A pilot investigation of bovine schistosomiasis on Unguja Island, Zanzibar, raises a new concern for elimination of urogenital schistosomiasis

Abstract

Our pilot parasitological investigation of cattle, supplemented with molecular DNA characterisation of encountered schistosomes, sheds first light upon bovine schistosomiasis on Unguja Island, Zanzibar. During February 2024, a total of 99 cattle were examined. Of these, 47 were exported animals from the Tanzanian mainland, designated for slaughter at two governmental abattoirs (Kisakasaka and Muwanda), and 52 were free-grazing animals sampled from four grazing locations within the island's North and West-B regions. Upon visual inspection of 31 cattle carcasses at Kisakasaka for adult worms, the prevalence of bovine schistosomiasis was 51.6%; however, upon faecal miracidia hatching test (MHT) it was 80.6%. At Muwanda, only faecal MHT was used, finding a much lower prevalence of 12.5%. In free-grazing animals, the prevalence of bovine schistosomiasis by MHT was 0.0%. At Muwanda, the animal quarantine paddock was in disrepair, inclusive of a large pond now acting as a watering point. Here, numerous Bulinus forskalii sp. were found. Whilst no snails were observed to shed schistosome cercariae, molecular xenomonitoring did detect a pre-patent infection prevalence of 10.8%, with Schistosoma bovis firmly incriminated. Molecular DNA characterisation of adult schistosomes (n = 19) by real-time polymerase chain reaction (PCR) and high-resolution melt profiling, alongside DNA sequencing, also identified S. bovis, although two worms were putative S. bovis-S. mattheei hybrids. Atypical intrauterine eggs of S. bovis were noted upon microscopy of a worm pair. A broader screen of 92 miracidia confirmed S. bovis and three miracidia as S. bovis-S. mattheei hybrids. Contrasting with Pemba Island, Zanzibar, where autochthonous transmission of S. bovis can occur, bovine schistosomiasis on Unguja Island currently appears restricted to imported animals alone. However, the seminal detection of putative S. bovis-mattheei hybrids, alongside the current inadequate quarantine facilities at Muwanda, raises a new concern that such hybrid schistosomes may escape and enter the island's hinterland. Should this happen, surveillance and control of urogenital schistosomiasis on Unguja would be compromised and further complicated. We therefore strongly recommend immediate repair and improved maintenance of governmental animal quarantine facilities. Future epidemiological surveys of imported cattle are now well justified, not only to better understand the full repertoire of hybrid schistosomes present but also to develop appropriate mitigating interventions.

Keywords: Bulinus forskalii sp.; Schistosoma bovis; Schistosoma mattheei; Hybrids; Molecular xenomonitoring; One Health; Urogenital schistosomiasis.

Fig. 1

The outline area where this pilot investigation took place, with pertinent photographs of the quarantine areas of each abattoir and a typical Bulinus forskalii sp. snail encountered at Muwanda abattoir quarantine holding area. A A sketch map of the sampling locations: red circle 1—Muwanda abattoir, red circle 2—Kisakasaka abattoir, and the four blue dots, 1–4, where field grazing cattle faecal sampling took place, 1—Dole-Kianga, 2—Mgeni Haji/Kwamba, 3—Kidimni, and 4—Koani within the central region (shaded area) where Bulinus globosus can be found; B On-site photos of quarantine areas where cattle were held in each abattoir for 2–3 days before slaughter: Muwanda (top) and Kisakasaka (bottom). C A typical shell of B. forskalii sp. snail (shell scale bar: 2 mm) found in large numbers around the drinking pond within Muwanda quarantine paddock

Fig. 2

Characterisation of schistosomes by egg morphology and identification by DNA HRM typing. A Representative view (×100) of numerous intrauterine eggs within the worm’s oviduct (top image), with an example of the two distinctive morphotypes of intrauterine eggs—typical egg with prominent equatorial bulge and an atypical egg without equatorial bulge, more rhomboid in shape and slightly shorter in length, seen at ×400. From later DNA profiling, the atypical egg was likely a S. bovis-mattheei hybrid. B Scatter plot of mitochondrial DNA (mtDNA) and nuclear DNA (nDNA) HRM temperatures with expected species plot locations indicated with the green diamonds (and species names) and adult worm and miracidial blue circles. Red circles indicate samples that were selected for sequencing, red squares indicate samples that produced a usable sequence. The isolated red squares marked i and ii are adult worm profiles sent for DNA sequencing