Diagnosis of helminths depends on worm fecundity and the distribution of parasites within hosts

Crellen, T. , Haswell, M., Sithithaworn, P., Sayasone, S., Odermatt, P., Lamberton, P. H.L. , Spencer, S. E.F. and Hollingsworth, T. D. (2023) Diagnosis of helminths depends on worm fecundity and the distribution of parasites within hosts. Proceedings of the Royal Society of London Series B: Biological Sciences, 290(1991), 20222. (doi: 10.1098/rspb.2022.2204) (PMID:36651047) (PMCID:PMC9845982)

Abstract

Helminth transmission and morbidity are dependent on the number of mature parasites within a host; however, observing adult worms is impossible for many natural infections. An outstanding challenge is therefore relating routine diagnostics, such as faecal egg counts, to the underlying worm burden. This relationship is complicated by density-dependent fecundity (egg output per worm reduces due to crowding at high burdens) and the skewed distribution of parasites (majority of helminths aggregated in a small fraction of hosts). We address these questions for the carcinogenic liver fluke Opisthorchis viverrini, which infects approximately 10 million people across Southeast Asia, by analysing five epidemiological surveys (n = 641) where adult flukes were recovered. Using a mechanistic model, we show that parasite fecundity varies between populations, with surveys from Thailand and Laos demonstrating distinct patterns of egg output and density-dependence. As the probability of observing faecal eggs increases with the number of mature parasites within a host, we quantify diagnostic sensitivity as a function of the worm burden and find that greater than 50% of cases are misdiagnosed as false negative in communities close to elimination. Finally, we demonstrate that the relationship between observed prevalence from routine diagnostics and true prevalence is nonlinear and strongly influenced by parasite aggregation.

• Item Type: Articles
• Additional Information: This research was funded in whole, or in part, by the Wellcome Trust (grant no. 215919/B/19/Z).
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Crellen, Dr Thomas and Lamberton, Professor Poppy

Creator Roles

Crellen, T.: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Software, Validation, Visualization, Writing – original draft, Writing – review and editing
Lamberton, P.: Supervision, Writing – review and editing

• Authors: Crellen, T., Haswell, M., Sithithaworn, P., Sayasone, S., Odermatt, P., Lamberton, P. H.L., Spencer, S. E.F., and Hollingsworth, T. D.
• College/School: College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
• Journal Name: Proceedings of the Royal Society of London Series B: Biological Sciences
• Publisher: The Royal Society
• ISSN: 0962-8452
• ISSN (Online): 1471-2954
• Published Online: 18 January 2023
• Copyright Holders: Copyright © 2023 The Authors
• First Published: First published in Proceedings of the Royal Society of London Series B: Biological Sciences 290(1991):20222204
• Publisher Policy: Reproduced under a Creative Commons License
• Data DOI: 10.5061/dryad.q83bk3jn6

Project Code	Award No	Project Name	Principal Investigator	Funder's Name	Funder Ref	Lead Dept
318104		Crellen WTSHD Fellowship	Thomas Crellen	Wellcome Trust (WELLCOTR)	215919/B/19/Z	Institute of Biodiversity, Animal Health and Comparative Medicine