The projected impact of geographic targeting of oral cholera vaccination in sub-Saharan Africa: A modeling study

English version

Autoři: Elizabeth C. Lee ^aff001; Andrew S. Azman ^aff001; Joshua Kaminsky ^aff001; Sean M. Moore ^aff002; Heather S. McKay ^aff001; Justin Lessler ^aff001
Působiště autorů: Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America ^aff001; Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana, United States of America ^aff002; Eck Institute for Global Health, University of Notre Dame, Notre Dame, Indiana, United States of America ^aff003
Vyšlo v časopise: The projected impact of geographic targeting of oral cholera vaccination in sub-Saharan Africa: A modeling study. PLoS Med 16(12): e32767. doi:10.1371/journal.pmed.1003003
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pmed.1003003

Souhrn

Background

Cholera causes an estimated 100,000 deaths annually worldwide, with the majority of burden reported in sub-Saharan Africa. In May 2018, the World Health Assembly committed to reducing worldwide cholera deaths by 90% by 2030. Oral cholera vaccine (OCV) plays a key role in reducing the near-term risk of cholera, although global supplies are limited. Characterizing the potential impact and cost-effectiveness of mass OCV deployment strategies is critical for setting expectations and developing cholera control plans that maximize the chances of success.

Methods and findings

We compared the projected impacts of vaccination campaigns across sub-Saharan Africa from 2018 through 2030 when targeting geographically according to historical cholera burden and risk factors. We assessed the number of averted cases, deaths, and disability-adjusted life years and the cost-effectiveness of these campaigns with models that accounted for direct and indirect vaccine effects and population projections over time. Under current vaccine supply projections, an approach optimized to targeting by historical burden is projected to avert 828,971 (95% CI 803,370–859,980) cases (equivalent to 34.0% of projected cases; 95% CI 33.2%–34.8%). An approach that balances logistical feasibility with targeting historical burden is projected to avert 617,424 (95% CI 599,150–643,891) cases. In contrast, approaches optimized for targeting locations with limited access to water and sanitation are projected to avert 273,939 (95% CI 270,319–277,002) and 109,817 (95% CI 103,735–114,110) cases, respectively. We find that the most logistically feasible targeting strategy costs US$1,843 (95% CI 1,328–14,312) per DALY averted during this period and that effective geographic targeting of OCV campaigns can have a greater impact on cost-effectiveness than improvements to vaccine efficacy and moderate increases in coverage. Although our modeling approach does not project annual changes in baseline cholera risk or directly incorporate immunity from natural cholera infection, our estimates of the relative performance of different vaccination strategies should be robust to these factors.

Conclusions

Our study suggests that geographic targeting substantially improves the cost-effectiveness and impact of oral cholera vaccination campaigns. Districts with the poorest access to improved water and sanitation are not the same as districts with the greatest historical cholera incidence. While OCV campaigns can improve cholera control in the near term, without rapid progress in developing water and sanitation services or dramatic increases in OCV supply, our results suggest that vaccine use alone is unlikely to allow us to achieve the 2030 goal.

Klíčová slova:

Africa – Public and occupational health – Vaccines – Cost-effectiveness analysis – Sanitation – Global health – Cholera – Cholera vaccines

Zdroje

1. Rebaudet S, Sudre B, Faucher B, Piarroux R. Environmental determinants of cholera outbreaks in inland Africa: a systematic review of main transmission foci and propagation routes. J Infect Dis. 2013;208(Suppl 1):S46–54.

2. Griffith DC, Kelly-Hope LA, Miller MA. Review of reported cholera outbreaks worldwide, 1995–2005. Am J Trop Med Hyg. 2006;75(5):973–7. 17123999

3. Moore SM, Azman AS, Zaitchik BF, Mintz ED, Brunkard J, Legros D, et al. El Niño and the shifting geography of cholera in Africa. Proc Natl Acad Sci U S A. 2017;114(17):4436–41. doi: 10.1073/pnas.1617218114 28396423

4. World Health Assembly. Cholera prevention and control. WHA71.4. Geneva: World Health Assembly; 2018 May [cited 2018 Oct 15]. http://apps.who.int/gb/ebwha/pdf_files/WHA71/A71_R4-en.pdf.

5. Deployments from the oral cholera vaccine stockpile, 2013–2017. Wkly Epidemiol Rec. 2017;92(32):437–42. 28799734

6. Global Task Force on Cholera Control. Ending cholera—a global roadmap to 2030. Geneva: World Health Organization; 2017 [cited 2019 Nov 22]. https://www.who.int/cholera/publications/global-roadmap/en/.

7. M’bangombe M, Pezzoli L, Reeder B, Kabuluzi S, Msyamboza K, Masuku H, et al. Oral cholera vaccine in cholera prevention and control, Malawi. Bull World Health Organ. 2018;96:428–35. doi: 10.2471/BLT.17.207175 29904226

8. Bi Q, Ferreras E, Pezzoli L, Legros D, Ivers LC, Date K, et al. Protection against cholera from killed whole-cell oral cholera vaccines: a systematic review and meta-analysis. Lancet Infect Dis. 2017;17(10):1080–8. doi: 10.1016/S1473-3099(17)30359-6 28729167

9. Sur D, Lopez AL, Kanungo S, Paisley A, Manna B, Ali M, et al. Efficacy and safety of a modified killed-whole-cell oral cholera vaccine in India: an interim analysis of a cluster-randomised, double-blind, placebo-controlled trial. Lancet. 2009;374(9702):1694–702. doi: 10.1016/S0140-6736(09)61297-6 19819004

10. Khan AI, Ali M, Chowdhury F, Saha A, Khan IA, Khan A, et al. Safety of the oral cholera vaccine in pregnancy: retrospective findings from a subgroup following mass vaccination campaign in Dhaka, Bangladesh. Vaccine. 2017;35(11):1538–43. doi: 10.1016/j.vaccine.2017.01.080 28196715

11. Lessler J, Moore SM, Luquero FJ, McKay HS, Grais R, Henkens M, et al. Mapping the burden of cholera in sub-Saharan Africa and implications for control: an analysis of data across geographical scales. Lancet. 2018;391(10133):1908–15. doi: 10.1016/S0140-6736(17)33050-7 29502905

12. Bi Q, Azman AS, Satter SM, Khan AI, Ahmed D, Riaj AA, et al. Micro-scale spatial clustering of cholera risk factors in urban Bangladesh. PLoS Negl Trop Dis. 2016;10(2):e0004400. doi: 10.1371/journal.pntd.0004400 26866926

13. Kim J-H, Mogasale V, Burgess C, Wierzba TF. Impact of oral cholera vaccines in cholera-endemic countries: a mathematical modeling study. Vaccine. 2016;34(18):2113–20. doi: 10.1016/j.vaccine.2016.03.004 26993337

14. Pullan RL, Freeman MC, Gething PW, Brooker SJ. Geographical inequalities in use of improved drinking water supply and sanitation across sub-Saharan Africa: mapping and spatial analysis of cross-sectional survey data. PLoS Med. 2014;11(4):e1001626. doi: 10.1371/journal.pmed.1001626 24714528

15. World Health Organization, UNICEF. Progress on sanitation and drinking-water—2013 update. Geneva: World Health Organization; 2013.

16. Tatem AJ. WorldPop, open data for spatial demography. Sci Data. 2017;4:170004. doi: 10.1038/sdata.2017.4 28140397

17. Linard C, Gilbert M, Snow RW, Noor AM, Tatem AJ. Population distribution, settlement patterns and accessibility across Africa in 2010. PLoS ONE. 2012;7(2):e31743. doi: 10.1371/journal.pone.0031743 22363717

18. Lam E, Al-Tamimi W, Russell SP, Butt MO, Blanton C, Musani AS, et al. Oral cholera vaccine coverage during an outbreak and humanitarian crisis, Iraq, 2015. Emerg Infect Dis. 2017;23(1):38–45. doi: 10.3201/eid2301.160881 27983502

19. Tohme RA, François J, Wannemuehler K, Iyengar P, Dismer A, Adrien P, et al. Oral cholera vaccine coverage, barriers to vaccination, and adverse events following vaccination, Haiti, 2013. Emerg Infect Dis. 2015;21(6):984–91. doi: 10.3201/eid2106.141797 25988350

20. Luquero FJ, Grout L, Ciglenecki I, Sakoba K, Traore B, Heile M, et al. First outbreak response using an oral cholera vaccine in Africa: vaccine coverage, acceptability and surveillance of adverse events, Guinea, 2012. PLoS Negl Trop Dis. 2013;7(10):e2465. doi: 10.1371/journal.pntd.0002465 24147164

21. Uddin MJ, Wahed T, Saha NC, Kaukab SST, Khan IA, Khan AI, et al. Coverage and acceptability of cholera vaccine among high-risk population of urban Dhaka, Bangladesh. Vaccine. 2014;32(43):5690–5. doi: 10.1016/j.vaccine.2014.08.021 25149429

22. Abubakar A, Azman AS, Rumunu J, Ciglenecki I, Helderman T, West H, et al. the first use of the global oral cholera vaccine emergency stockpile: lessons from South Sudan. PLoS Med. 2015;12(11):e1001901. doi: 10.1371/journal.pmed.1001901 26576044

23. Massing LA, Aboubakar S, Blake A, Page A-L, Cohuet S, Ngandwe A, et al. Highly targeted cholera vaccination campaigns in urban setting are feasible: the experience in Kalemie, Democratic Republic of Congo. PLoS Negl Trop Dis. 2018;12(5):e0006369. doi: 10.1371/journal.pntd.0006369 29734337

24. Kar SK, Sah B, Patnaik B, Kim YH, Kerketta AS, Shin S, et al. Mass vaccination with a new, less expensive oral cholera vaccine using public health infrastructure in India: the Odisha model. PLoS Negl Trop Dis. 2014;8(2):e2629. doi: 10.1371/journal.pntd.0002629 24516675

25. Khan IA, Saha A, Chowdhury F, Khan AI, Uddin MJ, Begum YA, et al. Coverage and cost of a large oral cholera vaccination program in a high-risk cholera endemic urban population in Dhaka, Bangladesh. Vaccine. 2013;31(51):6058–64. doi: 10.1016/j.vaccine.2013.10.021 24161413

26. Khatib AM, Ali M, von Seidlein L, Kim DR, Hashim R, Reyburn R, et al. Effectiveness of an oral cholera vaccine in Zanzibar: findings from a mass vaccination campaign and observational cohort study. Lancet Infect Dis. 2012;12(11):837–44. doi: 10.1016/S1473-3099(12)70196-2 22954655

27. Ali M, Emch M, von Seidlein L, Yunus M, Sack DA, Rao M, et al. Herd immunity conferred by killed oral cholera vaccines in Bangladesh: a reanalysis. Lancet. 2005;366(9479):44–9. doi: 10.1016/S0140-6736(05)66550-6 15993232

28. Ali M, Sur D, You YA, Kanungo S, Sah B, Manna B, et al. Herd protection by a bivalent killed whole-cell oral cholera vaccine in the slums of Kolkata, India. Clin Infect Dis. 2013;56(8):1123–31. doi: 10.1093/cid/cit009 23362293

29. Cholera vaccines: WHO position paper—August 2017. Wkly Epidemiol Rec. 2017;92(34):477–98. 28845659

30. Ilboudo PG, Le Gargasson J-B. Delivery cost analysis of a reactive mass cholera vaccination campaign: a case study of Shanchol™ vaccine use in Lake Chilwa, Malawi. BMC Infect Dis. 2017;17(1):779. doi: 10.1186/s12879-017-2885-8 29258447

31. Ciglenecki I, Sakoba K, Luquero FJ, Heile M, Itama C, Mengel M, et al. Feasibility of mass vaccination campaign with oral cholera vaccines in response to an outbreak in Guinea. PLoS Med. 2013;10(9):e1001512. doi: 10.1371/journal.pmed.1001512 24058301

32. Cavailler P, Lucas M, Perroud V, McChesney M, Ampuero S, Guérin PJ, et al. Feasibility of a mass vaccination campaign using a two-dose oral cholera vaccine in an urban cholera-endemic setting in Mozambique. Vaccine. 2006;24(22):4890–5. doi: 10.1016/j.vaccine.2005.10.006 16298025

33. Schaetti C, Weiss MG, Ali SM, Chaignat C-L, Khatib AM, Reyburn R, et al. Costs of illness due to cholera, costs of immunization and cost-effectiveness of an oral cholera mass vaccination campaign in Zanzibar. PLoS Negl Trop Dis. 2012;6(10):e1844. doi: 10.1371/journal.pntd.0001844 23056660

34. Tan-Torres Edejer T, Balthussen R, Adam T, Hutubessy R, Acharya A, Evans DB, et al., editors. Making choices in health: WHO guide to cost-effectiveness analysis. Geneva: World Health Organization; 2003. 318 p.

35. Longini IM Jr, Nizam A, Ali M, Yunus M, Shenvi N, Clemens JD. Controlling endemic cholera with oral vaccines. PLoS Med. 2007;4(11):e336. doi: 10.1371/journal.pmed.0040336 18044983

36. Department of Economic and Social Affairs Population Division. World population prospects: the 2017 revision. Volume I: comprehensive tables. ST/ESA/SER.A/399. New York: United Nations; 2017.

37. World Bank. World development indicators 2017. Washington (DC): World Bank; 2017. doi: 10.1596/26447

38. Hsiao A, Hall AH, Mogasale V, Quentin W. The health economics of cholera: a systematic review. Vaccine. 2018;36(30):4404–24. doi: 10.1016/j.vaccine.2018.05.120 29907482

39. Freeman MC, Garn JV, Sclar GD, Boisson S, Medlicott K, Alexander KT, et al. The impact of sanitation on infectious disease and nutritional status: a systematic review and meta-analysis. Int J Hyg Environ Health. 2017;220(6):928–49. doi: 10.1016/j.ijheh.2017.05.007 28602619

40. Wolf J, Hunter PR, Freeman MC, Cumming O, Clasen T, Bartram J, et al. Impact of drinking water, sanitation and handwashing with soap on childhood diarrhoeal disease: updated meta-analysis and meta-regression. Trop Med Int Health. 2018;23(5):508–25. doi: 10.1111/tmi.13051 29537671

41. Nygren BL, Blackstock AJ, Mintz ED. Cholera at the crossroads: the association between endemic cholera and national access to improved water sources and sanitation. Am J Trop Med Hyg. 2014;91(5):1023–8. doi: 10.4269/ajtmh.14-0331 25200265

42. Cumming O, Curtis V. Implications of WASH Benefits trials for water and sanitation. Lancet Global Health. 2018;6(6):e613–4. doi: 10.1016/S2214-109X(18)30192-X 29706563

43. World Health Organization. Progress on drinking water, sanitation and hygiene: 2017 update and SDG baselines. Geneva: World Health Organization; 2017. 112 p.

44. Qadri F, Wierzba TF, Ali M, Chowdhury F, Khan AI, Saha A, et al. Efficacy of a single-dose, inactivated oral cholera vaccine in Bangladesh. N Engl J Med. 2016;374(18):1723–32. doi: 10.1056/NEJMoa1510330 27144848

45. Qadri F, Ali M, Lynch J, Chowdhury F, Khan AI, Wierzba TF, et al. Efficacy of a single-dose regimen of inactivated whole-cell oral cholera vaccine: results from 2 years of follow-up of a randomised trial. Lancet Infect Dis. 2018;18(6):666–74. doi: 10.1016/S1473-3099(18)30108-7 29550406

46. Azman AS, Parker LA, Rumunu J, Tadesse F, Grandesso F, Deng LL, et al. Effectiveness of one dose of oral cholera vaccine in response to an outbreak: a case-cohort study. Lancet Glob Health. 2016;4(11):e856–63. doi: 10.1016/S2214-109X(16)30211-X 27765293