The potential impact of case-area targeted interventions in response to cholera outbreaks: A modeling study

1. World Health Organization. Cholera, 2016. Wkly Epidemiol Rec. 2017;92(36):521–36. 28884993

2. Ali M, Nelson AR, Lopez AL, Sack DA. Updated global burden of cholera in endemic countries. PLoS Negl Trop Dis. 2015;9(6):e0003832. doi: 10.1371/journal.pntd.0003832 26043000

3. Luquero FJ, Rondy M, Boncy J, Munger A, Mekaoui H, Rymshaw E, et al. Mortality rates during cholera epidemic, Haiti, 2010–2011. Emerg Infect Dis. 2016;22(3):410–6. doi: 10.3201/eid2203.141970 26886511

4. Rebaudet S, Sudre B, Faucher B, Piarroux R. Cholera in coastal Africa: a systematic review of its heterogeneous environmental determinants. J Infect Dis. 2013;208(Suppl 1):S98–106. doi: 10.1093/infdis/jit202 24101653

5. 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. doi: 10.1093/infdis/jit195 24101645

6. Fewtrell L, Kaufmann RB, Kay D, Enanoria W, Haller L, Colford JM Jr. Water, sanitation, and hygiene interventions to reduce diarrhoea in less developed countries: a systematic review and meta-analysis. Lancet Infect Dis. 2005;5(1):42–52. doi: 10.1016/S1473-3099(04)01253-8 15620560

7. Guévart É, Noeske J, Sollé J, Mouangue A, Bikoti JM. Antibioprophylaxie ciblée à large échelle au cours de l’épidémie de choléra de Douala en 2004. Santé. 2007;17(2):63–8.

8. Reveiz L, Chapman E, Ramon-Pardo P, Koehlmoos TP, Cuervo LG, Aldighieri S, et al. Chemoprophylaxis in contacts of patients with cholera: systematic review and meta-analysis. PLoS ONE. 2011;6(11):e27060. doi: 10.1371/journal.pone.0027060 22102873

9. Desai SN, Pezzoli L, Martin S, Costa A, Rodriguez C, Legros D, et al. A second affordable oral cholera vaccine: implications for the global vaccine stockpile. Lancet Glob Health. 2016;4(4):e223–4. doi: 10.1016/S2214-109X(16)00037-1 27013303

10. Martin S, Costa A, Perea W. Stockpiling oral cholera vaccine. Bull World Health Organ. 2012;90(10):714. doi: 10.2471/BLT.12.112433 23109735

11. Parker LA, Rumunu J, Jamet C, Kenyi Y, Lino RL, Wamala JF, et al. Adapting to the global shortage of cholera vaccines: targeted single dose cholera vaccine in response to an outbreak in South Sudan. Lancet Infect Dis. 2017;17(4):e123–7. doi: 10.1016/S1473-3099(16)30472-8 28109819

12. Bhattacharya SK, Sur D, Ali M, Kanungo S, You YA, Manna B, et al. 5 year efficacy of a bivalent killed whole-cell oral cholera vaccine in Kolkata, India: a cluster-randomised, double-blind, placebo-controlled trial. Lancet Infect Dis. 2013;13(12):1050–6. doi: 10.1016/S1473-3099(13)70273-1 24140390

13. 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

14. 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

15. 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

16. 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

17. Ivers LC, Hilaire IJ, Teng JE, Almazor CP, Jerome JG, Ternier R, et al. Effectiveness of reactive oral cholera vaccination in rural Haiti: a case-control study and bias-indicator analysis. Lancet Glob Health. 2015;3(3):e162–8. doi: 10.1016/S2214-109X(14)70368-7 25701994

18. Parker LA, Rumunu J, Jamet C, Kenyi Y, Lino RL, Wamala JF, et al. Neighborhood-targeted and case-triggered use of a single dose of oral cholera vaccine in an urban setting: feasibility and vaccine coverage. PLoS Negl Trop Dis. 2017;11(6):e0005652. doi: 10.1371/journal.pntd.0005652 28594891

19. Piarroux R, Bompangue D, Oger PY, Boinet A, Haaser F, Vandevelde T. From research to field action: example of the fight against cholera in the Democratic Republic of Congo. Field Actions Sci Rep. 2009;2.

20. Farmer P, Almazor CP, Bahnsen ET, Barry D, Bazile J, Bloom BR, et al. Meeting cholera’s challenge to Haiti and the world: a joint statement on cholera prevention and care. PLoS Negl Trop Dis. 2011;5(5):e1145. doi: 10.1371/journal.pntd.0001145 21655350

21. Santa-Olalla P, Gayer M, Magloire R, Barrais R, Valenciano M, Aramburu C, et al. Implementation of an alert and response system in Haiti during the early stage of the response to the cholera epidemic. Am J Trop Med Hyg. 2013;89(4):688–97. doi: 10.4269/ajtmh.13-0267 24106196

22. Debes AK, Ali M, Azman AS, Yunus M, Sack DA. Cholera cases cluster in time and space in Matlab, Bangladesh: implications for targeted preventive interventions. Int J Epidemiol. 2016;45(6):2134–9. doi: 10.1093/ije/dyw267 27789673

23. Snow J. On the mode of communication of cholera. John Churchill; 1855.

24. Blackburn JK, Diamond U, Kracalik IT, Widmer J, Brown W, Morrissey BD, et al. Household-level spatiotemporal patterns of incidence of cholera, Haiti, 2011. Emerg Infect Dis. 2014;20(9):1516–9. doi: 10.3201/eid2009.131882 25148590

25. Ali M, Debes AK, Luquero FJ, Kim DR, Park JY, Digilio L, et al. Potential for controlling cholera using a ring vaccination strategy: re-analysis of data from a cluster-randomized clinical trial. PLoS Med. 2016;13(9):e1002120. doi: 10.1371/journal.pmed.1002120 27622507

26. Luquero FJ, Banga CN, Remartnez D, Palma PP, Baron E, Grais RF. Cholera epidemic in Guinea-Bissau (2008): the importance of “place”. PLoS ONE. 2011;6(5):e19005. doi: 10.1371/journal.pone.0019005 21572530

27. You YA, Ali M, Kanungo S, Sah B, Manna B, Puri M, et al. risk map of cholera infection for vaccine deployment: the eastern Kolkata case. PLoS ONE. 2013;8(8):e71173. doi: 10.1371/journal.pone.0071173 23936491

28. Carrel M, Emch M, Streatfield PK, Yunus M. Spatio-temporal clustering of cholera: the impact of flood control in Matlab, Bangladesh, 1983–2003. Health Place. 2009;15(3):771–82. doi: 10.1016/j.healthplace.2008.12.008 19217821

29. Azman A, Luquero FJ, Salje H, Naibei N, Adalbert N, Ali M, et al. Micro-hotspots of risk in urban cholera epidemics. bioRxiv. 2018 Jan 18. doi: 10.1101/248476

30. Azman AS, Lessler J. Reactive vaccination in the presence of disease hotspots. Proc Biol Sci. 2015;282(1798):20141341. doi: 10.1098/rspb.2014.1341 25392464

31. Azman AS, Rumunu J, Abubakar A, West H, Ciglenecki I, Helderman T, et al. Population-level effect of cholera vaccine on displaced populations, South Sudan, 2014. Emerg Infect Dis. 2016;22(6):1067–70. doi: 10.3201/eid2206.151592 27192187

32. Lessler J, Salje H, Grabowski MK, Cummings DAT. Measuring spatial dependence for infectious disease epidemiology. PLoS ONE. 2016;11(5):e0155249. doi: 10.1371/journal.pone.0155249 27196422

33. Salje H, Lessler J, Endy TP, Curriero FC, Gibbons RV, Nisalak A, et al. Revealing the microscale spatial signature of dengue transmission and immunity in an urban population. Proc Natl Acad Sci U S A. 2012;109(24):9535–8. doi: 10.1073/pnas.1120621109 22645364

34. Grabowski MK, Lessler J, Redd AD, Kagaayi J, Laeyendecker O, Ndyanabo A, et al. The role of viral introductions in sustaining community-based HIV epidemics in rural Uganda: evidence from spatial clustering, phylogenetics, and egocentric transmission models. PLoS Med. 2014;11(3):e1001610. doi: 10.1371/journal.pmed.1001610 24595023

35. Salje H, Cauchemez S, Alera MT, Rodriguez-Barraquer I, Thaisomboonsuk B, Srikiatkhachorn A, et al. Reconstruction of 60 years of chikungunya epidemiology in the Philippines demonstrates episodic and focal transmission. J Infect Dis. 2016;213(4):604–10. doi: 10.1093/infdis/jiv470 26410592

36. Salje H, Lessler J, Berry IM, Melendrez MC, Endy T, Kalayanarooj S, et al. Dengue diversity across spatial and temporal scales: local structure and the effect of host population size. Science. 2017;355(6331):1302–6. doi: 10.1126/science.aaj9384 28336667

37. Esch T, Schenk A, Ullmann T, Thiel M, Roth A, Dech S. Characterization of land cover types in TerraSAR-X images by combined analysis of speckle statistics and intensity information. IEEE Trans Geosci Remote Sens. 2011;49(6):1911–25. doi: 10.1109/TGRS.2010.2091644

38. Esch T, Heldens W, Hirner A, Keil M, Marconcini M, Roth A, et al. Breaking new ground in mapping human settlements from space—the Global Urban Footprint. ISPRS J Photogramm Remote Sens. 2017;134:30–42. doi: 10.1016/j.isprsjprs.2017.10.012

39. Rinaldo A, Bertuzzo E, Mari L, Righetto L, Blokesch M, Gatto M, et al. Reassessment of the 2010–2011 Haiti cholera outbreak and rainfall-driven multiseason projections. Proc Natl Acad Sci U S A. 2012;109(17):6602–7. doi: 10.1073/pnas.1203333109 22505737

40. de Magny GC, Thiaw W, Kumar V, Manga NM, Diop BM, Gueye L, et al. Cholera outbreak in Senegal in 2005: was climate a factor? PLoS ONE. 2012;7(8):e44577. doi: 10.1371/journal.pone.0044577 22952995

41. Gaudart J, Rebaudet S, Barrais R, Boncy J, Faucher B, Piarroux M, et al. Spatio-temporal dynamics of cholera during the first year of the epidemic in Haiti. PLoS Negl Trop Dis. 2013;7(4):e2145. doi: 10.1371/journal.pntd.0002145 23593516

42. Finger F, Genolet T, Mari L, de Magny GC, Manga NM, Rinaldo A, et al. Mobile phone data highlights the role of mass gatherings in the spreading of cholera outbreaks. Proc Natl Acad Sci U S A. 2016;113(23):6421–6. doi: 10.1073/pnas.1522305113 27217564

43. Ngwa MC, Liang S, Kracalik IT, Morris L, Blackburn JK, Mbam LM, et al. Cholera in Cameroon, 2000–2012: spatial and temporal analysis at the operational (health district) and sub climate levels. PLoS Negl Trop Dis. 2016;10(11):e0005105. doi: 10.1371/journal.pntd.0005105 27855171

44. Azman AS, Rudolph KE, Cummings DAT, Lessler J. The incubation period of cholera: a systematic review. J Infect. 2013;66(5):432–8. doi: 10.1016/j.jinf.2012.11.013 23201968

45. Nelson EJ, Harris JB, Glenn Morris J, Calderwood SB, Camilli A. Cholera transmission: the host, pathogen and bacteriophage dynamic. Nat Rev Microbiol. 2009;7(10):693–702. doi: 10.1038/nrmicro2204 19756008

46. Fung ICH. Cholera transmission dynamic models for public health practitioners. Emerging Themes in Epidemiology. 2014;11:1. doi: 10.1186/1742-7622-11-1 24520853

47. Kaper JB, Morris JG, Levine MM. Cholera. Clin Microbiol Rev. 1995;8(1):48–86. 7704895

48. Akeret J, Refregier A, Amara A, Seehars S, Hasner C. Approximate Bayesian computation for forward modeling in cosmology. J Cosmol Astropart Phys. 2015;2015(08):043. doi: 10.1088/1475-7516/2015/08/043

49. Lewnard JA, Antillón M, Gonsalves G, Miller AM, Ko AI, Pitzer VE. Strategies to prevent cholera introduction during international personnel deployments: a computational modeling analysis based on the 2010 Haiti outbreak. PLoS Med. 2016;13(1):e1001947. doi: 10.1371/journal.pmed.1001947 26812236

50. 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

51. Leibovici-Weissman Y, Neuberger A, Bitterman R, Sinclair D, Salam MA, Paul M. Antimicrobial drugs for treating cholera. Cochrane Database Syst Rev. 2014;6:CD008625.

52. Taylor DL, Kahawita TM, Cairncross S, Ensink JHJ. The impact of water, sanitation and hygiene interventions to control cholera: a systematic review. PLoS ONE. 2015;10(8):e0135676. doi: 10.1371/journal.pone.0135676 26284367

53. Khan WA, Saha D, Rahman A, Salam MA, Bogaerts J, Bennish ML. Comparison of single-dose azithromycin and 12-dose, 3-day erythromycin for childhood cholera: a randomised, double-blind trial. Lancet. 2002;360(9347):1722–7. doi: 10.1016/S0140-6736(02)11680-1 12480424

54. Echevarria J, Seas C, Carrillo C, Mostorino R, Ruiz R, Gotuzzo E. Efficacy and tolerability of ciprofloxacin prophylaxis in adult household contacts of patients with cholera. Clin Infect Dis. 1995;20(6):1480–4. doi: 10.1093/clinids/20.6.1480 7548495

55. Cash RA, Music SI, Libonati JP, Snyder MJ, Wenzel RP, Hornick RB. Response of man to infection with Vibrio cholerae. I. Clinical, serologic, and bacteriologic responses to a known inoculum. J Infect Dis. 1974;129(1):45–52. doi: 10.1093/infdis/129.1.45 4809112

56. Hornick RB, Music SI, Wenzel R, Cash R, Libonati JP, Snyder MJ, et al. The Broad Street pump revisited: response of volunteers to ingested cholera vibrios. Bull N Y Acad Med. 1971;47(10):1181–91. 5286453

57. Grad YH, Miller JC, Lipsitch M. Cholera modeling: challenges to quantitative analysis and predicting the impact of interventions. Epidemiology. 2012;23(4):523–30. doi: 10.1097/EDE.0b013e3182572581 22659546

58. Hitchings MDT, Grais RF, Lipsitch M. Using simulation to aid trial design: ring-vaccination trials. PLoS Negl Trop Dis. 2017;11(3):e0005470. doi: 10.1371/journal.pntd.0005470 28328984

59. Kucharski AJ, Eggo RM, Watson CH, Camacho A, Funk S, Edmunds WJ. Effectiveness of ring vaccination as control strategy for Ebola virus disease. Emerg Infect Dis. 2016;22(1):105–8. doi: 10.3201/eid2201.151410 26691346

60. Merler S, Ajelli M, Fumanelli L, Parlamento S, y Piontti AP, Dean NE, et al. Containing Ebola at the source with ring vaccination. PLoS Negl Trop Dis. 2016;10(11):e0005093. doi: 10.1371/journal.pntd.0005093 27806049

61. Debes AK, Ateudjieu J, Guenou E, Lopez AL, Bugayong MP, Retiban PJ, et al. Evaluation in Cameroon of a novel, simplified methodology to assist molecular microbiological analysis of V. cholerae in resource-limited settings. PLoS Negl Trop Dis. 2016;10(1):e0004307. doi: 10.1371/journal.pntd.0004307 26735969

62. Cox W. Demographia world urban areas. 13th annual edition. Belleville (IL): Demographia; 2017 [cited 2018 Jan 22]. Available from: http://www.demographia.com/db-worldua.pdf.

63. Rebaudet S, Gazin P, Barrais R, Moore S, Rossignol E, Barthelemy N, et al. The dry season in Haiti: a window of opportunity to eliminate cholera. PLoS Curr. 2013 Jun 10. doi: 10.1371/currents.outbreaks.2193a0ec4401d9526203af12e5024ddc 23873011

64. Wernli D, Jørgensen PS, Harbarth S, Carroll SP, Laxminarayan R, Levrat N, et al. Antimicrobial resistance: the complex challenge of measurement to inform policy and the public. PLoS Med. 2017;14(8):e1002378. doi: 10.1371/journal.pmed.1002378 28817562

65. Hartley DM, Morris JG Jr, Smith DL. Hyperinfectivity: a critical element in the ability of V. cholerae to cause epidemics? PLoS Med. 2006;3(1):e7. doi: 10.1371/journal.pmed.0030007 16318414

66. Faruque SM, Biswas K, Udden SMN, Ahmad QS, Sack DA, Nair GB, et al. Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc Natl Acad Sci U S A. 2006;103(16):6350–5. doi: 10.1073/pnas.0601277103 16601099

67. Fewtrell L, Colford JM Jr. Water, sanitation and hygiene: interventions and diarrhoea—a systematic review and meta-analysis. Washington (DC): World Bank; 2004.

68. Clasen T, Schmidt WP, Rabie T, Roberts I, Cairncross S. Interventions to improve water quality for preventing diarrhoea: systematic review and meta-analysis. BMJ. 2007;334(7597):782. doi: 10.1136/bmj.39118.489931.BE 17353208

69. Salje H, Lessler J, Paul KK, Azman AS, Rahman MW, Rahman M, et al. How social structures, space, and behaviors shape the spread of infectious diseases using chikungunya as a case study. Proc Natl Acad Sci U S A. 2016;113(47):13420–5. doi: 10.1073/pnas.1611391113 27821727

70. Weil AA, Begum Y, Chowdhury F, Khan AI, Leung DT, LaRocque RC, et al. Bacterial shedding in household contacts of cholera patients in Dhaka, Bangladesh. Am J Trop Med Hyg. 2014;91(4):738–42. doi: 10.4269/ajtmh.14-0095 25114012