Morphobiological analysis of Trichuris vulpis (Nematoda, Trichuridae), obtained from domestic dogs

  • V. А. Yevstafieva Poltava State Agrarian Academy
  • S. O. Kravchenko Poltava State Agrarian Academy
  • B. V. Gutyj Lviv National University of Veterinary Medicine and Biotechnologies named after S. Z. Gzhytskyj
  • V. V. Melnychuk Poltava State Agrarian Academy
  • P. N. Kovalenko Poltava State Agrarian Academy
  • L. B. Volovyk Poltava State Agrarian Academy
Keywords: trichuriasis; nematodes; identification; metric characters; biological specifics.

Abstract

The parasitic nematode Trichuris vulpis Frölich, 1789 is the pathogen of trichuriasis in domestic and wild carnivores, and humans. This helminth species is distributed world-wide in populations of domestic dog (Canis lupus familiaris). The prevalence of T. vulpis in dogs depends to a large degree on the morphofunctional and biological adaptations of the parasite which support its high survivability in various environmental conditions. The present study considers the species-specific peculiarities of morphology, and metric parameters of the mature and embryonic stages of Trichuris nematodes parasitizing in C. lupus familiaris. We studied the periods of stages of development and infectious egg formation, and their survivability under optimal conditions for T. vulpis in laboratory culture. The differential characteristics of both female and male adult T. vulpis nematodes include the metric characteristics of cuticular protrusions at the surface of the anterior body part. The male T. vulpis nematodes can be distinguished from males of other species by the specifics of spicule sheath ornamentation, the shape and size of spicule, and the width of spicule sheath at different sections. In identification of the female nematodes of this species, it is necessary to consider the presence and size of papillary processes in the vulval area and metric parameters of vulva location. Nine metric characters of sexual dimorphism are described for T. vulpis nematodes. In laboratory conditions, five embryonic stages were observed for T. vulpis: protoplast, blastomere cleavage, and formation of bean-like embryo, larva and mobile larva. These stages are characterized by specific morphological features. The egg develops to the infectious stage at 27 °С in 18 days of culture, and their survivability is up to 76.6%. The egg development is associated with changes in their metric characters, such as decreasing egg length and width of egg shell, and increasing egg width and egg plug width.

References

Adriko, M., Tinkitina, B., Arinaitwe, M., Kabatereine, N. B., Nanyunja, M., & Tukahebwa, E. M. (2018). Impact of a national deworming campaign on the prevalence of soil-transmitted helminthiasis in Uganda (2004–2016): Implications for national control programs. PLOS Neglected Tropical Diseases, 12(7), e0006520.

Anderson, R. C. (2000). Nematode parasites of vertebrates: Their development and transmission. CABI Publishing, Wallingford.

Areekul, P., Putaporntip, C., Pattanawong, U., Sitthicharoenchai, P., & Jongwutiwes, S. (2010). Trichuris vulpis and T. trichiura infections among schoolchildren of a rural community in Northwestern Thailand: The possible role of dogs in disease transmission. Asian Biomedicine, 4, 49–60.

Barutzki, D., & Schaper, R. (2003). Endoparasites in dogs and cats in Germany 1999–2002. Parasitology Research, 90(3), 148–150.

Bethony, J., Brooker, S., Albonico, M., Geiger, S. M., Loukas, A., Diemert, D., & Hotez, P. J. (2006). Soil-transmitted helminth infections: Ascariasis, trichuriasis, and hookworm. Lancet, 367, 1521–1532.

Betson, M., Søe, M. J., & Nejsum, P. (2015). Human trichuriasis: Whipworm genetics, phylogeny, transmission and future research directions. Current Tropical Medicine Reports, 2(4), 209–217.

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. A., & Brygadyrenko, V. V. (2017). Changes in the viability of the eggs of Ascaris suum under the influence of flavourings and source materials approved for use in and on foods. Biosystems Diversity, 25(2), 162–166.

Callejón, R., Robles, M. D. R., Panei, C. J., & Cutillas, C. (2016). Molecular diversification of Trichuris spp. from Sigmodontinae (Cricetidae) rodents from Argentina based on mitochondrial DNA sequences. Parasitology Research, 115, 1–13.

Conboy, G. A. (2009). Helminth parasites of the canine and feline respiratory tract. Veterinary Clinics of North America: Small Animal Practice, 39, 1109–1126.

Di Cesare, A., Castagna, G., Meloni, S., Otranto, D., & Traversa, D. (2012). Mixed trichuroid infestation in a dog from Italy. Parasites and Vectors, 5, 128.

Dunn, J. J., Columbus, S. T., Aldeen, W. E., Davis, M., & Carroll, K. C. (2002). Trichuris vulpis recovered from a patient with chronic diarrhea and five dogs. Journal of Clinical Microbiology, 40(7), 2703–2704.

Eo, K. Y., Seo, M. G., Lee, H. H., Jung, Y. M., Kwak, D., & Kwon, O. D. (2019). Severe whipworm (Trichuris spp.) infection in the hamadryas baboon (Papio hamadryas). Journal of Veterinary Medical Science, 81(1), 53–56.

Fahmy, M. A. M. (1954). An investigation on the life cycle of Trichuris muris. Parasitology, 44(1–2), 50–57.

Fataliev, G. G. (2013). Influence of abiotic factors on the embryonal development of Trichocephalus myocastoris (Nematoda, Trichocephalidae). Zoological Journal, 92(12), 1475–1477.

Ghai, R. R., Simons, N. D., Chapman, C. A., Omeja, P. A., Davies, T. J., Ting, N., & Goldberg, T. L. (2014). Hidden population structure and cross-species transmission of whipworms (Trichuris sp.) in humans and non-human primates in Uganda. PLoS Neglected Tropical Diseases, 8(10), e3256.

Hall, J. E., & Sonnenberg, B. (1956). An apparent case of human infection with the whipworm of dogs, Trichuris vulpis (Froelich, 1789). Journal of Parasitology, 42, 197–199.

Hasegawa, H., & Dewi, K. (2017). Two new species of Тrichuris (Nematoda: Trichuridae) collected from endemic murines of Indonesia. Zootaxa, 4254(1), 127–135.

Kagei, N., Hayashi, S., & Kato, K. (1986). Human cases of infection with canine whipworms, Trichuris vulpis (Froelich, 1789), in Japan. Japanese Journal of Medical Science and Biology, 39, 177–184.

Karamon, J., Dąbrowska, J., Kochanowski, М., Samorek-Pieróg, М., Sroka, J., Różycki, М., Bilska-Zając, E., Zdybel, J., & Cencek, Т. (2018). Prevalence of intestinal helminths of red foxes (Vulpes vulpes) in Central Europe (Poland): A significant zoonotic threat. Parasites and Vectors, 11, 436.

Kenney, M., & Eveland, L. K. (1978). Infection of man with Trichuris vulpis, the whipworm of dogs. American Journal of Clinical Pathology, 69(2), 199.

Kenney, M., & Yermakov, V. (1980). Infection of man with Trichuris vulpis, the whipworm of dogs. American Journal of Tropical Medicine and Hygiene, 29, 1205–1208.

Ketzis, J. K. (2015). Trichuris spp. infecting domestic cats on St. Kitts: Identification based on size or vulvar structure? Springerplus, 4, 115.

Lee, D. L. (2002). The biology of nematodes. Taylor and Francis, London.

Márquez-Navarro, A., García-Bracamontes, G., Alvarez-Fernández, B. E., Ávila-Caballero, L. P., Santos-Aranda, I., Díaz-Chiguer, D. L., Sánchez-Manzano, R. M., Rodríguez-Bataz, E., & Nogueda-Torres, B. (2012). Trichuris vulpis (Froelich, 1789) infection in a child: A case report. Korean Journal of Parasitology, 50(1), 69–71.

Melnychuk, V. V., & Berezovsky, А. V. (2018). Comparative embryonic development of nematodes of the genus Тrichuris (Nematoda, Trichuridae) obtained from sheep (Ovis aries). Biosystems Diversity, 26(4), 257–262.

Mohd-Shaharuddin, N., Lim, Y. A. L., Hassan, N. A., Nathan, S., & Ngui, R. (2019). Molecular characterization of Trichuris species isolated from humans, dogs and cats in a rural community in Peninsular Malaysia. Acta Tropica, 190, 269–272.

Morand, S. (1996). Life-history traits in parasitic nematodes: A comparative approach for the search of invariants. Functional Ecology, 10, 210–218.

Mukaratirwa, S., & Singh, V. P. (2010). Prevalence of gastrointestinal parasites of stray dogs impounded by the Society for the Prevention of Cruelty to Animals (SPCA), Durban and Coast, South Africa. Journal of the South African Veterinary Association, 81(2), 123–125.

Opazo, А., Barrientos, С., Sanhueza, A. M., Urrutia, N., & Fernández, I. (2019). Fauna parasitaria en caninos (Canis lupus familiaris) de un sector rural de la región central de Chile. Revista de Investigaciones Veterinarias del Perú, 30(1), 330–338.

Poulin, R. (1997). Covariation of sexual size dimorphism and adult sex ratio in parasitic nematodes. Biological Journal of the Linnean Society, 62(4), 567–580.

Pullan, R. L., Smith, J. L., Jasrasaria, R., & Brooker, S. J. (2014). Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasites and Vectors, 7, 37.

Ramos, D. G. de S., Zocco, B. K. A., Torres, M. de M., Нsis, A. B., Pacheco R. de C., & Sinkoc, A. L. (2015). Helminths parasites of stray dogs (Canis lupus familiaris) from Cuiabá, Midwestern of Brazil. Semina Ciencias Agrarias, 36(2), 889–894.

Redman, W. K., Bryant, J. E., & Ahmad, G. (2016). Gastrointestinal helminths of Coyotes (Canis latrans) from Southeast Nebraska and Shenandoah area of Iowa. Veterinary World, 9(9), 970–975.

Robles, M. R., Navone, G. T., & Notarnicola, J. (2006). A new species of Trichuris (Nematoda: Trichuriidae) from Phyllotini rodents in Argentina. Journal of Parasitology, 92, 100–104.

Sakano, T., Hamamoto, K., Kobayashi, Y., Sakata, Y., Tsuji, M., & Usui, T. (1980). Visceral larva migrans caused by Trichuris vulpis. Archives of Disease in Childhood, 55(8), 631–633.

Scaramozzino, Р., Carvelli, А., Iacoponi, F., & De Liberato, С. (2018). Endoparasites in household and shelter dogs from Central Italy. International Journal of Veterinary Science and Medicine, 6(1), 45–47.

Singh, S., Samantaray, J. C., Singh, H., Das, G. B., & Verma, I. C. (1993). Trichuris vulpis infection in an Indian tribal population. Journal of Parasithology, 79(3), 457–458.

Skrjabin, K. I. (1928). Metod polnyh gel'mintologicheskih vskrytij pozvonochnyh, vkljuchaja cheloveka [The method of complete helminthological autopsy of vertebrates, including humans]. First Moscow State University, Moscow (in Russian).

Skrjabin, K. I., Shikhobalova, N. P., & Orlov, I. V. (1957). Trihocefalidy i kapilljariidy zhivotnyh i cheloveka i vyzyvaemye imi zabolevanija [Trichocephalids and capillariids of animals and man and the diseases caused by them. The essentials of nematodology]. Academy of Sciences of the USSR, Moscow (in Russian).

Soulsby, E. J. L. (1982). Helminths, arthropods and protozoa of domesticated animals (7th edition). Bailliere Tindall, London.

Spakulová, M. (1994). Discriminant analysis as a method for the numerical evaluation of taxonomic characters in male trichurid nematodes. Systematic Parasitology, 29, 113–119.

Stephenson, L. S., Holland, C. V., & Cooper, E. S. (2000). The public health significance of Trichuris trichiura. Parasitology, 121(l), 73–95.

Stroehlein, A. J., Young, N. D., Korhonen, P. K., Chang, B. C. H., Nejsum, P., Pozio, E., La Rosa, G., Sternberg, P. W., & Gasser, R. B. (2017). Whipworm kinomes reflect a unique biology and adaptation to the host animal. International Journal for Parasitology, 47(13), 857–866.

Taylor, M. A., Coop, R. L., & Wall, R. L. (2007). Veterinary parasitology (3th edition). Blackwell Publishing, Oxford.

Thapar, G. S., & Singh, K. S. (1954). Studies on the life-history of Trichuris ovis (Abildgaard, 1795) (fam. Trichuridae: Nematoda). Proceedings of the Indian Academy of Sciences, 40(3), 69–88.

Varodi, E. I., Malega, A. M., Kuzmin, Y. I., & Kornyushin, V. V. (2017). Helminths of wild predatory mammals of Ukraine. Nematodes. Vestnik Zoologii, 51(3), 187–202.

Vásquez, T. O., Martínez, B. I., Romero, C. R., Valencia, R. S., & Tay, Z. J. (1997). Mixed infection by Trichuris trichiura and Trichuris vulpis. Revista de Gastroenterología del Perú, 17, 255–258.

Xie, Y., Zhao, B., Hoberg, E. P., Li, M., Zhou, X., Gu, X., Lai, W., Peng, X., & Yang, G. (2018). Genetic characterisation and phylogenetic status of whipworms (Trichuris spp.) from captive non-human primates in China, determined by nuclear and mitochondrial sequencing. Parasites and Vectors, 11(1), 516.

Yevstafieva, V. A., Yuskiv, І. D., Melnychuk, V. V., Yasnolob, І. O., Kovalenkо, V. A., & Horb, K. O. (2018). Nematodes of the genus Тrichuris (Nematoda, Trichuridae) parasitizing sheep in central and south-eastern regions of Ukraine. Vestnik Zoologii, 52(3), 553–556.

Yevstafieva, V. А., Melnichuk, V. V., Sharavara, T. A., Sirenko, E. V., Makarevich, N. A., Kutsenko, Y. P., & Khlevnaya, G. S. (2018). Osobennosti embrional'nogo razvitija jaic nematod Trichuris skrjabini (Baskakov, 1924), parazitirujushhih u ovec [Specific features of embryonic development of Trichuris skrjabini (Baskakov, 1924) nematode eggs parasitizing in sheep]. An Agrarian Science of Euro-North-East, 62(1), 65–69 (in Russian).

Yevstafieva, V. А., Yuskiv, I. D., & Melnychuk, V. V. (2015). An investigation of embryo and eggshell development in Trichuris suis (Nematoda, Trichuridae) under laboratory conditions. Vestnik Zoologii, 50(2), 173–178.

Yoshikawa, H., Yamada, M., Matsumoto, Y., & Yoshida, Y. (1989). Variations in egg size of Trichuris trichiura. Parasitology Research, 75, 649–654.

Zanzani, S. A., Gazzonis, A. L., Scarpa, P., Berrilli, F., & Manfredi, M. T. (2014). Intestinal parasites of owned dogs and cats from metropolitan and micropolitan areas: Prevalence, zoonotic risks, and pet owner awareness in Northern Italy. BioMed Research International, 2014, 696508.

Published
2019-05-12
How to Cite
YevstafievaV. А., Kravchenko, S. O., Gutyj, B. V., Melnychuk, V. V., Kovalenko, P. N., & Volovyk, L. B. (2019). Morphobiological analysis of Trichuris vulpis (Nematoda, Trichuridae), obtained from domestic dogs . Regulatory Mechanisms in Biosystems, 10(2), 165-171. https://doi.org/10.15421/021924

Most read articles by the same author(s)