Molecular and phylogenetic insights into the novel Brugia sp. in Sri Lanka with new evidence for zoonotic transmission

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Abstract

The World Health Organization (WHO) validated Sri Lanka had eliminated lymphatic filariasis as a public health problem in 2016, the second country in Southeast Asia to attain this status. However, post-validation surveillance has identified sporadic cases of brugian filariasis. The reemergence of Brugia malayi infections in Sri Lanka warrants urgent investigations. Recent studies have shown that the parasite responsible for the reemergence is a novel zoonotic Brugia sp. maintained among dogs that is closely related but distinct to the human-infecting B. malayi species. The current study employed morphological and morphometric assessments, revealing that this novel zoonotic Brugia sp. is within the B. malayi morphological range. Molecular characterization of three genomic regions, the nuclear genomic region SLXI , the non-coding region HhaI, and the mitochondrial genomic region COXI confirmed it as a genetic variant more closely related to B. malayi than to B. pahangi . Phylogenetic analysis further indicated it as a distinct genomic variant, closely related to a B. malayi -like parasite reported from India. Notably, that same parasite was identified in infected humans, animals, and potential vector mosquitoes. This, together with the detection of both human and animal blood within the same brugian infective mosquitoes, and delineating the canine origin of the parasites in human infections, provides compelling evidence supporting zoonotic transmission of this parasite. To our knowledge, this is the first report demonstrating the presence of the same brugian parasite in humans, domestic animals, and potentially infective mosquitoes in Sri Lanka, supported by multi-genomic evidence. The recent identification of multiple potential mosquito vector species suggests that this parasite may have undergone adaptive changes, facilitating its ability to overcome the species barrier. These findings substantiate the long-held hypothesis of zoonotic transmission of the reemerged brugian parasite, highlighting significant implications for ongoing surveillance and control strategies.

Author Summary

Brugian filariasis was eradicated from Sri Lanka in 1969 but has reemerged. The parasite driving this reemergence remains unclear, but recently, a novel, potentially zoonotic Brugia sp. has been identified. The current study morphologically and molecularly characterized this human brugian parasite. Morphologically, the parasite was identified as Brugia sp., with body measurements corresponding to the size range of previously reported Brugia malayi . Molecular analysis revealed higher similarity to B. malayi than to B. pahangi . Phylogenetic analysis revealed close similarity to another novel B. malayi -like parasite reported from India. Analysis of brugian parasites across humans, animals, and mosquitoes identified the same brugian parasite within humans, cats, dogs, and mosquitoes. Additionally, blood meal analysis of potentially infective mosquitoes further supported zoonotic transmission of the disease. These potential vector mosquitoes breed in different sites, and their biting and resting behaviors also vary. As a result, conventional vector control methods are often ineffective. In addition, the presence of animal reservoir species (cats and dogs) has contributed to active transmission of the parasite among suburban and rural human populations. Therefore, reemergence of a genetic variant brugian parasite and zoonotic transmission is a concern for health authorities in terms of surveillance and planning new control strategies.

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