Modelling onchocerciasis-associated epilepsy and the impact of ivermectin treatment on its prevalence and incidence.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
25 Jul 2024
25 Jul 2024
Historique:
received:
20
03
2024
accepted:
15
07
2024
medline:
26
7
2024
pubmed:
26
7
2024
entrez:
25
7
2024
Statut:
epublish
Résumé
Retrospective cohort studies in Cameroon found an association between Onchocerca volvulus microfilarial load in childhood (measured in 1991-1993) and risk of developing epilepsy later in life (measured in 2017). We parameterised and integrated this relationship (across children aged 3-15 years) into the previously published, stochastic transmission model, EPIONCHO-IBM, for Simulium damnosum sensu lato-transmitted onchocerciasis. We simulated 19 years (1998-2017) of annual ivermectin mass drug administration (MDA) reflecting coverage in the study area, and modelled epilepsy prevalence and incidence. Scenario-based simulations of 25 years of (annual and biannual) MDA in hyper- and holoendemic settings, with 65% and 80% therapeutic coverage, were also conducted. EPIONCHO-IBM predicted 7.6% epilepsy prevalence (compared to 8.2% in the Cameroon study) and incidence of 317 cases/100,000 person-years (compared to 350). In hyperendemic areas, 25 years of biannual MDA (80% coverage) eliminated onchocerciasis-associated epilepsy (OAE) and protected untreated under-fives from its development. Strengthening onchocerciasis programmes, implementing alternative strategies, and evaluating treatment for under-fives and school-age children are crucial to prevent OAE in highly-endemic settings.
Identifiants
pubmed: 39054334
doi: 10.1038/s41467-024-50582-9
pii: 10.1038/s41467-024-50582-9
doi:
Substances chimiques
Ivermectin
70288-86-7
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6275Subventions
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S502388/1
Organisme : Bill & Melinda Gates Foundation
ID : INV-030046
Pays : United States
Organisme : Bill & Melinda Gates Foundation
ID : INV-030046
Pays : United States
Informations de copyright
© 2024. The Author(s).
Références
World Health Organization. Status of endemicity of onchocerciasis. https://www.who.int/data/gho/data/indicators/indicator-details/GHO/status-of-endemicity-of-onchocerciasis (2022).
Burnham, G. Onchocerciasis. Lancet 351, 1341–1346 (1998).
doi: 10.1016/S0140-6736(97)12450-3
pubmed: 9643811
GBD 2019 Diseases and Injuries Collaborators. Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet 396:1204–1222. Onchocerciasis—Level 3 cause. https://www.thelancet.com/pb-assets/Lancet/gbd/summaries/diseases/onchocerciasis.pdf (2020).
Boatin, B. A. & Richards, F. O. Jr. Control of onchocerciasis. Adv. Parasitol. 61, 349–394 (2006).
doi: 10.1016/S0065-308X(05)61009-3
pubmed: 16735169
Walker, M. et al. Density-dependent mortality of the human host in onchocerciasis: relationships between microfilarial load and excess mortality. PLoS Negl. Trop. Dis. 6, e1578 (2012).
doi: 10.1371/journal.pntd.0001578
pubmed: 22479660
pmcid: 3313942
Van Cutsem, G. et al. Case definitions for onchocerciasis-associated epilepsy and nodding syndrome: A focused review. Seizure 107, 132–135 (2023).
doi: 10.1016/j.seizure.2023.03.024
pubmed: 37023626
Pion, S. D. S. et al. Epilepsy in onchocerciasis endemic areas: systematic review and meta-analysis of population-based surveys. PLoS Negl. Trop. Dis. 3, e461 (2009).
doi: 10.1371/journal.pntd.0000461
pubmed: 19529767
pmcid: 2691484
Colebunders, R. et al. Onchocerca volvulus and epilepsy: a comprehensive review using the Bradford Hill criteria for causation. PLoS Negl. Trop. Dis. 15, e0008965 (2021).
doi: 10.1371/journal.pntd.0008965
pubmed: 33411705
pmcid: 7790236
Colebunders, R., Nelson Siewe, F. J. & Hotterbeekx, A. Onchocerciasis-associated epilepsy, an additional reason for strengthening onchocerciasis elimination programs. Trends Parasitol. 34, 208–216 (2018).
doi: 10.1016/j.pt.2017.11.009
pubmed: 29288080
Chesnais, C. B. et al. The temporal relationship between onchocerciasis and epilepsy: a population-based cohort study. Lancet Infect. Dis. 18, 1278–1286 (2018).
doi: 10.1016/S1473-3099(18)30425-0
pubmed: 30268645
Chesnais, C. B. et al. A second population-based cohort study in Cameroon confirms the temporal relationship between onchocerciasis and epilepsy. Open Forum Infect. Dis. 7, ofaa206 (2020).
doi: 10.1093/ofid/ofaa206
pubmed: 32587878
pmcid: 7304933
Turner, H. C., Walker, M., Churcher, T. S. & Basáñez, M. G. Modelling the impact of ivermectin on River Blindness and its burden of morbidity and mortality in African Savannah: EpiOncho projections. Parasit. Vectors 7, 241 (2014).
doi: 10.1186/1756-3305-7-241
pubmed: 24886747
pmcid: 4037555
Hamley, J. I. D., Milton, P., Walker, M. & Basáñez, M. G. Modelling exposure heterogeneity and density dependence in onchocerciasis using a novel individual-based transmission model, EPIONCHO-IBM: implications for elimination and data needs. PLoS Negl. Trop. Dis. 13, e0007557 (2019).
doi: 10.1371/journal.pntd.0007557
pubmed: 31805049
pmcid: 7006940
Pion, S. D. S., Clément, M. C. A. & Boussinesq, M. Impact of four years of large-scale ivermectin treatment with low therapeutic coverage on the transmission of Onchocerca volvulus in the Mbam Valley focus, central Cameroon. Trans. R. Soc. Trop. Med Hyg. 98, 520–528 (2004).
doi: 10.1016/j.trstmh.2003.11.010
pubmed: 15251400
Barbazan, P., Escaffre, H., Mbentengam, R. & Boussinesq, M. Etude entomologique sur la transmission de l’onchocercose dans une zone de transition forêt-savane du Cameroun. Bull. Soc. Pathol. Exot. 91, 178–182 (1998).
pubmed: 9642481
Boullé, C. et al. Impact of 19 years of mass drug administration with ivermectin on epilepsy burden in a hyperendemic onchocerciasis area in Cameroon. Parasit. Vectors 12, 114 (2019).
doi: 10.1186/s13071-019-3345-7
pubmed: 30890155
pmcid: 6423875
Colebunders, R. & Titulaer, M. J. Nodding syndrome: preventable and treatable. Sci. Transl. Med. 9, eaam8532 (2017).
doi: 10.1126/scitranslmed.aam8532
pubmed: 28202778
Ba-Diop, A. et al. Epidemiology, causes, and treatment of epilepsy in sub-Saharan Africa. Lancet Neurol. 13, 1029–1044 (2014).
doi: 10.1016/S1474-4422(14)70114-0
pubmed: 25231525
pmcid: 5497080
Kamga, G. R. et al. Still mesoendemic onchocerciasis in two Cameroonian community-directed treatment with ivermectin projects despite more than 15 years of mass treatment. Parasit. Vectors 9, 581 (2016).
doi: 10.1186/s13071-016-1868-8
pubmed: 27842567
pmcid: 5109673
Hendy, A. et al. Onchocerca volvulus transmission in the Mbam Valley of Cameroon following 16 years of annual community-directed treatment with ivermectin, and the description of a new cytotype of Simulium squamosum. Parasit. Vectors 14, 563 (2021).
doi: 10.1186/s13071-021-05072-y
pubmed: 34727965
pmcid: 8561987
Siewe Fodjo, J. N. et al. Slash and clear’ vector control for onchocerciasis elimination and epilepsy prevention: a protocol of a cluster randomised trial in Cameroonian villages. BMJ Open 11, e050341 (2021).
doi: 10.1136/bmjopen-2021-050341
pubmed: 34475178
pmcid: 8413955
Kipp, W., Burnham, G., Bamuhiiga, J. & Leichsenring, M. The Nakalanga syndrome in Kabarole District, Western Uganda. Am. J. Trop. Med. Hyg. 54, 80–83 (1996).
doi: 10.4269/ajtmh.1996.54.80
pubmed: 8651377
Fischer, P. et al. Parasitological and clinical characterization of Simulium neavei-transmitted onchocerciasis in western Uganda. Trop. Med. Parasitol. 44, 311–321 (1993).
pubmed: 8134773
Siewe, J. F. N. et al. Clinical presentations of onchocerciasis-associated epilepsy (OAE) in Cameroon. Epilepsy Behav. 90, 70–78 (2019).
doi: 10.1016/j.yebeh.2018.11.008
pubmed: 30513438
Boussinesq, M., Pion, S. D. S., Demanga-Ngangue & Kamgno, J. Relationship between onchocerciasis and epilepsy: a matched case-control study in the Mbam Valley, Republic of Cameroon. Trans. R. Soc. Trop. Med. Hyg. 96, 537–541 (2002).
doi: 10.1016/S0035-9203(02)90433-5
pubmed: 12474484
Dongmo, L. et al. Cysticercose et épilepsie: étude cas-témoins dans la Vallée du Mbam, Cameroun. Bull. Soc. Pathol. Exot. 97, 105–108 (2004).
pubmed: 15255351
Otabil, K. B. et al. Prevalence of epilepsy in the onchocerciasis endemic middle belt of Ghana after 27 years of mass drug administration with ivermectin. Infect. Dis. Poverty 12, 75 (2023).
doi: 10.1186/s40249-023-01117-9
pubmed: 37587500
pmcid: 10433588
Bhattacharyya, S. et al. Onchocerciasis-associated epilepsy in Maridi, South Sudan: modelling and exploring the impact of control measures against river blindness. PLoS Negl. Trop. Dis. 17, e0011320 (2023).
doi: 10.1371/journal.pntd.0011320
pubmed: 37235598
pmcid: 10249816
Routledge, I. et al. Modelling the impact of larviciding on the population dynamics and biting rates of Simulium damnosum (s.l.): implications for vector control as a complementary strategy for onchocerciasis elimination in Africa. Parasit. Vectors 11, 316 (2018).
doi: 10.1186/s13071-018-2864-y
pubmed: 29843770
pmcid: 5972405
Domche, A. et al. Significant reduction of blackfly densities in persistent onchocerciasis area following pilot implementation of an environment friendly approach (slash and clear). Sci. Rep. 14, 408 (2024).
doi: 10.1038/s41598-023-50747-4
pubmed: 38172522
pmcid: 10764779
Kura, K. et al. Can mass drug administration of moxidectin accelerate onchocerciasis elimination in Africa? Philos. Trans. R. Soc. Lond. B Biol. Sci. 378, 20220277 (2023).
doi: 10.1098/rstb.2022.0277
pubmed: 37598705
pmcid: 10440165
Medicines Development for Global Health. A pharmacokinetic and safety study of moxidectin to identify an optimal dose for treatment of children 4 to 11 years. US National Library of Medicine https://classic.clinicaltrials.gov/ct2/show/NCT03962062 (2022).
Colebunders, R. et al. Reducing onchocerciasis-associated morbidity in onchocerciasis-endemic foci with high ongoing transmission: a focus on the children. Int J. Infect. Dis. 116, 302–305 (2022).
doi: 10.1016/j.ijid.2022.01.042
pubmed: 35074518
pmcid: 8866381
World Health Organization. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021– 2030. Geneva: World Health Organization, https://www.who.int/publications/i/item/9789240010352 (2021).
R Core Team. R, Version 4.3.2. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2023).
Remme, J., Ba, O., Dadzie, K. Y. & Karam, M. 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 (1986).
pubmed: 3492300
pmcid: 2490951
Behrend, M. R. et al. NTD Modelling Consortium. Modelling for policy: the five principles of the Neglected Tropical Diseases Modelling Consortium. PLoS Negl. Trop. Dis. 14, e0008033 (2020).
doi: 10.1371/journal.pntd.0008033
pubmed: 32271755
pmcid: 7144973
Stapley J. N., Dixon M. A. GitHub repository: mrc-ide/EPIONCHO.IBM: v1.0.0, https://zenodo.org/doi/10.5281/zenodo.12570420 (2024).