How does onchocerciasis-related skin and eye disease in Africa depend on cumulative exposure to infection and mass treatment?

PLoS Negl Trop Dis. 2021 Jun 11;15(6):e0009489. doi: 10.1371/journal.pntd.0009489. eCollection 2021 Jun.

Abstract

Background: Onchocerciasis (river-blindness) in Africa is targeted for elimination through mass drug administration (MDA) with ivermectin. Onchocerciasis may cause various types of skin and eye disease. Predicting the impact of MDA on onchocercal morbidity is useful for future policy development. Here, we introduce a new disease module within the established ONCHOSIM model to predict trends over time in prevalence of onchocercal morbidity.

Methods: We developed novel generic model concepts for development of symptoms due to cumulative exposure to dead microfilariae, accommodating both reversible (acute) and irreversible (chronic) symptoms. The model was calibrated to reproduce pre-control age patterns and associations between prevalences of infection, eye disease, and various types of skin disease as observed in a large set of population-based studies. We then used the new disease module to predict the impact of MDA on morbidity prevalence over a 30-year time frame for various scenarios.

Results: ONCHOSIM reproduced observed age-patterns in disease and community-level associations between infection and disease reasonably well. For highly endemic settings with 30 years of annual MDA at 60% coverage, the model predicted a 70% to 89% reduction in prevalence of chronic morbidity. This relative decline was similar with higher MDA coverage and only somewhat higher for settings with lower pre-control endemicity. The decline in prevalence was lowest for mild depigmentation and visual impairment. The prevalence of acute clinical manifestations (severe itch, reactive skin disease) declined by 95% to 100% after 30 years of annual MDA, regardless of pre-control endemicity.

Conclusion: We present generic model concepts for predicting trends in acute and chronic symptoms due to history of exposure to parasitic worm infections, and apply this to onchocerciasis. Our predictions suggest that onchocercal morbidity, in particular chronic manifestations, will remain a public health concern in many epidemiological settings in Africa, even after 30 years of MDA.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adolescent
  • Adult
  • Africa / epidemiology
  • Animals
  • Anthelmintics / administration & dosage*
  • Child
  • Child, Preschool
  • Eye Diseases / drug therapy*
  • Eye Diseases / epidemiology
  • Eye Diseases / parasitology
  • Female
  • Humans
  • Ivermectin / administration & dosage*
  • Male
  • Mass Drug Administration
  • Middle Aged
  • Onchocerca / drug effects
  • Onchocerca / physiology
  • Onchocerciasis / drug therapy*
  • Onchocerciasis / epidemiology
  • Onchocerciasis / parasitology
  • Skin Diseases / drug therapy*
  • Skin Diseases / epidemiology
  • Skin Diseases / parasitology
  • Young Adult

Substances

  • Anthelmintics
  • Ivermectin

Grants and funding

NVSVM, WAS, BP, and LEC received funding (grant no. AID-OAA-G14-00010) from United States Agency for International Development (USAID, www.usaid.gov) through the Drugs for Neglected Diseases initiative (DNDi, www.dndi.org). The contents are the responsibility of the authors and do not necessarily reflect the views of USAID or the United States Government. WAS, SJdV, and LEC also gratefully acknowledge funding of the NTD Modelling Consortium(www.ntdmodelling.org) by the Bill & Melinda Gates Foundation (www.gatesfoundation.org) through grant OPP1184344. In addition, LEC was financially supported through an Innovational Research Incentives Scheme Veni by the Dutch Research Council (NWO, www.nwo.nl/en) via ZonMw (www.zonmw.nl/en, grant 016.Veni.178.023). The multi-country study on pre-control onchocercal skin disease by MM received financial support from the UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (TDR, tdr.who.int). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.