Genotyping for human papillomavirus types 16 and 18 in women with minor cervical lesions: A systematic review and meta-analysis

Annals of Internal Medicine

Volumn 166, Issue 2, 2017, Pages 118-127

  Arbyn, Marc ^a   Xu, Lan ^a   Verdoodt, Freija ^a   Cuzick, Jack ^b   Szarewski, Anne ^f   Belinson, Jerome L ^c   Wentzensen, Nicolas ^d   Gage, Julia C ^d   Khan, Michelle J ^e  

^a SCIENTIFIC INSTITUTE OF PUBLIC HEALTH   (Belgium)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c LERNER RESEARCH INSTITUTE   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e KAISER PERMANENTE   (United States)

^f NONE

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; CANCER RISK; GENOTYPE; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; META ANALYSIS; PRECANCER; PRIORITY JOURNAL; REVIEW; SENSITIVITY AND SPECIFICITY; SQUAMOUS INTRAEPITHELIAL LESION OF THE CERVIX; SYSTEMATIC REVIEW; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA IN SITU; EARLY CANCER DIAGNOSIS; EMERGENCY HEALTH SERVICE; FEMALE; GENETICS; PAPILLOMAVIRUS INFECTIONS; PRECANCEROUS CONDITIONS; RISK FACTOR; UTERINE CERVICAL NEOPLASMS; VIROLOGY;

EARLY DETECTION OF CANCER; FEMALE; GENOTYPE; HUMAN PAPILLOMAVIRUS 16; HUMAN PAPILLOMAVIRUS 18; HUMANS; PAPILLOMAVIRUS INFECTIONS; PRECANCEROUS CONDITIONS; RISK FACTORS; SENSITIVITY AND SPECIFICITY; TRIAGE; UTERINE CERVICAL NEOPLASMS;

EID: 85020299197     PISSN: 00034819     EISSN: 15393704     Source Type: Journal    
DOI: 10.7326/M15-2735     Document Type: Review

References (54)

1. Holowaty P, Miller AB, Rohan T, To T. Natural history of dysplasia of the uterine cervix. J Natl Cancer Inst. 1999;91:252-8. [PMID: 10037103]
2. ASCUS-LSIL Triage Study (ALTS) Group. Results of a randomized trial on the management of cytology interpretations of atypical squamous cells of undetermined significance. Am J Obstet Gynecol. 2003;188:1383-92. [PMID: 12824967]
3. Arbyn M, Buntinx F, Van Ranst M, Paraskevaidis E, Martin-Hirsch P, Dillner J. Virologic versus cytologic triage of women with equivocal Pap smears: a meta-analysis of the accuracy to detect high-grade intraepithelial neoplasia. J Natl Cancer Inst. 2004;96:280-93. [PMID: 14970277]
4. Arbyn M, Ronco G, Anttila A, Meijer CJ, Poljak M, Ogilvie G, et al. Evidence regarding human papillomavirus testing in secondary prevention of cervical cancer. Vaccine. 2012;30 Suppl 5:F88-99. [PMID: 23199969] doi:10.1016/j.vaccine.2012.06.095
5. Saslow D, Solomon D, Lawson HW, Killackey M, Kulasingam SL, Cain J, et al; ACS-ASCCP-ASCP Cervical Cancer Guideline Committee. American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer. CA Cancer J Clin. 2012;62:147-72. [PMID: 22422631] doi:10.3322/caac.21139
6. Provencher DM, Murphy KJ. Canadian consensus guidelines on human papillomavirus: chapter 3: the role of HPV testing. J Obstet Gynaecol Can. 2008;8:15-23.
7. Medical Services Advisory Committee. Human Papillomavirus Triage Test for Women with Possible or Definite Low-Grade Squamous Intraepithelial Lesions. Vol. 39. Canberra: Medical Services Advisory Committee; 2009.
8. Arbyn M, Anttila A, Jordan J, Ronco G, Schenck U, Segnan N, et al. European guidelines for quality assurance in cervical cancer screening. Second edition - summary document. Ann Oncol. 2010; 21:448-58. [PMID: 20176693] doi:10.1093/annonc/mdp471
9. ASCUS-LSIL Triage Study (ALTS) Group. A randomized trial on the management of low-grade squamous intraepithelial lesion cytology interpretations. Am J Obstet Gynecol. 2003;188:1393-400. [PMID: 12824968]
10. Zuna RE, Wang SS, Rosenthal DL, Jeronimo J, Schiffman M, Solomon D; ALTS Group. Determinants of human papillomavirusnegative, low-grade squamous intraepithelial lesions in the Atypical Squamous Cells of Undetermined Significance/Low-Grade Squamous Intraepithelial Lesions Triage Study (ALTS). Cancer. 2005;105: 253-62. [PMID: 15991244]
11. Arbyn M, Martin-Hirsch P, Buntinx F, Van Ranst M, Paraskevaidis E, Dillner J. Triage of women with equivocal or low-grade cervical cytology results: a meta-analysis of the HPV test positivity rate. J Cell MolMed.2009;13:648-59.[PMID:19166485]doi:10.1111/j.1582-4934 .2008.00631.x
12. Arbyn M, Roelens J, Simoens C, Buntinx F, Paraskevaidis E, Martin-Hirsch PP, et al. Human papillomavirus testing versus repeat cytology for triage of minor cytological cervical lesions. Cochrane Database Syst Rev. 2013:CD008054. [PMID: 23543559] doi:10.1002/14651858.CD008054.pub2
13. Leeflang MM, Deeks JJ, Takwoingi Y, Macaskill P. Cochrane diagnostic test accuracy reviews. Syst Rev. 2013;2:82. [PMID: 24099098] doi:10.1186/2046-4053-2-82
14. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264-9. [PMID: 19622511] doi:10.7326/0003-4819-151-4-200908180-00135
15. The 1988 Bethesda System for reporting cervical/vaginal cytological diagnoses. National Cancer Institute Workshop. JAMA. 1989; 262:931-4. [PMID: 2754794]
16. Solomon D, Davey D, Kurman R, Moriarty A, O'Connor D, Prey M, et al; Forum Group Members. The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA. 2002;287: 2114-9. [PMID: 11966386]
17. Evans DM, Hudson EA, Brown CL, Boddington MM, Hughes HE, Mackenzie EF, et al. Terminology in gynaecological cytopathology: report of the Working Party of the British Society for Clinical Cytology. J Clin Pathol. 1986;39:933-44. [PMID: 3760239]
18. Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol. 2003;3:25. [PMID: 14606960]
19. Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al; QUADAS-2 Group. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155:529-36. [PMID: 22007046] doi:10.7326/0003-4819-155-8- 201110180-00009
20. Harbord RM, Deeks JJ, Egger M, Whiting P, Sterne JA. A unification of models for meta-analysis of diagnostic accuracy studies. Biostatistics. 2007;8:239-51. [PMID: 16698768]
21. Harbord RM, Whiting P. metandi: meta-analysis of diagnostic accuracy using hierarchical logistic regression. Stata J. 2009;9: 211-29.
22. Deeks JJ, Bossuyt PM, Gatsonis C. Cochrane Handbook for Systematic Reviews of Diagnostic Test Accuracy. Version 1.0.0. London: The Cochrane Collaboration; 2013.
23. Takwoingi Y, Leeflang MM, Deeks JJ. Empirical evidence of the importance of comparative studies of diagnostic test accuracy. Ann Intern Med. 2013;158:544-54. [PMID: 23546566] doi:10.7326/0003- 4819-158-7-201304020-00006
24. Deeks JJ, Macaskill P, Irwig L. The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol. 2005;58: 882-93. [PMID: 16085191]
25. Katki HA, Schiffman M, Castle PE, Fetterman B, Poitras NE, Lorey T, et al. Benchmarking CIN 3+ risk as the basis for incorporating HPV and Pap cotesting into cervical screening and management guidelines. J Low Genit Tract Dis. 2013;17:S28-35. [PMID: 23519302] doi: 10.1097/LGT.0b013e318285423c
26. Wentzensen N, Fetterman B, Castle PE, Schiffman M, Wood SN, Stiemerling E, et al. p16/Ki-67 dual stain cytology for detection of cervical precancer in HPV-positive women. J Natl Cancer Inst. 2015; 107:djv257. [PMID: 26376685] doi:10.1093/jnci/djv257
27. Arbyn M, Roelens J, Martin-Hirsch P, Leeson S, Wentzensen N. Use of HC2 to triage women with borderline and mild dyskaryosis in the UK [Editorial]. Br J Cancer. 2011;105:877-80. [PMID: 21952649] doi:10.1038/bjc.2011.351
28. Belinson JL, Wu R, Belinson SE, Qu X, Yang B, Du H, et al. A population-based clinical trial comparing endocervical high-risk HPV testing using Hybrid Capture 2 and Cervista from the SHENCCAST II Study. Am J Clin Pathol. 2011;135:790-5. [PMID: 21502436] doi:10.1309/AJCPKA6ATAPBZ6JQ
29. Cuzick J, Thomas Cox J, Zhang G, Einstein MH, Stoler M, Trupin S, et al. Human papillomavirus testing for triage of women with lowgrade squamous intraepithelial lesions. Int J Cancer. 2013;132:959-66. [PMID: 22806936] doi:10.1002/ijc.27723
30. Einstein MH, Martens MG, Garcia FA, Ferris DG, Mitchell AL, Day SP, et al. Clinical validation of the Cervista HPV HR and 16/18 genotyping tests for use in women with ASC-US cytology. Gynecol Oncol. 2010;118:116-22. [PMID: 20488510] doi:10.1016/j.ygyno.2010.04 .013
31. Fröberg M, Johansson B, Hjerpe A, Andersson S. Human papillomavirus 'reflex' testing as a screening method in cases of minor cytological abnormalities. Br J Cancer. 2008;99:563-8. [PMID: 18682715] doi:10.1038/sj.bjc.6604504
32. Gage JC, Schiffman M, Solomon D, Wheeler CM, Gravitt PE, Castle PE, et al. Risk of precancer determined by HPV genotype combinations in women with minor cytologic abnormalities. Cancer Epidemiol Biomarkers Prev. 2013;22:1095-101. [PMID: 23603204] doi:10.1158/1055-9965.EPI-12-1455
33. Guo M, Lin CY, Gong Y, Cogdell DE, Zhang W, Lin E, et al. Human papillomavirus genotyping for the eight oncogenic types can improve specificity of HPV testing in women with mildly abnormal Pap results. Mod Pathol. 2008;21:1037-43. [PMID: 18500260] doi:10.1038/modpathol.2008.93
34. Halfon P, Benmoura D, Agostini A, Khiri H, Penaranda G, Martineau A, et al. Evaluation of the clinical performance of the Abbott RealTime High-Risk HPV for carcinogenic HPV detection. J Clin Virol. 2010;48:246-50. [PMID: 20541966] doi:10.1016/j.jcv.2010.05.008
35. Huang S, Erickson B, Tang N, Mak WB, Salituro J, Robinson J, et al. Clinical performance of Abbott RealTime High Risk HPV test for detection of high-grade cervical intraepithelial neoplasia in women with abnormal cytology. J Clin Virol. 2009;45 Suppl 1:S19-23. [PMID: 19651364] doi:10.1016/S1386-6532(09)70004-6
36. Lapierre SG, Sauthier P, Mayrand MH, Dufresne S, Petignat P, Provencher D, et al. Human papillomavirus (HPV) DNA triage of women with atypical squamous cells of undetermined significance with cobas 4800 HPV and Hybrid Capture 2 tests for detection of high-grade lesions of the uterine cervix. J Clin Microbiol. 2012;50: 1240-4. [PMID: 22301023] doi:10.1128/JCM.06656-11
37. Wong AK, Chan RC, Nichols WS, Bose S. Invader human papillomavirus (HPV) type 16 and 18 assays as adjuncts to HPV screening of cervical Papanicolaou smears with atypical squamous cells of undetermined significance. Cancer. 2009;115:823-32. [PMID: 19127558] doi:10.1002/cncr.24091
38. Monsonego J, Pollini G, Evrard MJ, Sednaoui P, Monfort L, Quinzat D, et al. Linear array genotyping and Hybrid Capture II assay in detecting human papillomavirus genotypes in women referred for colposcopy due to abnormal Papanicolaou smear. Int J STD AIDS. 2008;19:385-92. [PMID: 18595876] doi:10.1258/ijsa.2007.007259
39. Oliveira A, Verdasca N, Pista Â. Use of the NucliSENS EasyQ HPV assay in the management of cervical intraepithelial neoplasia. J Med Virol. 2013;85:1235-41. [PMID: 23918542] doi:10.1002/jmv.23590
40. Depuydt CE, Makar AP, Ruymbeke MJ, Benoy IH, Vereecken AJ, Bogers JJ. BD-ProExC as adjunct molecular marker for improved detection of CIN2+ after HPV primary screening. Cancer Epidemiol Biomarkers Prev. 2011;20:628-37. [PMID: 21297040] doi:10.1158/1055-9965.EPI-10-0818
41. Donà MG, Vocaturo A, Giuliani M, Ronchetti L, Rollo F, Pescarmona E, et al. p16/Ki-67 dual staining in cervico-vaginal cytology: correlation with histology, human papillomavirus detection and genotyping in women undergoing colposcopy. Gynecol Oncol. 2012;126:198-202. [PMID: 22588180] doi:10.1016/j.ygyno.2012.05 .004
42. Spathis A, Kottaridi C, Chranioti A, Meristoudis C, Chrelias C, Panayiotides IG, et al. mRNA and DNA detection of human papillomaviruses in women of all ages attending two colposcopy clinics. PLoS One. 2012;7:e49205. [PMID: 23166611] doi:10.1371/journal.pone.0049205
43. Stoler MH, Wright TC Jr, Sharma A, Apple R, Gutekunst K, Wright TL; ATHENA (Addressing THE Need for Advanced HPV Diagnostics) HPV Study Group. High-risk human papillomavirus testing in women with ASC-US cytology: results from the ATHENA HPV study. Am J Clin Pathol. 2011;135:468-75. [PMID: 21350104] doi:10.1309/AJCPZ5JY6FCVNMOT
44. Szarewski A, Ambroisine L, Cadman L, Austin J, Ho L, Terry G, et al. Comparison of predictors for high-grade cervical intraepithelial neoplasia in women with abnormal smears. Cancer Epidemiol Biomarkers Prev. 2008;17:3033-42. [PMID: 18957520] doi:10.1158/1055-9965.EPI-08-0508
45. Szarewski A, Mesher D, Cadman L, Austin J, Ashdown-Barr L, Ho L, et al. Comparison of seven tests for high-grade cervical intraepithelial neoplasia in women with abnormal smears: the Predictors 2 study. J Clin Microbiol. 2012;50:1867-73. [PMID: 22422852] doi:10.1128/JCM.00181-12
46. Wentzensen N, Schwartz L, Zuna RE, Smith K, Mathews C, Gold MA, et al. Performance of p16/Ki-67 immunostaining to detect cervical cancer precursors in a colposcopy referral population. Clin Cancer Res. 2012;18:4154-62. [PMID: 22675168] doi:10.1158/1078-0432 .CCR-12-0270
47. Wong OG, Lo CK, Szeto E, Cheung AN. Efficacy of Abbott Real- Time High Risk HPV test in evaluation of atypical squamous cells of undetermined significance from an Asian screening population. J Clin Virol. 2011;51:136-8. [PMID: 21530385] doi:10.1016/j.jcv.2011.03.010
48. Lin CQ, Cui JF, Zhang X, Pan QJ, Chen W, Qiao YL. Human papillomavirus genotyping to predict the risk of cervical precancerous lesions or cancer in women with minor abnormal cytology in China. Acta Cytol. 2015;59:405-11. [PMID: 26565687] doi:10.1159/000441290
49. Iwata T, Hasegawa T, Ochiai K, Takizawa K, Umezawa S, Kuramoto H, et al. Human papillomavirus test for triage of Japanese women with low-grade squamous intraepithelial lesions. Reprod Sci. 2015;22:1509-15. [PMID: 26092278] doi:10.1177/1933719115589408
50. Nakamura Y, Matsumoto K, Satoh T, Nishide K, Nozue A, Shimabukuro K, et al. HPV genotyping for triage of women with abnormal cervical cancer screening results: a multicenter prospective study. Int J Clin Oncol. 2015;20:974-81. [PMID: 25652908] doi:10.1007/s10147-015-0789-4
51. Khunamornpong S, Settakorn J, Sukpan K, Srisomboon J, Intaraphet S, Siriaunkgul S. High performance of combined HPV testing and genotyping for HPV16/18/52/58 in triaging women with minor cervical cytological abnormalities in northern Thailand. J Med Virol. 2016;88:135-43. [PMID: 26129775] doi:10.1002/jmv.24290
52. Arbyn M, Sasieni P, Meijer CJ, Clavel C, Koliopoulos G, Dillner J. Chapter 9: clinical applications of HPV testing: a summary of metaanalyses. Vaccine. 2006;24 Suppl 3:S78-89. [PMID: 16950021]
53. Schünemann HJ, Schünemann AH, Oxman AD, Brozek J, Glasziou P, Jaeschke R, et al; GRADE Working Group. Grading quality of evidence and strength of recommendations for diagnostic tests and strategies. BMJ. 2008;336:1106-10. [PMID: 18483053] doi:10.1136/bmj.39500.677199.AE
54. Huang LW, Lin YH, Pan HS, Seow KM, Lin CY. Human papillomavirus genotyping as a predictor of high-grade cervical dysplasia in women with mildly cytologic abnormalities: a two-year follow-up report. Diagn Cytopathol. 2012;40:673-7. [PMID: 21442773] doi:10.1002/dc.21591