Pathomorphological changes in the large intestine of rabbits parasitised by Passalurus ambiguus (Nematoda, Oxyuridae)
AbstractPassaluriasis is a common infestation of lagomorphs, which clinically manifests in intense itching around the anus, various disorders of digestion and loss of weight. We performed a study of infested rabbits of the seryi veleten breed, which were kept in individual farms in Poltava Oblast (Ukraine). During the autopsy, in the cavity of the large intestine, there were found small, spindle-like helminths of white colour. Out of 10 rabbits, 846 nematodes were extracted (369 males and 477 females, identified as Passalurus ambiguus (Rudolphi, 1819) Dujardin, 1845. It was determined that the extensity of infestation in female rabbits reached 56.4%, male rabbits – 43.6%. The results of metric parameters of the nematodes are as follows: mean body length of males equaled 4.6 ± 0.4, females – 9.7 ± 1.21 mm, and maximum width – 257.4 ± 17.8 and 546.2 ± 37.1 µm respectively. A common feature of mature nematodes of this species is the presence of a rounded extension (bulbus) at the end of the esophagus. During chronic course of passaluriasis in rabbits, pathomorphological changes developed in the large intestine. The upper epithelium of the large intestine was damaged in some places, certain epithelian cells were found in the lumen of the intestine. The intestinal glands are widened, filled with slimy content of mostly dark blue-violet colour, especially in the upper sections of the glands. In the deep sections of the glands, slime was almost transparent. In deep sections of the glands the slime was almost transparent. In the epithelium cells of the glands, slimy granules were also of basophilic colour. The muscularis mucosae of the mucous membrane, especially between the intestinal glands was swollen, had practically no colour, the collagen fibers were stretched, thinned-out. Edemas were also recorded in the tela submucosa. In some preparations, the muscularis mucosae was notably infiltrated by lymphoid cells and histiocytes. On large extensions, we found some signs of hypersecretion of slime in goblet cells of the intestinal glands as accumulations of granules of slime in the cytoplasm, which had poorly developed colouration. On the side of the muscular and serous membranes, no pathological changes were found. The information presented here indicates the relevance of passaluriasis infestation as an etiological factor of occurrence of chronic catarrhal colitis with lymphohistiocytosis.
Batte, E. G., Mclamb, R. D., Muse, K. E., Tally, S. D., & Vestal, T. J. (1977). Patho physiology of swine trichuriasis. American Journal of Veterinary Research, 38, 1075–1079.
Bordes, F., Langand, J., Feliu, C., & Morand, S. (2007). Helminth communities of an introduced hare (Lepus granatensis) and a native hare (Lepus europaeus) in Southern France. Journal of Wildlife Diseases, 43(4), 747–751.
Boyko, O. O., Zazharska, N. M., & Brygadyrenkо, V. V. (2016). The influence of the extent of infestation by helminths upon changes in body weight of sheep in Ukraine. Biosystems Diversity, 24(1), 3–7.
Camps-Bossacoma, M., Perez-Cano, F. J., Franch, A., Untersmayr, E., & Castell, M. (2017). Effect of a cocoa diet on the small intestine and gut-associated lymphoid tissue composition in an oral sensitization model in rats. Journal of Nutritional Biochemistry, 42, 182–193.
Duda, Y. V., Kunieva, L. V., & Khrystian, O. P. (2017). Pokaznyky bilkovoho obminu kroliv za pasaluroznoi invazii [Indicators of protein metabolism of rabbits for pasaluronic invasion]. Science and Technology Bulletin of SRC for Biosafety аnd Environmental Control of AIC, 5(1), 93–96 (in Ukrainian).
Edwards, E. E., Garner, B. C., Williamson, L. H., Storey, B. E., & Sakamoto, K. (2016). Pathology of Haemonchus contortus in New World camelids in the southeastern United States: A retrospective review. Journal of Veterinary Diagnostic Investigation, 28(2), 105–109.
Eira, C., Torres, J., Miquel, J., & Vingada, J. (2007). The helminth parasites of the wild rabbit Oryctolagus cuniculus and their effect on host condition in Dunas de Mira, Portugal. Journal of Helminthology, 81(3), 239–246.
Elshahawy, І., & Elgoniemy, А. (2018). An epidemiological study on endoparasi tes of domestic rabbits (Oryctolagus cuniculus) in Egypt with special reference to their health impact. Sains Malaysiana, 47(1), 9–18.
Emerya, D. L., Huntb, P. W., & Le Jambrec, L. F. (2016). Haemonchus contortus: The then and now, and where to from here? International Journal for Parasi tology, 46(12), 755–769.
Eslampanah, M., Paykari, H., Moharami, M., Motamedi, G., & Omraninava A. (2014). A survey on the gastrointestinal parasites of rabbit and guinea pig in a laboratory animal house. Archives of Razi Institute, 69(1), 77–81.
Fernández-Aguilar, X., Alzaga, V., Villanúa, D., Cabezón, O., García-Bocanegra, I., Dubey, J. P., & Almería, S. (2013). Epidemiology and prevalence of Toxoplasma gondii infection in the Iberian hare (Lepus granatensis). Veteri nary Parasitology, 196, 194–198.
Florian, D. D. (1997). Passaluroz krolikov v usloviyah Moskovskoy oblasti: Bio logiya vozbuditelya, epizootologiya i meryi borbyi [Passalurosis of rabbits in the conditions of the Moscow region: Pathogen biology, epizootology and control measures]. Moscow (in Russian).
Frank, R., Kuhn, T., Mehlhorn, H., Rueckert, S., Pham, D., & Klimpel, S. (2013). Parasites of wild rabbits (Oryctolagus cuniculi) from an urban area in Germa ny, in relation to worldwide results. Parasitology Research, 112, 4255–4266.
Gavrylin, P. M., & Nikitina, M. O. (2017). Morphometric parameters of the intes tine and aggregated lymphatic nodules of meat rabbits. Regulatory Mecha nisms in Biosystems, 8(4), 649–655.
Georgieva, K., Yoneva, A., Mizinska-Boevska, Y., & Todev, I. (2005). Ultra structure of the contact surfaces of Passalurus ambiguus (Rudolphi, 1819) (Nematoda). Acta Biologica Hungarica, 56(3–4), 297–303.
Goral's'kyj, L. P., Homych, V. T., & Konons'kyj, O. I. (2005). Osnovy gistologich noji tehniky i morfofunkcional'ni metody doslidzhen' u normi ta pry patologiji [Fundamentals of histological technique and morphofunctional methods of research in norm and in pathology]. Polissja, Zhytomyr (in Ukrainian).
Ilić, T., Stepanović, P., Nenadović, K., & Dimitrijević, S. (2018). Improving agri cultural production of domestic rabbits in Serbia by follow-up study of their parasitic infections. Iranian Journal of Veterinary Research, 19(4), 290–297.
Iliev, P. T., Ivanov, A., Kirkova, Z., Hristov, K., Dinkova, K., & Ananiev, J. (2017). Some parasitological, pathological and immunohistochemical examinations in sheep naturally infected by Trichuris ovis. Trakia Journal of Sciences, 2, 174–178.
Jabbar, A., Campbell, A. J. D., Charles, J. A., & Gasser, R. B. (2013). First report of anthelmintic resistance in Haemonchus contortus in alpacas in Australia. Parasites and Vectors, 6, 243.
Kruchynenko, O. V., Skrypka, M. V., & Panikar, I. I. (2017). Osoblyvosti pato morfolohichnykh zmin v stintsi kyshechnyku za shlunkovo-kyshkovykh stronhiliatoziv velykoi rohatoi khudoby [Features of the pathological changes in the intestinal wall at gastrointestinal strongylyatosis of cattle]. The Animal Biology, 19(2), 44–49 (in Ukranian).
Kumar, S., Jakhar, K. K., & Singh, A. D. (2015). Etio-pathological investigations to study the gross and histopathological lesions affecting gastrointestinal tract of sheep. Academic Journals, 10, 356–361.
Laakkonen, J., Nyyssönen, T., Hiltunen, M., Kauhala, K., Nikander, S., & Soveri, T. (2006). Effects of Protostrongylus sp. and Pneumocystis sp. on the pulmonary tissue and the condition of mountain and brown hares from Finland. Journal of Wildlife Diseases, 42(4), 780–787.
Lello, J., Boag, B., & Hudson, P. J. (2005). The effect of single and concomitant pathogen infections on condition and fecundity of the wild rabbit (Oryctola gus cuniculus). International Journal for Parasitology, 32, 1509–1515.
Lopes Torres, E. J., Nascimento, A. P. F., Menezes, A. O., Garcia, J., José dos Santos, M. A., Maldonado Jr., A., Miranda, K., Lanfredi, R. M., & Souza, W. (2011). A new species of Trichuris from Thrichomys apereoides (Rodentia: Echimyidae) in Brazil: Morphological and histological studies. Veterinary Parasitology, 176, 226–235.
Mohanta, U. K., Anisuzzaman, A., Farjana, T., Das, P. M., Majumder, S. & Mondal, M. M. H. (2007). Prevalence, population dynamics and pathological effects of intestinal helminths in black Bengal goats. Bangladesh Journal of Veterinary Medicine, 5, 563–569.
Mowat, A. M. (2003). Anatomical basis of tolerance and immunity to intestinal antigens. Nature Reviews Immunology, 3, 331–341.
Okumu, P. O., Gathumbi, P. K., Karanja, D. N., Mande, J. D., Wanyoike, M. M., Gachuiri, C. K., Kiarie, N., Mwanza, R. N., & Borter, D. K. (2014). Preva lence, pathology and risk factors for coccidiosis in domestic rabbits (Oryctolagus cuniculus) in selected regions in Kenya. Veterinary Quarterly, 34(4), 205–210.
Ola-Fadunsin, S. D., & Ibitoye, E. B. (2017). A retrospective evaluation of parasitic conditions and their associated risk factors in sheep and goats in Osun state, Nigeria. Sokoto Journal of Veterinary Sciences, 15(3), 15–24.
Ola-Fadunsin, S. D., Hussain, K., Rabiu, M., & Ganiyu, I. A. (2018). Parasitic conditions of domestic owned rabbits in Osun State, Southwestern Nigeria: Retrospective evaluation, risk factors and co-infestations. International Jour nal of Veterinary Science and Medicine, 6(2), 208–212.
Pehlivanoğlu, B., Doğanavşargil, B., Sezak, M., Nalbantoğlu, İ., Korkmaz, M. (2016). Gastrointestinal parasitosis: Histopathological insights to rare but int riguing lesions of the gastrointestinal tract. Türkiye Parazitoloji Dergisi, 32(2), 82–90.
Pinto, R. M., Gomes, D. C., Menezes, R. C., Gomes, C. T., & Noronha, D. (2004). Helminths of rabbits (Lagomorpha, Leporidae) deposited in the helmintho logical collection of the Oswaldo Cruz Institute. Revista Brasileira de Zoologia, 21(3), 599–604.
Rewatkar, S. G., Deshmukh, S. S., Prem Kumar, G., Maske, D. K., & Bhangale, G. N. (2013). Occurrence of gastrointestinal helminthes in rabbits with special reference to importance of Giardia spp. as parasitic zoonoses. Science, Technology and Arts Research Journal, 2(3), 142–143.
Rinaldi, L., Russo, T., Schioppi, M., Pennacchio, S., & Cringoli, G. (2007). Passa lurus ambiguus: New insights into copromicroscopic diagnosis and circadian rhythm of egg excretion. Parasitology Research, 101(3), 557–561.
Rose, H., Hoar, B., Kutz, S. J., & Morgan, E. R. (2014). Exploiting parallels between livestock and wildlife: Predicting the impact of climate change on gastrointestinal nematodes in ruminants. International Journal for Parasito logy: Parasites and Wildlife, 15(2), 209–219.
Sharma, R., Kapoor, D., & Kumar, R. (2017). A rare case of verminous pneumo nia in domestic rabbit. Journal of Parasitic Diseases, 41(3), 716–717.
Sheng, L., Cui, P., Fang, S. F., Lin, R. Q., Zou, F. C., & Zhu, X. Q. (2014). Sequence variability in four mitochondrial genes among rabbit pinworm (Passalurus ambiguus) isolates from different localities in China. The Journal of DNA Mapping, Sequencing, and Analysis, 26(4), 501–504.
Sicherer, S. H., & Sampson, H. A. (2010). Food allergy. Allergy and Clinical Immunology, 125, 116–125.
Sultan, K., Elhawary, N. M., Sorour, S. S. G., & Sharaf, H. M. (2015). Observati ons of the rabbit pinworm Passalurus ambiguus (Rudolphi, 1819) in domes tic rabbits (Oryctolagus cuniculus) in Egypt using a scanning electron microscope. Tropical Biomedicine, 32(4), 745–752.
Sürsal, N., Gökpinar, S., & Yildiz, K. (2014). Prevalence of intestinal parasites in hamsters and rabbits in some pet shops of Turkey. Türkiye Parazitoloji Dergisi, 38(2), 102–105.
Szkucik, K., Pyz-Łukasik, R., Szczepaniak, K. O., & Paszkiewicz, W. (2014). Occurrence of gastrointestinal parasites in slaughter rabbits. The Journal Parasitology Research, 113(1), 59–64.
Vighi, G., Marcucci, F., Sensi, L., Di Cara, G., & Frati, F. (2008). Allergy and the gastrointestinal system. Clinical and Experimental Immunology, 153, 3–6.
Yevstafieva, V. А., Yeresko, V. I., Pishchalenko, M. А., & Nagorna, L. V. (2018). Differential species characters of Baruscapillaria anseris and B. obsignata nematodes obtained from the domestic goose. Regulatory Mechanisms in Biosystems, 9(4), 578–583.
Yevstafіeva, V. A., Melnychuk, V. V., Nikiforova, О. V., Suprunenko, К. V., Korchan, L. N., Lokes-Krupka, Т. Р., Nehrebetskyi, I. S., & Korchan, N. І. (2018). Comparative morphology and biology of nematodes of genus Heterakis (Nematoda, Heterakidae), parasites of the domestic goose (Anser anser). Regulatory Mechanisms in Biosystems, 9(2), 229–236.
Zon, H. A., (2005). Patolohichna anatomiia parazytarnykh khvorob tvaryn [Patho logical anatomy of parasitic animal diseases]. Dzherelo, Sumy (in Ukrainian).
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