1887

Journal of General Virology header logo

Volume 86, Issue 10

Variants of human papillomaviruses 16 and 18 and their natural history in human immunodeficiency virus-positive women Free

Abstract

Highly oncogenic human papillomavirus (HPV) 16 and 18 variants might be expected to be particularly aggressive in HIV-positive women. The association of HPV16 and 18 variant lineages with race, human immunodeficiency virus (HIV) coinfection, CD4 T-cell count, HIV-RNA level, time-to-clearance of HPV infection and presence of squamous intraepithelial lesions (SIL) among women in the Women's Interagency HIV Study was studied. Subjects were followed semi-annually with Pap smear and cervicovaginal lavage (CVL). HPV DNA was detected in CVLs using MY09/11 L1 PCR assay. Specimens positive for HPV16/18 underwent E6 PCR and sequencing to determine the variant present. Specimens from 195 HPV16- and 162 HPV18-positive women were classified into variant lineages based on sequencing results. African variants of HPV16 and HPV18 were significantly more prevalent among African-Americans than among Caucasians [42 versus 14 % (=0·001) and 60 versus 13 % (<0·001), respectively]. However, it was not possible to detect associations between the HPV16 or 18 variant lineages and other factors studied. African variants of HPV16/18 were more common in women of African descent living outside Africa, which could reflect mixing behaviours and/or immunogenetic factors. However, in a large population of HIV-infected women, the variant of HPV16 or 18 was unrelated to persistence of infection or presence of SIL. If non-European variants are more oncogenic, the effect may involve a late stage in cervical tumorigenesis.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81060-0
2005-10-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/10/2709.html?itemId=/content/journal/jgv/10.1099/vir.0.81060-0&mimeType=html&fmt=ahah

References

  1. Ahdieh L., Klein R. S., Burk R. 7 other authors 2001; Prevalence, incidence, and type-specific persistence of human papillomavirus in human immunodeficiency virus (HIV)-positive and HIV-negative women. J Infect Dis 184:682–690 [CrossRef]
     [Google Scholar]
  2. Barkan S. E., Melnick S. L., Preston-Martin S. 7 other authors 1998; The Women's Interagency HIV Study. WIHS Collaborative Study Group. Epidemiology 9:117–125 [CrossRef]
     [Google Scholar]
  3. Bernard H. U., Chan S. Y., Manos M. M., Ong C. K., Villa L. L., Delius H., Peyton C. L., Bauer H. M., Wheeler C. M. 1994; Identification and assessment of known and novel human papillomaviruses by polymerase chain reaction amplification, restriction fragment length polymorphisms, nucleotide sequence, and phylogenetic algorithms. J Infect Dis 170:1077–1085 [CrossRef]
     [Google Scholar]
  4. Berumen J., Ordonez R. M., Lazcano E. 7 other authors 2001; Asian-American variants of human papillomavirus 16 and risk for cervical cancer: a case-control study. J Natl Cancer Inst 93:1325–1330 [CrossRef]
     [Google Scholar]
  5. Bontkes H. J., van Duin M., de Gruijl T. D. 11 other authors 1998; HPV 16 infection and progression of cervical intra-epithelial neoplasia: analysis of HLA polymorphism and HPV 16 E6 sequence variants. Int J Cancer 78:166–171 [CrossRef]
     [Google Scholar]
  6. Bosch F. X., Manos M. M., Munoz N. 7 other authors 1995; Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group. J Natl Cancer Inst 87:796–802 [CrossRef]
     [Google Scholar]
  7. Burk R. D., Terai M., Gravitt P. E. 10 other authors 2003; Distribution of human papillomavirus types 16 and 18 variants in squamous cell carcinomas and adenocarcinomas of the cervix. Cancer Res 63:7215–7220
     [Google Scholar]
  8. Casas L., Galvan S. C., Ordonez R. M., Lopez N., Guido M., Berumen J. 1999; Asian-american variants of human papillomavirus type 16 have extensive mutations in the E2 gene and are highly amplified in cervical carcinomas. Int J Cancer 83:449–455 [CrossRef]
     [Google Scholar]
  9. Chaturvedi A. K., Brinkman J. A., Gaffga A. M., Dumestre J., Clark R. A., Braly P. S., Dunlap K., Kissinger P. J., Hagensee M. E. 2004; Distribution of human papillomavirus type 16 variants in human immunodeficiency virus type 1-positive and -negative women. J Gen Virol 85:1237–1241 [CrossRef]
     [Google Scholar]
  10. Da Costa M. M., Hogeboom C. J., Holly E. A., Palefsky J. M. 2002; Increased risk of high-grade anal neoplasia associated with a human papillomavirus type 16 E6 sequence variant. J Infect Dis 185:1229–1237 [CrossRef]
     [Google Scholar]
  11. de Boer M. A., Peters L. A., Aziz M. F., Siregar B., Cornain S., Vrede M. A., Jordanova E. S., Kolkman-Uljee S., Fleuren G. J. 2004; Human papillomavirus type 16 E6, E7, and L1 variants in cervical cancer in Indonesia, Suriname, and The Netherlands. Gynecol Oncol 94:488–494 [CrossRef]
     [Google Scholar]
  12. de Boer M. A., Peters L. A., Aziz M. F., Siregar B., Cornain S., Vrede M. A., Jordanova E. S., Fleuren G. J. 2005; Human papillomavirus type 18 variants: histopathology and E6/E7 polymorphisms in three countries. Int J Cancer 114:422–425 [CrossRef]
     [Google Scholar]
  13. del Refugio Gonzalez-Losa M., Laviada Mier y Teran M. A., Puerto-Solis M., Garcia-Carranca A. 2004; Molecular variants of HPV type 16 E6 among Mexican women with LSIL and invasive cancer. J Clin Virol 29:95–98 [CrossRef]
     [Google Scholar]
  14. Franco E. L., Villa L. L., Sobrinho J. P., Prado J. M., Rousseau M. C., Desy M., Rohan T. E. 1999; Epidemiology of acquisition and clearance of cervical human papillomavirus infection in women from a high-risk area for cervical cancer. J Infect Dis 180:1415–1423 [CrossRef]
     [Google Scholar]
  15. Gemignani F., Landi S., Chabrier A., Smet A., Zehbe I., Canzian F., Tommasino M. 2004; Generation of a DNA microarray for determination of E6 natural variants of human papillomavirus type 16. J Virol Methods 119:95–102 [CrossRef]
     [Google Scholar]
  16. Giannoudis A., Herrington C. S. 2001; Human papillomavirus variants and squamous neoplasia of the cervix. J Pathol 193:295–302 [CrossRef]
     [Google Scholar]
  17. Giuliano A. R., Harris R., Sedjo R. L. 7 other authors 2002; Incidence, prevalence, and clearance of type-specific human papillomavirus infections: The Young Women's Health Study. J Infect Dis 186:462–469 [CrossRef]
     [Google Scholar]
  18. Hecht J. L., Kadish A. S., Jiang G., Burk R. D. 1995; Genetic characterization of the human papillomavirus (HPV) 18 E2 gene in clinical specimens suggests the presence of a subtype with decreased oncogenic potential. Int J Cancer 60:369–376 [CrossRef]
     [Google Scholar]
  19. Hildesheim A., Schiffman M., Bromley C. 12 other authors 2001; Human papillomavirus type 16 variants and risk of cervical cancer. J Natl Cancer Inst 93:315–318 [CrossRef]
     [Google Scholar]
  20. Ho L., Chan S. Y., Burk R. D. 7 other authors 1993; The genetic drift of human papillomavirus type 16 is a means of reconstructing prehistoric viral spread and the movement of ancient human populations. J Virol 67:6413–6423
     [Google Scholar]
  21. 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 [CrossRef]
     [Google Scholar]
  22. Hu X., Pang T., Guo Z., Mazurenko N., Kisseljov F., Ponten J., Nister M. 2001a; HPV16 E6 gene variations in invasive cervical squamous cell carcinoma and cancer in situ from Russian patients. Br J Cancer 84:791–795 [CrossRef]
     [Google Scholar]
  23. Hu X., Pang T., Guo Z., Ponten J., Nister M., Bernard Afink G. 2001b; Oncogene lineages of human papillomavirus type 16 E6, E7 and E5 in preinvasive and invasive cervical squamous cell carcinoma. J Pathol 195:307–311 [CrossRef]
     [Google Scholar]
  24. Icenogle J. P., Laga M., Miller D., Manoka A. T., Tucker R. A., Reeves W. C. 1992; Genotypes and sequence variants of human papillomavirus DNAs from human immunodeficiency virus type 1-infected women with cervical intraepithelial neoplasia. J Infect Dis 166:1210–1216 [CrossRef]
     [Google Scholar]
  25. Kammer C., Tommasino M., Syrjanen S., Delius H., Hebling U., Warthorst U., Pfister H., Zehbe I. 2002; Variants of the long control region and the E6 oncogene in European human papillomavirus type 16 isolates: implications for cervical disease. Br J Cancer 86:269–273 [CrossRef]
     [Google Scholar]
  26. Liaw K. L., Hildesheim A., Burk R. D. 9 other authors 2001; A prospective study of human papillomavirus (HPV) type 16 DNA detection by polymerase chain reaction and its association with acquisition and persistence of other HPV types. J Infect Dis 183:8–15 [CrossRef]
     [Google Scholar]
  27. Lizano M., Berumen J., Guido M. C., Casas L., Garcia-Carranca A. 1997; Association between human papillomavirus type 18 variants and histopathology of cervical cancer. J Natl Cancer Inst 89:1227–1231 [CrossRef]
     [Google Scholar]
  28. Londesborough P., Ho L., Terry G., Cuzick J., Wheeler C., Singer A. 1996; Human papillomavirus genotype as a predictor of persistence and development of high-grade lesions in women with minor cervical abnormalities. Int J Cancer 69:364–368 [CrossRef]
     [Google Scholar]
  29. Matsumoto K., Yoshikawa H., Nakagawa S. 8 other authors 2000; Enhanced oncogenicity of human papillomavirus type 16 (HPV16) variants in Japanese population. Cancer Lett 156:159–165 [CrossRef]
     [Google Scholar]
  30. Mayrand M. H., Coutlee F., Hankins C., Lapointe N., Forest P., de Ladurantaye M., Roger M. 2000; Detection of human papillomavirus type 16 DNA in consecutive genital samples does not always represent persistent infection as determined by molecular variant analysis. J Clin Microbiol 38:3388–3393
     [Google Scholar]
  31. Moscicki A. B., Ellenberg J. H., Farhat S., Xu J. 2004; Persistence of human papillomavirus infection in HIV-infected and -uninfected adolescent girls: risk factors and differences, by phylogenetic type. J Infect Dis 190:37–45 [CrossRef]
     [Google Scholar]
  32. Nindl I., Rindfleisch K., Lotz B., Schneider A., Durst M. 1999; Uniform distribution of HPV 16 E6 and E7 variants in patients with normal histology, cervical intra-epithelial neoplasia and cervical cancer. Int J Cancer 82:203–207 [CrossRef]
     [Google Scholar]
  33. Ong C. K., Chan S. Y., Campo M. S. 7 other authors 1993; Evolution of human papillomavirus type 18: an ancient phylogenetic root in Africa and intratype diversity reflect coevolution with human ethnic groups. J Virol 67:6424–6431
     [Google Scholar]
  34. Palefsky J. M., Minkoff H., Kalish L. A. 7 other authors 1999; Cervicovaginal human papillomavirus infection in human immunodeficiency virus-1 (HIV)-positive and high-risk HIV-negative women. J Natl Cancer Inst 91:226–236 [CrossRef]
     [Google Scholar]
  35. Perez-Gallego L., Moreno-Bueno G., Sarrio D., Suarez A., Gamallo C., Palacios J. 2001; Human papillomavirus-16 E6 variants in cervical squamous intraepithelial lesions from HIV-negative and HIV-positive women. Am J Clin Pathol 116:143–148 [CrossRef]
     [Google Scholar]
  36. Picconi M. A., Alonio L. V., Sichero L., Mbayed V., Villa L. L., Gronda J., Campos R., Teyssie A. 2003; Human papillomavirus type-16 variants in Quechua aboriginals from Argentina. J Med Virol 69:546–552 [CrossRef]
     [Google Scholar]
  37. Richardson H., Kelsall G., Tellier P., Voyer H., Abrahamowicz M., Ferenczy A., Coutlee 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
     [Google Scholar]
  38. Rousseau M. C., Pereira J. S., Prado J. C., Villa L. L., Rohan T. E., Franco E. L. 2001; Cervical coinfection with human papillomavirus (HPV) types as a predictor of acquisition and persistence of HPV infection. J Infect Dis 184:1508–1517 [CrossRef]
     [Google Scholar]
  39. Strickler H. D., Palefsky J. M., Shah K. V. 16 other authors 2003; Human papillomavirus type 16 and immune status in human immunodeficiency virus-seropositive women. J Natl Cancer Inst 95:1062–1071 [CrossRef]
     [Google Scholar]
  40. Terry G., Ho L., Cuzick J. 1997; Analysis of E2 amino acid variants of human papillomavirus types 16 and 18 and their associations with lesion grade and HLA DR/DQ type. Int J Cancer 73:651–655 [CrossRef]
     [Google Scholar]
  41. van Duin M., Snijders P. J., Vossen M. T., Klaassen E., Voorhorst F., Verheijen R. H., Helmerhorst T. J., Meijer C. J., Walboomers J. M. 2000; Analysis of human papillomavirus type 16 E6 variants in relation to p53 codon 72 polymorphism genotypes in cervical carcinogenesis. J Gen Virol 81:317–325
     [Google Scholar]
  42. Villa L. L., Sichero L., Rahal P., Caballero O., Ferenczy A., Rohan T., Franco E. L. 2000; Molecular variants of human papillomavirus types 16 and 18 preferentially associated with cervical neoplasia. J Gen Virol 81:2959–2968
     [Google Scholar]
  43. Walboomers J. M., Jacobs M. V., Manos M. M. 7 other authors 1999; Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189:12–19 [CrossRef]
     [Google Scholar]
  44. Wheeler C. M., Yamada T., Hildesheim A., Jenison S. A. 1997; Human papillomavirus type 16 sequence variants: identification by E6 and L1 lineage-specific hybridization. J Clin Microbiol 35:11–19
     [Google Scholar]
  45. Xi L. F., Demers G. W., Koutsky L. A., Kiviat N. B., Kuypers J., Watts D. H., Holmes K. K., Galloway D. A. 1995; Analysis of human papillomavirus type 16 variants indicates establishment of persistent infection. J Infect Dis 172:747–755 [CrossRef]
     [Google Scholar]
  46. Xi L. F., Koutsky L. A., Galloway D. A., Kuypers J., Hughes J. P., Wheeler C. M., Holmes K. K., Kiviat N. B. 1997; Genomic variation of human papillomavirus type 16 and risk for high grade cervical intraepithelial neoplasia. J Natl Cancer Inst 89:796–802 [CrossRef]
     [Google Scholar]
  47. Xi L. F., Critchlow C. W., Wheeler C. M. 9 other authors 1998; Risk of anal carcinoma in situ in relation to human papillomavirus type 16 variants. Cancer Res 58:3839–3844
     [Google Scholar]
  48. Xi L. F., Carter J. J., Galloway D. A., Kuypers J., Hughes J. P., Lee S. K., Adam D. E., Kiviat N. B., Koutsky L. A. 2002; Acquisition and natural history of human papillomavirus type 16 variant infection among a cohort of female university students. Cancer Epidemiol Biomarkers Prev 11:343–351
     [Google Scholar]
  49. Yamada T., Wheeler C. M., Halpern A. L., Stewart A. C., Hildesheim A., Jenison S. A. 1995; Human papillomavirus type 16 variant lineages in United States populations characterized by nucleotide sequence analysis of the E6, L2, and L1 coding segments. J Virol 69:7743–7753
     [Google Scholar]
  50. Yamada T., Manos M. M., Peto J., Greer C. E., Munoz N., Bosch F. X., Wheeler C. M. 1997; Human papillomavirus type 16 sequence variation in cervical cancers: a worldwide perspective. J Virol 71:2463–2472
     [Google Scholar]
  51. Zehbe I., Wilander E., Delius H., Tommasino M. 1998; Human papillomavirus 16 E6 variants are more prevalent in invasive cervical carcinoma than the prototype. Cancer Res 58:829–833
     [Google Scholar]
  52. Zehbe I., Tachezy R., Mytilineos J. 7 other authors 2001a; Human papillomavirus 16 E6 polymorphisms in cervical lesions from different European populations and their correlation with human leukocyte antigen class II haplotypes. Int J Cancer 94:711–716 [CrossRef]
     [Google Scholar]
  53. Zehbe I., Voglino G., Wilander E., Delius H., Marongiu A., Edler L., Klimek F., Andersson S., Tommasino M. 2001b; p53 codon 72 polymorphism and various human papillomavirus 16 E6 genotypes are risk factors for cervical cancer development. Cancer Res 61:608–611
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81060-0
Loading
Variants of human papillomaviruses 16 and 18 and their natural history in human immunodeficiency virus-positive women
J. Gen. Virol. 86, 2709 (2005); https://doi.org/10.1099/vir.0.81060-0
/content/journal/jgv/10.1099/vir.0.81060-0
/content/journal/jgv/10.1099/vir.0.81060-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error