Morphological variation of four species of Strongyloides (Nematoda, Rhabditida) parasitising various mammal species

Keywords: morphometric parameters; Strongyloides papillosus; S. westeri; S. ransomi; S. stercoralis


Study of the morphologic peculiarities of free-living stages of nematodes of the Strongyloides genus is important in differential diagnostics of pathogens. We studied the parasite of goats (Capra aegagrus hircus Linnaeus, 1758) – Strongyloides papillosus (Wedl, 1856); the parasite of horses (Equus ferus caballus Linnaeus, 1758) – S. westeri Ihle, 1917; the parasite of swine (Sus scrofa Linnaeus, 1758 ) – S. ransomi Schwartz & Alicata, 1930; the parasite of dogs (Canis lupus familiaris Linnaeus, 1758) – S. stercoralis (Bavay, 1876). Rhabditiform larvae (L1, L2), filarial larvae (L3), mature males (M) and free-living females (F) were analyzed for each of the four species by five morphological parameters: body length (Lb), total maximum body width (Sb), length of the esophagus (Lo), length of the intestine (Le), length of the tail end (Lc); for females, we additionally examined length from the head end to the vulva (Lv) and the number of formed eggs in the uterus cavity (E), and for males – length of spicules (Ls). First stage larvae of S. papillosus and S. stercoralis significantly differed in all parameters, and first stage larvae of S. westeri and S. stercoralis significantly differed in four out of five parameters. By indices of ratios of total maximum body width (Sb) to body length (Lb), length of the esophagus (Lo) to length of the intestine (Le), length of the tail end (Lc) to body length (Lb), length of the intestine (Le) to body length (Lb), a reliable difference was recorded between L1 of S. papillosus and S. ransomi, L3 of S. papillosus and S. westeri, S. westeri and S. ransomi, between males of S. papillosus and S. westeri, S. westeri and S. stercoralis, between females of S. papillosus and S. westeri, S. papillosus and S. stercoralis. All four examined species were observed to have reliable differences of ratio of length of esophagus to length of intestine in third stage larvae.


Agyei, A. D. (2003). Epidemiological studies on gastrointestinal parasitic infections of lambs in the coastal savanna regions of Ghana. Tropical Animal Health and Production, 35(1), 207–217.
Basir, M. A. (1950). The morphology and development of the sheep nematode, Strongyloides papillosus (Wedl, 1856). Canadian Journal of Research, 28(3), 173–196.
Bekele, T. (2002). Epidemiological studies on gastrointestinal helminths of dromedary (Camelus dromedarius) in semi-arid lands of Eastern Ethiopia. Veterinary Parasitology, 105(2), 139–152.
Boyko, A. A., & Brygadyrenko, V. V. (2016). Influence of water infusion of medicinal plants on larvae of Strongyloides papillosus (Nematoda, Strongyloididae). Visnyk of Dnipropetrovsk University. Biology, Ecology, 24(2), 519–525.
Boyko, A., Brygadyrenko, V., Shendryk, L., & Loza, I. (2009). Estimation of the role of antropo-zoonosis invasion agents in the counteraction to bioterrorism. Counteraction to Chemical and Biological Terrorism in East European Countries. NATO Science for Peace and Security Series A: Chemistry and Biology. Springer Nature, 309–315.
Boyko, O. O., Duda, Y. V., Pakhomov, O. Y., & Brygadyrenko, V. V. (2016). Comparative analysis of different methods of staining the larvae Haemonchus contortus, Mullerius sp. (Nematoda, Strongylida) and Strongyloides papillosus (Nematoda, Rhabditida). Folia Oecologica, 43(2), 129–137.
Catalano, C., Aron, J., Bansal, R., & Leytin, A. (2017). Colorectal cancer associated with Strongyloides stercoralis colitis. ACG Case Reports Journal, 4(1), e104.
Dewes, H. F., & Townsend, K. G. (1990). Further observations on Strongyloides westeri dermatitis: Recovery of larvae from soil and bedding, and survival in treated sites. New Zealand Veterinary Journal, 38(1), 34–37.
Dos Santos, K. R., Carlos, B. C., Paduan, K. S., Kadri, S. M., Barrella, T. H., Amarante, M. R. V., & Silva, R. J. (2009). Morphological and molecular characterization of Strongyloides ophidiae (Nematoda, Strongyloididae). Journal of Helminthology, 84(02), 136–142.
Eberhardt, A. G., Mayer, W. E., Bonfoh, B., & Streit, A. (2008). The Strongyloides (Nematoda) of sheep and the predominant Strongyloides of cattle form at least two different, genetically isolated populations. Veterinary Parasitology, 157(1–2), 89–99.
Eydal, M., & Skírnisson, K. (2016). Strongyloides stercoralis found in imported dogs, household dogs and kennel dogs in Iceland. Icelandic Agricultural Sciences, 29, 39–51.
Eysker, M., Bakker, N., Kooyman, F. N. J., & Ploeger, H. W. (2005). The possibilities and limitations of evasive grazing as a control measure for parasitic gastroenteritis in small ruminants in temperate climates. Veterinary Parasitology, 129, 95–104.
Greer, G. J., Bello, T. R., & Amborski, G. F. (1974). Experimental infection of Strongyloides westeri in parasite-free ponies. The Journal of Parasitology, 60(3), 466–472.
Greiner, E. C., Mays, M. B. C., Smart, G. C., & Weisbrode, S. E. (1991). Verminous mastitis in a mare caused by a free-living nematode. The Journal of Parasitology, 77(2), 320–322.
Gugosyan, Y. A., Yevstafyeva, V. A., Gorb, О. А., Melnychuk, V. V., Yasnolob, I. О., Shendryk, C. M., & Pishchalenko, M. А. (2018). Morphological features of development of Strongyloides westeri (Nematoda, Rhabditida) in vitro. Regulatory Mechanisms in Biosystems, 9(1), 75–79.
Huang, R.-E., Li, R., & Zhao, Z. (2016). Discovery of a free-living nematode phylogenetically related to vertebrate parasites of the genus Strongyloides (Nematoda: Strongyloidoidea): Morphological, anatomical and molecular characterisation. Invertebrate Systematics, 30(4), 387–397.
Hunt, V. L., Hino, A., Yoshida, A., & Kikuchi, T. (2018). Comparative transcriptomics gives insights into the evolution of parasitism in Strongyloides nematodes at the genus, subclade and species level. Scientific Reports, 8(1), 5192.
Huong Giang, N. T., Hoan, T. D., Thu Huyen, N. T., Kim Lan, N. T., & Doanh, P. N. (2017). Morphological and molecular characterisation of Strongyloides ransomi (Nematoda: Strongyloididae) collected from domestic pigs in Bac Giang province, Vietnam. Tap Chi Sinh Hoc, 39(3), 270–275.
Jäger, M., Gauly, M., Bauer, C., Failing, K., Erhardt, G., & Zahner, H. (2005). Endoparasites in calves of beef cattle herds: Management systems dependent and genetic influences. Veterinary Parasitology, 131(3–4), 173–191.
Jaleta, T. G., Zhou, S., Bemm, F. M., Schär, F., Khieu, V., Muth, S., & Streit, A. (2017). Different but overlapping populations of Strongyloides stercoralis in dogs and humans – Dogs as a possible source for zoonotic strongyloidiasis. PLoS Neglected Tropical Diseases, 11(8), e0005752.
Jongwutiwes, S., Charoenkorn, M., Sitthichareonchai, P., Akaraborvorn, P., & Putaporntip, C. (1999). Increased sensitivity of routine laboratory detection of Strongyloides stercoralis and hookworm by agar-plate culture. Transactions of the Royal Society of Tropical Medicine and Hygiene, 93(4), 398–400.
Kabululu, M. L., Ngowi, H. A., Kimera, S. I., Lekule, F. P., Kimbi, E. C., & Johansen, M. V. (2015). Risk factors for prevalence of pig parasitoses in Mbeya Region, Tanzania. Veterinary Parasitology, 212(3–4), 460–464.
Kagira, J. M., Kanyari, P. N., Githigia, S. M., Maingi, N., Ng’ang’a, J. C., & Gachohi, J. M. (2011). Risk factors associated with occurrence of nematodes in free range pigs in Busia District, Kenya. Tropical Animal Health and Production, 44(3), 657–664.
Khanna, V., Tilak, K., Prakash, P., & Mukhopadhyay, C. (2015). Modified agar plate culture method for culture of Strongyloides stercoralis. Tropical Parasitology, 5(2), 136–138.
Kváč, M., & Vítovec, J. (2007). Occurrence of Strongyloides papillosus associated with extensive pulmonary lesions and sudden deaths in calves on a beef farm in a highland area of South Bohemia (Czech Republic). Helminthologia, 44(1), 10–13.
Lee, D. Z. J., Amin, R., Baksi, J., & Gerber, R. (2017). A clinical enigma of ongoing constrictive pericarditis. Clinical Medicine, 17(3), 248–250.
Little, M. D. (1966). Seven new species of Strongyloides (Nematoda) from Louisiana. The Journal of Parasitology, 52(1), 85–97.
Lok, J. B., Shao, H., Massey, H. C., & Li, X. (2017). Transgenesis in Strongyloides and related parasitic nematodes: Historical perspectives, current functional genomic applications and progress towards gene disruption and editing. Parasitology, 144(3), 327–342.
Lopez, P. M., Nolan, T., & Schad, G. A. (2000). Growth of the genital primordium as a marker to describe a time course for the heterogonic larval development in Strongyloides stercoralis. The Journal of Parasitology, 86(4), 882–883.
Lucena, R. B., Fighera, R. A., & Barros, C. S. L. (2012). Mortalidade em potros associada ao parasitismo por Strongyloides westeri. Pesquisa Veterinária Brasileira, 32(5), 401–404.
Nabeya, D., Haranaga, S., Parrott, G. L., Kinjo, T., Nahar, S., Tanaka, T., & Fujita, J. (2017). Pulmonary strongyloidiasis: Assessment between manifestation and radiological findings in 16 severe strongyloidiasis cases. BMC Infectious Diseases, 17(1), 320.
Nagayasu, E., Aung, M. P. P. T. H. H., Hortiwakul, T., Hino, A., Tanaka, T., Higashiarakawa, M., & Maruyama, H. (2017). A possible origin population of pathogenic intestinal nematodes, Strongyloides stercoralis, unveiled by molecular phylogeny. Scientific Reports, 7(1), 4844.
Nakamura, Y., & Motokawa, M. (2000). Hypolipemia associated with the wasting condition of rabbits infected with Strongyloides papillosus. Veterinary Parasitology, 88, 147–151.
Nganga, C. J., Karanja, D. N., & Mutune, M. N. (2007). The prevalence of gastrointestinal helminth infections in pigs in Kenya. Tropical Animal Health and Production, 40(5), 331–334.
Nugroho, W., Cargill, C. F., Putra, I. M., Kirkwood, R. N., Trott, D. J., Salasia, S. I. O., & Reichel, M. P. (2015). Investigations of selected pathogens among village pigs in Central Papua, Indonesia. Tropical Animal Health and Production, 48(1), 29–36.
Politis, D. S. (2017). Strongyloides stercoralis infection: An “exotic” cause of chronic diarrhea. Annals of Gastroenterology, 30(4), 467.
Poveda, J., El-Sharkawy, F., Arosemena, L. R., Garcia-Buitrago, M. T., & Rojas, C. P. (2017). Strongyloides colitis as a harmful mimicker of inflammatory Bowel disease. Case Reports in Pathology, 2017, 1–4.
Roesel, K., Dohoo, I., Baumann, M., Dione, M., Grace, D., & Clausen, P.-H. (2016). Prevalence and risk factors for gastrointestinal parasites in small-scale pig enterprises in Central and Eastern Uganda. Parasitology Research, 116(1), 335–345.
Sato, H., Tanaka, S., Une, Y., Torii, H., Yokoyama, M., Suzuki, K., & Hasegawa, H. (2007). The stomal morphology of parasitic females of Strongyloides spp. by scanning electron microscopy. Parasitology Research, 102(3), 541–546.
Schuurmans, J. H., & Stekhoven, J. (1930). Untersuchungen über Nematoden und ihre Larven V. Strongyloides westeri Ihle und Ihre Larven. Zeitschrift für Parasitenkunde, 2(3), 297–309.
Schwartz, B., & Alicata, J. E. (1930). Species of the nematode genus Strongyloides parasitic in domestic swine. Journal of Agricultural Research, 40(1), 11–23.
Singh, D., Swarnkar, C. P., Khan, F. A., Srivastava, C. P., & Bhagwan, P. S. K. (1997). Epidemiology of ovine gastrointestinal nematodes at an organized farm in Rajasthan, India. Small Ruminant Research, 26, 31–37.
Spratt, D. M. (2018). A review of species of Parastrongyloides (Nematoda: Rhabditoidea: Strongyloididae) from Australian marsupials with descriptions of three new species. Transactions of the Royal Society of South Australia, 142(2), 162–182.
Tamboura, H. H., Banga-Mboko, H., Maes, D., Youssao, I., Traore, A., Bayala, B., & Dembele, M. A. (2006). Prevalence of common gastrointestinal nematode parasites in scavenging pigs of different ages and sexes in Eastern Centre province, Burkina Faso. Onderstepoort Journal of Veterinary Research, 73(1), 53–60.
Umur, Ş., Meral, Y., Bölükbaş, C. S., Gürler, A. T., & Açici, M. (2017). First clinical Strongyloides stercoralis case in a dog in Turkey. Turkish Journal of Veterinary and Animal Sciences, 41, 312–315.
Wymann, M. N., Traore, K., Bonfoh, B., Tembely, S., Tembely, S., & Zinsstag, J. (2008). Gastrointestinal parasite egg excretion in young calves in periurban livestock production in Mali. Research in Veterinary Science, 84(2), 225–231.

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