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Comparing Papanicolau smear, visual inspection with acetic acid and human papillomavirus cervical cancer screening methods among HIV-positive women by immune status and antiretroviral therapy

Chung, Michael H.a,b,c; McKenzie, Kevin P.a; De Vuyst, Hugoe; Richardson, Barbra A.a,d,f; Rana, Farzanag,†; Pamnani, Riteshh; Njoroge, Julia W.a; Nyongesa-Malava, Evansa; Sakr, Samah R.i; John-Stewart, Grace C.a,b,c; Mugo, Nelly R.a,h

doi: 10.1097/01.aids.0000432472.92120.1b
Epidemiology and Social

Background: A rigorous comparison of cervical cancer screening methods utilizing data on immune status, antiretroviral therapy (ART) and colposcopy-directed biopsy has not been performed among HIV-positive women.

Methods: Between June and November 2009, 500 HIV-positive women were enrolled at an HIV treatment clinic in Nairobi, Kenya, and underwent Papanicolau (Pap) smear, visual inspection with acetic acid (VIA), human papillomavirus (HPV) and colposcopy-directed biopsy (gold standard). Positive Pap smear (ASCUS+, LSIL+, HSIL+), VIA, HPV and their combinations were compared with CIN2/3+. Sensitivity, specificity and AUC (sensitivity and 1–specificity) were compared using pairwise tests and multivariate logistic regression models that included age, CD4+ cell count and ART duration.

Results: Of 500 enrolled, 498 samples were collected. On histology, there were 172 (35%) normal, 186 (37%) CIN1, 66 (13%) CIN2, 47 (9%) CIN3 and 27 (5%) indeterminate. Pap (ASCUS+) was the most sensitive screening method (92.7%), combination of both Pap (HSIL+) and VIA positive was the most specific (99.1%) and Pap (HSIL+) had the highest AUC (0.85). In multivariate analyses, CD4+ cell count of 350 cells/μl or less was associated with decreased HPV specificity (P = 0.002); ART duration of less than 2 years was associated with decreased HPV (P = 0.01) and VIA (P = 0.03) specificity; and age less than 40 years was associated with increased VIA sensitivity (P < 0.001) and decreased HPV specificity (P = 0.005).

Conclusion: Pap smear is a robust test among HIV-positive women regardless of immune status or ART duration. Results should be cautiously interpreted when using HPV among those younger, immunosuppressed or on ART less than 2 years, and when using VIA among those aged 40 years or more.

aDepartment of Global Health

bDepartment of Medicine

cDepartment of Epidemiology

dDepartment of Biostatistics, University of Washington, Seattle, Washington, USA

eInfections and Cancer Epidemiology Group, International Agency for Research on Cancer, Lyon, France

fVaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA

gAga Khan University Hospital

hKenyatta National Hospital

iCoptic Hospital, Nairobi, Kenya.


Correspondence to Dr Michael H. Chung, MD, MPH, University of Washington, 325 Ninth Ave, Box 359909, Seattle, WA 98104, USA. Tel: +1 206 543 4278; fax: +1 206 543 4818; e-mail:

Received 26 February, 2013

Revised 20 March, 2013

Accepted 24 June, 2013

© 2013 Lippincott Williams & Wilkins, Inc.