Lack of type-specific concordance between human papillomavirus (HPV) serology and HPV DNA detection in the uterine cervix and oral mucosa Free

Abstract

There is limited knowledge about longitudinal genotype-specific concordance between human papillomavirus (HPV) serology and co-existent presence of HPV DNA in the uterine cervix. The role of oral HPV infections in inducing serological response is unclear, as is the effect of HPV antibodies on the outcome of oral HPV infections. The present study is part of the Finnish Family HPV Study designed to evaluate dynamics of HPV infections within families. Here, we correlated the point prevalence of HPV6, 11, 16, 18 and 45 antibodies and concomitant genotype-specific HPV DNA detection in cervical and oral samples of 323 mothers during their 3 year (mean 37.5 months) follow-up. The mean age of these pregnant mothers at enrolment (third trimester) was 25.5 years. HPV antibodies were analysed with multiplex HPV serology and HPV genotyping was performed using a Multimetrix kit (Progen Biotechnik). There was no concordance between cervical DNA detection and co-existent seropositivity, and the same was true even in samples taken 12 months apart. Women who cleared their cervical HPV16 infection had the highest HPV16 antibody levels, whereas those who acquired incident HPV16 infections had the lowest antibody levels. Neither the presence nor the dynamics of oral HPV DNA had any correlation with HPV serology.

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2011-09-01
2024-03-29
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References

  1. Anttila M., Syrjänen S., Ji H., Saarikoski S., Syrjänen K. 1999; Failure to demonstrate human papillomavirus DNA in epithelial ovarian cancer by general primer PCR. Gynecol Oncol 72:337–341 [View Article][PubMed]
    [Google Scholar]
  2. Bosch F. X., Burchell A. N., Schiffman M., Giuliano A. R., de Sanjose S., Bruni L., Tortolero-Luna G., Kjaer S. K., Muñoz N. 2008; Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia. Vaccine 26:(Suppl. 10)K1–K16 [View Article][PubMed]
    [Google Scholar]
  3. Carter J. J., Koutsky L. A., Wipf G. C., Christensen N. D., Lee S. K., Kuypers J., Kiviat N., Galloway D. A. 1996; The natural history of human papillomavirus type 16 capsid antibodies among a cohort of university women. J Infect Dis 174:927–936 [View Article][PubMed]
    [Google Scholar]
  4. Carter J. J., Koutsky L. A., Hughes J. P., Lee S. K., Kuypers J., Kiviat N., Galloway D. A. 2000; Comparison of human papillomavirus types 16, 18, and 6 capsid antibody responses following incident infection. J Infect Dis 181:1911–1919 [View Article][PubMed]
    [Google Scholar]
  5. Castle P. E., Wacholder S., Lorincz A. T., Scott D. R., Sherman M. E., Glass A. G., Rush B. B., Schussler J. E., Schiffman M. 2002; A prospective study of high-grade cervical neoplasia risk among human papillomavirus-infected women. J Natl Cancer Inst 94:1406–1414[PubMed] [CrossRef]
    [Google Scholar]
  6. Chen H. S., Conway M. J., Christensen N. D., Alam S., Meyers C. 2011; Papillomavirus capsid proteins mutually impact structure. Virology 412:378–383 [View Article][PubMed]
    [Google Scholar]
  7. Clifford G. M., Shin H. R., Oh J. K., Waterboer T., Ju Y. H., Vaccarella S., Quint W., Pawlita M., Franceschi S. 2007; Serologic response to oncogenic human papillomavirus types in male and female university students in Busan, South Korea. Cancer Epidemiol Biomarkers Prev 16:1874–1879 [View Article][PubMed]
    [Google Scholar]
  8. Combita A.-L., Bravo M.-M., Touzé A., Orozco O., Coursaget P. 2002; Serologic response to human oncogenic papillomavirus types 16, 18, 31, 33, 39, 58 and 59 virus-like particles in colombian women with invasive cervical cancer. Int J Cancer 97:796–803 [View Article][PubMed]
    [Google Scholar]
  9. de Gruijl T. D., Bontkes H. J., Walboomers J. M., Schiller J. T., Stukart M. J., Groot B. S., Chabaud M. M., Remmink A. J., Verheijen R. H. et al. 1997; Immunoglobulin G responses against human papillomavirus type 16 virus-like particles in a prospective nonintervention cohort study of women with cervical intraepithelial neoplasia. J Natl Cancer Inst 89:630–638 [View Article][PubMed]
    [Google Scholar]
  10. Dillner J., Kallings I., Brihmer C., Sikström B., Koskela P., Lehtinen M., Schiller J. T., Sapp M., Mårdh P. A. 1996; Seropositivities to human papillomavirus types 16, 18, or 33 capsids and to Chlamydia trachomatis are markers of sexual behavior. J Infect Dis 173:1394–1398 [View Article][PubMed]
    [Google Scholar]
  11. Domža G., Gudlevičienė Z., Didžiapetrienė J., Valuckas K. P., Kazbarienė B., Drąsutienė G. 2010; Human papillomavirus infection in pregnant women. Arch Gynecol Obstet 2010: [View Article][PubMed]
    [Google Scholar]
  12. Frazer I. H. 1996; Immunology of papillomavirus infection. Curr Opin Immunol 8:484–491 [View Article][PubMed]
    [Google Scholar]
  13. Frazer I. H., Leggatt G. R., Mattarollo S. R. 2011; Prevention and treatment of papillomavirus-related cancers through immunization. Annu Rev Immunol 29:111–138[PubMed] [CrossRef]
    [Google Scholar]
  14. Furniss C. S., McClean M. D., Smith J. F., Bryan J., Applebaum K. M., Nelson H. H., Posner M. R., Kelsey K. T. 2009; Human papillomavirus 6 seropositivity is associated with risk of head and neck squamous cell carcinoma, independent of tobacco and alcohol use. Ann Oncol 20:534–541 [View Article][PubMed]
    [Google Scholar]
  15. Giorgi C., Di Bonito P., Grasso F., Mochi S., Accardi L., Donà M. G., Branca M., Costa S., Mariani L. et al. 2008; Clinical and epidemiological correlates of antibody response to human papillomaviruses (HPVs) as measured by a novel ELISA based on denatured recombinant HPV16 late (L) and early (E) antigens. Infect Agent Cancer 3:9 [View Article][PubMed]
    [Google Scholar]
  16. Goodman M. T., Shvetsov Y. B., McDuffie K., Wilkens L. R., Zhu X., Thompson P. J., Ning L., Killeen J., Kamemoto L., Hernandez B. Y. 2008; Prevalence, acquisition, and clearance of cervical human papillomavirus infection among women with normal cytology: Hawaii Human Papillomavirus Cohort Study. Cancer Res 68:8813–8824 [View Article][PubMed]
    [Google Scholar]
  17. Hagensee M. E., Slavinsky J. III, Gaffga C. M., Suros J., Kissinger P., Martin D. H. 1999; Seroprevalence of human papillomavirus type 16 in pregnant women. Obstet Gynecol 94:653–658 [View Article][PubMed]
    [Google Scholar]
  18. Hagensee M. E., Koutsky L. A., Lee S. K., Grubert T., Kuypers J., Kiviat N. B., Galloway D. A. 2000; Detection of cervical antibodies to human papillomavirus type 16 (HPV-16) capsid antigens in relation to detection of HPV-16 DNA and cervical lesions. J Infect Dis 181:1234–1239 [View Article][PubMed]
    [Google Scholar]
  19. Ho G. Y., Bierman R., Beardsley L., Chang C. J., Burk R. D. 1998; Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 338:423–428 [View Article][PubMed]
    [Google Scholar]
  20. Ho G. Y., Studentsov Y., Hall C. B., Bierman R., Beardsley L., Lempa M., Burk R. D. 2002; Risk factors for subsequent cervicovaginal human papillomavirus (HPV) infection and the protective role of antibodies to HPV-16 virus-like particles. J Infect Dis 186:737–742 [View Article][PubMed]
    [Google Scholar]
  21. Ho G. Y., Studentsov Y. Y., Bierman R., Burk R. D. 2004; Natural history of human papillomavirus type 16 virus-like particle antibodies in young women. Cancer Epidemiol Biomarkers Prev 13:110–116 [View Article][PubMed]
    [Google Scholar]
  22. Kellokoski J., Syrjänen S., Yliskoski M., Syrjänen K. 1992; Dot blot hybridization in detection of human papillomavirus (HPV) infections in the oral cavity of women with genital HPV infections. Oral Microbiol Immunol 7:19–23 [View Article][PubMed]
    [Google Scholar]
  23. Kirnbauer R., Hubbert N. L., Wheeler C. M., Becker T. M., Lowy D. R., Schiller J. T. 1994; A virus-like particle enzyme-linked immunosorbent assay detects serum antibodies in a majority of women infected with human papillomavirus type 16. J Natl Cancer Inst 86:494–499 [View Article][PubMed]
    [Google Scholar]
  24. Kreimer A. R., Alberg A. J., Viscidi R., Gillison M. L. 2004; Gender differences in sexual biomarkers and behaviors associated with human papillomavirus-16, -18, and -33 seroprevalence. Sex Transm Dis 31:247–256 [View Article][PubMed]
    [Google Scholar]
  25. Lehtinen M., Kaasila M., Pasanen K., Patama T., Palmroth J., Laukkanen P., Pukkala E., Koskela P. 2006; Seroprevalence atlas of infections with oncogenic and non-oncogenic human papillomaviruses in Finland in the 1980s and 1990s. Int J Cancer 119:2612–2619 [View Article][PubMed]
    [Google Scholar]
  26. Li N., Franceschi S., Howell-Jones R., Snijders P. J., Clifford G. M. 2011; Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: variation by geographical region, histological type and year of publication. Int J Cancer 128:927–935 [View Article][PubMed]
    [Google Scholar]
  27. Louvanto K., Rintala M. A., Syrjänen K. J., Grénman S. E., Syrjänen S. M. 2010a; Genotype-specific persistence of genital human papillomavirus (HPV) infections in women followed for 6 years in the Finnish Family HPV Study. J Infect Dis 202:436–444 [View Article][PubMed]
    [Google Scholar]
  28. Louvanto K., Syrjänen K. J., Rintala M. A., Grénman S. E., Syrjänen S. M. 2010b ). Genotype-specific clearance of genital human papillomavirus (HPV) infections among mothers in the Finnish family HPV study. J Clin Microbiol 48:2665–2671 [View Article][PubMed]
    [Google Scholar]
  29. Louvanto K., Syrjänen K. J., Rintala M. A., Grénman S. E., Syrjänen S. M. 2011; Human papillomavirus and predictors of cervical intraepithelial neoplasia among young mothers in a prospective follow-up study. Acta Obstet Gynecol Scand 90:167–173 [View Article][PubMed]
    [Google Scholar]
  30. Michael K. M., Waterboer T., Sehr P., Rother A., Reidel U., Boeing H., Bravo I. G., Schlehofer J., Gärtner B. C., Pawlita M. 2008; Seroprevalence of 34 human papillomavirus types in the German general population. PLoS Pathog 4:e1000091 [View Article][PubMed]
    [Google Scholar]
  31. Miller S. A., Dykes D. D., Polesky H. F. 1988; A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215 [View Article][PubMed]
    [Google Scholar]
  32. Mork J., Lie A. K., Glattre E., Clark S., Hallmans G., Jellum E., Koskela P., Møller B., Pukkala E. et al. 2001; Human papillomavirus infection as a risk factor for squamous-cell carcinoma of the head and neck. N Engl J Med 344:1125–1131 [View Article][PubMed]
    [Google Scholar]
  33. Nielsen A., Kjaer S. K., Munk C., Osler M., Iftner T. 2010; Persistence of high-risk human papillomavirus infection in a population-based cohort of Danish women. J Med Virol 82:616–623 [View Article][PubMed]
    [Google Scholar]
  34. Olsen A. O., Dillner J., Gjøen K., Magnus P. 1997; Seropositivity against HPV 16 capsids: a better marker of past sexual behaviour than presence of HPV DNA. Genitourin Med 73:131–135[PubMed]
    [Google Scholar]
  35. Pintos J., Black M. J., Sadeghi N., Ghadirian P., Zeitouni A. G., Viscidi R. P., Herrero R., Coutlée F., Franco E. L. 2008; Human papillomavirus infection and oral cancer: a case-control study in Montreal, Canada. Oral Oncol 44:242–250 [View Article][PubMed]
    [Google Scholar]
  36. Puranen M., Yliskoski M., Saarikoski S., Syrjänen K., Syrjänen S. 1996; Vertical transmission of human papillomavirus from infected mothers to their newborn babies and persistence of the virus in childhood. Am J Obstet Gynecol 174:694–699 [View Article][PubMed]
    [Google Scholar]
  37. Ralston Howe E., Li Z., McGlennen R. C., Hellerstedt W. L., Downs L. S. Jr 2009; Type-specific prevalence and persistence of human papillomavirus in women in the United States who are referred for typing as a component of cervical cancer screening. Am J Obstet Gynecol 245:e1–e7 [View Article][PubMed]
    [Google Scholar]
  38. Richardson H., Kelsall G., Tellier P., Voyer H., Abrahamowicz M., Ferenczy A., Coutlée F., Franco E. L. 2003; The natural history of type-specific human papillomavirus infections in female university students. Cancer Epidemiol Biomarkers Prev 12:485–490[PubMed]
    [Google Scholar]
  39. Rintala M. A., Grénman S. E., Järvenkylä M. E., Syrjänen K. J., Syrjänen S. M. 2005a; High-risk types of human papillomavirus (HPV) DNA in oral and genital mucosa of infants during their first 3 years of life: experience from the Finnish HPV Family Study. Clin Infect Dis 41:1728–1733 [View Article][PubMed]
    [Google Scholar]
  40. Rintala M. A., Grénman S. E., Puranen M. H., Isolauri E., Ekblad U., Kero P. O., Syrjänen S. M. 2005b ). Transmission of high-risk human papillomavirus (HPV) between parents and infant: a prospective study of HPV in families in Finland. J Clin Microbiol 43:376–381 [View Article][PubMed]
    [Google Scholar]
  41. Rintala M., Grénman S., Puranen M., Syrjänen S. 2006; Natural history of oral papillomavirus infections in spouses: a prospective Finnish HPV Family Study. J Clin Virol 35:89–94 [View Article][PubMed]
    [Google Scholar]
  42. Safaeian M., Porras C., Schiffman M., Rodriguez A. C., Wacholder S., Gonzalez P., Quint W., van Doorn L. J., Sherman M. E. et al. 2010; Epidemiological study of anti-HPV16/18 seropositivity and subsequent risk of HPV16 and -18 infections. J Natl Cancer Inst 102:1653–1662 [View Article][PubMed]
    [Google Scholar]
  43. Sarkola M. E., Grénman S. E., Rintala M. A., Syrjanen K. J., Syrjanen S. M. 2009; Effect of second pregnancy on maternal carriage and outcome of high-risk human papillomavirus (HPV). Experience from the prospective Finnish family HPV study. Gynecol Obstet Invest 67:208–216 [View Article][PubMed]
    [Google Scholar]
  44. Schiffman M., Kjaer S. K. 2003; Chapter 2: Natural history of anogenital human papillomavirus infection and neoplasia. J Natl Cancer Inst Monogr 31:14–19[PubMed] [CrossRef]
    [Google Scholar]
  45. Schmitt M., Bravo I. G., Snijders P. J., Gissmann L., Pawlita M., Waterboer T. 2006; Bead-based multiplex genotyping of human papillomaviruses. J Clin Microbiol 44:504–512 [View Article][PubMed]
    [Google Scholar]
  46. Skjeldestad F. E., Mehta V., Sings H. L., Øvreness T., Turpin J., Su L., Boerckel P., Roberts C., Bryan J. et al. 2008; Seroprevalence and genital DNA prevalence of HPV types 6, 11, 16 and 18 in a cohort of young Norwegian women: study design and cohort characteristics. Acta Obstet Gynecol Scand 87:81–88 [View Article][PubMed]
    [Google Scholar]
  47. Snijders P. J., van den Brule A. J., Schrijnemakers H. F., Snow G., Meijer C. J., Walboomers J. M. 1990; The use of general primers in the polymerase chain reaction permits the detection of a broad spectrum of human papillomavirus genotypes. J Gen Virol 71:173–181 [View Article][PubMed]
    [Google Scholar]
  48. Stone K. M., Karem K. L., Sternberg M. R., McQuillan G. M., Poon A. D., Unger E. R., Reeves W. C. 2002; Seroprevalence of human papillomavirus type 16 infection in the United States. J Infect Dis 186:1396–1402 [View Article][PubMed]
    [Google Scholar]
  49. Syrjänen S., Waterboer T., Sarkola M., Michael K., Rintala M., Syrjänen K., Grenman S., Pawlita M. 2009; Dynamics of human papillomavirus serology in women followed up for 36 months after pregnancy. J Gen Virol 90:1515–1526 [View Article][PubMed]
    [Google Scholar]
  50. Syrjänen S., Lodi G., von Bültzingslöwen I., Aliko A., Arduino P., Campisi G., Challacombe S., Ficarra G., Flaitz C. et al. 2011; Human papillomaviruses in oral carcinoma and oral potentially malignant disorders: a systematic review. Oral Dis 17:(Suppl. 1)58–72 [View Article][PubMed]
    [Google Scholar]
  51. Thompson D. L., Douglas J. M. Jr, Foster M., Hagensee M. E., Diguiseppi C., Barón A. E., Cameron J. E., Spencer T. C., Zenilman J. et al. 2004; Seroepidemiology of infection with human papillomavirus 16, in men and women attending sexually transmitted disease clinics in the United States. J Infect Dis 190:1563–1574 [View Article][PubMed]
    [Google Scholar]
  52. Trottier H., Franco E. L. 2006; Human papillomavirus and cervical cancer: burden of illness and basis for prevention. Am J Manag Care 12:(Suppl.)S462–S472[PubMed]
    [Google Scholar]
  53. Trottier H., Ferreira S., Thomann P., Costa M. C., Sobrinho J. S., Prado J. C., Rohan T. E., Villa L. L., Franco E. L. 2010; Human papillomavirus infection and reinfection in adult women: the role of sexual activity and natural immunity. Cancer Res 70:8569–8577 [View Article][PubMed]
    [Google Scholar]
  54. Vaccarella S., Franceschi S., Clifford G. M., Touzé A., Hsu C. C., de Sanjosé S., Anh P. T. H., Hieu N.T., Matos E. et al. 2010; Seroprevalence of antibodies against human papillomavirus (HPV) types 16 and 18 in four continents: the International Agency for Research on Cancer HPV Prevalence Surveys. Cancer Epidemiol Biomarkers Prev 19:2379–2388 [View Article][PubMed]
    [Google Scholar]
  55. Villa L. L., Ault K. A., Giuliano A. R., Costa R. L., Petta C. A., Andrade R. P., Brown D. R., Ferenczy A., Harper D. M., Koutsky L. 2006; Immunologic responses following administration of a vaccine targeting human papillomavirus types 6, 11, 16, and 18. Vaccine 24:5571–5583 [View Article][PubMed]
    [Google Scholar]
  56. Viscidi R. P., Kotloff K. L., Clayman B., Russ K., Shapiro S., Shah K. V. 1997; Prevalence of antibodies to human papillomavirus (HPV) type 16 virus-like particles in relation to cervical HPV infection among college women. Clin Diagn Lab Immunol 4:122–126[PubMed]
    [Google Scholar]
  57. Waterboer T., Sehr P., Michael K. M., Franceschi S., Nieland J. D., Joos T. O., Templin M. F., Pawlita M. 2005; Multiplex human papillomavirus serology based on in situ-purified glutathione S-transferase fusion proteins. Clin Chem 51:1845–1853 [View Article][PubMed]
    [Google Scholar]
  58. Waterboer T., Sehr P., Pawlita M. 2006; Suppression of non-specific binding in serological Luminex assays. J Immunol Methods 309:200–204 [View Article][PubMed]
    [Google Scholar]
  59. Wideroff L., Schiffman M. H., Hoover R., Tarone R. E., Nonnenmacher B., Hubbert N., Kirnbauer R., Greer C. E., Lorincz A. T. et al. 1996; Epidemiologic determinants of seroreactivity to human papillomavirus (HPV) type 16 virus-like particles in cervical HPV-16 DNA-positive and-negative women. J Infect Dis 174:937–943 [View Article][PubMed]
    [Google Scholar]
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