Molecular epidemiology and population genetics of Schistosoma mansoni infecting school-aged children situated along the southern shoreline of Lake Malawi, Malawi.


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:
Oct 2024
Historique:
received: 25 04 2024
accepted: 02 09 2024
medline: 7 10 2024
pubmed: 7 10 2024
entrez: 7 10 2024
Statut: epublish

Résumé

In areas of low disease endemicity, highly sensitive diagnostic tools to identify, diagnose, and monitor intestinal schistosomiasis transmission are needed to reliably measure the burden and risk of infection. Here, we used highly sensitive molecular diagnostic methods to investigate Schistosoma mansoni prevalence and transmission along the southern shoreline of Lake Malawi, five years post-disease outbreak. Faecal and urine samples were provided by school-aged children situated along the southern shoreline of Lake Malawi. Kato-Katz faecal-egg microscopy and point-of-care circulating cathodic antigen (POC-CCA) rapid diagnostic tests were then performed to diagnose infection with S. mansoni. Urine-egg microscopy was also used to diagnose infection with Schistosoma haematobium. In addition, Schistosoma miracidia were isolated from faecal material using a standard miracidium hatching technique. A two-step real-time PCR approach was then used to diagnose infection with S. mansoni using DNA isolated from faecal samples. Furthermore, isolated miracidia were genotyped to species level through PCR and Sanger sequencing. Phylogenetic analyses were then carried out to identify which previously defined S. mansoni cox1 lineage group S. mansoni miracidia were most closely related to. The measured prevalence of S. mansoni infection varied considerably depending on which diagnostic assay was used. When compared to real-time PCR, faecal-egg microscopy had a sensitivity of 9% and a specificity of 100%. When POC-CCA 'trace' results were considered positive, POC-CCA had a sensitivity of 73% and a specificity of 81% when compared to real-time PCR. However, when considered negative, POC-CCA sensitivity was reduced to 56%, whereas specificity was increased to 90%. In addition, a high degree of S. haematobium DNA was detected in DNA isolated from faecal samples and motile S. haematobium miracidia were recovered from faecal samples. Schistosoma mansoni miracidia were closely related to two independent cox1 lineage groups, suggesting multiple recent introduction and colonisation events originating from surrounding east African countries. Intestinal schistosomiasis is now highly prevalent along the southern shoreline of Lake Malawi just five years post-disease outbreak. In addition, a high prevalence of urogenital schistosomiasis persists. The revision of ongoing schistosomiasis control programmes in this area is therefore recommended. Our study also highlights the need for reliable diagnostic assays capable of distinguishing between Schistosoma species in multispecies co-endemic areas.

Sections du résumé

BACKGROUND BACKGROUND
In areas of low disease endemicity, highly sensitive diagnostic tools to identify, diagnose, and monitor intestinal schistosomiasis transmission are needed to reliably measure the burden and risk of infection. Here, we used highly sensitive molecular diagnostic methods to investigate Schistosoma mansoni prevalence and transmission along the southern shoreline of Lake Malawi, five years post-disease outbreak.
METHODOLOGY AND PRINCIPAL FINDINGS RESULTS
Faecal and urine samples were provided by school-aged children situated along the southern shoreline of Lake Malawi. Kato-Katz faecal-egg microscopy and point-of-care circulating cathodic antigen (POC-CCA) rapid diagnostic tests were then performed to diagnose infection with S. mansoni. Urine-egg microscopy was also used to diagnose infection with Schistosoma haematobium. In addition, Schistosoma miracidia were isolated from faecal material using a standard miracidium hatching technique. A two-step real-time PCR approach was then used to diagnose infection with S. mansoni using DNA isolated from faecal samples. Furthermore, isolated miracidia were genotyped to species level through PCR and Sanger sequencing. Phylogenetic analyses were then carried out to identify which previously defined S. mansoni cox1 lineage group S. mansoni miracidia were most closely related to. The measured prevalence of S. mansoni infection varied considerably depending on which diagnostic assay was used. When compared to real-time PCR, faecal-egg microscopy had a sensitivity of 9% and a specificity of 100%. When POC-CCA 'trace' results were considered positive, POC-CCA had a sensitivity of 73% and a specificity of 81% when compared to real-time PCR. However, when considered negative, POC-CCA sensitivity was reduced to 56%, whereas specificity was increased to 90%. In addition, a high degree of S. haematobium DNA was detected in DNA isolated from faecal samples and motile S. haematobium miracidia were recovered from faecal samples. Schistosoma mansoni miracidia were closely related to two independent cox1 lineage groups, suggesting multiple recent introduction and colonisation events originating from surrounding east African countries.
CONCLUSIONS AND SIGNIFICANCE CONCLUSIONS
Intestinal schistosomiasis is now highly prevalent along the southern shoreline of Lake Malawi just five years post-disease outbreak. In addition, a high prevalence of urogenital schistosomiasis persists. The revision of ongoing schistosomiasis control programmes in this area is therefore recommended. Our study also highlights the need for reliable diagnostic assays capable of distinguishing between Schistosoma species in multispecies co-endemic areas.

Identifiants

pubmed: 39374309
doi: 10.1371/journal.pntd.0012504
pii: PNTD-D-24-00602
doi:

Substances chimiques

DNA, Helminth 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0012504

Informations de copyright

Copyright: © 2024 Archer 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 have declared that no competing interests exist.

Auteurs

John Archer (J)

Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, Cromwell Road, London, United Kingdom.

Lucas J Cunningham (LJ)

Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.

Alexandra Juhász (A)

Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.
Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary.

Sam Jones (S)

Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.

Angus M O'Ferrall (AM)

Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.

Sarah Rollason (S)

School of Biosciences, University of Cardiff, Cardiff, United Kingdom.

Bright Mainga (B)

Laboratory Department, Mangochi District Hospital, Mangochi, Malawi.

Priscilla Chammudzi (P)

Malawi-Liverpool-Wellcome Trust Clinical Research Programme, Queen Elizabeth Central Hospital, Blantyre, Malawi.
Department of Pathology, School of Medicine and Oral Health, Kamuzu University of Health Sciences (KUHeS), Blantyre, Malawi.

Donales R Kapira (DR)

Malawi-Liverpool-Wellcome Trust Clinical Research Programme, Queen Elizabeth Central Hospital, Blantyre, Malawi.
Department of Pathology, School of Medicine and Oral Health, Kamuzu University of Health Sciences (KUHeS), Blantyre, Malawi.

David Lally (D)

Malawi-Liverpool-Wellcome Trust Clinical Research Programme, Queen Elizabeth Central Hospital, Blantyre, Malawi.
Department of Pathology, School of Medicine and Oral Health, Kamuzu University of Health Sciences (KUHeS), Blantyre, Malawi.

Gladys Namacha (G)

Malawi-Liverpool-Wellcome Trust Clinical Research Programme, Queen Elizabeth Central Hospital, Blantyre, Malawi.
Department of Pathology, School of Medicine and Oral Health, Kamuzu University of Health Sciences (KUHeS), Blantyre, Malawi.

Peter Makaula (P)

Malawi-Liverpool-Wellcome Trust Clinical Research Programme, Queen Elizabeth Central Hospital, Blantyre, Malawi.

James E LaCourse (JE)

Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.

Sekeleghe A Kayuni (SA)

Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.
Malawi-Liverpool-Wellcome Trust Clinical Research Programme, Queen Elizabeth Central Hospital, Blantyre, Malawi.
Department of Pathology, School of Medicine and Oral Health, Kamuzu University of Health Sciences (KUHeS), Blantyre, Malawi.

Bonnie L Webster (BL)

Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, Cromwell Road, London, United Kingdom.

Janelisa Musaya (J)

Malawi-Liverpool-Wellcome Trust Clinical Research Programme, Queen Elizabeth Central Hospital, Blantyre, Malawi.
Department of Pathology, School of Medicine and Oral Health, Kamuzu University of Health Sciences (KUHeS), Blantyre, Malawi.

J Russell Stothard (JR)

Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.

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Classifications MeSH