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Archer, John (2024) Molecular epidemiology and a One Health appraisal of waterborne intestinal parasitic diseases giardiasis and intestinal schistosomiasis along the southern shoreline of Lake Malawi, Malawi, Thesis (Doctoral), Liverpool School of Tropical Medicine.
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J Archer thesis_POST_VIVA_CLEAN_FEB25.pdf - Accepted Version Restricted to Repository staff only until 2 July 2025. Download (6MB) |
Abstract
Background
Waterborne intestinal parasitic diseases giardiasis and intestinal schistosomiasis are likely highly co-endemic across many rural areas of lower- and middle-income countries (LMICs), including those in sub-Saharan Africa, where the provision of water, sanitation, and hygiene (WASH) infrastructure is inadequate. However, given the many challenges associated with accurately diagnosing these infections and monitoring their transmission, the true burden of these diseases in these areas is largely unknown. In addition, more work is
needed to better understand the pathogenic impact of co-infection with both giardiasis (caused by infection with the protozoan parasite Giardia duodenalis) and intestinal schistosomiasis (caused predominantly by the parasitic trematode Schistosoma mansoni) in co-endemic areas, requiring reliable and easy-to-use diagnostic and transmission monitoring tools.
Both giardiasis and intestinal schistosomiasis are known to be co-endemic along the southern shoreline of Lake Malawi, Mangochi District, Malawi. However, the true burden of these diseases in this area is not fully understood as only few studies assessing their prevalence and transmission have been carried out using unreliable diagnosis and transmission monitoring approaches. As such, here, we aimed to measure the prevalence of giardiasis and intestinal schistosomiasis in school-aged children attending four primary schools in this area using highly sensitive and specific molecular diagnostic tools. We then also aimed to compare and critically assess both routinely used and novel approaches used to diagnose these diseases in order to make recommendations towards what should be prioritised when developing future diagnostic tools.
In addition, we aimed to genotype all G. duodenalis infections to assemblage level in order to assess any associations between G. duodenalis infection status and intestinal pathology, as well as genotype S. mansoni infections to identify which previously defined S. mansoni mitochondrial cytochrome oxidase subunit 1 (cox1) lineage group(s) Mangochi District S. mansoni isolates were most closely related to. Any associations between infection with S. mansoni and intestinal pathology were also assessed, as were any associations between co-infection with both G. duodenalis and S. mansoni, and intestinal pathology. Furthermore, we also aimed to identify active intestinal schistosomiasis transmission foci along the southern shoreline of Lake Malawi through the malacological collection of Biomphalaria spp. freshwater snail intermediate hosts of S. mansoni and through the development, validation, and use of a novel, reliable, and high throughput molecular xenomonitoring PCR assay to screen collected Biomphalaria for S. mansoni infection.
Finally, using data generated here, and elsewhere, we aimed to critically appraise the feasibility of a One Health approach for the simultaneous surveillance and control of both giardiasis and intestinal schistosomiasis in rural areas of sub-Saharan Africa, considering key similarities and key differences between the epidemiology of both waterborne intestinal parasites and highlighting potential opportunities for integrated surveillance and control.
Principal findings
Both giardiasis and intestinal schistosomiasis were found to be highly prevalent in school-aged children situated along the southern shoreline of Lake Malawi, Mangochi District, Malawi when using highly sensitive and specific molecular diagnostic tools. Whilst point-of-care assays used to diagnose infection with G. duodenalis were found to be extremely reliable (when compared to molecular diagnostic approaches), point-of-care assays used to diagnose infection with S. mansoni were deemed unreliable (when compared to molecular diagnostic approaches), likely owing to low-intensity S. mansoni infections observed in study participants. As such, we make several recommendations towards what should be prioritised when developing future tools for diagnosing intestinal schistosomiasis in resource-poor endemic settings.
Of all identified G. duodenalis infections, 35% were identified as single G. duodenalis assemblage A infections, 32% were identified as single G. duodenalis assemblage B infections, and 33% were identified as mixed G. duodenalis assemblage A and B infections. Within this study cohort, there was a statistically significant positive association between single infection with G. duodenalis assemblage B and both self-reporting of abdominal (stomach) pain and self-reporting of loose stool (diarrhoea), but no identified association between single infection with G. duodenalis assemblage A and any form of intestinal pathology. In addition, there was a statistically significant positive association between mixed infection with both G. duodenalis assemblages A and B and self-reporting of abdominal (stomach) pain. Schistosoma mansoni miracidia recovered from faecal samples provided by study participants were closely related to two independent cox1 lineage groups, suggesting multiple recent introduction and colonisation events originating from surrounding east African countries. Furthermore, and interestingly, a high degree of Schistosoma haematobium DNA was detected in DNA isolated from faecal samples, motile S. haematobium miracidia were recovered from faecal samples, and S. haematobium eggs were identified in faecal samples during faecal-egg microscopy. Whilst co-infection with both giardiasis and intestinal schistosomiasis was identified in 14.1% of study participants, the pathogenic impact of co-infection with both intestinal parasites could not be determined here, likely owing to a limited sample size of study participants and low-intensity S. mansoni infections observed in study participants. In addition, through the development and use of a novel and high throughput S. mansoni species-specific molecular xenomonitoring PCR assay, we identified many active intestinal schistosomiasis transmission foci along the southern shoreline of Lake Malawi that had been missed by prior Biomphalaria cercarial shedding analyses.
Conclusions
Here, we demonstrate that giardiasis and intestinal schistosomiasis are highly co-endemic along the southern shoreline of Lake Malawi, Mangochi District, Malawi, and believe that this area is very likely representative of many areas across sub-Saharan Africa. Our findings also highlight the importance of highly sensitive and specific diagnostic and transmission monitoring tools capable of distinguishing between infecting G. duodenalis assemblages and Schistosoma species in (co)endemic areas. As such, using data generated here, and elsewhere, we critically appraised the feasibility of adopting a One Health approach for the simultaneous surveillance and control of giardiasis and intestinal schistosomiasis in co-endemic rural areas of LMICs and made key recommendations towards the effective and impactful implementation of this One Health approach. It is our belief that, through adopting this One Health approach and by integrating giardiasis surveillance and control activities into ongoing intestinal schistosomiasis control programmes, not only can the debilitating pathological impacts of giardiasis and intestinal schistosomiasis (co)infection be better understood, but a reduction in infections and concurrent reduction in disease-associated morbidities can also be achieved, significantly improving the health and wellbeing of those in endemic areas.
| Item Type: | Thesis (Doctoral) |
|---|---|
| Subjects: | QX Parasitology > QX 20 Research (General) QX Parasitology > Helminths. Annelida > QX 355 Schistosoma WC Communicable Diseases > Tropical and Parasitic Diseases > WC 698 Parasitic intestinal diseases (General) WC Communicable Diseases > Tropical and Parasitic Diseases > WC 810 Schistosomiasis |
| Faculty: Department: | Biological Sciences > Department of Tropical Disease Biology |
| Depositing User: | Lynn Roberts-Maloney |
| Date Deposited: | 02 Apr 2025 10:21 |
| Last Modified: | 02 Apr 2025 10:27 |
| URI: | https://archive.lstmed.ac.uk/id/eprint/26485 |
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