Persistent human papillomavirus infection and cervical neoplasia: A systematic review and meta-analysis

American Journal of Epidemiology

Volumn 168, Issue 2, 2008, Pages 123-137

  Koshiol, Jill ^a   Lindsay, Lisa ^b   Pimenta, Jeanne M ^c   Poole, Charles ^d   Jenkins, David ^b   Smith, Jennifer S ^d  

^a NATIONAL CANCER INSTITUTE   (United States)

^b GLAXOSMITHKLINE BIOLOGICALS   (Belgium)

^c GLAXOSMITHKLINE   (United Kingdom)

^d IL   (United States)

Author keywords

Human papillomavirus 16; Human papillomavirus 18; Longitudinal studies; Papillomavirus infections; Uterine cervical neoplasms

Indexed keywords

VIRUS DNA;

CANCER; CARCINOGEN; DETECTION METHOD; META-ANALYSIS; REPRODUCTIVE DISORDER; TESTING METHOD;

CONFIDENCE INTERVAL; DISEASE DURATION; HUMAN; MEDLINE; REVIEW; RISK FACTOR; SAMPLING; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA IN SITU; VIRUS INFECTION; WART VIRUS;

CARCINOMA, SQUAMOUS CELL; CERVICAL INTRAEPITHELIAL NEOPLASIA; DNA, VIRAL; FEMALE; HUMAN PAPILLOMAVIRUS 16; HUMAN PAPILLOMAVIRUS 18; HUMANS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; RISK; UTERINE CERVICAL NEOPLASMS;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS - 16; HUMAN PAPILLOMAVIRUS - 18; HUMAN PAPILLOMAVIRUS TYPE 16; PAPILLOMAVIRIDAE;

EID: 46749137498     PISSN: 00029262     EISSN: 14766256     Source Type: Journal    
DOI: 10.1093/aje/kwn036     Document Type: Review

References (105)

1. Bosch FX, Lorincz A, Munoz N, et al. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 2002;55:244-65.
2. International Agency for Research on Cancer. Human papillomaviruses. (IARC monographs on the evaluation of carcinogenic risks to humans, vol 90). Lyon, France: International Agency for Research on Cancer, 2007.
3. Muñoz N. Human papillomavirus and cancer: the epidemiological evidence. J Clin Virol 2000;19:1-5.
4. Ferlay J, Bray F, Pisani P, et al. GLOBOCAN 2002: cancer incidence, mortality and prevalence worldwide, version 2.0. Lyon, France: International Agency for Research on Cancer, 2004. (IARC Cancer Base no. 5).
5. Muñoz N, Bosch FX, de Sanjosé S, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003;348:518-27.
6. Smith JS, Lindsay L, Hoots B, et al. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer 2007; 121:621-32.
7. Walboomers JM, Jacobs MV, Manos MM, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-19.
8. Bosch FX, Muñoz N. The viral etiology of cervical cancer. Virus Res 2002;89:183-90.
9. Burd EM. Human papillomavirus and cervical cancer. Clin Microbiol Rev 2003;16:1-17.
10. Ho GY, Bierman R, Beardsley L, et al. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998;338:423-8.
11. Moscicki AB, Shiboski S, Boroering J, et al. The natural history of human papillomavirus infection as measured by repeated DNA testing in adolescent and young women. J Pediatr 1998;132:277-84.
12. Moscicki AB, Schiffman M, Kjaer S, et al. Chapter 5: updating the natural history of HPV and anogenital cancer. Vaccine 2006;24(suppl 3):S42-51.
13. Snijders PJ, Steenbergen RD, Heideman DA, et al. HPV-mediated cervical carcinogenesis: concepts and clinical implications. J Pathol 2006;208:152-64.
14. Schiffman M, Herrero R, DeSalle R, et al. The carcinogenicity of human papillomavirus types reflects viral evolution. Virology 2005;337:76-84.
15. Ho GY, Burk RD, Klein S, et al. Persistent genital human papillomavirus infection as a risk factor for persistent cervical dysplasia. J Natl Cancer Inst 1995;87:1365-71.
16. Wallin KL, Wiklund F, Angstrom T, et al. Type-specific persistence of human papillomavirus DNA before the development of invasive cervical cancer. N Engl J Med 1999;341:1633-8.
17. Harper DM, Franco EL, Wheeler C, et al. Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial. Lancet 2004;364:1757-65.
18. Mao C, Koutsky LA, Ault KA, et al. Efficacy of human papillomavirus-16 vaccine to prevent cervical intraepithelial neoplasia: a randomized controlled trial. Obstet Gynecol 2006;107:18-27.
19. Kulasingam SL, Hughes JP, Kiviat NB, et al. Evaluation of human papillomavirus testing in primary screening for cervical abnormalities: comparison of sensitivity, specificity, and frequency of referral. JAMA 2002;288:1749-57.
20. Perrons C, Brink N, Jalal H, et al. The impact of high risk human papillomavirus testing in an inner London colposcopy clinic. J Med Virol 2005;76:576-82.
21. Schiffman M, Kjaer SK. Chapter 2: natural history of anogenital human papillomavirus infection and neoplasia. J Natl Cancer Inst Monogr 2003;(31):14-19.
22. Woodman CB, Collins S. A critique of cohort studies examining the role of human papillomavirus infection in cervical neoplasia. BJOG 2002;109:1311-18.
23. Giuliano AR, Harris R, Sedjo RL, et al. Incidence, prevalence, and clearance of type-specific human papillomavirus infections: The Young Women's Health Study. J Infect Dis 2002;186:462-9.
24. Molano M, Van den BA, Plummer M, et al. Determinants of clearance of human papillomavirus infections in Colombian women with normal cytology: a population-based, 5-year follow-up study. Am J Epidemiol 2003;158:486-94.
25. Moscicki AB, Ellenberg JH, Crowley-Nowick P, et al. Risk of high-grade squamous intraepithelial lesion in HIV-infected adolescents. J Infect Dis 2004;190:1413-21.
26. Ahdieh L, Klein RS, Burk R, et al. Prevalence, incidence, and type-specific persistence of human papillomavirus in human immunodeficiency virus (HIV)-positive and HIV-negative women. J Infect Dis 2001;184:682-90.
27. Paraskevaidis E, Kaponis A, Malamou-Mitsi V, et al. The natural history of HPV infection of the uterine cervix. Long-term observational and histological data. Anticancer Res 2002;22:1177-81.
28. Beskow AH, Gyllensten UB. Host genetic control of HPV 16 titer in carcinoma in situ of the cervix uteri. Int J Cancer 2002;101:526-31.
29. Beskow AH, Josefsson AM, Gyllensten UB. HLA class II alleles associated with infection by HPV16 in cervical cancer in situ. Int J Cancer 2001;93:817-22.
30. Moberg M, Gustavsson I, Gyllensten U. Type-specific associations of human papillomavirus load with risk of developing cervical carcinoma in situ. Int J Cancer 2004;112:854-9.
31. Ylitalo N, Josefsson A, Melbye M, et al. A prospective study showing long-term infection with human papillomavirus 16 before the development of cervical carcinoma in situ. Cancer Res 2000;60:6027-32.
32. Bory JP, Cucherousset J, Lorenzato M, et al. Recurrent human papillomavirus infection detected with the hybrid capture II assay selects women with normal cervical smears at risk for developing high grade cervical lesions: a longitudinal study of 3,091 women. Int J Cancer 2002;102:519-25.
33. Clavel C, Masure M, Levert M, et al. Human papillomavirus detection by the hybrid capture II assay: a reliable test to select women with normal cervical smears at risk for developing cervical lesions. Diagn Mol Pathol 2000;9:145-50.
34. Clavel C, Masure M, Bory JP, et al. Human papillomavirus testing in primary screening for the detection of high-grade cervical lesions: a study of 7932 women. Br J Cancer 2001;84:1616-23.
35. Lorenzato M, Bory JP, Cucherousset J, et al. Usefulness of DNA ploidy measurement on liquid-based smears showing conflicting results between cytology and high-risk human papillomavirus typing. Am J Clin Pathol 2002;118:708-13.
36. Kjaer SK, Chackerian B, van den Brule AJ, et al. High-risk human papillomavirus is sexually transmitted: evidence from a follow-up study of virgins starting sexual activity (intercourse). Cancer Epidemiol Biomarkers Prev 2001;10:101-6.
37. Kjaer SK, van den Brule AJ, Paull G, et al. Type specific persistence of high risk human papillomavirus (HPV) as indicator of high grade cervical squamous intraepithelial lesions in young women: population based prospective follow up study. BMJ 2002;325:572.
38. Cuschieri KS, Whitley MJ, Cubie HA. Human papillomavirus type specific DNA and RNA persistence - implications for cervical disease progression and monitoring. J Med Virol 2004;73:65-70.
39. Cuschieri KS, Cubie HA, Whitley MW, et al. Persistent high risk HPV infection associated with development of cervical neoplasia in a prospective population study. J Clin Pathol 2005;58:946-50.
40. Moscicki AB, Palefsky JM, Gonzales J, et al. Colposcopic and histologic findings and human papillomavirus (HPV) DNA test variability in young women positive for HPV DNA. J Infect Dis 1992;166:951-7.
41. Moscicki AB, Hills N, Shiboski S, et al. Risks for incident human papillomavirus infection and low-grade squamous intraepithelial lesion development in young females. JAMA 2001;285:2995-3002.
42. American College of Obstetricians and Gynecologists. Management of abnormal cervical cytology and histology. (ACOG Practice Bulletin no. 66). Obstet Gynecol 2005;106:645-64.
43. Wright TC Jr, Cox JT, Massad LS, et al. 2001 consensus guidelines for the management of women with cervical cytological abnormalities. JAMA 2002;287:2120-9.
44. Wright TC Jr, Cox JT, Massad LS, et al. 2001 consensus guidelines for the management of women with cervical intraepithelial neoplasia. Am J Obstet Gynecol 2003;189:295-304.
45. Hardy RJ, Thompson SG. Detecting and describing heterogeneity in meta-analysis. Stat Med 1998;17:841-56.
46. Sterne JA, Gavaghan D, Egger M. Publication and related bias in meta-analysis: power of statistical tests and prevalence in the literature. J Clin Epidemiol 2000;53:1119-29.
47. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994;50:1088-101.
48. Egger M, Davey SG, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629-34.
49. Duval S, Tweedie R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000;56:455-63.
50. Thompson SG, Sharp SJ. Explaining heterogeneity in meta-analysis: a comparison of methods. Stat Med 1999;18:2693-708.
51. Liaw KL, Glass AG, Manos MM, et al. Detection of human papillomavirus DNA in cytologically normal women and subsequent cervical squamous intraepithelial lesions. J Natl Cancer Inst 1999;91:954-60.
52. Harris TG, Kulasingam SL, Kiviat NB, et al. Cigarette smoking, oncogenic human papillomavirus, Ki-67 antigen, and cervical intraepithelial neoplasia. Am J Epidemiol 2004;159:834-42.
53. Bais AG, Rebolj M, Snijders PJ, et al. Triage using HPV-testing in persistent borderline and mildly dyskaryotic smears: proposal for new guidelines. Int J Cancer 2005;116:122-9.
54. Cuzick J, Szarewski A, Cubie H, et al. Management of women who test positive for high-risk types of human papillomavirus: The HART Study. Lancet 2003;362:1871-6.
55. Dannecker C, Siebert U, Thaler CJ, et al. Primary cervical cancer screening by self-sampling of human papillomavirus DNA in internal medicine outpatient clinics. Ann Oncol 2004;15:863-9.
56. Elfgren K, Kalantari M, Moberger B, et al. A population-based five-year follow-up study of cervical human papillomavirus infection. Am J Obstet Gynecol 2000;183:561-7.
57. Hildesheim A, Schiffman MH, Gravitt PE, et al. Persistence of type-specific human papillomavirus infection among cytologically normal women. J Infect Dis 1994;169:235-40.
58. Hopman EH, Rozendaal L, Voorhorst FJ, et al. High risk human papillomavirus in women with normal cervical cytology prior to the development of abnormal cytology and colposcopy. BJOG 2000;107:600-4.
59. Hoyer H, Scheungraber C, Kuehne-Heid R, et al. Cumulative 5-year diagnoses of CIN2, CIN3 or cervical cancer after concurrent high-risk HPV and cytology testing in a primary screening setting. Int J Cancer 2005;116:136-43.
60. Peto J, Gilham C, Deacon J, et al. Cervical HPV infection and neoplasia in a large population-based prospective study: the Manchester cohort. Br J Cancer 2004;91:942-53.
61. Rosenfeld WD, Rose E, Vermund SH, et al. Follow-up evaluation of cervicovaginal human papillomavirus infection in adolescents. J Pediatr 1992;121:307-11.
62. Schlecht NF, Kulaga S, Robitaille J, et al. Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA 2001;286:3106-14.
63. Ahdieh L, Muñoz A, Vlahov D, et al. Cervical neoplasia and repeated positivity of human papillomavirus infection in human immunodeficiency virus-seropositive and -seronegative women. Am J Epidemiol 2000;151:1148-57.
64. Kotloff KL, Wasserman SS, Russ K, et al. Detection of genital human papillomavirus and associated cytological abnormalities among college women. Sex Transm Dis 1998;25:243-50.
65. Smith EM, Ritchie JM, Levy BT, et al. Prevalence and persistence of human papillomavirus in postmenopausal age women. Cancer Detect Prev 2003;27:472-80.
66. Smith EM, Johnson SR, Ritchie JM, et al. Persistent HPV infection in postmenopausal age women. Int J Gynaecol Obstet 2004;87:131-7.
67. Koutsky LA, Holmes KK, Critchlow CW, et al. A cohort study of the risk of cervical intraepithelial neoplasia grade 2 or 3 in relation to papillomavirus infection. N Engl J Med 1992;327:1272-8.
68. Aho J, Hankins C, Tremblay C, et al. Genomic polymorphism of human papillomavirus type 52 predisposes toward persistent infection in sexually active women. J Infect Dis 2004;190:46-52.
69. del Mistro A, Bertorelle R, Franzetti M, et al. Antiretroviral therapy and the clinical evolution of human papillomavirus-associated genital lesions in HIV-positive women. Clin Infect Dis 2004;38:737-42.
70. Ellerbrock TV, Chiasson MA, Bush TJ, et al. Incidence of cervical squamous intraepithelial lesions in HIV-infected women. JAMA 2000;283:1031-7.
71. Gagnon S, Hankins C, Tremblay C, et al. Polymorphism of human papillomavirus type 31 isolates infecting the genital tract of HIV-seropositive and HIV-seronegative women at risk for HIV infection. J Med Virol 2005;75:213-21.
72. Massad LS, Ahdieh L, Benning L, et al. Evolution of cervical abnormalities among women with HIV-1: evidence from surveillance cytology in the Women's Interagency HIV Study. J Acquir Immune Defic Syndr 2001;27:432-42.
73. Schuman P, Ohmit SE, Klein RS, et al. Longitudinal study of cervical squamous intraepithelial lesions in human immunodeficiency virus (HIV)-seropositive and at-risk HIV-seronegative women. J Infect Dis 2003;188:128-36.
74. Strickler HD, Palefsky JM, Shah KV, et al. Human papillomavirus type 16 and immune status in human immunodeficiency virus-seropositive women. J Natl Cancer Inst 2003;95:1062-71.
75. ter Harmsel B, Smedts F, Kuijpers J, et al. Relationship between human papillomavirus type 16 in the cervix and intraepithelial neoplasia. Obstet Gynecol 1999;93:46-50.
76. Cox JT, Schiffman M, Solomon D. Prospective follow-up suggests similar risk of subsequent cervical intraepithelial neoplasia grade 2 or 3 among women with cervical intraepithelial neoplasia grade 1 or negative colposcopy and directed biopsy. Am J Obstet Gynecol 2003;188:1406-12.
77. Kitchener HC, Castle PE, Cox JT. Chapter 7: achievements and limitations of cervical cytology screening. Vaccine 2006;24(suppl 3):S63-70.
78. Melnikow J, Nuovo J, Willan AR, et al. Natural history of cervical squamous intraepithelial lesions: a meta-analysis. Obstet Gynecol 1998;92:727-35.
79. Ostor AG. Natural history of cervical intraepithelial neoplasia: a critical review. Int J Gynecol Pathol 1993;12:186-92.
80. Winer RL, Kiviat NB, Hughes JP, et al. Development and duration of human papillomavirus lesions, after initial infection. J Infect Dis 2005;191:731-8.
81. Woodman CB, Collins S, Winter H, et al. Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet 2001;357:1831-6.
82. Woodman CB, Collins SI, Young LS. The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer 2007;7:11-22.
83. Castle PE, Solomon D, Schiffman M, et al. Human papillomavirus type 16 infections and 2-year absolute risk of cervical precancer in women with equivocal or mild cytologic abnormalities. J Natl Cancer Inst 2005;97:1066-71.
84. Khan MJ, Castle PE, Lorincz AT, et al. The elevated 10-year risk of cervical precancer and cancer in women with human papillomavirus (HPV) type 16 or 18 and the possible utility of type-specific HPV testing in clinical practice. J Natl Cancer Inst 2005;97:1072-9.
85. Coutlee F, Gravitt P, Kornegay J, et al. Use of PGMY primers in L1 consensus PCR improves detection of human papillomavirus DNA in genital samples. J Clin Microbiol 2002;40:902-7.
86. Daniel RW, Ahdieh L, Hayden D, et al. Intra-laboratory reproducibility of human papillomavirus identification in cervical specimens by a polymerase chain reaction-based assay. J Clin Virol 2000;19:187-93.
87. Kornegay JR, Roger M, Davies PO, et al. International proficiency study of a consensus L1 PCR assay for the detection and typing of human papillomavirus DNA: evaluation of accuracy and intralaboratory and interlaboratory agreement. J Clin Microbiol 2003;41:1080-6.
88. Qu W, Jiang G, Cruz Y, et al. PCR detection of human papillomavirus: comparison between MY09/MY11 and GP5+/ GP6+ primer systems. J Clin Microbiol 1997;35:1304-10.
89. Schiffman MH, Bauer HM, Lorincz AT, et al. Comparison of Southern blot hybridization and polymerase chain reaction methods for the detection of human papillomavirus DNA. J Clin Microbiol 1991;29:573-7.
90. Jeronimo J, Schiffman M. Colposcopy at a crossroads. Am J Obstet Gynecol 2006;195:349-53.
91. Stoler MH, Schiffman M. Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ASCUS-LSIL Triage Study. JAMA 2001;285:1500-5.
92. Schwartz LM, Woloshin S, Dvorin EL, et al. Ratio measures in leading medical journals: structured review of accessibility of underlying absolute risks. BMJ 2006;333:1248.
93. Franco EL, Villa LL, Sobrinho JP, et al. Epidemiology of acquisition and clearance of cervical human papillomavirus infection in women from a high-risk area for cervical cancer. J Infect Dis 1999;180:1415-23.
94. Koshiol JE, Schroeder JC, Jamieson DJ, et al. Time to clearance of human papillomavirus infection by type and human immunodeficiency virus serostatus. Int J Cancer 2006;119:1623-9.
95. Richardson H, Kelsal G, Tellier P, et al. The natural history of type-specific human papillomavirus infections in female university students. Cancer Epidemiol Biomarkers Prev 2003;12:485-90.
96. Schiffman M, Castle PE, Jeronimo J, et al. The natural history and prevention of HPV infection and cervical cancer. Lancet 2007;370:890-907.
97. Plummer M, Schiffman M, Castle PE, et al. A 2-year prospective study of human papillomavirus persistence among women with a cytological diagnosis of atypical squamous cells of undetermined significance or low-grade squamous intraepithelial lesion. J Infect Dis 2007;195:1582-9.
98. Belinson J, Qiao YL, Pretorius R, et al. Shanxi Province Cervical Cancer Screening Study: a cross-sectional comparative trial of multiple techniques to detect cervical neoplasia. Gynecol Oncol 2001;83:439-44.
99. Cuzick J, Clavel C, Petry KU, et al. Overview of the European and North American studies on HPV testing in primary cervical cancer screening. Int J Cancer 2006;119:1095-101.
100. Gage JC, Hanson VW, Abbey K, et al. Number of cervical biopsies and sensitivity of colposcopy. Obstet Gynecol 2006;108:264-72.
101. Pretorius RG, Kim RJ, Belinson JL, et al. Inflation of sensitivity of cervical cancer screening tests secondary to correlated error in colposcopy. J Low Genit Tract Dis 2006;10:5-9.
102. Dalstein W, Riethmuller D, Pretet JL, et al. Persistence and load of high-risk HPVare predictors for development of high-grade cervical lesions: a longitudinal French cohort study. Int J Cancer 2003;106:396-403.
103. Hawes SE, Critchlow CW, Sow PS, et al. Incident high-grade squamous intraepithelial lesions in Senegalese women with and without human immunodeficiency virus type 1 (HIV-1) and HIV-2. J Natl Cancer Inst 2006;98:100-9.
104. Saito J, Sumiyoshi M, Nakatani H, et al. Dysplasia and HPV infection initially detected by DNA analysis in cytomorphologically normal cervical smears. Int J Gynaecol Obstet 1995;51:43-8.
105. Koutsky LA, Ault KA, Wheeler CM, et al. A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med 2002;347:1645-51.