Cost-effectiveness analysis of alternative screening strategies for the detection of cervical cancer among women in rural areas of Western Kenya.

HPV DNA test cervical cancer screening cost‐effectiveness analyses dual staining visual inspection with acetic acid

Journal

International journal of cancer
ISSN: 1097-0215
Titre abrégé: Int J Cancer
Pays: United States
ID NLM: 0042124

Informations de publication

Date de publication:
27 May 2024
Historique:
revised: 21 03 2024
received: 29 10 2023
accepted: 18 04 2024
medline: 27 5 2024
pubmed: 27 5 2024
entrez: 27 5 2024
Statut: aheadofprint

Résumé

While the incidence of cervical cancer has dropped in high-income countries due to organized cytology-based screening programs, it remains the leading cause of cancer death among women in Eastern Africa. Therefore, the World Health Organization (WHO) now urges providers to transition from widely prevalent but low-performance visual inspection with acetic acid (VIA) screening to primary human papillomavirus (HPV) DNA testing. Due to high HPV prevalence, effective triage tests are needed to identify those lesions likely to progress and so avoid over-treatment. To identify the optimal cost-effective strategy, we compared the VIA screen-and-treat approach to primary HPV DNA testing with p16/Ki67 dual-stain cytology or VIA as triage. We used a Markov model to calculate the budget impact of each strategy with incremental quality-adjusted life years and incremental cost-effectiveness ratios (ICER) as the main outcome. Deterministic cost-effectiveness analyses show that the screen-and-treat approach is highly cost-effective (ICER 2469 Int$), while screen, triage, and treat with dual staining is the most effective with favorable ICER than triage with VIA (ICER 9943 Int$ compared with 13,177 Int$). One-way sensitivity analyses show that the results are most sensitive to discounting, VIA performance, and test prices. In the probabilistic sensitivity analyses, the triage option using dual stain is the optimal choice above a willingness to pay threshold of 7115 Int$ being cost-effective as per WHO standards. The result of our analysis favors the use of dual staining over VIA as triage in HPV-positive women and portends future opportunities and necessary research to improve the coverage and acceptability of cervical cancer screening programs.

Identifiants

pubmed: 38801325
doi: 10.1002/ijc.35036
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Bundesministerium für Bildung und Forschung
ID : 01DG13007
Organisme : Ladenburg Foundation New York
Organisme : Fogarty International Centre, National Institutes of Health (NIH), United States
ID : 1K43TW011164
Organisme : Medical Data Scientist Fellowship, Medical Faculty Heidelberg, University of Heidelberg, Germany

Informations de copyright

© 2024 The Authors. International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.

Références

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394‐424. doi:10.3322/caac.21492
Ferlay J, Colombet M, Soerjomataram I, et al. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer. 2019;144(8):1941‐1953. doi:10.1002/ijc.31937
Ferlay J, Ervik M, Lam F, et al. Cervix uteri. The Global Cancer Observatory. Cancer Today. 2018 https://gco.iarc.fr/today/data/factsheets/cancers/23-Cervix-uteri-fact-sheet.pdf
Schiller JT, Castellsague X, Garland SM. A review of clinical trials of human papillomavirus prophylactic vaccines. Vaccine. 2012;30:F123‐F138. doi:10.1016/j.vaccine.2012.04.108
Bouvard V, Wentzensen N, Mackie A, et al. The IARC perspective on cervical cancer screening. N Engl J Med. 2021;385(20):1908‐1918. doi:10.1056/NEJMsr2030640
Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S. Human papillomavirus and cervical cancer. Lancet. 2007;370(9590):890‐907. doi:10.1016/s0140‐6736(07)61416‐0
Schiffman M, Wentzensen N. Human papillomavirus infection and the multistage carcinogenesis of cervical cancer. Cancer Epidemiol Biomarkers Prev. 2013;22(4):553‐560. doi:10.1158/1055‐9965.EPI‐12‐1406
WHO. Global Strategy to Accelerate the Elimination of Cervical Cancer as a Public Health Problem. WHO; 2020.
Yang DX, Soulos PR, Davis B, Gross CP, Yu JB. Impact of widespread cervical cancer screening: number of cancers prevented and changes in race‐specific incidence. Am J Clin Oncol. 2018;41(3):289‐294. doi:10.1097/COC.0000000000000264
Nygard M. Screening for cervical cancer: when theory meets reality. BMC Cancer. 2011;11:240. doi:10.1186/1471‐2407‐11‐240
Dijkstra MG, van Zummeren M, Rozendaal L, et al. Safety of extending screening intervals beyond five years in cervical screening programmes with testing for high risk human papillomavirus: 14 year follow‐up of population based randomised cohort in the Netherlands. BMJ. 2016;355:i4924. doi:10.1136/bmj.i4924
Qiao YL, Jeronimo J, Zhao FH, et al. Lower cost strategies for triage of human papillomavirus DNA‐positive women. Int J Cancer. 2014;134(12):2891‐2901. doi:10.1002/ijc.28616
Ajenifuja KO, Gage JC, Adepiti AC, et al. A population‐based study of visual inspection with acetic acid (VIA) for cervical screening in rural Nigeria. Int J Gynecol Cancer. 2013;23(3):507‐512. doi:10.1097/IGC.0b013e318280f395
Bigoni J, Gundar M, Tebeu PM, et al. Cervical cancer screening in sub‐Saharan Africa: a randomized trial of VIA versus cytology for triage of HPV‐positive women. Int J Cancer. 2015;137(1):127‐134. doi:10.1002/ijc.29353
Mustafa RA, Santesso N, Khatib R, et al. Systematic reviews and meta‐analyses of the accuracy of HPV tests, visual inspection with acetic acid, cytology, and colposcopy. Int J Gynaecol Obstet. 2016;132(3):259‐265. doi:10.1016/j.ijgo.2015.07.024
Fokom Domgue J, Valea FA. Is it relevant to keep advocating visual inspection of the cervix with acetic acid for primary cervical cancer screening in limited‐resource settings? J Glob Oncol. 2018;4:1‐5. doi:10.1200/JGO.17.00048
Silkensen S, Schiffman M, Sahasrabuddhe V, Flanigan J. Is it time to move beyond visual inspection with acetic acid for cervical cancer screening? Glob Health Sci Pract. 2018;6(2):242‐246.
WHO. WHO Guideline for Screening and Treatment of Cervical Pre‐Cancer Lesions for Cervical Cancer Prevention. 2nd ed. WHO; 2021.
Bulkmans NW, Berkhof J, Bulk S, et al. High‐risk HPV type‐specific clearance rates in cervical screening. Br J Cancer. 2007;96(9):1419‐1424. doi:10.1038/sj.bjc.6603653
Basu P, Meheus F, Chami Y, Hariprasad R, Zhao F, Sankaranarayanan R. Management algorithms for cervical cancer screening and precancer treatment for resource‐limited settings. Int J Gynaecol Obstet. 2017;138:26‐32. doi:10.1002/ijgo.12183
Huchko MJ, Olwanda E, Choi Y, Kahn JG. HPV‐based cervical cancer screening in low‐resource settings: maximizing the efficiency of community‐based strategies in rural Kenya. Int J Gynaecol Obstet. 2020;148(3):386‐391. doi:10.1002/ijgo.13090
Chauhan AS, Prinja S, Srinivasan R, et al. Cost effectiveness of strategies for cervical cancer prevention in India. PLoS One. 2020;15(9):e0238291. doi:10.1371/journal.pone.0238291
Shen J, Olwanda E, Kahn JG, Huchko MJ. Cost of HPV screening at community health campaigns (CHCs) and health clinics in rural Kenya. BMC Health Serv Res. 2018;18:378. doi:10.1186/s12913‐018‐3195‐6
Zimmermann MR, Vodicka E, Babigumira JB, et al. Cost‐effectiveness of cervical cancer screening and preventative cryotherapy at an HIV treatment clinic in Kenya. Cost Eff Resour Alloc. 2017;15:13. doi:10.1186/s12962‐017‐0075‐6
Tin KN, Ngamjarus C, Rattanakanokchai S, et al. Interventions to increase the uptake of cervical cancer screening in low‐ and middle‐income countries: a systematic review and meta‐analysis. BMC Womens Health. 2023;23:120. doi:10.1186/s12905‐023‐02265‐8
Kamath Mulki A, Withers M. Human papilloma virus self‐sampling performance in low‐ and middle‐income countries. BMC Womens Health. 2021;21(1):12. doi:10.1186/s12905‐020‐01158‐4
Nishimura H, Yeh PT, Oguntade H, Kennedy CE, Narasimhan M. HPV self‐sampling for cervical cancer screening: a systematic review of values and preferences. BMJ Glob Health. 2021;6(5):e003743. doi:10.1136/bmjgh‐2020‐003743
Herrick T, Thomson KA, Shin M, Gannon S, Tsu V, de Sanjose S. Acting on the call for cervical cancer elimination: planning tools for low‐and middle‐income countries to increase the coverage and effectiveness of screening and treatment. BMC Health Serv Res. 2022;22:1246. doi:10.1186/s12913‐022‐08423‐2
Luckett R, Mogowa N, Li HJ, et al. Performance of two‐stage cervical cancer screening with primary high‐risk human papillomavirus testing in women living with human immunodeficiency virus. Obstet Gynecol. 2019;134(4):840‐849. doi:10.1097/AOG.0000000000003496
Simms KT, Keane A, Nguyen DTN, et al. Benefits, harms and cost‐effectiveness of cervical screening, triage and treatment strategies for women in the general population. Nat Med. 2023;29(12):3050‐3058. doi:10.1038/s41591‐023‐02600‐4
Taghavi K, Rohner E, Basu P, Low N, Rutjes A, Bohlius J. Screening test accuracy of portable devices that can be used to perform colposcopy for detecting CIN2+ in low‐ and middle‐income countries: a systematic review and meta‐analysis. BMC Womens Health. 2020;20(1):253. doi:10.1186/s12905‐020‐01121‐3
Desai KT, Befano B, Xue Z, et al. The development of “automated visual evaluation” for cervical cancer screening: the promise and challenges in adapting deep‐learning for clinical testing: interdisciplinary principles of automated visual evaluation in cervical screening. Int J Cancer. 2022;150(5):741‐752. doi:10.1002/ijc.33879
Wright TC Jr, Stoler MH, Ranger‐Moore J, et al. Clinical validation of p16/Ki‐67 dual‐stained cytology triage of HPV‐positive women: results from the IMPACT trial. Int J Cancer. 2022;150(3):461‐471. doi:10.1002/ijc.33812
Petry KU, Schmidt D, Scherbring S, et al. Triaging pap cytology negative, HPV positive cervical cancer screening results with p16/Ki‐67 dual‐stained cytology. Gynecol Oncol. 2011;121(3):505‐509. doi:10.1016/j.ygyno.2011.02.033
Wentzensen N, Clarke MA, Bremer R, et al. Clinical evaluation of human papillomavirus screening with p16/Ki‐67 dual stain triage in a large organized cervical cancer screening program. JAMA Intern Med. 2019;179(7):881‐888. doi:10.1001/jamainternmed.2019.0306
Campos NG, Tsu V, Jeronimo J, Mvundura M, Kim JJ. Evidence‐based policy choices for efficient and equitable cervical cancer screening programs in low‐resource settings. Cancer Med. 2017;6(8):2008‐2014. doi:10.1002/cam4.1123
Campos NG, Jeronimo J, Tsu V, Castle PE, Mvundura M, Kim JJ. The cost‐effectiveness of visual triage of human papillomavirus‐positive women in three low‐ and middle‐income countries. Cancer Epidemiol Biomarkers Prev. 2017;26(10):1500‐1510. doi:10.1158/1055‐9965.EPI‐16‐0787
Tantitamit T, Khemapech N, Havanond P, Termrungruanglert W. Cost‐effectiveness of primary HPV screening strategies and triage with cytology or dual stain for cervical cancer. Cancer Control. 2020;27(1):1073274820922540. doi:10.1177/1073274820922540
Mwenda V, Mburu W, Bor JP, et al. Cervical cancer programme, Kenya, 2011–2020: lessons to guide elimination as a public health problem. Ecancermedicalscience. 2022;16:1442. doi:10.3332/ecancer.2022.1442
Kenya National Bureau of Statistics. 2019 Kenya Population and Housing Census: Volume II. 2019 http://www.knbs.or.ke
The World Bank. Rural Polupation‐Kenya. https://data.worldbank.org/indicator/SP.RUR.TOTL.ZS?locations=KE
Orang'o EO, Were E, Rode O, et al. Novel concepts in cervical cancer screening: a comparison of VIA, HPV DNA test and p16INK4a/Ki‐67 dual stain cytology in Western Kenya. Infect Agent Cancer. 2020;15:57. doi:10.1186/s13027‐020‐00323‐6
Edejer TT‐A, Baltussen R, Adam T, et al. WHO Guide to Cost‐Effectiveness Analysis. World Health Organization; 2003.
Canfell K, Barnabas R, Patnick J, Beral V. The predicted effect of changes in cervical screening practice in the UK: results from a modelling study. Br J Cancer. 2004;91(3):530‐536. doi:10.1038/sj.bjc.6602002
WHO. Adult Mortality. Data by Country Global Health Observatory Data Repository. Accessed March 30, 2023. http://apps.who.int/gho/data/view.main.1360?lang=en
Moscicki AB, Shiboski S, Broering J, et al. The natural history of human papillomavirus infection as measured by repeated DNA testing in adolescent and young women. J Pediatr. 1998;132(2):277‐284. doi:10.1016/s0022‐3476(98)70445‐7
Praditsitthikorn N, Teerawattananon Y, Tantivess S, et al. Economic evaluation of policy options for prevention and control of cervical cancer in Thailand. Pharmacoeconomics. 2011;29(9):781‐806. doi:10.2165/11586560‐000000000‐00000
Bhatla N, Aoki D, Sharma DN, Sankaranarayanan R. Cancer of the cervix uteri: 2021 update. Int J Gynaecol Obstet. 2021;155:28‐44. doi:10.1002/ijgo.13865
Jansen EEL, Zielonke N, Gini A, et al. Effect of organised cervical cancer screening on cervical cancer mortality in Europe: a systematic review. Eur J Cancer. 2020;127:207‐223. doi:10.1016/j.ejca.2019.12.013
Mezei AK, Armstrong HL, Pedersen HN, et al. Cost‐effectiveness of cervical cancer screening methods in low‐ and middle‐income countries: a systematic review. Int J Cancer. 2017;141(3):437‐446. doi:10.1002/ijc.30695
Woods B, Revill P, Sculpher M, Claxton K. Country‐level cost‐effectiveness thresholds: initial estimates and the need for further research. Value Health. 2016;19(8):929‐935. doi:10.1016/j.jval.2016.02.017
Elizabeth Glaser Pediatric AIDS Foundation. Ensuring Access to Molecular Testing for Human Papillomavirus (HPV): A Core Component of the Effort to Eliminate Cervical Cancer. Policy Brief. 2023.
Nandini NM, Nandish SM, Pallavi P, et al. Manual liquid based cytology in primary screening for cervical cancer—a cost effective preposition for scarce resource settings. Asian Pac J Cancer Prev. 2012;13(8):3645‐3651. doi:10.7314/apjcp.2012.13.8.3645
Mansfield C, Tangka FK, Ekwueme DU, et al. Stated preference for cancer screening: a systematic review of the literature, 1990–2013. Prev Chronic Dis. 2016;13:E27. doi:10.5888/pcd13.150433
Myers E, McCrory DC, Subramanian S, et al. Setting the target for a better cervical screening test: characteristics of a cost‐effective test for cervical neoplasia screening. Obstet Gynecol. 2000;96:645‐652. doi:10.1016/s0029‐7844(00)00979‐0
Yamada R, Sasagawa T, Kirumbi LW, et al. Human papillomavirus infection and cervical abnormalities in Nairobi, Kenya, an area with a high prevalence of human immunodeficiency virus infection. J Med Virol. 2008;80(5):847‐855. doi:10.1002/jmv.21170

Auteurs

Christopher Lobin (C)

Applied Tumor Biology, Institute of Pathology, Heidelberg University Hospital, Heidelberg, Germany.

Elkanah Omenge Orang'o (EO)

Department of Reproductive Health, School of Medicine, College of Health Sciences, Moi University, Eldoret, Kenya.
Department of Obstetrics and Gynaecology, Aga Khan University, Nairobi, Kenya.

Edwin Were (E)

Department of Reproductive Health, School of Medicine, College of Health Sciences, Moi University, Eldoret, Kenya.

Kapten Muthoka (K)

Department of Reproductive Health, School of Medicine, College of Health Sciences, Moi University, Eldoret, Kenya.

Kavita Singh (K)

Heidelberg Institute of Global Health, Heidelberg University Hospital, Heidelberg, Germany.
Public Health Foundation of India, New Delhi, India.

Manuela De Allegri (M)

Heidelberg Institute of Global Health, Heidelberg University Hospital, Heidelberg, Germany.

Konrad Obermann (K)

CPD Center for Preventive Medicine and Digital Health, Ruprecht-Karls University Heidelberg, Germany.

Magnus von Knebel Doeberitz (M)

Applied Tumor Biology, Institute of Pathology, Heidelberg University Hospital, Heidelberg, Germany.

Hermann Bussmann (H)

Applied Tumor Biology, Institute of Pathology, Heidelberg University Hospital, Heidelberg, Germany.

Classifications MeSH