Identification of tungiasis infection hotspots with a low-cost, high-throughput method for extracting Tunga penetrans (Siphonaptera) off-host stages from soil samples-An observational study.


Journal

PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488

Informations de publication

Date de publication:
20 Feb 2024
Historique:
received: 18 08 2023
accepted: 02 02 2024
medline: 20 2 2024
pubmed: 20 2 2024
entrez: 20 2 2024
Statut: aheadofprint

Résumé

The sand flea, Tunga penetrans, is the cause of a severely neglected parasitic skin disease (tungiasis) in the tropics and has received little attention from entomologists to understand its transmission ecology. Like all fleas, T. penetrans has environmental off-host stages presenting a constant source of reinfection. We adapted the Berlese-Tullgren funnel method using heat from light bulbs to extract off-host stages from soil samples to identify the major development sites within rural households in Kenya and Uganda. Simple, low-cost units of multiple funnels were designed to allow the extraction of >60 soil samples in parallel. We calibrated the method by investigating the impact of different bulb wattage and extraction time on resulting abundance and quality of off-host stages. A cross-sectional field survey was conducted in 49 tungiasis affected households. A total of 238 soil samples from indoor and outdoor living spaces were collected and extracted. Associations between environmental factors, household member infection status and the presence and abundance of off-host stages in the soil samples were explored using generalized models. The impact of heat (bulb wattage) and time (hours) on the efficiency of extraction was demonstrated and, through a stepwise approach, standard operating conditions defined that consistently resulted in the recovery of 75% (95% CI 63-85%) of all present off-host stages from any given soil sample. To extract off-host stages alive, potentially for consecutive laboratory bioassays, a low wattage (15-25 W) and short extraction time (4 h) will be required. The odds of finding off-host stages in indoor samples were 3.7-fold higher than in outdoor samples (95% CI 1.8-7.7). For every one larva outdoors, four (95% CI 1.3-12.7) larvae were found indoors. We collected 67% of all off-host specimen from indoor sleeping locations and the presence of off-host stages in these locations was strongly associated with an infected person sleeping in the room (OR 10.5 95% CI 3.6-28.4). The indoor sleeping areas are the transmission hotspots for tungiasis in rural homes in Kenya and Uganda and can be targeted for disease control and prevention measures. The soil extraction methods can be used as a simple tool for monitoring direct impact of such interventions.

Sections du résumé

BACKGROUND BACKGROUND
The sand flea, Tunga penetrans, is the cause of a severely neglected parasitic skin disease (tungiasis) in the tropics and has received little attention from entomologists to understand its transmission ecology. Like all fleas, T. penetrans has environmental off-host stages presenting a constant source of reinfection. We adapted the Berlese-Tullgren funnel method using heat from light bulbs to extract off-host stages from soil samples to identify the major development sites within rural households in Kenya and Uganda.
METHODS AND FINDINGS RESULTS
Simple, low-cost units of multiple funnels were designed to allow the extraction of >60 soil samples in parallel. We calibrated the method by investigating the impact of different bulb wattage and extraction time on resulting abundance and quality of off-host stages. A cross-sectional field survey was conducted in 49 tungiasis affected households. A total of 238 soil samples from indoor and outdoor living spaces were collected and extracted. Associations between environmental factors, household member infection status and the presence and abundance of off-host stages in the soil samples were explored using generalized models. The impact of heat (bulb wattage) and time (hours) on the efficiency of extraction was demonstrated and, through a stepwise approach, standard operating conditions defined that consistently resulted in the recovery of 75% (95% CI 63-85%) of all present off-host stages from any given soil sample. To extract off-host stages alive, potentially for consecutive laboratory bioassays, a low wattage (15-25 W) and short extraction time (4 h) will be required. The odds of finding off-host stages in indoor samples were 3.7-fold higher than in outdoor samples (95% CI 1.8-7.7). For every one larva outdoors, four (95% CI 1.3-12.7) larvae were found indoors. We collected 67% of all off-host specimen from indoor sleeping locations and the presence of off-host stages in these locations was strongly associated with an infected person sleeping in the room (OR 10.5 95% CI 3.6-28.4).
CONCLUSION CONCLUSIONS
The indoor sleeping areas are the transmission hotspots for tungiasis in rural homes in Kenya and Uganda and can be targeted for disease control and prevention measures. The soil extraction methods can be used as a simple tool for monitoring direct impact of such interventions.

Identifiants

pubmed: 38377105
doi: 10.1371/journal.pntd.0011601
pii: PNTD-D-23-01051
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0011601

Informations de copyright

Copyright: © 2024 Matharu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors declare that they have no competing interests.

Auteurs

Abneel K Matharu (AK)

Freie Universität Berlin, Institute for Parasitology and Tropical Veterinary Medicine, Berlin, Germany.
International Centre of Insect Physiology and Ecology, Human Health Theme, Nairobi, Kenya.

Paul Ouma (P)

International Centre of Insect Physiology and Ecology, Human Health Theme, Nairobi, Kenya.

Margaret M Njoroge (MM)

International Centre of Insect Physiology and Ecology, Human Health Theme, Nairobi, Kenya.

Billy L Amugune (BL)

International Centre of Insect Physiology and Ecology, Human Health Theme, Nairobi, Kenya.

Ayako Hyuga (A)

International Centre of Insect Physiology and Ecology, Human Health Theme, Nairobi, Kenya.

Francis Mutebi (F)

Makerere University, College of Veterinary Medicine, Animal Resources and Biosecurity, Kampala, Uganda.

Jürgen Krücken (J)

Freie Universität Berlin, Institute for Parasitology and Tropical Veterinary Medicine, Berlin, Germany.

Hermann Feldmeier (H)

Charité-Universitätsmedizin Berlin, Institute of Microbiology, Infectious Diseases and Immunology, Berlin, Germany.

Lynne Elson (L)

KEMRI-Wellcome Trust Research Programme, Centre for Geographic Medicine Research (Coast), Kilifi, Kenya.
University of Oxford, Centre for Tropical Medicine and Global Health, Oxford, United Kingdom.

Ulrike Fillinger (U)

International Centre of Insect Physiology and Ecology, Human Health Theme, Nairobi, Kenya.

Classifications MeSH