Histopathological changes in the organism of rats under the chronic course of experimental infection with larvae of Eustrongylides excisus (nematoda: Dioctophymatidae)

  • S. L. Honcharov National University of Life and Environmental Sciences of Ukraine, the Ministry of Education and Science of Ukraine, 16, Polkovnyka Potekhina Str., Kyiv, Ukraine, 03041 https://orcid.org/0000-0001-7464-6689
  • N. M. Soroka National University of Life and Environmental Sciences of Ukraine, the Ministry of Education and Science of Ukraine, 16, Polkovnyka Potekhina Str., Kyiv, Ukraine, 03041 https://orcid.org/0000-0003-4559-6666
  • M. V. Galat National University of Life and Environmental Sciences of Ukraine, the Ministry of Education and Science of Ukraine, 16, Polkovnyka Potekhina Str., Kyiv, Ukraine, 03041 https://orcid.org/0000-0001-8881-0865
  • I. Yu. Pashkevich National University of Life and Environmental Sciences of Ukraine, the Ministry of Education and Science of Ukraine, 16, Polkovnyka Potekhina Str., Kyiv, Ukraine, 03041 https://orcid.org/0000-0003-0673-6249
  • R. O. Slobodian National University of Life and Environmental Sciences of Ukraine, the Ministry of Education and Science of Ukraine, 16, Polkovnyka Potekhina Str., Kyiv, Ukraine, 03041 https://orcid.org/0000-0001-8446-3851
  • A. I. Dubovyi Department of Molecular Medicine and Pathology, the University of Auckland, 85 Park Road, Auckland, Grafton 1023, New Zealand https://orcid.org/0000-0003-1979-9163
  • О. P. Lytvynenko State Scientific and Research Institute of Laboratory Diagnostics and Veterinary and Sanitary Expertise, State Service of Ukraine on Food Safety and Consumer Protection, 30, Donetska Str, Kyiv, 03151 Ukraine https://orcid.org/0009-0003-0682-8917
Keywords: Eustrongylides excisus, rats, experimental infection, histological testing, chronic course

Abstract

Aim. To evaluate the pathological effect of Eustrongylides excisus nematode larvae (L3–L4) on the organism of laboratory rats, the latter were infected per os by these parasites. The larvae of Eustrongylides excisus were obtained from perch (Perca fluviatialis, Linnaeus, 1758), caught in the Dnipro-Buh estuary – 46°37’48.45” N, 31°51’43.72” E, near the village of Dniprovske, Mykolaiv region (Ukraine). Methods. The experimental studies, which lasted for 30 days, were conducted using 15 non-linear male laboratory rats, which composed the experimental group by the analogy principle, three other animals were used as control. The intensity of the pathological process under the chronic course of eustrongylidosis was evaluated by the histological testing of the damaged organs of animals under investigation, which were euthanized after the completion of the waiting period. Results. The histological testing found pathological changes in the tissues of the brain, lungs, spleen, and organs of the gastrointestinal tract. There was a notable formation of non-specific granulomas (i.e. the ones, which were not found in the control group of animals), which consisted of adipose and connective tissue of mesostenium, mesocolon, and mesogaster. These granulomas had vivid exudative-proliferative inflammation and contained the elements of parasitic larvae (remnants of larvae bodies: fragments of cephalic and caudal ends, cuticles), which were subjected to considerable destructive changes. The walls of these granulomas consisted of fibrin and necrotic detritus. It was found that the animals of the group (the waiting period of 30 days) had mostly fibrino-purulent type of inflammatory reaction with the prevailing exudative-proliferative processes and the formation of non-specific granulomas. Conclusions. The results of scientific studies demonstrated necrotic and hypoxic-ischemic changes in the brain tissues; signs of cardiovascular deficiency, dystrophic and hypertrophic changes in the myocardium tissues; purulent inflammation of pleura and interstitial tissue of the lungs; changes in kidney tissues in the form of balloon dystrophy and granular degeneration of tubular epithelium; acute exudative-proliferative inflammation of the liver capsule and parenchyma; proliferation of white pulp with necrotic changes in lymphoid follicles; the thickness of the walls of gastrointestinal organs was considerably infiltrated with eosinophils, plasma cells, and macrophages. The phenomena of tissue hypertrophy and sclerosis as a pathomorphological response of the organism to the chronic course of the disease were determined.

References

Barros LA, Tortelly R, Pinto RM, Gomes DC (2004) Effects of experimental infections with larvae of Eustrongylides ignotus Jäegerskiold, 1909 and Contracaecum multipapillatum (Drasche, 1882) Baylis, 1920 in rabbits. Arq Bras Med Vet Zootec 56:325–332. https://doi.org/10.1590/S0102-09352004000300007

Biswas JK, Pramanik S, Kumar M (2023) Fish parasites as proxy bioindicators of degraded water quality of River Saraswati, India. Environ Monit Assess 195:818. https://doi.org/10.1007/s10661-023-11411-6

Branciari R, Ranucci D, Miraglia D, Valiani A, Veronesi F, Urbani E (2016) Occurrence of parasites of the genus Eustrongylides spp. (Nematoda: Dioctophymatidae) in fish caught in Trasimeno Lake, Italy. Italian Jour of Food Safety 5(6130):206–209. https://doi.org/10.4081/ijfs.2016.6130

Bruschi F, Chiumiento L (2011) Trichinella inflammatory myopathy: host or parasite strategy? Parasit Vectors 4:42. https://doi.org/10.1186/1756-3305-4-42

Cole RA (1999) Eustrongylidosis. In Field Manual of Wildlife Diseases: General Field Procedures and Diseases of Birds; U.S. Department of the Interior Fish and Wildlife Service: Washington, DC, USA 223–228

Clements TW, Tolonen M, Ball CG, Kirkpatrick AW (2021) Secondary Peritonitis and Intra-Abdominal Sepsis: An Increasingly Global Disease in Search of Better Systemic Therapies. Scandinavian Journal of Surgery 110(2):139–149. https://doi.org/10.1177/1457496920984078

Deardorff TL, Overstreet RM (1991) Sea food transmitted zoonoses in the United States: the fishes, the dishes, and the worms. In: Microbiology of marine food products (eds. DR. Ward and CR. Hackney). Van Nostrand Reinhold, New York 211–265

Dezfuli BS, Manera M, Lorenzoni M, Pironi F, Shinn AP, Giari L (2015) Histopathology and the inflammatory response of European perch, Perca fluviatilis muscle infected with Eustrongylides sp. (Nematoda). Parasit Vectors 8:227. https://doi.org/10.1186/s13071-015-0838-x

Eberhard ML, Hurwitz H, Sun AM, Coletta D (1989) Intestinal perforation caused by larval Eustrongylides (Nematoda: Dioctophymatoidae) in New Jersey. Am J Trop Med Hyg 40:648–650. https://doi.org/10.4269/ajtmh.1989.40.648

Eberhard ML, Ruiz-Tiben E (2014) Cutaneous emergence of Eustrongylides in two persons from South Sudan. Am J Trop Med Hyg 90:315–317. https://doi.org/10.4269/ajtmh.13-0638

El-Dakhly KM, El-Nahass E, Uni S, Tuji H, Sakai H, Yanai T (2012) Levels of infection of gastric nematodes in a flock of great cormorants (Phalacrocorax carbo) from Lake Biwa, Japan J Helminthol 86:54–63. https://doi.org/10.1017/S0022149X11000046

Franson JC, Cluster TW (1994) Eustronglyidosis in wading birds from colonies in California Texas and Rhode Island USA. Colonial Waterbirds 7(2):168–172. https://doi.org/10.2307/1521295

Fusco MA, Rizzo-Valente VS, Vizzoni VF, Miranda RS, Aguiar CC, Escaleira RDC (2023) An Outbreak of the Nematode Parasite Eustrongylides spp. (Nematoda: Dioctophymatidae) in a Zebrafish (Danio rerio) Facility. Zebrafish 20(3):126–130. https://doi.org/10.1089/zeb.2022.0041

Goncharov SL, Soroka NM, Pashkevich IY, Dubovyi AI, Bondar AO (2018) Infection of Predatory Fish with Larvae of Eustrongylides excisus (Nematoda, Dioctophymatidae) in the Delta of the Dnipro River and the Dnipro-Buh Estuary in Southern Ukraine. Vestnik Zoologii 52(2):137–144. https://doi.org/10.2478/vzoo-2018-0015

Guardone L, Ricci E, Susini F, Polsinelli E, Guglielmone G, Armani A (2021) First detection of Eustrongylides excisus (Nematoda: Dioctophymatidae) in big-scale sand smelt (Atherina boyeri) from the lake Massaciuccoli (Northwest Tuscany, Italy): implications for public health and seafood quality. Food Control 120:107517. https://doi.org/10.1016/j.foodcont.2020.107517

Guerin PF, Marapendi S, Grail SL (1982) Intestinal perforation caused by larval Eustrongylides. Maryland. MMWR Morb Mortal Wkly Rep 31:383–384. PMID: 6813668

Gunby P (1982) One worm in the minnow equals too many in the gut. JAMA 248:163. https://doi.org/10.1001/jama.1982.03330020011004

Honcharov SL (2019) Experimental infection of laboratory rats with larvae of the nematode Eustrongylides excisus (Nematoda: Dioctophymatidae). Ukrainian Journal of Veterinary Sciences 10(3):70–77. (In Ukrainian). https://doi.org/10.31548/ujvs2019.03.011

Honcharov SL (2020a) Pathological anatomic changes among laboratory rats in case of experimental infection with the larvae of the nematode Eustrongylides excisus (Nematoda: Dioctophymatidae). Animal Biol 22(1):30–37. https://doi.org/10.15407/animbiol22.01.003

Honcharov SL (2020b) Results of experimental infestation of laboratory rats with larvae of the nematode Eustrongylides excisus (Nematoda: Dioctophymatidae), selected from the roach (Rutilis rutilis Linnaeus 1758). Ukr J Veterin Sci 11(1):97–111. (In Ukrainian). https://doi.org/10.31548/ujvs2020.01.011

Honcharov SL (2020c) Prevalence of the nematodes Eustrongylides excisus Jägerskiöld, 1909 – larvae (Nematoda: Dioctophymatidae) infection in the Rutilis rutilis, Linnaeus, 1758 and the seasonal dynamics of the infection in the waters of the Dnipro-Buh Estuary in Southern Ukraine. Scientific Messenger of Lviv National University of Veterinary Medicine and Biotechnologies. Series: Veterinary sciences 22(97):31–38. (In Ukrainian). https://doi.org/10.32718/nvlvet9706

Honcharov SL, Kupriianova OM, Soroka NM, Halat MV, Dubovyi AI, Zhurenko OV (2022) The experimental invasion of rats with Eustrongylides excisus (Nematoda: Dioctophymatidae) larvae during the acute course of infection. Regulatory Mechanisms in Biosystems 13(2):99–104. https://doi.org/10.15421/022214

Karmanova EM (1968) Dioctophymidea of Animals and Man and the Diseases Caused by Them. Nauka Publishing: Moscow: 383. (In Russian)

Korniychuk YM, Pronkina NV, Belofastova IP (2008) Nematode Fauna of the round goby Apollonia (Neogobius) melanostomus in the Black Sea and Sea of Azov. Ecology of the sea 17–22

Lichtenfels JR, Stroup CF (1985) Eustrongylides sp. (Nematoda: Dioctophymatoidea): First Report of an Invertebrate Host (Oligochaeta: Tubificidae) in North America Proc Helminthol Soc Wash 52(2):320–323

Ljubojevica D, Novakov N, Djordjevicc V, Radosavljevicd V. Pelica M (2015) Potential parasitic hazards for humans in fish meat. Procedia Food Science 5:172–175. https://doi.org/10.1016/j.profoo.2015.09.049

Locke LN (1961) Heron and egret losses due to verminous peritonitis. Avian Dis 5:135–138

Measures LN (1988) Revision of the genus Eustrongylides Jägerskiöld, 1909 (Nematoda: Dioctophymatoidea) of piscivorous birds. Can J Zool 66:885–895. https://doi.org/10.1139/z88-131

Melo FT, Melo CS, Nascimento LC (2015) Morphological characterization of Eustrongylides ssp. Larvae (Nematoda, Dioctophymatoidea) parasite of Rhinella marina (Amphibia: Bufonidae) from Eastern Amazonia. Braz J Vet Parasitol Jaboticabal 25(2):7–12. https://doi.org/10.1590/S1984-29612016024

Narr LL, O’Donnell JG, Libster B, Alessi P, Abraham D (1996) Eustrongylidiasis – a parasitic infection acquired by eating live minnows. J Am Ost Assoc 96:400–402

Noei MR, Ibrahimov S, Sattari M (2015) Parasitic worms of the Persian sturgeon, Acipenser persicus Borodin, 1897 from the southwestern shores of the Caspian Sea. Iran J Ichthyol 2:287–295

Novakov N, Bjelic-Cabrilo O, Circovic M, Jubojevik D, Lujic J (2013) Eustrongylidosis of European Catfish (Siluris glanis). Bulg J Agric Sci 1:72–76

Panesar TS, Beaver PC (1979) Morphology of the Advanced-Stage Larva of Eustrongylides wenrichi Canavan, 1929 Occurring Encapsulated in the Tissues of Amphiuma in Louisiana. J Parasitol 65(1):96

Pazooki J, Masoumian M, Yahyazadeh M, Abbasi J (2007) Metazoan Parasites from Freshwater Fishes of Northwest Iran. J Agric Sci Technol 9:25–33

Rohlenová K, Morand S, Hyršl P, Tolarová S, Flajšhans M, Šimková A (2011) Are fish immune systems really affected by parasites? An immunoecological study of common carp (Cyprinus carpio). Parasit Vectors 4:120. https://doi.org/10.1186/1756-3305-4-120

Rusconi A, Prati P, Bragoni R, Castelli M, Postiglione U, Rigamonti S, Sassera D, Olivieri E (2022) Occurrence of Eustrongylides excisus (Nematoda: Dioctophymatidae) in European Perch (Perca fluviatilis) and Great Cormorant (Phalacrocorax carbo) in Lake Annone, Northern Italy. J Parasitol 108(2):209–216. https://doi.org/10.1645/20-175

Shirazian D, Schller EL, Glaser CA, Vondeerfecht SL (1984) Pathology of larval Eustrongylides in the rabbit. J Parasitol 70(5):803–806

Sinyaeva DM (2014) Potentially dangerous for humans nematodes of our region. Materials of the I All-Ukrainian scientific-practical conference of young scientists and students with international participation. October 8–9, 2014, Dnepropetrovsk, Ukraine 170–172. (In Russian)

Sloboda M, Mihalca A, Falka I, Petrzelkova K, Carlsson M, Ghira I, Modry D (2010) Are gobiid fish more susceptible to predation if parasitized by Eustrongylides excisus? An answer from robbed snakes. Ecological Research 25:469–473. https://doi.org/10.1007/s11284-009-0676-4

Soylu E (2013) Metazoan Parasites of Perch Perca fluviatilis L. From Lake Sığırcı, Ipsala, Turkey. Pakistan J Zool 45(1):47–52

Wittner M, Turner JW, Jacquette G, Ash RL, Salgo MP, Tanowitz HB (1989) Eustrongylidiasis – A Parasitic Infection Acquired by Eating Sushi. The England Journal of Medicine 320:1124–1126. https://doi.org/10.1056/NEJM198904273201706

Yermolenko SV, Gasso VA, Hahut AM, Spirina VA (2022) Infection of Dice Snake, Natrix tessellata (Reptilia, Colubridae), with Eustrongylides excisus (Nematoda, Dioctophymatidae) in the Middle and Lower Dnipro River Basin. Zoodiversity 56(4). https://doi.org/10.15407/zoo2022.04.341

Published
2023-11-01
How to Cite
Honcharov, S. L., Soroka, N. M., Galat, M. V., Pashkevich, I. Y., Slobodian, R. O., Dubovyi, A. I., & LytvynenkoО. P. (2023). Histopathological changes in the organism of rats under the chronic course of experimental infection with larvae of Eustrongylides excisus (nematoda: Dioctophymatidae). Agricultural Science and Practice, 10(2), 16-27. https://doi.org/10.15407/agrisp10.02.016