Strongyloides in non-human primates: significance for public health control

Primates are an important source of infectious disease in humans. Strongyloidiasis affects an estimated 600 million people worldwide, with a global distribution and hotspots of infection in tropical and subtropical regions. Recently added to the list of neglected tropical diseases, global attention has been demanded in the drive for its control. Through a literature review of Strongyloides in humans and non-human primates (NHP), we analysed the most common identification methods and gaps in knowledge about this nematode genus. The rise of molecular-based methods for Strongyloides detection is evident in both humans and NHP and provides an opportunity to analyse all data available from primates. Dogs were also included as an important host species of Strongyloides and a potential bridge host between humans and NHP. This review highlights the lack of molecular data across all hosts—humans, NHP and dogs—with the latter highly underrepresented in the database. Despite the cosmopolitan nature of Strongyloides, there are still large gaps in our knowledge for certain species when considering transmission and pathogenicity. We suggest that a unified approach to Strongyloides detection be taken, with an optimized, repeatable molecular-based method to improve our understanding of this parasitic infection. This article is part of the Theo Murphy meeting issue ‘Strongyloides: omics to worm-free populations’.

[1]  Brian H. Herrin,et al.  Identification and treatment of Strongyloides cebus in captive ring-tailed lemurs (Lemur catta) in the midwestern United States. , 2023, Veterinary parasitology, regional studies and reports.

[2]  B. Pafčo,et al.  Identification of potentially zoonotic parasites in captive orangutans and semi‐captive mandrills: Phylogeny and morphological comparison , 2023, American journal of primatology.

[3]  Y. Qvarnstrom,et al.  Genetic characterization of Strongyloides fuelleborni infecting free-roaming African vervets (Chlorocebus aethiops sabaeus) on the Caribbean island of St. Kitts , 2023, International journal for parasitology. Parasites and wildlife.

[4]  K. Kyuregyan,et al.  Measles in non‐human primates , 2022, Journal of medical primatology.

[5]  E. Nagayasu,et al.  Population genetics study of Strongyloides fuelleborni and phylogenetic considerations on primate-infecting species of Strongyloides based on their mitochondrial genome sequences. , 2022, Parasitology international.

[6]  P. Rodari,et al.  Current pharmacotherapeutic strategies for Strongyloidiasis and the complications in its treatment , 2022, Expert opinion on pharmacotherapy.

[7]  J. R. Guimarães,et al.  Effects of Avermectins on the Environment Based on Its Toxicity to Plants and Soil Invertebrates—a Review , 2022, Water, Air, & Soil Pollution.

[8]  R. Mahmoudi,et al.  Global prevalence and epidemiology of Strongyloides stercoralis in dogs: a systematic review and meta-analysis , 2022, Parasites & Vectors.

[9]  J. Keiser,et al.  Optimizing moxidectin dosing for Strongyloides stercoralis infections: Insights from pharmacometric modeling , 2021, Clinical and translational science.

[10]  B. Pafčo,et al.  Strongyloides genotyping: a review of methods and application in public health and population genetics. , 2021, International journal for parasitology.

[11]  M. Peeters,et al.  Soil-transmitted helminth infections in free-ranging non-human primates from Cameroon and Gabon , 2021, Parasites & Vectors.

[12]  Y. Une,et al.  First demonstration of Strongyloides parasite from an imported pet meerkat - Possibly a novel species in the stercoralis/procyonis group. , 2021, Parasitology international.

[13]  A. Streit Strongyloidiasis: Really a Zoonosis? , 2020, Parasitology Research Monographs.

[14]  M. van Esbroeck,et al.  A rare case of imported Strongyloides fuelleborni infection in a Belgian student , 2020 .

[15]  R. Rodpai,et al.  Possible transmission of Strongyloides fuelleborni between working Southern pig-tailed macaques (Macaca nemestrina) and their owners in Southern Thailand: Molecular identification and diversity. , 2020, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[16]  D. Raoult,et al.  Parasitic Infections in African Humans and Non-Human Primates , 2020, Pathogens.

[17]  J. Barratt,et al.  Machine learning-based analyses support the existence of species complexes for Strongyloides fuelleborni and Strongyloides stercoralis , 2020, Parasitology.

[18]  E. Gotuzzo,et al.  Phylogenetic relationships of Strongyloides species in carnivore hosts. , 2020, Parasitology international.

[19]  D. Bisanzio,et al.  The Global Prevalence of Strongyloides stercoralis Infection , 2020, Pathogens.

[20]  C. Rödelsperger,et al.  Genomic studies on Strongyloides stercoralis in northern and western Thailand , 2020, Parasites & Vectors.

[21]  Laura S. P. Bloomfield Global mapping of landscape fragmentation, human-animal interactions, and livelihood behaviors to prevent the next pandemic , 2020, Agriculture and human values.

[22]  S. Wich,et al.  DNA Barcoding of Nematodes Using the MinION , 2020, Frontiers in Ecology and Evolution.

[23]  R. Rodpai,et al.  Dogs are reservoir hosts for possible transmission of human strongyloidiasis in Thailand: molecular identification and genetic diversity of causative parasite species. , 2019, Journal of helminthology.

[24]  D. Raoult,et al.  Infectious Disease Risk Across the Growing Human-Non Human Primate Interface: A Review of the Evidence , 2019, Front. Public Health.

[25]  D. Harbecke,et al.  From the feces to the genome: a guideline for the isolation and preservation of Strongyloides stercoralis in the field for genetic and genomic analysis of individual worms , 2019, Parasites & Vectors.

[26]  B. Pritt,et al.  A global genotyping survey of Strongyloides stercoralis and Strongyloides fuelleborni using deep amplicon sequencing , 2019, PLoS neglected tropical diseases.

[27]  H. Whiley,et al.  A Review of Strongyloides spp. Environmental Sources Worldwide , 2019, Pathogens.

[28]  J. Barratt,et al.  Detection of classic and cryptic Strongyloides genotypes by deep amplicon sequencing: A preliminary survey of dog and human specimens collected from remote Australian communities , 2019, bioRxiv.

[29]  J. Šlapeta,et al.  Efficacy of ivermectin to control Strongyloides stercoralis infection in sheltered dogs. , 2019, Acta tropica.

[30]  Kevin E. Langergraber,et al.  Simultaneous outbreaks of respiratory disease in wild chimpanzees caused by distinct viruses of human origin , 2019, Emerging microbes & infections.

[31]  J. Utzinger,et al.  Diagnostic comparison of Baermann funnel, Koga agar plate culture and polymerase chain reaction for detection of human Strongyloides stercoralis infection in Maluku, Indonesia , 2018, Parasitology Research.

[32]  P. Intapan,et al.  First molecular identification of Strongyloides fuelleborni in long-tailed macaques in Thailand and Lao People's Democratic Republic reveals considerable genetic diversity , 2018, Journal of Helminthology.

[33]  Danica J. Stark,et al.  Lurking in the dark: Cryptic Strongyloides in a Bornean slow loris , 2018, International journal for parasitology. Parasites and wildlife.

[34]  M. Kinney,et al.  Treatment of disseminated Strongyloides spp. infection in an infant Sumatran orangutan (Pongo abelii) , 2018, Journal of medical primatology.

[35]  S. Deem,et al.  Pathogen Transmission from Humans to Great Apes is a Growing Threat to Primate Conservation , 2018, EcoHealth.

[36]  T. Giles-Vernick,et al.  Rethinking Human–Nonhuman Primate Contact and Pathogenic Disease Spillover , 2017, EcoHealth.

[37]  J. Benavides,et al.  Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas? , 2017, Parasitology Research.

[38]  D. Otranto,et al.  Zoonotic Parasites of Sheltered and Stray Dogs in the Era of the Global Economic and Political Crisis. , 2017, Trends in parasitology.

[39]  Sinuon Muth,et al.  Different but overlapping populations of Strongyloides stercoralis in dogs and humans—Dogs as a possible source for zoonotic strongyloidiasis , 2017, PLoS neglected tropical diseases.

[40]  C. Cantacessi,et al.  Occurrence of strongyloidiasis in privately owned and sheltered dogs: clinical presentation and treatment outcome , 2017, Parasites & Vectors.

[41]  T. Horii,et al.  A possible origin population of pathogenic intestinal nematodes, Strongyloides stercoralis, unveiled by molecular phylogeny , 2017, Scientific Reports.

[42]  B. Losson,et al.  Gastrointestinal parasites in captive and free-ranging Cebus albifrons in the Western Amazon, Ecuador , 2017, International journal for parasitology. Parasites and wildlife.

[43]  P. Radomyos,et al.  First molecular identification and genetic diversity of Strongyloides stercoralis and Strongyloides fuelleborni in human communities having contact with long-tailed macaques in Thailand , 2017, Parasitology Research.

[44]  G. Pérez‐Ponce de León,et al.  Helminth parasites of howler and spider monkeys in Mexico: Insights into molecular diagnostic methods and their importance for zoonotic diseases and host conservation , 2017, International journal for parasitology. Parasites and wildlife.

[45]  K. Petrželková,et al.  Strongyloides infections of humans and great apes in Dzanga-Sangha Protected Areas, Central African Republic and in degraded forest fragments in Bulindi, Uganda. , 2016, Parasitology international.

[46]  S. Thamsborg,et al.  Strongyloides spp. infections of veterinary importance , 2016, Parasitology.

[47]  R. Bradbury,et al.  The laboratory diagnosis of Strongyloides stercoralis , 2016 .

[48]  B. Simmen,et al.  Intestinal Helminths of Wild Bonobos in Forest-Savanna Mosaic: Risk Assessment of Cross-Species Transmission with Local People in the Democratic Republic of the Congo , 2015, EcoHealth.

[49]  S. Stehman,et al.  Gastrointestinal Parasites of Ecuadorian Mantled Howler Monkeys (Alouatta palliata aequatorialis) Based on Fecal Analysis , 2015, The Journal of parasitology.

[50]  T. Nutman,et al.  Accuracy of Five Serologic Tests for the Follow up of Strongyloides stercoralis Infection , 2015, PLoS neglected tropical diseases.

[51]  A. L. de Melo,et al.  Strongyloides stercoralis infection in marmosets: replication of complicated and uncomplicated human disease and parasite biology , 2014, Parasites & Vectors.

[52]  D. Travis,et al.  Global Positioning System Data-Loggers: A Tool to Quantify Fine-Scale Movement of Domestic Animals to Evaluate Potential for Zoonotic Transmission to an Endangered Wildlife Population , 2014, PloS one.

[53]  Santhosh Puthiyakunnon,et al.  Strongyloidiasis—An Insight into Its Global Prevalence and Management , 2014, PLoS neglected tropical diseases.

[54]  Rogan Lee,et al.  A loop-mediated isothermal amplification (LAMP) assay for Strongyloides stercoralis in stool that uses a visual detection method with SYTO-82 fluorescent dye. , 2014, The American journal of tropical medicine and hygiene.

[55]  T. Nutman,et al.  Diagnostic Accuracy of Five Serologic Tests for Strongyloides stercoralis Infection , 2014, PLoS neglected tropical diseases.

[56]  F. C. F. Junior,et al.  Strongyloides cebus (Nematoda: Strongyloididae) in Lagothrix cana (Primates: Atelidae) from the Brazilian Amazon: Aspects of Clinical Presentation, Anatomopathology, Treatment, and Parasitic Biology , 2013, The Journal of parasitology.

[57]  P. Vounatsou,et al.  Strongyloides stercoralis: Global Distribution and Risk Factors , 2013, PLoS neglected tropical diseases.

[58]  P. Chiodini,et al.  Strongyloides stercoralis: A Plea for Action , 2013, PLoS neglected tropical diseases.

[59]  S. Ho,et al.  Dating the origin and dispersal of hepatitis B virus infection in humans and primates , 2013, Hepatology.

[60]  K. Mansfield,et al.  Viral Diseases of Nonhuman Primates , 2012, Nonhuman Primates in Biomedical Research.

[61]  J. T. Williams,et al.  Trichuris sp. and Strongyloides sp. Infections in a Free-Ranging Baboon Colony , 2012, The Journal of parasitology.

[62]  Alexander Mathis,et al.  Genetic characterization of Strongyloides spp. from captive, semi-captive and wild Bornean orangutans (Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia , 2011, Parasitology.

[63]  S. O’Brien,et al.  A Molecular Phylogeny of Living Primates , 2011, PLoS genetics.

[64]  M. Lebreton,et al.  Prevalence of gastrointestinal parasites in primate bushmeat and pets in Cameroon. , 2011, Veterinary parasitology.

[65]  J. Rayner,et al.  Origin of the human malaria parasite Plasmodium falciparum in gorillas , 2010, Nature.

[66]  T. Nishida,et al.  Molecular identification of the causative agent of human strongyloidiasis acquired in Tanzania: dispersal and diversity of Strongyloides spp. and their hosts. , 2010, Parasitology international.

[67]  P. Sharp,et al.  The evolution of HIV-1 and the origin of AIDS , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[68]  K. Polman,et al.  Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. , 2009, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[69]  C. Chapman,et al.  COPROLOGIC EVIDENCE OF GASTROINTESTINAL HELMINTHS OF FOREST BABOONS, PAPIO ANUBIS, IN KIBALE NATIONAL PARK, UGANDA , 2008, Journal of wildlife diseases.

[70]  Nathan D. Wolfe,et al.  Origins of major human infectious diseases , 2007, Nature.

[71]  C. Schäfer,et al.  Malaria , 2006, Der Internist.

[72]  J. Dufour,et al.  Comparison of efficacy of moxidectin and ivermectin in the treatment of Strongyloides fulleborni infection in rhesus macaques , 2006, Journal of medical primatology.

[73]  G. M. Karere,et al.  Some gastro-intestinal tract parasites in wild De Brazza's monkeys (Cercopithecus neglectus) in Kenya. , 2002, Veterinary parasitology.

[74]  M. Blaxter,et al.  Molecular phylogenetic analysis of the genus Strongyloides and related nematodes. , 2002, International journal for parasitology.

[75]  M E Woolhouse,et al.  Risk factors for human disease emergence. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[76]  S. Mikota,et al.  Mycobacterium tuberculosis in zoo and wildlife species. , 2001, Revue scientifique et technique.

[77]  C. Hill Conflict of Interest Between People and Baboons: Crop Raiding in Uganda , 2000, International Journal of Primatology.

[78]  L. Hagelskjær A fatal case of systemic strongyloidiasis and review of the literature , 1994, European Journal of Clinical Microbiology and Infectious Diseases.

[79]  G. Barnish,et al.  Strongyloides fuelleborni kellyi: infection and disease in Papua New Guinea. , 1992, Parasitology today.

[80]  D. Freedman,et al.  Experimental infection of human subject with Strongyloides species. , 1991, Reviews of infectious diseases.

[81]  G. Barnish,et al.  A taxonomic study of Strongyloides Grassi, 1879 (Nematoda) with special reference to Strongyloides fuelleborni von linstow, 1905 in man in Papua New Guinea and the description of a new subspecies , 1991, Systematic Parasitology.

[82]  R. Genta Global prevalence of strongyloidiasis: critical review with epidemiologic insights into the prevention of disseminated disease. , 1989, Reviews of infectious diseases.

[83]  J. Catford,et al.  Human cysticercosis and intestinal parasitism amongst the Ekari people of Irian Jaya. , 1987, The Journal of tropical medicine and hygiene.

[84]  R. Genta,et al.  Experimental disseminated strongyloidiasis in Erythrocebus patas. II. Immunology. , 1984, The American journal of tropical medicine and hygiene.

[85]  J. D. Toft The Pathoparasitology of the Alimentary Tract and Pancreas of Nonhuman Primates: A Review , 1982, Veterinary pathology. Supplement.

[86]  S. Pampiglione,et al.  The presence of Strongyloides fülleborni von Linstow, 1905, in man in Central and East Africa. , 1971, Parassitologia.

[87]  M. D. Little Comparative morphology of six species of Strongyloides (Nematoda) and redefinition of the genus. , 1966, The Journal of parasitology.

[88]  Premvati STUDIES ON STRONGYLOIDES OF PRIMATES: V. SYNONYMY OF THE SPECIES IN MONKEYS AND APES , 1959 .

[89]  D. L. Augustine EXPERIMENTAL STUDIES ON THE VALIDITY OF SPECIES IN THE GENUS STRONGYLOIDES , 1940 .

[90]  T. D. Beach EXPERIMENTAL STUDIES ON HUMAN AND PRIMATE SPECIES OF STRONGYLOIDES V. THE FREE-LIVING PHASE OF THE LIFE CYCLE , 1936 .

[91]  W. Blackie A Helminthological Survey of Southern Rhodesia , 1932, The Indian Medical Gazette.

[92]  T. Goodey Observations on Strongyloides fülleborni von Linstow, 1905, with Some Remarks on the Genus Strongyloides , 1926, Journal of Helminthology.

[93]  J. H. Sandground Speciation and Specificity in the Nematode Genus Strongyloides. , 1925 .

[94]  S. T. Darling STRONGYLOIDES INFECTIONS IN MAN AND ANIMALS IN THE ISTHMIAN CANAL ZONE , 1911, The Journal of experimental medicine.

[95]  R. Bradbury Strongyloides fuelleborni kellyi in New Guinea: neglected, ignored and unexplored , 2021, Microbiology Australia.

[96]  R. Wolf,et al.  Pilot Study to Assess the Efficacy of Ivermectin and Fenbendazole for Treating Captive-Born Olive Baboons (Papio anubis) Coinfected with Strongyloides fülleborni and Trichuris trichiura. , 2017, Journal of the American Association for Laboratory Animal Science : JAALAS.

[97]  R. Genta,et al.  Experimental disseminated strongyloidiasis in Erythrocebus patas. I. Pathology. , 1984, The American journal of tropical medicine and hygiene.

[98]  J. Harper,et al.  Disseminated strongyloidiasis in Erythrocebus patas , 1982, American journal of primatology.

[99]  L. Penner Concerning Threadworm (Strongyloides stercoralis) in Great Apes: Lowland Gorillas (Gorilla gorilla) and Chimpanzees (Pan troglodytes) , 1981 .

[100]  L. Junginger,et al.  Parasitological survey on pygmies in Central Africa. III. Bambuti group (Zaïre). , 1979 .

[101]  S. Pampiglione,et al.  Parasitological survey on Pygmies in Central Africa. I. Babinga group (Central African Republic). , 1974 .

[102]  C. Desportes Sur Strongyloides stercoralis (bavay 1876) et sur les Strongyloides de primates , 1944 .