Gastrointestinal parasites in captive olive baboons in a UK safari park.

From the safety inside vehicles, Knowsley Safari offers visitors a close-up encounter with captive olive baboons. As exiting vehicles may be contaminated with baboon stool, a comprehensive coprological inspection was conducted to address public health concerns. Baboon stools were obtained from vehicles, and sleeping areas, inclusive of video analysis of baboon­vehicle interactions. A purposely selected 4-day sampling period enabled comparative inspections of 2662 vehicles, with a total of 669 baboon stools examined (371 from vehicles and 298 from sleeping areas). As informed by our pilot study, front-line diagnostic methods were: QUIK-CHEK rapid diagnostic test (RDT) (Giardia and Cryptosporidium), Kato­Katz coproscopy (Trichuris) and charcoal culture (Strongyloides). Some 13.9% of vehicles were contaminated with baboon stool. Prevalence of giardiasis was 37.4% while cryptosporidiosis was <0.01%, however, an absence of faecal cysts by quality control coproscopy, alongside lower than the expected levels of Giardia-specific DNA, judged RDT results as misleading, grossly overestimating prevalence. Prevalence of trichuriasis was 48.0% and strongyloidiasis was 13.7%, a first report of Strongyloides fuelleborni in UK. We advise regular blanket administration(s) of anthelminthics to the colony, exploring pour-on formulations, thereafter, smaller-scale indicator surveys would be adequate.

Machine learning-based analyses support the existence of species complexes for Strongyloides fuelleborni and Strongyloides stercoralis.

Human strongyloidiasis is a serious disease mostly attributable to Strongyloides stercoralis and to a lesser extent Strongyloides fuelleborni, a parasite mainly of non-human primates. The role of animals as reservoirs of human-infecting Strongyloides is ill-defined, and whether dogs are a source of human infection is debated. Published multi-locus sequence typing (MLST) studies attempt to elucidate relationships between Strongyloides genotypes, hosts, and distributions, but typically examine relatively few worms, making it difficult to identify population-level trends. Combining MLST data from multiple studies is often impractical because they examine different combinations of loci, eliminating phylogeny as a means of examining these data collectively unless hundreds of specimens are excluded. A recently-described machine learning approach that facilitates clustering of MLST data may offer a solution, even for datasets that include specimens sequenced at different combinations of loci. By clustering various MLST datasets as one using this procedure, we sought to uncover associations among genotype, geography, and hosts that remained elusive when examining datasets individually. Multiple datasets comprising hundreds of S. stercoralis and S. fuelleborni individuals were combined and clustered. Our results suggest that the commonly proposed 'two lineage' population structure of S. stercoralis (where lineage A infects humans and dogs, lineage B only dogs) is an over-simplification. Instead, S. stercoralis seemingly represents a species complex, including two distinct populations over-represented in dogs, and other populations vastly more common in humans. A distinction between African and Asian S. fuelleborni is also supported here, emphasizing the need for further resolving these taxonomic relationships through modern investigations.

First molecular identification of Strongyloides fuelleborni in long-tailed macaques in Thailand and Lao People's Democratic Republic reveals considerable genetic diversity.

Strongyloides fuelleborni is a soil-transmitted nematode parasite of non-human primates. The worm is prevalent also in human populations in Africa and South-East Asia. In this study, we amplified and sequenced a portion of the 18S ribosomal RNA gene (rRNA) and of the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene of Strongyloides adult males recovered from faecal samples from long-tailed macaques (Macaca fascicularis) in Thailand and Lao PDR. The prevalence in Thailand was 31.1% (55/177) and in Lao PDR it was 62.1% (41/66), with an overall prevalence of 39.5% (96/243). All 18S rRNA sequences that we obtained (n = 96) showed 100% identity with published S. fuelleborni sequences. The 96 cox1 sequences that we obtained represented 32 new haplotypes. When included with the 17 previously known haplotypes from S. fuelleborni, the cox1 sequences fell into four clusters, which had clear geographical structure. This is the first molecular confirmation of S. fuelleborni in long-tailed macaques in Thailand and Lao PDR. Clearly, awareness needs to be raised of the zoonotic potential of S. fuelleborni. A monitoring programme should be organized, taking into account the role of reservoir hosts (i.e. monkeys) in the natural background of human strongyloidiasis caused by S. fuelleborni.

First molecular identification and genetic diversity of Strongyloides stercoralis and Strongyloides fuelleborni in human communities having contact with long-tailed macaques in Thailand.

The parasitic nematodes, Strongyloides stercoralis and Strongyloides fuelleborni, can infect humans and non-human primates. We amplified and sequenced a portion of the 18S ribosomal RNA gene (rRNA) and of the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene of Strongyloides from humans in the study area in Thailand, where people have frequent contact with long-tailed macaques. Fresh stool samples were obtained from 213 people and were examined using the agar plate culture method. The overall prevalence of Strongyloides infection was 8.92% (19/213). From a total of 19 worms (one per infected person), 18 adult males had 18S rRNA sequences identical with that of S. stercoralis and one adult female had a sequence almost identical with that of S. fuelleborni. A median-joining network of cox1 sequences revealed nine new haplotypes from S. stercoralis, and an overall haplotype diversity (Hd) of 0.9309. The single haplotype of S. fuelleborni was also new and contributed to an overall haplotype diversity for that species of 0.9842. This is the first molecular identification of S. stercoralis and S. fuelleborni in a human community having contact with long-tailed macaques in Thailand. It is also the first report of S. fuelleborni infecting a human in Thailand.

Genetic characterization of Strongyloides fuelleborni infecting free-roaming African vervets (Chlorocebus aethiops sabaeus) on the Caribbean island of St. Kitts.

Human strongyloidiasis is an important neglected tropical disease primarily caused by the nematode Strongyloides stercoralis, and to a lesser extent Strongyloides fuelleborni which mainly infects non-human primates. Zoonotic sources of infection have important implications for control and prevention of morbidity and mortality caused by strongyloidiasis. Recent molecular evidence suggests that for S. fuelleborni, primate host specificity is variable among genotypes across the Old World, and consequently that these types likely vary in their capacity for human spillover infections. Populations of free-roaming vervet monkeys (Chlorocebus aethiops sabaeus), introduced to the Caribbean Island of Staint Kitts from Africa, live in close contact with humans, and concern has arisen regarding their potential to serve as reservoirs of zoonotic infections. In this study, we sought to determine the genotypes of S. fuelleborni infecting St. Kitts vervets to explore whether they are potential reservoirs for human-infecting S. fuelleborni types. Fecal specimens were collected from St. Kitts vervets and S. fuelleborni infections were confirmed microscopically and by PCR. Strongyloides fuelleborni genotypes were determined from positive fecal specimens using an Illumina amplicon sequencing-based genotyping approach targeting the mitochondrial cox1 locus and 18S rDNA hypervariable regions I and IV of Strongyloides species. Phylogenetic analysis of resultant genotypes supported that S. fuelleborni from St. Kitts vervets is of an exclusively African variety, falling within the same monophyletic group as an isolate which has been detected previously in a naturally infected human from Guinea-Bissau. This observation highlights that St. Kitts vervets may serve as potential reservoirs for zoonotic S. fuelleborni infection, which warrants further exploration.

Population genetics study of Strongyloides fuelleborni and phylogenetic considerations on primate-infecting species of Strongyloides based on their mitochondrial genome sequences.

Strongyloides is a genus of parasitic nematodes of vertebrates comprising approximately 50 documented species, each with various host ranges. Among these, three species (S. stercoralis, S. fuelleborni, and S. cebus) are known to infect primate hosts. S. fuelleborni typically infects non-human primates in the Old World. To complement the existing information on the global genetic structure of this species, we conducted a genotyping study of S. fuelleborni samples collected from rhesus macaques in Myanmar, Japanese macaques in Japan, and some zoo-kept primates. This study identified a novel haplotype group in isolates from the Myanmar rhesus macaques. Subsequently, we obtained the complete or nearly complete mitochondrial genome sequences of S. fuelleborni, S. cebus (Strongyloides of New World monkeys), and S. vituli (Strongyloides of cattle). Phylogenetic analysis based on concatenated mitochondrial protein sequences of various Strongyloides species indicated a close relationship between S. fuelleborni, S. vituli and S. papillosus (Strongyloides in sheep and cattle). S. cebus is quite distantly related to both S. fuelleborni and S. stercoralis, which led to the hypothesis that the three primate Strongyloides species evolved independently as parasites of primates.

Molecular identification of Oesophagostomum and Trichuris eggs isolated from wild Japanese macaques.

Natural habitat fragmentation and reducing habitat quality have resulted in an increased appearance of Japanese macaques, Macaca fuscata (Gray, 1870), in suburban areas in Japan. To investigate the risk of zoonotic infections, a coprological survey of helminth eggs passed by wild Japanese macaques was carried out in 2009 and 2010 in Shiga Prefecture, Japan. Microscopic examination found helminth eggs in high prevalence, and nucleotide sequencing of DNA extracted from the eggs identified Oesophagostomum cf. aculeatum and Trichuris trichiura. A fecal culture also detected infective larvae of Strongyloides fuelleborni. These zoonotic nematodes pose a potential health issue to local people in areas frequented by Japanese macaques.

HTLV-I and Strongyloides in Australia: The worm lurking beneath.

Strongyloidiasis and HTLV-I (human T-lymphotropic virus-1) are important infections that are endemic in many countries around the world with an estimated 370 million infected with Strongyloides stercoralis alone, and 5-10 million with HTVL-I. Co-infections with these pathogens are associated with significant morbidity and can be fatal. HTLV-I infects T-cells thus causing dysregulation of the immune system which has been linked to dissemination and hyperinfection of S. stercoralis leading to bacterial sepsis which can result in death. Both of these pathogens are endemic in Australia primarily in remote communities in Queensland, the Northern Territory, and Western Australia. Other cases in Australia have occurred in immigrants and refugees, returned travellers, and Australian Defence Force personnel. HTLV-I infection is lifelong with no known cure. Strongyloidiasis is a long-term chronic disease that can remain latent for decades, as shown by infections diagnosed in prisoners of war from World War II and the Vietnam War testing positive decades after they returned from these conflicts. This review aims to shed light on concomitant infections of HTLV-I with S. stercoralis primarily in Australia but in the global context as well.

Strongyloides genotyping: a review of methods and application in public health and population genetics.

Strongyloidiasis represents a major medical and veterinary helminthic disease. Human infection is caused by Strongyloides stercoralis, Strongyloides fuelleborni fuelleborni and Strongyloides fuelleborni kellyi, with S.stercoralis accounting for the majority of cases. Strongyloides f. fuelleborni likely represents a zoonosis acquired from non-human primates (NHPs), while no animal reservoir for S. f. kellyi infection has been found. Whether S. stercoralis represents a zoonosis acquired from dogs and cats remains unanswered. Over the past two decades various tools have been applied to genotype Strongyloides spp. The most commonly sequenced markers have been the hyper-variable regions I and IV of the 18S rRNA gene and selected portions of the cytochrome c oxidase subunit I gene. These markers have been sequenced and compared in Strongyloides from multiple hosts and geographical regions. More recently, a machine learning algorithm multi-locus sequence typing approach has been applied using these markers, while others have applied whole genome sequencing. Genotyping of Strongyloides from dogs, cats, NHPs and humans has identified that S. stercoralis likely originated in dogs and adapted to human hosts. It has also been demonstrated that S. stercoralis is distinct from S. f. fuelleborni and S. f. kellyi. Two distinct genetic clades of S. stercoralis exist, one restricted to dogs and another infecting humans, NHPs, dogs and cats. Genotyping of S. f. fuelleborni has identified two separate clades, one associated with African isolates and another Indochinese peninsular clade. This review summarises the history and development of genotyping tools for Strongyloides spp. It describes the findings of major studies to date in the context of the epidemiology and evolutionary biology of these helminths, with a specific focus on human-infecting species.

Possible transmission of Strongyloides fuelleborni between working Southern pig-tailed macaques (Macaca nemestrina) and their owners in Southern Thailand: Molecular identification and diversity.

Human strongyloidiasis is caused by Strongyloides stercoralis, S. fuelleborni fuelleborni and Strongyloides f. kellyi. Strongyloides fuelleborni is a soil-transmitted nematode parasite typically infecting non-human primates. The southern pig-tailed macaque (Macaca nemestrina) is distributed throughout the southern part of Thailand and could be a source of zoonotic transmission of this nematode. Here, we extracted DNA from Strongyloides speciescultured from the feces of southern pig-tailed macaques and their owners. Using PCR and sequencing of the extracted DNA, we compared the nucleotide sequences of these worms using portions of the 18S rDNA hypervariable region IV (HVR-IV) and the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene. Sequences from the 18S rRNA gene were obtained from worms from 23 southern pig-tailed macaques and from one owner. These sequences were identical with each other and with all East and Southeast Asian S. fuelleborni sequences (from Japan, Thailand, and Lao PDR) in the GenBank database. A median-joining network of published cox1 sequences (n = 123), in combination with the present 24 new sequences, represented 107 haplotypes distributed among six clusters, which corresponded to geographical localities but did not relate to host species. The S. fuelleborni cox1 sequences from some southern pig-tailed macaques and the one infected owner shared the same cox1 haplotype. This is the first evidence of likely zoonotic transmission of S. fuelleborni from a reservoir host, M. nemestrina.

A Review of Strongyloides spp. Environmental Sources Worldwide.

Strongyloides spp. are parasitic nematodes that are transmitted through the environment and are capable of causing disease. These nematodes affect an estimated 3-300 million humans worldwide. Identifying the environmental reservoirs of Strongyloides spp. is essential for the development of appropriate control strategies. This systematic literature review examined all published studies that identified Strongyloides stercoralis, Strongyloides fuelleborni, Strongyloides fuelleborni kellyi, and Strongyloides spp. from an environmental source. Most studies detected the nematode from dog and primate fecal samples. Other environmental sources identified were ruminants, cats, rodents, insects, water, soil, as well as fruit and vegetables. Most studies used microscopy-based identification techniques; however, several employed molecular-based techniques, which have become increasingly popular for the detection of Strongyloides spp. A limitation identified was a lack of studies that comprehensively screened all potential environmental samples in a region. Future research should undertake this holistic screening process to identify which environmental reservoirs pose the greatest significance to human health. Potential controls can be identified through the identification of environmental sources. Understanding where Strongyloides spp. is commonly found within the environment of endemic areas will inform environmental control strategies to reduce this neglected disease.

Strongyloidiasis with emphasis on human infections and its different clinical forms.

Strongyloidiasis (caused by Strongyloides stercoralis, and to a lesser extent by Strongyloides fuelleborni) is one of the most neglected tropical diseases with endemic areas and affecting more than 100 million people worldwide. Chronic infections in endemic areas can be maintained for decades through the autoinfective cycle with the L3 filariform larvae. In these endemic areas, misdiagnosis, inadequate treatment and the facilitation of the hyperinfection syndrome by immunosuppression are frequent and contribute to a high mortality rate. Despite the serious health impact of strongyloidiasis, it is a neglected disease and very little is known about this parasite and the disease when compared to other helminth infections. Control of the disease is difficult because of the many gaps in our knowledge of strongyloidiasis. We examine the recent literature on different aspects of strongyloidiasis with emphasis in those aspects that need further research.

Parasites of free-ranging Cayo Santiago macaques after 46 years of isolation.

Three hundred and thirty seven Macaca mulatta from a population that had been isolated on a small island off the coast of Puerto Rico for 46 years were examined for parasites. Anatrichosoma cynamolgi (26%), Strongyloides fuelleborni (54%); Trichuris trichiura (23%); and Balantidium coli (2%) were detected. Toxoplasma antibodies were found in 10% of the sera examined. Milk was examined for Stronglyloides, and blood was examined for microfilariae and protozoa, but no parasites were found in these specimens. The animals in this colony harbored intestinal parasites but were in excellent physical condition, with a high reproductive rate and a low mortality rate. It is concluded that the presence of intestinal and tissue parasites has little measurable effect on the overall health of rhesus in this free-ranging environment.