When and how often to screen for cervical cancer in three low- and middle-income countries: A cost-effectiveness analysis

Papillomavirus Research

Volumn 1, Issue , 2015, Pages 38-58

  Campos, Nicole G ^a   Tsu, Vivien ^b   Jeronimo, Jose ^b   Mvundura, Mercy ^b   Lee, Kyueun ^a   Kim, Jane J ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b PATH   (United States)

Author keywords

Cancer screening; Cervical cancer; Cost effectiveness analysis; Human papillomavirus (HPV); Visual inspection with acetic acid

Indexed keywords

ADULT; AGE DISTRIBUTION; ARTICLE; BUDGET; CANCER RISK; CANCER SCREENING; CERVICAL SAMPLING; COLPOSCOPY; CONTROLLED STUDY; COST EFFECTIVENESS ANALYSIS; CRYOTHERAPY; ELECTROSURGERY; FEMALE; GYNECOLOGICAL EXAMINATION; HEALTH CARE COST; HUMAN; INCOME; INDIA; INTERMETHOD COMPARISON; LOOP ELECTROSURGICAL EXCISION PROCEDURE; MAJOR CLINICAL STUDY; MATHEMATICAL MODEL; NICARAGUA; PRIORITY JOURNAL; RISK REDUCTION; UGANDA; UTERINE CERVIX BIOPSY; UTERINE CERVIX CANCER; UTERINE CERVIX CYTOLOGY; VAGINAL SAMPLING; VISUAL INSPECTION WITH ACETIC ACID; WART VIRUS;

EID: 84947913845     PISSN: None     EISSN: 24058521     Source Type: Journal    
DOI: 10.1016/j.pvr.2015.05.003     Document Type: Article

References (62)

1. Ferlay J., Soerjomataram I., Ervik M., et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet] 2013, International Agency for Research on Cancer, Lyon, France.
2. Denny L. Control of cancer of the cervix in low- and middle-income countries. Ann. Surg. Oncol. 2015, 22(3):728-733.
3. Sankaranarayanan R., Nene B.M., Shastri S.S., et al. HPV screening for cervical cancer in rural India. N. Engl. J. Med. 2009, 360(14):1385-1394.
4. Shastri S.S., Mittra I., Mishra G.A., et al. Effect of VIA screening by primary health workers: randomized controlled study in Mumbai, India. J. Natl. Cancer Inst. 2014, 106(3). dju009.
5. Goldie S.J., Gaffikin L., Goldhaber-Fiebert J.D., et al. Cost-effectiveness of cervical-cancer screening in five developing countries. N. Engl. J. Med. 2005, 353(20):2158-2168.
6. Diaz M., Kim J.J., Albero G., et al. Health and economic impact of HPV 16 and 18 vaccination and cervical cancer screening in India. Br. J. Cancer 2008, 99(2):230-238.
7. Jeronimo J., Bansil P., Lim J., et al. A multicountry evaluation of careHPV testing, visual inspection with acetic acid, and papanicolaou testing for the detection of cervical cancer. Int. J. Gynecol. Cancer 2014, 24(3):576-585.
8. Qiao Y.L., Sellors J.W., Eder P.S., 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):929-936.
9. Zhao F.H., Lin M.J., Chen F., et al. Performance of high-risk human papillomavirus DNA testing as a primary screen for cervical cancer: a pooled analysis of individual patient data from 17 population-based studies from China. Lancet Oncol. 2010, 11(12):1160-1171.
10. N.G. Campos M. Maza, K. Alfaro, J. Gage, P.E. Castle, J.C. Felix, M. Cremer, J.J. Kim. The comparative and cost-effectiveness of HPV-based cervical cancer screening algorithms in El Salvador. Int. J. Cancer 137 (2015) 893-902.
11. World Health Organization, WHO Guidelines for Screening and Treatment of Precancerous Lesions for Cervical Cancer Prevention, World Health Organization, Geneva, 2013.
12. World Heath Organization Comprehensive Cervical Cancer Control: A Guide to Essential Practice 2014, World Health Organization, Geneva. second ed.
13. Campos N.G., Burger E.A., Sy S., et al. An updated natural history model of cervical cancer: derivation of model parameters. Am. J. Epidemiol. 2014, 180(5):545-555.
14. Kim J.J., Kuntz K.M., Stout N.K., et al. Multiparameter calibration of a natural history model of cervical cancer. Am. J. Epidemiol. 2007, 166(2):137-150.
15. Campos N.G., Kim J.J., Castle P.E., et al. Health and economic impact of HPV 16/18 vaccination and cervical cancer screening in Eastern Africa. Int. J. Cancer 2012, 130(11):2672-2684.
16. Goldie S.J., Kim J.J., Kobus K., et al. Cost-effectiveness of HPV 16, 18 vaccination in Brazil. Vaccine 2007, 25(33):6257-6270.
17. Mvundura M., Tsu V. Estimating the costs of cervical cancer screening in high-burden Sub-Saharan African countries. Int. J. Gynaecol. Obstet. 2014, 126(2):151-155.
18. World Health Organization Macroeconomics and Health: Investing in Health for Economic Development: Report of the Commission on Macroeconomics and Health 2001, World Health Organization, Geneva.
19. Making Choices in Health: WHO Guide to Cost-Effectiveness Analysis 2003, World Health Organization, Geneva. T. Tan-Torres Edejer, R. Baltussen, T. Adam, R. Hutubessy, A. Acharya, D.B. Evans, C.J.L. Murray (Eds.).
20. Disease Control Priorities in Developing Countries 2006, Oxford University Press and The World Bank, Washington, DC. second ed. D.T. Jamison, J.G. Breman, A.R. Measham, G. Alleyne, M. Claeson, D.B. Evans, P. Jha, A. Mills, P. Musgrove (Eds.).
21. M.R. Gold, J.E. Siegel, L.B. Russell, M.C. Weinstein, eds. Cost-effectiveness in Health and Medicine, Oxford University Press, New York, NY, 1996.
22. Munoz N., Mendez F., Posso H., et al. Incidence, duration, and determinants of cervical human papillomavirus infection in a cohort of Colombian women with normal cytological results. J. Infect. Dis. 2004, 190(12):2077-2087.
23. Herrero R., Hildesheim A., Rodriguez A.C., et al. Rationale and design of a community-based double-blind randomized clinical trial of an HPV 16 and 18 vaccine in Guanacaste, Costa Rica. Vaccine 2008, 26(37):4795-4808.
24. McCredie M.R., Sharples K.J., Paul C., et al. Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: a retrospective cohort study. Lancet Oncol. 2008, 9(5):425-434.
25. Surveillance, Epidemiology, and End Results (SEER) Program. SEERStat Database: Incidence - SEER 18 Regs Research Data+Hurricane Katrina Impacted Louisiana Cases Nov 2011 Sub (1973-2009 varying) - Linked to County Attributes - Total U.S., 1969-2010 Counties.
26. Sankaranarayanan R., Swaminathan R., Brenner H., et al. Cancer survival in Africa, Asia, and Central America: a population-based study. Lancet Oncol. 2010, 11(2):165-173.
27. Goldhaber-Fiebert J.D., Stout N.K., Ortendahl J., et al. Modeling human papillomavirus and cervical cancer in the United States for analyses of screening and vaccination. Popul. Health Metr. 2007, 5:11.
28. Stinnett A.A., Paltiel A.D. Estimating CE ratios under second-order uncertainty: the mean ratio versus the ratio of means. Med. Decis. Making 1997, 17(4):483-489.
29. Blumenthal P.D., Gaffikin L., Deganus S., et al. Cervical cancer prevention: safety, acceptability, and feasibility of a single-visit approach in Accra, Ghana. Am. J. Obstet. Gynecol. 2007, 196(4):e408-409. 407 e401-408; discussion 407.
30. Castle P.E., Qiao Y.L., Zhao F.H., et al. Clinical determinants of a positive visual inspection after treatment with acetic acid for cervical cancer screening. BJOG 2014, 121(6):739-746.
31. Cremer M., Conlisk E., Maza M., et al. Adequacy of visual inspection with acetic acid in women of advancing age. Int. J. Gynaecol. Obstet. 2011, 113(1):68-71.
32. Li N., Shi J.F., Franceschi S., et al. Different cervical cancer screening approaches in a Chinese multicentre study. Br. J. Cancer 2009, 100(3):532-537.
33. Cremer M., Bullard K., Maza M., et al. Cytology versus visual inspection with acetic acid among women treated previously with cryotherapy in a low-resource setting. Int. J. Gynaecol. Obstet. 2010, 111(3):249-252.
34. Chirenje Z.M., Rusakaniko S., Kirumbi L., et al. Situation analysis for cervical cancer diagnosis and treatment in east, central and southern African countries. Bull. World Health Organ. 2001, 79(2):127-132.
35. Sauvaget C., Muwonge R., Sankaranarayanan R. Meta-analysis of the effectiveness of cryotherapy in the treatment of cervical intraepithelial neoplasia. Int. J. Gynaecol. Obstet. 2013, 120(3):218-223.
36. United Nations Development Programme. International Human Development Indicators. Available from: [September 14, 2014]. http://hdr.undp.org/en/data.
37. World Health Organization WHO Guidance Note: Comprehensive Cervical Cancer Prevention and Control: A Healthier Future for Girls and Women 2013, World Health Organization, Geneva.
38. World Health Organization Statistical Information System: CHOICE (CHOosing Interventions that are Cost Effective). Available from: [October 17, 2007]. http://www.who.int/choice/en/.
39. Marseille E., Larson B., Kazi D.S., et al. Thresholds for the cost-effectiveness of interventions: alternative approaches. Bull. World Health Organ. 2015, 93(2):118-124.
40. Human papillomavirus vaccines: WHO position paper, October 2014. Wkly. Epidemiol. Rec. 2014;89(43):465-491.
41. FDA approves Gardasil 9 for Prevention of Certain Cancers Caused by Five Additional Types of HPV. FDA News Release December 11, 2014; Available from: [February 4, 2015]. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm426485.htm.
42. Skinner S.R., Szarewski A., Romanowski B., et al. Efficacy, safety, and immunogenicity of the human papillomavirus 16/18 AS04-adjuvanted vaccine in women older than 25 years: 4-year interim follow-up of the phase 3, double-blind, randomised controlled VIVIANE study. Lancet 2014, 384(9961):2213-2227.
43. Castellsague X., Munoz N., Pitisuttithum P., et al. End-of-study safety, immunogenicity, and efficacy of quadrivalent HPV (types 6, 11, 16, 18) recombinant vaccine in adult women 24-45 years of age. Br. J. Cancer 2011, 105(1):28-37.
44. Arrossi S., Thouyaret L., Herrero R., et al. Effect of self-collection of HPV DNA offered by community health workers at home visits on uptake of screening for cervical cancer (the EMA study): a population-based cluster-randomised trial. Lancet Global Health 2015, 3(2):e85-94.
45. Racey C.S., Withrow D.R., Gesink D. Self-collected HPV testing improves participation in cervical cancer screening: a systematic review and meta-analysis. Can. J. Public Health 2013, 104(2):e159-166.
46. United States Census Bureau. International Data Base. 2013; Available from: [April 14, 2015]. http://www.census.gov/population/international/data/idb/informationGateway.php.
47. Campos N.G., Burger E.A., Sy S., Sharma M., Schiffman M., Rodriguez A.C., et al. An updated natural history model of cervical cancer: derivation of model parameters. Am. J. Epidemiol. 2014, 180:545-555.
48. Munoz N., Mendez F., Posso H., Molano M., van den Brule A.J., Ronderos M., et al. Incidence, duration, and determinants of cervical human papillomavirus infection in a cohort of Colombian women with normal cytological results. J. Infect. Dis. 2004, 190:2077-2087.
49. Herrero R., Hildesheim A., Rodriguez A.C., Wacholder S., Bratti C., Solomon D., et al. Rationale and design of a community-based double-blind randomized clinical trial of an HPV 16 and 18 vaccine in Guanacaste, Costa Rica. Vaccine 2008, 26:4795-4808.
50. McCredie M.R., Sharples K.J., Paul C., Baranyai J., Medley G., Jones R.W., et al. Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: a retrospective cohort study. Lancet Oncol. 2008, 9:425-434.
51. Meyskens F.L., Surwit E., Moon T.E., Childers J.M., Davis J.R., Dorr R.T., et al. Enhancement of regression of cervical intraepithelial neoplasia II (moderate dysplasia) with topically applied all-trans-retinoic acid: a randomized trial. J. Natl. Cancer Inst. 1994, 86:539-543.
52. Keefe K.A., Schell M.J., Brewer C., McHale M., Brewster W., Chapman J.A., et al. A randomized, double blind, Phase III trial using oral beta-carotene supplementation for women with high-grade cervical intraepithelial neoplasia. Cancer Epidemiol. Biomarkers Prev. 2001, 10:1029-1035.
53. Castle P.E., Schiffman M., Wheeler C.M., Solomon D. Evidence for frequent regression of cervical intraepithelial neoplasia-grade 2. Obstet. Gynecol. 2009, 113:18-25.
54. Wang S.M., Colombara D., Shi J.F., Zhao F.H., Li J., Chen F., et al. Six-year regression and progression of cervical lesions of different human papillomavirus viral loads in varied histological diagnoses. Int. J. Gynecol. Cancer 2013, 23:716-723.
55. Moscicki A.B., Ma Y., Wibbelsman C., Darragh T.M., Powers A., Farhat S., et al. Rate of and risks for regression of cervical intraepithelial neoplasia 2 in adolescents and young women. Obstet. Gynecol. 2010, 116:1373-1380.
56. Cancer Incidence in Five Continents 2013, vol. X. International Agency for Research on Cancer, Lyon, France.
57. Ferlay J., Soerjomataram I., Ervik M., Dikshit R., Eser S., Mathers C., et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet] 2013, International Agency for Research on Cancer, Lyon, France.
58. World Bank. (2013) World Development Indicators. Available from: http://data.worldbank.org/data-catalog/world-development-indicators [July 24, 2014].
59. Goldie S.J., Gaffikin L., Goldhaber-Fiebert J.D., Gordillo-Tobar A., Levin C., Mahe C., et al. Cost-effectiveness of cervical-cancer screening in five developing countries. N. Engl. J. Med. 2005, 353:2158-2168.
60. Campos N.G., Kim J.J., Castle P.E., Ortendahl J.D., O'Shea M., Diaz M., et al. Health and economic impact of HPV 16/18 vaccination and cervical cancer screening in Eastern Africa. Int. J. Cancer 2012, 130:2672-2684.
61. Campos N.G., Maza M., Alfaro K., Gage J.C., Castle P.E., Felix J.C., et al. The comparative and cost-effectiveness of HPV-based cervical cancer screening algorithms in El Salvador. Int. J. Cancer 2015.
62. Goldhaber-Fiebert J.D., Denny L.E., De Souza M., Wright T.C., Kuhn L., Goldie S.J. The costs of reducing loss to follow-up in South African cervical cancer screening. Cost Eff. Resour. Alloc. 2005, 3:11.