Impact of human movement between hypo- and hyperendemic areas on sustainability of elimination of Onchocerca volvulus transmission

medRxiv (Cold Spring Harbor Laboratory)(2023)

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摘要
Background Onchocerciasis is a vector-borne disease caused by the filarial nematode Onchocerca volvulus . Endemic countries target elimination of parasite transmission using primarily annual ivermectin mass administration. Elimination is particularly challenging in sub-Saharan Africa, where there are large contiguous areas with varying levels of endemicity and intervention history. We examined one challenge to elimination that has received little attention to date: movement of people between areas. Methodology/Principal Findings We extended one of the commonly used onchocerciasis transmission models, EPIONCHO, to allow modelling the effect of movement of people and/or flies between areas (“patches”). We explored the impact of humans travelling between a hypoendemic area (i.e., with low vector biting rates) with no history of interventions and a hyperendemic area (high vector biting rates) that stopped intervention (ivermectin mass administration) after infection prevalence decreased below 1.4%. Our results suggest that human travel in either direction will accelerate recrudescence in the hyperendemic area to pre-intervention levels, relative to recrudescence without travel, and can reduce the annual biting rate required for parasite transmission within hypoendemic areas. Conclusions/Significance Our results emphasize the importance of decisions on which hypoendemic areas to include in interventions and suggest that transmission mediated by human movement needs to be considered when planning (a) the geographic areas and sampling density for evaluations for decisions on when and where to stop interventions, (b) where, how often, and for how long to conduct post-intervention surveillance for verification of elimination of transmission and (c) where and how frequently to conduct post-elimination surveillance. Given the cost implications of stopping interventions too early or later than necessary, we encourage the development of models such as the one presented here for quantitating the impact of human and vector movement between areas on the risk and timeframe of recrudescence after interventions are stopped to inform economic analyses. Author summary Onchocerciasis is an infectious parasitic disease that causes significant morbidity, from incessant skin itching to blindness. Onchocerciasis has also been implicated as the cause of high epilepsy rates. Efforts are underway to eliminate the parasite. Mathematical models for parasite transmission between humans via blackflies can be used to explore how interventions (e.g., mass drug administration or blackfly control) impact the percentage of people infected (infection prevalence). We extended a commonly used model to explore how people travelling between areas that differ in blackfly abundance, infection prevalence, and past interventions affects infection prevalence. We found that people travelling between an area with few blackflies (hypoendemic), low infection prevalence, and no interventions and an area with many blackflies (hyperendemic) but very low infection prevalence thanks to many years of mass drug administration which was then stopped will accelerate the increase in infection prevalence in the hyperendemic area compared to a situation where no people travel between these areas. This means that strategies for onchocerciasis elimination need to consider the effect of humans travelling. ### Competing Interest Statement ACK is staff of TDR which provided funding for this work. ### Funding Statement This work was supported by funding from UNICEF/UNDP/World Bank/World Health Organization Special Programme for Research and Training in Tropical Diseases (TDR; ) to WNG (B80149, B80153, and B80296), and from an NHMRC (PRISM Centre of Research Excellence, GNT 1078068) (prism.edu.au) grant to KM and SMH. JMcV is supported by an NHMRC Principal Research Fellowship (GNT1117140). The funders had no role in study design, data collection and analysis. TDR, via co-author ACK, had a role in the preparation of the manuscript and the decision to publish. ### Author Declarations I confirm all relevant ethical guidelines have been followed, and any necessary IRB and/or ethics committee approvals have been obtained. Yes I confirm that all necessary patient/participant consent has been obtained and the appropriate institutional forms have been archived, and that any patient/participant/sample identifiers included were not known to anyone (e.g., hospital staff, patients or participants themselves) outside the research group so cannot be used to identify individuals. Yes I understand that all clinical trials and any other prospective interventional studies must be registered with an ICMJE-approved registry, such as ClinicalTrials.gov. I confirm that any such study reported in the manuscript has been registered and the trial registration ID is provided (note: if posting a prospective study registered retrospectively, please provide a statement in the trial ID field explaining why the study was not registered in advance). Yes I have followed all appropriate research reporting guidelines and uploaded the relevant EQUATOR Network research reporting checklist(s) and other pertinent material as supplementary files, if applicable. Yes The code for the model is available through GitHub. [https://github.com/shedtke/Onchocerciasis\_patch\_model][1] [1]: https://github.com/shedtke/Onchocerciasis_patch_model
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hyperendemic areas,human movement
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