Cited by 199Cervical Cancer and HPV ResearchWomen's cancer prevention and managementReproductive tract infections research

Systematic reviews and meta-analyses of the accuracy of HPV tests, visual inspection with acetic acid, cytology, and colposcopy

Open access
Mustafa, Reem A., Santesso, Nancy, Khatib, Rasha, Mustafa, Ahmad A., Wiercioch, Wojtek, Kehar, Rohan, Gandhi, Shreyas, Chen, Yaolong +7 more·2016·International Journal of Gynecology & Obstetrics

Abstract

BACKGROUND: Cervical cancer screening is offered to women to identify and treat cervical intraepithelial neoplasia (CIN). OBJECTIVES: To support WHO guidelines, a systematic review was performed to compare test accuracy of the HPV test, cytology (cervical smear), and unaided visual inspection with acetic acid (VIA); and to determine test accuracy of HPV and colposcopy impression. SEARCH STRATEGY: Medline and Embase were searched up to September 2012, and experts were contacted for references. SELECTION CRITERIA: Studies of at least 100 nonpregnant women (aged ≥18years) not previously diagnosed with CIN were included. DATA COLLECTION AND ANALYSIS: Two investigators independently screened and collected data. Pooled sensitivity and specificity, and absolute differences were calculated, and the quality of evidence assessed using GRADE (Grading of Recommendations Assessment, Development and Evaluation). MAIN RESULTS: High to moderate quality evidence was found. The greatest difference in overtreatment occurred with VIA instead of the cervical smear (58 more per 1000 women). Differences in missed treatment ranged from 2-5 per 1000 women. For 1000 women screened positive and then sent to colposcopy, 464 would be falsely diagnosed with CIN grade 2-3 and treated. CONCLUSIONS: Although differences in sensitivity between tests could be interpreted as large, absolute differences in missed diagnoses were small. By contrast, small differences in specificity resulted in fairly large absolute differences in overtreatment.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.ijgo.2015.07.024

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Sensitivity and specificity of each screening strategy and colposcopy, and efficacy of HPV vaccine, were based on published meta-analysis studies.

    “Sensitivity and specificity of each of the screening strategy and colposcopy and efficacy of HPV vaccine was based on the published meta-analysis studies (Table 1). [29, 33, 34]”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 37

  1. Schünemann HJ, Mustafa R, Brozek J. Diagnostic accuracy and linked evidence-testing the chain [in German]. Z Evid Fortbild Qual Gesundhwes 2012;106(3):153-60.
  2. Santesso N, Mustafa RA, Schünemann HJ, Arbyn M, Blumenthal PD, Cain J, et al. World Health Organization Guidelines: Treatment of cervical intraepithelial neoplasia 2-3 and Screen and Treat strategies to prevent cervical cancer. Int J Gynecol Obstet 2016;132(3):252-8.
  3. Irwig L, Bossuyt P, Glasziou P, Gatsonis C, Lijmer J. Designing studies to ensure that estimates of test accuracy are transferable. BMJ 2002;324(7338):669-71.
  4. 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.
  5. Belinson J, Qiao YL, Pretorius R, Zhang WH, Elson P, Li L, et al. Shanxi Province Cervical Cancer Screening Study: a cross-sectional comparative trial of multiple techniques to detect cervical neoplasia. Gynecol Oncol 2001;83(2):439-44.
  6. De Vuyst H, Claeys P, Njiru S, Muchiri L, Steyaert S, De Sutter P, et al. Comparison of pap smear, visual inspection with acetic acid, human papillomavirus DNA-PCR testing and cervicography. Int J Gynecol Obstet 2005;89(2):120-6.
  7. Qiao YL, Sellors JW, Eder PS, Bao YP, Lim JM, Zhao FH, et al. A new HPV-DNA test for cervical-cancer screening in developing regions: a cross-sectional study of clinical accuracy in rural China. Lancet Oncol 2008;9(10):929-36.
  8. Shastri SS, Dinshaw K, Amin G, Goswami S, Patil S, Chinoy R, et al. Concurrent evaluation of visual, cytological and HPV testing as screening methods for the early detection of cervical neoplasia in Mumbai, India. Bull World Health Organ 2005;83(3):186-94.
  9. Sodhani P, Gupta S, Sharma JK, Parashari A, Halder K, Singh V, et al. Test characteristics of various screening modalities for cervical cancer: a feasibility study to develop an alternative strategy for resource-limited settings. Cytopathology 2006;17(6):348-52.
  10. Cremer M, Conlisk E, Maza M, Bullard K, Peralta E, Siedhoff M, et al. Adequacy of visual inspection with acetic acid in women of advancing age. Int J Gynecol Obstet 2011;113(1):68-71.
  11. Elit L, Baigal G, Tan J, Munkhtaivan A. Assessment of 2 cervical screening methods in Mongolia: cervical cytology and visual inspection with acetic acid. J Low Genit Tract Dis 2006;10(2):83-8.
  12. Ghaemmaghami F, Behtash N, Gilani MM, Mousavi A, Marjani M, Moghimi R. Visual inspection with acetic acid as a feasible screening test for cervical neoplasia in Iran. Int J Gynecol Cancer 2004;14(3):465-9.
  13. Goel A, Gandhi G, Batra S, Bhambhani S, Zutshi V, Sachdeva P. Visual inspection of the cervix with acetic acid for cervical intraepithelial lesions. Int J Gynecol Obstet 2005;88(1):25-30.
  14. Hedge D, Shetty H, Shetty PK, Rai S. Diagnostic value of acetic acid comparing with conventional Pap smear in the detection of colposcopic biopsy-proved CIN. J Cancer Res Ther 2011;7(4):454-8.
  15. Sahasrabuddhe VV, Bhosale RA, Kavatkar AN, Nagwanshi CA, Joshi SN, Jenkins CA, et al. Comparison of visual inspection with acetic acid and cervical cytology to detect high-grade cervical neoplasia among HIV-infected women in India. Int J Cancer 2012;130(1):234-40.
  16. Sankaranarayanan R, Wesley R, Thara S, Dhakad N, Chandralekha B, Sebastian P, et al. Test characteristics of visual inspection with 4% acetic acid (VIA) and Lugol's iodine (VILI) in cervical cancer screening in Kerala, India. Int J Cancer 2003; 106(3):404-8.
  17. Agorastos T, Dinas K, Lloveras B, de Sanjose S, Kornegay JR, Bonti H, et al. Human papillomavirus testing for primary screening in women at low risk of developing cervical cancer. The Greek experience. Gynecol Oncol 2005;96(3):714-20.
  18. Bigras G, de Marval F. The probability for a Pap test to be abnormal is directly proportional to HPV viral load: results from a Swiss study comparing HPV testing and liquid-based cytology to detect cervical cancer precursors in 13,842 women. Br J Cancer 2005;93(5):575-81.
  19. Cárdenas-Turanzas M, Nogueras-Gonzalez GM, Scheurer ME, Adler-Storthz K, Benedet JL, Beck JR, et al. The performance of human papillomavirus high-risk DNA testing in the screening and diagnostic settings. Cancer Epidemiol Biomarkers Prev 2008;17(10):2865-71.
  20. de Cremoux P, Coste J, Sastre-Garau X, Thioux M, Bouillac C, Labbé S, et al. Efficiency of the hybrid capture 2 HPV DNA test in cervical cancer screening. A study by the French Society of Clinical Cytology. Am J Clin Pathol 2003;120(4):492-9.
  21. 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(4):628-37.
  22. Hovland S, Arbyn M, Lie AK, Ryd W, Borge B, Berle EJ, et al. A comprehensive evalu- ation of the accuracy of cervical pre-cancer detection methods in a high-risk area in East Congo. Br J Cancer 2010;102(6):957-65.
  23. Mahmud SM, Sangwa-Lugoma G, Nasr SH, Kayembe PK, Tozin RR, Drouin P, et al. Comparison of human papillomavirus testing and cytology for cervical cancer screening in a primary health care setting in the Democratic Republic of the Congo. Gynecol Oncol 2012;124(2):286-91.
  24. Monsonego J, Hudgens MG, Zerat L, Zerat JC, Syrjänen K, Halfon P, et al. Evaluation of oncogenic human papillomavirus RNA and DNA tests with liquid-based cytology in primary cervical cancer screening: the FASE study. Int J Cancer 2011;129(3): 691-701.
  25. Petry KU, Menton S, Menton M, van Loenen-Frosch F, de Carvalho Gomes H, Holz B, et al. Inclusion of HPV testing in routine cervical cancer screening for women above 29 years in Germany: results for 8466 patients. Br J Cancer 2003;88(10):1570-7.
  26. Blumenthal PD, Gaffikin L, Chirenje ZM, McGrath J, Womack S, Shah K. Adjunctive testing for cervical cancer in low resource settings with visual inspection, HPV, and the Pap smear. Int J Gynecol Obstet 2001;72(1):47-53.
  27. Cantor SB, Cárdenas-Turanzas M, Cox DD, Atkinson EN, Nogueras-Gonzalez GM, Beck JR, et al. Accuracy of colposcopy in the diagnostic setting compared with the screening setting. Obstet Gynecol 2008;111(1):7-14.
  28. Cremer ML, Peralta EI, Dheming SG, Jimenez ME, Davis-Dao CA, Alonzo TA, et al. Digital assessment of the reproductive tract versus colposcopy for directing biopsies in women with abnormal Pap smears. J Low Genit Tract Dis 2010;14(1):5-10.
  29. Cristoforoni PM, Gerbaldo D, Perino A, Piccoli R, Montz FJ, Capitanio GL. Computerized colposcopy: results of a pilot study and analysis of its clinical relevance. Obstet Gynecol 1995;85(6):1011-6.
  30. Durdi GS, Sherigar BY, Dalal AM, Desai BR, Malur PR. Correlation of colposcopy using Reid colposcopic index with histopathology-a prospective study. J Turk Ger Gynecol Assoc 2009;10(4):205-7.
  31. Ferris DG, Miller MD. Colposcopic accuracy in a residency training program: defining competency and proficiency. J Fam Pract 1993;36(5):515-20.
  32. Homesley HD, Jobson VW, Reish RL. Use of colposcopically directed, four-quadrant cervical biopsy by the colposcopy trainee. J Reprod Med 1984;29(5):311-6.
  33. Jones DE, Creasman WT, Dombroski RA, Lentz SS, Waeltz JL. Evaluation of the atypical Pap smear. Am J Obstet Gynecol 1987;157(3):544-9.
  34. Kierkegaard O, Byrjalsen C, Frandsen KH, Hansen KC, Frydenberg M. Diagnostic accuracy of cytology and colposcopy in cervical squamous intraepithelial lesions. Acta Obstet Gynecol Scand 1994;73(8):648-51.
  35. Mousavi AS, Fakour F, Gilani MM, Behtash N, Ghaemmaghami F, Karimi Zarchi M. A prospective study to evaluate the correlation between Reid colposcopic index impression and biopsy histology. J Low Genit Tract Dis 2007;11(3):147-50.
  36. Patil K, Durdi G, Lakshmi KS, Swamy MK. Comparison of diagnostic efficacy of visual inspection of cervix with acetic acid and pap smear for prevention of cervical cancer: Is VIA superseding pap smear? J SAFOG 2011;3(3):131-4.
  37. Hsu J, Brożek JL, Terracciano L, Kreis J, Compalati E, Stein AT, et al. Application of GRADE: making evidence-based recommendations about diagnostic tests in clinical practice guidelines. Implement Sci 2011;6:62.

Cited by

Sorted by citations

Authors
Mustafa, R. A., Santesso, N., Khatib, R., Mustafa, A. A., Wiercioch, W., Kehar, R., Gandhi, S., Chen, Y., Cheung, A., Hopkins, J., Ma, B., Lloyd, N., Wu, D., Broutet, N., & Schünemann, H. J.
Affiliations
  • University of Missouri–Kansas City (US)
  • McMaster University (CA)
  • Population Health Research Institute (CA)
  • Jordan University of Science and Technology (JO)
  • Lanzhou University (CN)
  • University of British Columbia (CA)
  • Guangzhou University of Chinese Medicine (CN)
  • World Health Organization (CH)
Corresponding author
Schünemann, Holger J
Venue
International Journal of Gynecology & Obstetrics
Publisher
Wiley
Published
2015-11-12
Volume
132
Issue
3
Pages
259-265
ISSN
  • 0020-6695 (ISSN-L)
  • 0020-7292
OpenAlex
W2176203755
Cited by
199
References
2
Citations by year
2026: 13 · 2025: 13 · 2024: 20 · 2023: 18 · 2022: 15 · 2021: 28 · 2020: 28 · 2019: 19 · 2018: 11 · 2017: 16 · 2016: 17 · 2015: 1
FWCI
1.94
Type
journal article
Language
en
Open access
Locations
  • International Journal of Gynecology & Obstetrics (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Lanzhou University Institutional Repository (submittedVersion)
Funders
  • WHO
  • World Health Organization
Topics
  • Health Sciences › Medicine › Epidemiology › Cervical Cancer and HPV Research
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Women's cancer prevention and management
  • Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
Keywords
cervical cancer screening, HPV testing, visual inspection with acetic acid, cervical cytology, colposcopy, cervical intraepithelial neoplasia, diagnostic accuracy, sensitivity and specificity, overtreatment, missed diagnosis
MeSH terms
Uterine Cervical Dysplasia, Uterine Cervical Neoplasms, Colposcopy, Female, Humans, Sensitivity and Specificity, Vaginal Smears, Acetic Acid, Papillomaviridae, Early Detection of Cancer, Papanicolaou Test

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review