.
        • Garcea R.L.
        • Pipkin P.A.
        • Minor P.D.
        • et al.
        Lack of serologic evidence for prevalent simian virus 40 infection in humans.
        J Natl Cancer Inst. 2003; 95: 1522-1530
        • Corallini A.
        • Mazzoni E.
        • Taronna A.
        • Manfrini M.
        • Carandina G.
        • Guerra G.
        • et al.
        Specific antibodies reacting with simian virus 40 capsid protein mimotopes in serum samples from healthy blood donors.
        Hum Immunol. 2012; 73: 502-510
        • Tognon M.
        • Corallini A.
        • Manfrini M.
        • Taronna A.
        • Butel J.S.
        • Pietrobon S.
        • et al.
        Specific antibodies reacting with SV40 large T antigen mimotopes in serum samples of healthy subjects.
        PLoS One. 2016; 11e0145720
        • Lundstig A.
        • Eliasson L.
        • Lehtinen M.
        • Sasnauskas K.
        • Koskela P.
        • Dillner J.
        Prevalence and stability of human serum antibodies to simian virus 40 VP1 virus-like particles.
        J Gen Virol. 2005; 86: 1703-1708
        • Shah K.V.
        Evidence for an SV40-related papovavirus infection of man.
        Am J Epidemiol. 1972; 95: 199-206
        • Shah K.V.
        • McCrumb F.R.J.
        • Daniel R.W.
        • Ozer H.L.
        Serologic evidence for a simian-virus-40-like infection of man.
        J Natl Cancer Inst. 1972; 48: 557-561
        • Zimmermann W.
        • Scherneck S.
        • Geissler E.
        Quantitative determination of papovavirus IgG antibodies in sera from cancer patients, labworkers and several groups of control persons by enzyme-linked immunosorbent assay (ELISA).
        Zentralbl Bakteriol Mikrobiol Hyg. 1983; 254: 187-196
        • Rollison D.E.M.
        • Helzlsouer K.J.
        • Alberg A.J.
        • Hoffman S.
        • Hou J.
        • Daniel R.
        • et al.
        Serum antibodies to JC virus, BK virus, simian virus 40, and the risk of incident adult astrocytic brain tumors.
        Cancer Epidemiol Biomark Prev. 2003; 12: 460-463
        • Knowles W.A.
        • Pipkin P.
        • Andrews N.
        • Vyse A.
        • Minor P.
        • Brown D.W.G.
        • et al.
        Population-based study of antibody to the human polyomaviruses BKV and JCV and the simian polyomavirus SV40.
        J Med Virol. 2003; 71: 115-123
        • Engels E.A.
        • Chen J.
        • Viscidi R.P.
        • Shah K.V.
        • Daniel R.W.
        • Chatterjee N.
        • et al.
        Poliovirus vaccination during pregnancy, maternal seroconversion to simian virus 40, and risk of childhood cancer.
        Am J Epidemiol. 2004; 160: 306-316
        • Engels E.A.
        • Viscidi R.P.
        • Galloway D.A.
        • Carter J.J.
        • Cerhan J.R.
        • Davis S.
        • et al.
        Case–control study of simian virus 40 and non-Hodgkin lymphoma in the United States.
        J Natl Cancer Inst. 2004; 96: 1368-1374
        • Rollison D.E.
        • Helzlsouer K.J.
        • Halsey N.A.
        • Shah K.V.
        • Viscidi R.P.
        Markers of past infection with simian virus 40 (SV40) and risk of incident non-Hodgkin lymphoma in a Maryland cohort.
        Cancer Epidemiol Biomark Prev. 2005; 14: 1448-1452
        • Mazzoni E.
        • Corallini A.
        • Cristaudo A.
        • Taronna A.
        • Tassi G.
        • Manfrini M.
        • et al.
        High prevalence of serum antibodies reacting with simian virus 40 capsid protein mimotopes in patients affected by malignant pleural mesothelioma.
        Proc Natl Acad Sci USA. 2012; 109: 18066-18071
        • Taronna A.
        • Mazzoni E.
        • Corallini A.
        • Bononi I.
        • Pietrobon S.
        • Guerra G.
        • et al.
        Serological evidence of an early seroconversion to simian virus 40 in healthy children and adolescents.
        PLoS One. 2013; 8: e61182
        • Comar M.
        • Wong C.
        • Tognon M.
        • Butel J.S.
        Neutralizing and IgG antibodies against simian virus 40 in healthy pregnant women in Italy.
        PLoS One. 2014; 9e110700
        • Mazzoni E.
        • Gerosa M.
        • Lupidi F.
        • Corallini A.
        • Taronna A.P.
        • D'Agostino A.
        • et al.
        Significant prevalence of antibodies reacting with simian virus 40 mimotopes in sera from patients affected by glioblastoma multiforme.
        Neuro-Oncology. 2014; 16: 513-519
        • Tognon M.
        • Luppi M.
        • Corallini A.
        • Taronna A.
        • Barozzi P.
        • Rotondo J.C.
        • et al.
        Immunologic evidence of a strong association between non-Hodgkin lymphoma and simian virus 40.
        Cancer. 2015; 121: 2618-2626
        • Mazzoni E.
        • Benassi M.S.
        • Corallini A.
        • Barbanti-Brodano G.
        • Taronna A.
        • Picci P.
        • et al.
        Significant association between human osteosarcoma and simian virus 40.
        Cancer. 2015; 121: 708-715
        • Mazzoni E.
        • Guerra G.
        • Casali M.V.
        • Pietrobon S.
        • Bononi I.
        • Puozzo A.
        • et al.
        Antibodies against mimotopes of simian virus 40 large T antigen, the oncoprotein, in serum samples from elderly healthy subjects.
        J Cell Physiol. 2017; 232: 176-181
        • Mazzoni E.
        • Di Stefano M.
        • Fiore J.R.
        • Destro F.
        • Manfrini M.
        • Rotondo J.C.
        • et al.
        Serum IgG antibodies from pregnant women reacting to mimotopes of simian virus 40 large T antigen, the viral oncoprotein.
        Front Immunol. 2017; 8: 411
        • Mazzoni E.
        • Bononi I.
        • Benassi M.S.
        • Picci P.
        • Torreggiani E.
        • Rossini M.
        • et al.
        Serum antibodies against simian virus 40 large T antigen, the viral oncoprotein, in osteosarcoma patients.
        Front Cell Dev Biol. 2018; 6: 64