The authors wish to acknowledge and thank Dr Moses Sinkala, Dr Bushimbwa Tambatamba, Dr Velepi Mtonga, Dr Ann Chao, and Mr Fresher Mapiri for their contributions to the program described herein; and Mr. Alain Degroot (CIDRZ) for his contribution to the data collection system. None of them received compensation.
The program was conceptualized and designed by G.P.P., M.H.M., V.V.S., S.H.V. and J.S.A.S. Clinical/laboratory training was provided by G.P.P., M.H.M., K.S.P., V.M. and M.L.H. Data were analyzed, interpreted, and managed by V.V.S., G.P.P., M.H.M., S.H.V. and J.S.A.S. The manuscript was drafted by M.H.M., V.V.S. and G.P.P., and critical revision of the manuscript for important intellectual content was provided by S.H.V., K.S.P., J.S.A.S., V.M. and M.L.H. Funding for the program was obtained by J.S.A.S. and G.P.P. Administrative and technical support was provided by J.S.A.S., G.P.P. and M.H.M. The program was led and supervised by G.P.P. and M.H.M.
This study was supported by the President's Emergency Plan for AIDS Relief grant through the Elizabeth Glaser Pediatric AIDS Foundation from the Centers for Disease Control and Prevention Global AIDS Program with additional support from the National Institutes of Health (NIH) through the Center for AIDS Research at UAB (NIH grant P30AI027767), the International Clinical Research Scholars/Vanderbilt-UAB AIDS International Training and Research Program (NIH grant D43TW001035 and R24TW007988), Career Development award (NIH grant K23AI01411), and an Elizabeth Glaser Pediatric AIDS Foundation Clinical Scholars Award.
1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55:74–108.
2. Sankaranarayanan R, Ferlay J. Worldwide burden of gynaecological cancer: the size of the problem. Best Pract Res Clin Obstet Gynaecol 2006; 20:207–225.
3. Miller AB, Nazeer S, Fonn S, Brandup-Lukanow A, Rehman R, Cronje H, et al
. Report on consensus conference on cervical cancer screening and management. Int J Cancer 2000; 86:440–447.
4. Miller AB, Sankaranarayanan R, Bosch FX, Sepulveda C. Can screening for cervical cancer be improved, especially in developing countries? Int J Cancer 2003; 107:337–340.
5. Monsonego J, Bosch FX, Coursaget P, Cox JT, Franco E, Frazer I, et al
. Cervical cancer control, priorities and new directions. Int J Cancer 2004; 108:329–333.
6. Harris TG, Burk RD, Palefsky JM, Massad LS, Bang JY, Anastos K, et al
. Incidence of cervical squamous intraepithelial lesions associated with HIV serostatus, CD4 cell counts, and human papillomavirus test results. JAMA 2005; 293:1471–1476.
7. Heard I, Palefsky JM, Kazatchkine MD. The impact of HIV antiviral therapy on human papillomavirus (HPV) infections and HPV-related diseases. Antivir Ther 2004; 9:13–22.
8. Heard I, Schmitz V, Costagliola D, Orth G, Kazatchkine MD. Early regression of cervical lesions in HIV-seropositive women receiving highly active antiretroviral therapy. AIDS 1998; 12:1459–1464.
9. Heard I, Tassie JM, Schmitz V, Mandelbrot L, Kazatchkine MD, Orth G. Increased risk of cervical disease among human immunodeficiency virus-infected women with severe immunosuppression and high human papillomavirus load (1). Obstet Gynecol 2000; 96:403–409.
10. Minkoff H, Ahdieh L, Massad LS, Anastos K, Watts DH, Melnick S, et al
. The effect of highly active antiretroviral therapy on cervical cytologic changes associated with oncogenic HPV among HIV-infected women. AIDS 2001; 15:2157–2164.
11. Palefsky JM, Minkoff H, Kalish LA, Levine A, Sacks HS, Garcia P, et al
. Cervicovaginal human papillomavirus infection in human immunodeficiency virus-1 (HIV)-positive and high-risk HIV-negative women. J Natl Cancer Inst 1999; 91:226–236.
12. Parham GP, Sahasrabuddhe VV, Mwanahamuntu MH, Shepherd BE, Hicks ML, Stringer EM, Vermund SH. Prevalence and predictors of squamous intraepithelial lesions of the cervix in HIV-infected women in Lusaka, Zambia. Gynecol Oncol 2006; 103:1017–1022.
13. Strickler HD, Burk RD, Fazzari M, Anastos K, Minkoff H, Massad LS, et al
. Natural history and possible reactivation of human papillomavirus in human immunodeficiency virus-positive women. J Natl Cancer Inst 2005; 97:577–586.
14. Tate DR, Anderson RJ. Recrudescence of cervical dysplasia among women who are infected with the human immunodeficiency virus: a case-control analysis. Am J Obstet Gynecol 2002; 186:880–882.
15. Gilks CF, Crowley S, Ekpini R, Gove S, Perriens J, Souteyrand Y, et al
. The WHO public-health approach to antiretroviral treatment against HIV in resource-limited settings. Lancet 2006; 368:505–510.
16. United States. Congress House Committee on Foreign Affairs. PEPFAR: an assessment of progress and challenges: hearing before the Committee on Foreign Affairs, House of Representatives.
In: One Hundred Tenth Congress
, first session; 24 April 2007. Washington, DC: U.S. G.P.O.; 2007.
17. Central Intelligence Agency. The World Factbook 2008
. Washington, DC, United States: Central Intelligence Agency; 2008.
18. United States. Congress House Committee on Foreign Affairs. PEPFAR reauthorization: from emergency to sustainability: hearing before the Committee on Foreign Affairs, House of Representatives.
In: One Hundred Tenth Congress
, first session; 25 September 2007. Washington, DC: U.S. G.P.O.; 2007.
19. Pfaendler KS, Mwanahamuntu MH, Sahasrabuddhe VV, Mudenda V, Stringer JS, Parham GP. Management of cryotherapy-ineligible women in a “screen-and-treat” cervical cancer prevention program targeting HIV-infected women in Zambia: lessons from the field. Gynecol Oncol 2008; 110:402–407.
20. Parham G, Mwanahamuntu M, Pfaendler K, Mkumba G, Sahasrabuddhe V, Hicks M, et al
. Building a cervical cancer prevention program into an HIV care and treatment infrastructure. In: Marlink R, Teitelman S, Brandt A, editors. From the ground up: a guide to building comprehensive HIV/AIDS Care Programs in resource-limited settings. Washington, DC: Elizabeth Glaser Pediatric AIDS Foundation; 2008.
21. Stringer JS, Zulu I, Levy J, Stringer EM, Mwango A, Chi BH, et al
. Rapid scale-up of antiretroviral therapy at primary care sites in Zambia: feasibility and early outcomes. JAMA 2006; 296:782–793.
22. Mullan F, Frehywot S. Nonphysician clinicians in 47 sub-Saharan African countries. Lancet 2007; 370:2158–2163.
23. Bowa K. Zambia's health-worker crisis. Lancet 2008; 371:1577–1578.
24. Samb B, Celletti F, Holloway J, Van Damme W, De Cock KM, Dybul M. Rapid expansion of the health workforce in response to the HIV epidemic. N Engl J Med 2007; 357:2510–2514.
25. Sankaranarayanan R, Basu P, Wesley RS, Mahe C, Keita N, Mbalawa CC, et al
. Accuracy of visual screening for cervical neoplasia: results from an IARC multicentre study in India and Africa. Int J Cancer 2004; 110:907–913.
26. Sankaranarayanan R, Esmy PO, Rajkumar R, Muwonge R, Swaminathan R, Shanthakumari S, et al
. Effect of visual screening on cervical cancer incidence and mortality in Tamil Nadu, India: a cluster-randomised trial. Lancet 2007; 370:398–406.
27. Sankaranarayanan R, Nene BM, Dinshaw KA, Mahe C, Jayant K, Shastri SS, et al
. A cluster randomized controlled trial of visual, cytology and human papillomavirus screening for cancer of the cervix in rural India. Int J Cancer 2005; 116:617–623.
28. Denny L, Kuhn L, De Souza M, Pollack AE, Dupree W, Wright TC Jr. Screen-and-treat approaches for cervical cancer prevention in low-resource settings: a randomized controlled trial. JAMA 2005; 294:2173–2181.
29. Denny L, Kuhn L, Pollack A, Wainwright H, Wright TC Jr. Evaluation of alternative methods of cervical cancer screening for resource-poor settings. Cancer 2000; 89:826–833.
30. Goldie SJ, Gaffikin L, Goldhaber-Fiebert JD, Gordillo-Tobar A, Levin C, Mahe C, Wright TC. Cost-effectiveness of cervical-cancer screening in five developing countries. N Engl J Med 2005; 353:2158–2168.
31. Goldie SJ, Kuhn L, Denny L, Pollack A, Wright TC. Policy analysis of cervical cancer screening strategies in low-resource settings: clinical benefits and cost-effectiveness. JAMA 2001; 285:3107–3115.
32. Sankaranarayanan R, Rajkumar R, Esmy PO, Fayette JM, Shanthakumary S, Frappart L, et al
. Effectiveness, safety and acceptability of ‘see and treat’ with cryotherapy by nurses in a cervical screening study in India. Br J Cancer 2007; 96:738–743.
33. Gaffikin L, Blumenthal PD, Emerson M, Limpaphayom K. Safety, acceptability, and feasibility of a single-visit approach to cervical-cancer prevention in rural Thailand: a demonstration project. Lancet 2003; 361:814–820.