Human onchocerciasis: Modelling the potential long-term consequences of a vaccination programme

PLoS Neglected Tropical Diseases

Volumn 9, Issue 7, 2015, Pages 1-19

  Turner, Hugo C ^a   Walker, Martin ^a   Lustigman, Sara ^b   Taylor, David W ^c   Basáñez, María Gloria ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NEW YORK BLOOD CENTER   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IVERMECTIN; ANTHELMINTIC AGENT; VACCINE;

ADULT; ARTICLE; CONTROL STRATEGY; DISEASE CONTROL; DISEASE TRANSMISSION; FEMALE; HUMAN; LOIASIS; LONG TERM EXPOSURE; MALE; MATHEMATICAL MODEL; NONHUMAN; ONCHOCERCIASIS; PARASITE PREVALENCE; SENSITIVITY ANALYSIS; SPECIES ENDEMICITY; VACCINATION; ADOLESCENT; AGED; AGING; BIOLOGICAL MODEL; CHILD; IMMUNOLOGY; INFANT; MIDDLE AGED; PRESCHOOL CHILD; PROCEDURES; RISK FACTOR; SEX DIFFERENCE; TIME FACTOR; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; ANTHELMINTICS; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; INFANT; IVERMECTIN; MALE; MIDDLE AGED; MODELS, BIOLOGICAL; ONCHOCERCIASIS; RISK FACTORS; SEX FACTORS; TIME FACTORS; VACCINATION; VACCINES; YOUNG ADULT;

EID: 84938562675     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003938     Document Type: Article

References (72)

1. World Health Organization. Accelerating work to overcome the global impact of neglected tropical diseases- A roadmap for implementation. Geneva: WHO. 2012. http://www.who.int/neglected_diseases/NTD_RoadMap_2012_Fullversion.pdf; accessed 17th June 2015
2. London Declaration on Neglected Tropical Diseases. Ending the neglect and reaching 2020 goals. London, UK. 2012. http://unitingtocombatntds.org/downloads/press/ntd_event_london_declaration_on_ntds.pdf; accessed 13th May 2015
3. World Health Organization. 18th Session of the Joint Action Forum. Bujumbura, Burundi. 2012. http://www.who.int/apoc/media/Journal_du_FAC_day_4_Anglais.pdf; accessed 13th May 2015
4. Bill & Melinda Gates Foundation. Gates Annual letter Our Big Bet for the Future. 2015. www.gatesletter.com; accessed 13th May 2015
5. Turner HC, Walker M, Churcher TS, Osei-Atweneboana MY, Biritwum N-K, Hopkins A, et al. Reaching the London Declaration on Neglected Tropical Diseases goals for onchocerciasis: an economic evaluation of increasing the frequency of ivermectin treatment in Africa. Clin Infect Dis. 2014; 59 (7): 923-932.doi: 10.1093/cid/ciu467 PMID: 24944228
6. Turner HC, Walker M, Attah SK, Opoku NO, Awadzi K, Kuesel AC, et al. The potential impact of moxidectin on onchocerciasis elimination in Africa: an economic evaluation based on the Phase II clinical trial data. Parasit Vectors. 2015; 8: 167.doi: 10.1186/s13071-015-0779-4 PMID: 25889256
7. Turner HC, Walker M, Churcher TS, Basáñez MG. Modelling the impact of ivermectin on River Blindness and its burden of morbidity and mortality in African savannah: EpiOncho projections. Parasit Vectors. 2014; 7: 241.doi: 10.1186/1756-3305-7-241 PMID: 24886747
8. Turner HC, Churcher TS, Walker M, Osei-Atweneboana MY, Prichard RK, Basáñez MG. Uncertainty surrounding projections of the long-term impact of ivermectin treatment for human onchocerciasis. PLoS Negl Trop Dis. 2013; 7 (4):: e2169.doi: 10.1371/journal.pntd.0002169 PMID: 23634234
9. Winnen M, Plaisier AP, Alley ES, Nagelkerke NJD, van Oortmarssen G, Boatin BA, et al. Can ivermectin mass treatments eliminate onchocerciasis in Africa? BullWorld Health Organ. 2002; 80 (5): 384-391. PMID: 12077614
10. Coffeng LE, Stolk WA, Hoerauf A, Habbema D, Bakker R, Hopkins AD, et al. Elimination of African onchocerciasis: modeling the impact of increasing the frequency of ivermectin mass treatment. PloS One. 2014; 9 (12): e115886.doi: 10.1371/journal.pone.0115886 PMID: 25545677
11. Duerr HP, Raddatz G, Eichner M. Control of onchocerciasis in Africa: threshold shifts, breakpoints and rules for elimination. Int J Parasitol. 2011; 41 (5): 581-589.doi: 10.1016/j.ijpara.2010.12.009 PMID: 21255577
12. Prichard RK, Basáñez MG, Boatin BA, McCarthy JS, Garcia HH, Yang GJ, et al. A research agenda for helminth diseases of humans: intervention for control and elimination. PLoS Negl Trop Dis. 2012; 6 (4): e1549.doi: 10.1371/journal.pntd.0001549 PMID: 22545163
13. Hotez PJ, Bottazzi ME, Zhan B, Makepeace BL, Klei TR, Abraham D, et al. The Onchocerciasis Vaccine for Africa—TOVA—Initiative. PLoS Negl Trop Dis. 2015; 9 (1): e0003422.doi: 10.1371/journal. pntd.0003422 PMID: 25634641
14. Zouré HGM, Wanji S, Noma M, Amazigo UV, Diggle PJ, Tekle AH, et al. The geographic distribution of Loa loa in Africa: results of large-scale implementation of the Rapid Assessment Procedure for Loiasis (RAPLOA). PLoS Negl Trop Dis. 2011; 5 (6): e1210.doi: 10.1371/journal.pntd.0001210 PMID: 21738809
15. Thomson MC, Obsomer V, Dunne M, Connor SJ, Molyneux DH. Satellite mapping of Loa loa prevalence in relation to ivermectin use in west and central Africa. Lancet. 2000; 356 (9235): 1077-1078. PMID: 11009145
16. Boussinesq M, Gardon J, Kamgno J, Pion SDS, Gardon-Wendel N, Chippaux JP. Relationships between the prevalence and intensity of Loa loa infection in the Central province of Cameroon. Ann Trop Med Parasitol. 2001; 95 (5): 495-507. PMID: 11487371
17. Kelly-Hope LA, Cano J, Stanton MC, Bockarie MJ, Molyneux DH. Innovative tools for assessing risks for severe adverse events in areas of overlapping Loa loa and other filarial distributions: the application of micro-stratification mapping. Parasit Vectors. 2014; 7: 307.doi: 10.1186/1756-3305-7-307 PMID: 24992829
18. Awadzi K, Attah SK, Addy ET, Opoku NO, Quartey BT, Lazdins-Helds JK, et al. Thirty-month follow-up of sub-optimal responders to multiple treatments with ivermectin, in two onchocerciasis-endemic foci in Ghana. Ann Trop Med Parasitol. 2004; 98 (4): 359-370. PMID: 15228717
19. Awadzi K, Boakye DA, Edwards G, Opoku NO, Attah SK, Osei-Atweneboana MY, et al. An investigation of persistent microfilaridermias despite multiple treatments with ivermectin, in two onchocerciasisendemic foci in Ghana. Ann Trop Med Parasitol. 2004; 98 (3): 231-249. PMID: 15119969
20. Osei-Atweneboana MY, Eng JKL, Boakye DA, Gyapong JO, Prichard RK. Prevalence and intensity of Onchocerca volvulus infection and efficacy of ivermectin in endemic communities in Ghana: a twophase epidemiological study. Lancet. 2007; 369 (9578): 2021-2029. PMID: 17574093
21. Churcher TS, Pion SDS, Osei-Atweneboana MY, Prichard RK, Awadzi K, Boussinesq M, et al. Identifying sub-optimal responses to ivermectin in the treatment of River Blindness. Proc Natl Acad Sci U S A. 2009; 106 (39): 16716-16721.doi: 10.1073/pnas.0906176106 PMID: 19805362
22. The onchocerciasis vaccine for Africa (TOVA) initiative. 2015. http://www.riverblindnessvaccinetova.org/; accessed 13th May 2015
23. The Onchocerciasis Vaccine for Africa (TOVA) Initiative prospectus. 2015 http://www.riverblindnessvaccinetova.org/sites/default/files/atoms/files/River_Blindness_Prospectus%20Final.pdf; accessed 13th May 2015
24. Cook JA, Steel C, Ottesen EA. Towards a vaccine for onchocerciasis. Trends Parasitol. 2001; 17 (12): 555-558. PMID: 11756017
25. Lustigman S, James ER, Tawe W, Abraham D. Towards a recombinant antigen vaccine against Onchocerca volvulus. Trends Parasitol. 2002; 18 (3): 135-141. PMID: 11854092
26. Hess JA, Zhan B, Bonne-Année S, Deckman JM, Bottazzi ME, Hotez PJ, et al. Vaccines to combat river blindness: expression, selection and formulation of vaccines against infection with Onchocerca volvulus in a mouse model. Int J Parasitol. 2014; 44 (9): 637-646.doi: 10.1016/j.ijpara.2014.04.006 PMID: 24907553
27. Babayan SA, Allen JE, Taylor DW. Future prospects and challenges of vaccines against filariasis. Parasite Immunol. 2012; 34 (5): 243-253.doi: 10.1111/j.1365-3024.2011.01350.x PMID:22150082
28. Arumugam S, Wei J, Ward D, Abraham D, Lustigman S, Zhan B, et al. Vaccination with a genetically modified Brugia malayi cysteine protease inhibitor-2 reduces adult parasite numbers and affects the fertility of female worms following a subcutaneous challenge of Mongolian gerbils (Meriones unguiculatus) with B. malayi infective larvae. Int J Parasitol. 2014; 44 (10): 675-679.doi: 10.1016/j.ijpara.2014.05.003 PMID: 24929131
29. Babayan SA, Luo H, Gray N, Taylor DW, Allen JE. Deletion of parasite immune modulatory sequences combined with immune activating signals enhances vaccine mediated protection against filarial nematodes. PLoS Negl Trop Dis. 2012; 6 (12): e1968.doi: 10.1371/journal.pntd.0001968 PMID: 23301106
30. Ziewer S, Hübner MP, Dubben B, Hoffmann WH, Bain O, Martin C, et al. Immunization with L. sigmodontis microfilariae reduces peripheral microfilaraemia after challenge infection by inhibition of filarial embryogenesis. PLoS Negl Trop Dis. 2012; 6 (3): e1558.doi: 10.1371/journal.pntd.0001558 PMID: 22413031
31. Basáñez MG, Boussinesq M. Population biology of human onchocerciasis. Philos Trans R Soc Lond B Biol Sci. 1999; 354 (1384): 809-826. PMID: 10365406
32. Filipe JAN, Boussinesq M, Renz A, Collins RC, Vivas-Martinez S, Grillet ME et al. Human infection patterns and heterogeneous exposure in river blindness. Proc Natl Acad Sci U S A. 2005; 102 (42): 15265-15270. PMID: 16217028
33. Basáñez MG, Pion SDS, Boakes E, Filipe JAN, Churcher TS, Boussinesq M. Effect of single-dose ivermectin on Onchocerca volvulus: a systematic review and meta-analysis. Lancet Infect Dis. 2008; 8 (5): 310-322.doi: 10.1016/S1473-3099(08)70099-9 PMID: 18471776
34. Churcher TS, Basáñez MG. Density dependence and the spread of anthelmintic resistance. Evolution. 2008; 62 (3): 528-537. PMID: 17983465
35. Anderson J, Fuglsang H, Hamilton PJS, de Marshall TF. Studies on onchocerciasis in the United Cameroon Republic II. Comparison of onchocerciasis in rain-forest and Sudan-savanna. Trans R Soc Trop Med Hyg. 1974; 68 (3): 209-222. PMID: 4421167
36. Renz A, Fuglsang H, Anderson J. Studies on the dynamics of transmission of onchocerciasis in a Sudan-savanna area of North Cameroon IV. The different exposure to Simulium bites and transmission of boys and girls and men and women, and the resulting manifestations of onchocerciasis. Ann Trop Med Parasitol. 1987; 81 (3): 253-262. PMID: 3662667
37. Bradley JE, Whitworth J, Basáñez MG. Onchocerciasis. In: Wakelin D, Cox F, Despommier D, Gillespie S, editors. Topley and Wilson’s Microbiology and Microbial Infections. 10th ed. London: London: Hodder Arnold; 2005. pp. 781-801.
38. Duke BOL (1990) Human onchocerciasis—an overview of the disease. Acta Leiden 59 (1-2): 9-24. PMID: 2198761
39. Remme JHF, Ba O, Dadzie KY, Karam M (1986) A force-of-infection model for onchocerciasis and its applications in the epidemiological evaluation of the Onchocerciasis Control Programme in the Volta River basin area. Bull World Health Organ 64: 667-681. PMID: 3492300
40. Chan MS, Woolhouse ME, Bundy DAP (1997) Human schistosomiasis: potential long-term consequences of vaccination programmes. Vaccine 15: 1545-1550. PMID: 9330466
41. Keja K, Chan C, Hayden G, Henderson RH (1988) Expanded programme on immunization. World Health Stat Q 41: 59-63. PMID: 3176515
42. World Health Organization. WHO recommendations for routine immunization—summary tables. 2015. http://www.who.int/immunization/policy/immunization_tables/en/; accessed 13th May 2015
43. The World Bank. Immunization, measles (%of children ages 12-23 months). 2013. http://data.worldbank.org/indicator/SH.IMM.MEAS?order=wbapi_data_value_2011+wbapi_data_value+w; accessed 13th May 2015
44. Woolhouse ME. Human schistosomiasis: potential consequences of vaccination. Vaccine. 1995; 13 (12): 1045-1050. PMID: 7491810
45. Walker M, Little MP, Wagner KS, Soumbey-Alley EW, Boatin BA, Basáñez MG. Density-dependent mortality of the human host in onchocerciasis: relationships between microfilarial load and excess mortality. PLoS Negl Trop Dis. 2012; 6 (3): e1578.doi: 10.1371/journal.pntd.0001578 PMID: 22479660
46. Turner HC, Walker M, French MD, Blake IM, Churcher TS, Basáñez MG. Neglected tools for neglected diseases: mathematical models in economic evaluations. Trends Parasitol. 2014; 30 (12): 562-570.doi: 10.1016/j.pt.2014.10.001 PMID: 25455565
47. Turner HC, Truscott JE, Hollingsworth TD, Bettis AA, Brooker SJ, Anderson RM. Cost and costeffectiveness of soil-transmitted helminth treatment programmes: systematic review and research needs. Parasit Vectors. 2015; In press.
48. Walker M, Specht S, Churcher TS, Hoerauf A, Taylor MJ, Basáñez MG. Therapeutic efficacy and macrofilaricidal activity of doxycycline for the treatment of River Blindness. Clin Infect Dis. 2015; 60 (8): 1199-1207.doi: 10.1093/cid/ciu1152 PMID: 25537873
49. Remme JHF, Feenstra P, Lever PR, Medici AC, Morel CM. Tropical diseases targeted for elimination: chagas disease, lymphatic dilariasis, onchocerciasis, and leprosy. In: Jamison DT, Breman JG, Measham AR, editors. Disease Control Priorities in Developing Countries. New York: Oxford University Press; 2006. pp. 433-449.
50. Coffeng LE, Stolk WA, Zouré HGM, Veerman JL, Agblewonu KB, Murdoch ME, et al. African Programme for Onchocerciasis Control 1995-2015: model-estimated health impact and cost. PLoS Negl Trop Dis. 2013; 7 (1): e2032.doi: 10.1371/journal.pntd.0002032 PMID: 23383355
51. Turner HC, Osei-Atweneboana MY, Walker M, Tettevi EJ, Churcher TS, Asiedu O, et al. The cost of annual versus biannual community-directed treatment with ivermectin: Ghana as a case study PLoS Negl Trop Dis. 2013; 7 (9): e2452.doi: 10.1371/journal.pntd.0002452 PMID: 24069497
52. Diawara L, Traoré MO, Badji A, Bissan Y, Doumbia K, Goita SF, et al. Feasibility of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: first evidence from studies in Mali and Senegal. PLoS Negl Trop Dis. 2009; 3 (7): e497.doi: 10.1371/journal.pntd.0000497 PMID: 19621091
53. Tekle A, Elhassan E, Isiyaku S, Amazigo U, Bush S, Noma M, et al. Impact of long-term treatment of onchocerciasis with ivermectin in Kaduna State, Nigeria: first evidence of the potential for elimination in the operational area of the African Programme for Onchocerciasis Control. Parasit Vectors. 2012; 5: 28.doi: 10.1186/1756-3305-5-28 PMID: 22313631
54. Plaisier AP, van Oortmarssen GJ, Habbema JDF, Remme JHF, Alley ES. ONCHOSIM: a model and computer simulation program for the transmission and control of onchocerciasis. Comput Methods Programs Biomed. 1990; 31 (1): 43-56. PMID: 2311368
55. African Programme for Onchocerciasis Control. Conceptual and operational framework of onchocerciasis elimination with ivermectin treatment. WHO/APOC. 2010. http://www.who.int/apoc/oncho_elimination_report_english.pdf; accessed 13th May 2015
56. Anderson RM, May RM. Infectious diseases of humans. Dynamics and control. Oxford: Oxford Science Publications; 1992
57. Basáñez MG, Churcher TS, Grillet ME. Onchocerca-Simulium interactions and the population and evolutionary biology of Onchocerca volvulus. Adv Parasitol. 2009; 68: 263-313.doi: 10.1016/S0065-308X (08)00611-8 PMID: 19289198
58. Traoré MO, Sarr MD, Badji A, Bissan Y, Diawara L, Doumbia K, et al. Proof-of-principle of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: final results of a study in Mali and Senegal. PLoS Negl Trop Dis. 2012; 6: e1825.doi: 10.1371/journal.pntd.0001825 PMID: 23029586
59. Lamberton PHL, Cheke RA, Walker M, Winskill P, Osei-Atweneboana MY, Tirados I, et al. Onchocerciasis transmission in Ghana: biting and parous rates of host-seeking sibling species of the Simulium damnosum complex. Parasit Vectors. 2014; 7: 511.doi: 10.1186/s13071-014-0511-9 PMID: 25413569
60. McCarthy JS, Lustigman S, Yang G-J, Barakat RM, García HH, Sripa B, et al. A research agenda for helminth diseases of humans: diagnostics for control and elimination programmes. PLoS Negl Trop Dis. 2012; 6 (4): e1601.doi: 10.1371/journal.pntd.0001601 PMID: 22545166
61. Davies JB. Description of a computer model of forest onchocerciasis transmission and its application to field scenarios of vector control and chemotherapy. Ann Trop Med Parasitol. 1993; 87 (1): 41-63. PMID: 8346991
62. Cheke RA, Garms R. Indices of onchocerciasis transmission by different members of the Simulium damnosum complex conflict with the paradigm of forest and savanna parasite strains. Acta Trop. 2013; 125 (1): 43-52.doi: 10.1016/j.actatropica.2012.09.002 PMID: 22995985
63. Duke BOL, Moore PJ, Anderson J. Studies on factors influencing the transmission of onchocerciasis. VII. A comparison of the Onchocerca volvulus transmission potentials of Simulium damnosum populations in four Cameroon rain-forest villages and the pattern of onchocerciasis associated therewith. Ann Trop Med Parasitol. 1972; 66 (2): 219-234. PMID: 5038247
64. Williams GM, Sleigh AC, Li Y, Feng Z, Davis GM, Chen H, et al. Mathematical modelling of schistosomiasis japonica: comparison of control strategies in the People's Republic of China. Acta Trop. 2002; 82 (2): 253-262. PMID: 12020899
65. Sabatelli L, Ghani AC, Rodrigues LC, Hotez PJ, Brooker S. Modelling heterogeneity and the impact of chemotherapy and vaccination against human hookworm. J R Soc Interface. 2008; 5 (28): 1329-1341.doi: 10.1098/rsif.2007.1255 PMID: 18331978
66. Hewitson JP, Maizels RM. Vaccination against helminth parasite infections. Expert Rev Vaccines. 2014; 13 (4): 473-487. PMID: 24606541
67. Kirch AK, Duerr HP, Boatin B, Alley WS, Hoffmann WH, Schulz-Key H, et al. Impact of parental onchocerciasis and intensity of transmission on development and persistence of Onchocerca volvulus infection in offspring: an 18 year follow-up study. Parasitology. 2003; 127 (4): 327-335.
68. Prost A, Gorim de Ponsay E. [The epidemiological significance of neo-natal parasitism with microfilariae of Onchocerca volvulus (author's transl)]. Tropenmed Parasitol. 1979; 30 (4): 477-481. [Article in French]. PMID: 575449
69. Globisch D, Moreno AY, Hixon MS, Nunes AA, Denery JR, Specht S, et al. Onchocerca volvulusneurotransmitter tyramine is a biomarker for river blindness. Proc Natl Acad Sci U S A. 2013; 110 (11): 4218-4223.doi: 10.1073/pnas.1221969110 PMID: 23440222
70. Quintana JF, Makepeace BL, Babayan SA, Ivens A, Pfarr KM, Blaxter M et al. Extracellular Onchocerca-derived small RNAs in host nodules and blood. Parasit Vectors. 2015; 8: 58.doi: 10.1186/s13071-015-0656-1 PMID: 25623184
71. Tendongfor N, Wanji S, Ngwa JC, Esum ME, Specht S, Enyong P, et al. The human parasite Loa loa in cytokine and cytokine receptor gene knock out BALB/c mice: survival, development and localization. Parasit Vectors. 2012; 5: 43.doi: 10.1186/1756-3305-5-43 PMID: 22348321
72. Prost A, Hervouet JP, Thylefors B. [Epidemiologic status of onchocerciasis]. Bull World Health Organ. 1979; 57 (4): 655-662. [Article in French]. PMID: 316743