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

Journal of General Virology

Volumn 92, Issue 9, 2011, Pages 2034-2046

  Paaso, A E ^a   Louvanto, K ^a,b   Syrjanen K J ^b   Waterboer, T ^c   Grenman S E ^b   Pawlita, M ^c   Syrjanen S M ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b TURKU UNIVERSITY HOSPITAL   (Finland)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS ANTIBODY; VIRUS DNA;

ARTICLE; FEMALE; FOLLOW UP; GENOTYPE; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 11; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN PAPILLOMAVIRUS TYPE 45; HUMAN PAPILLOMAVIRUS TYPE 6; MAJOR CLINICAL STUDY; MALE; MOUTH MUCOSA; PAPILLOMAVIRUS INFECTION; PREGNANT WOMAN; PRIORITY JOURNAL; SEROLOGY; UTERINE CERVIX; WART VIRUS;

ADULT; ANTIBODIES, VIRAL; CERVIX UTERI; COHORT STUDIES; DNA, VIRAL; FAMILY HEALTH; FEMALE; FINLAND; GENOTYPE; HUMANS; LONGITUDINAL STUDIES; MOUTH MUCOSA; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PREGNANCY;

HUMAN PAPILLOMAVIRUS;

EID: 80051765328     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.032011-0     Document Type: Article

References (59)

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.
2. Bosch, F. X., Burchell, A. N., Schiffman, M., Giuliano, A. R., de Sanjose, S., Bruni, L., Tortolero-Luna, G., Kjaer, S. K. & Muññoz, N. (2008). Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia. Vaccine 26 (Suppl. 10), K1-K16.
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.
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.
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.
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.
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.
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.
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. & other authors (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.
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.
11. Domz ̌a, G., Gudlevičiene, Z., Didz ̌ iapetriene, J., Valuckas, K. P., Kazbariene, B. & Dra sutiene, G. (2010). Human papillomavirus infection in pregnant women. Arch Gynecol Obstet 2010 doi:10.1007/ S00404-010-1787-4.
12. Frazer, I. H. (1996). Immunology of papillomavirus infection. Curr Opin Immunol 8, 484-491.
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.
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.
15. Giorgi, C., Di Bonito, P., Grasso, F., Mochi, S., Accardi, L., Doná, M. G., Branca, M., Costa, S., Mariani, L. & other authors (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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
32. Mork, J., Lie, A. K., Glattre, E., Clark, S., Hallmans, G., Jellum, E., Koskela, P., Møller, B., Pukkala, E. & other authors (2001). Human papillomavirus infection as a risk factor for squamous-cell carcinoma of the head and neck. N Engl J Med 344, 1125-1131.
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.
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.
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.
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.
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.
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.
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.
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.
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.
42. Safaeian, M., Porras, C., Schiffman, M., Rodriguez, A. C., Wacholder, S., Gonzalez, P., Quint, W., van Doorn, L. J., Sherman, M. E. & other authors (2010). Epidemiological study of anti-HPV16/18 seropositivity and subsequent risk of HPV16 and -18 infections. J Natl Cancer Inst 102, 1653-1662.
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.
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.
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.
46. Skjeldestad, F. E., Mehta, V., Sings, H. L., Øvreness, T., Turpin, J., Su, L., Boerckel, P., Roberts, C., Bryan, J. & other authors (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.
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.
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.
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.
50. Syrjänen, S., Lodi, G., von Bültzingslöwen, I., Aliko, A., Arduino, P., Campisi, G., Challacombe, S., Ficarra, G., Flaitz, C. & other authors (2011). Human papillomaviruses in oral carcinoma and oral potentially malignant disorders: a systematic review. Oral Dis 17 (Suppl. 1), 58-72.
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. & other authors (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.
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.
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.
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. & other authors (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.
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.
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.
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 Stransferase fusion proteins. Clin Chem 51, 1845-1853.
58. Waterboer, T., Sehr, P. & Pawlita, M. (2006). Suppression of nonspecific binding in serological Luminex assays. J Immunol Methods 309, 200-204.
59. Wideroff, L., Schiffman, M. H., Hoover, R., Tarone, R. E., Nonnenmacher, B., Hubbert, N., Kirnbauer, R., Greer, C. E., Lorincz, A. T. & other authors (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.