Intestinal helminths of dogs in Samarkand and the Samarkand region and their epidemiological significance

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Abstract

BACKGROUND: Dogs can be a source of various diseases for humans. The study of the helminth fauna of domestic and neglected dogs allows us to assess their danger to humans as a source of infection.

AIMS: To study the intestinal helminth fauna of domestic and neglected dogs living in the city of Samarkand and adjacent areas of the Samarkand region and to assess their epidemiological significance.

MATERIALS AND METHODS: 112 dogs of different ages from Samarkand and the surrounding area were examined. 45 animals were examined by the method of incomplete helminthological autopsy; diagnostic deworming was performed in 12 priotarny dogs; in 55 dogs, feces were examined once by the Fulleborn method.

RESULTS: In the examined dogs, 4 types of cestodes and 4 types of nematodes were found in the intestines. The most common type was dog tapeworm (Dipylidium caninum). The extent of invasion (EI) is 73.7%, the intensity of invasion (AI) is 5–56 copies. Taenia hydatigena tapeworm was detected during preventive deworming in 5 animals out of 12 (41.7%), and at autopsy in 18 dogs out of 45 (40%), AI 1–4 copies. The tapeworm of Echinicoccus granulosus was found in the autopsy of one dog out of 45 (EI 4.4%, AI-more than 350 copies). Mesocestoides lineatus cestodes were observed in the autopsy of 3 dogs (EI 6.7%, AI 1–2 copies). Trichuris (Trichocephalus) vulpis lived in the caecum of 20 dissected animals (EI 88%, AI 5–23 copies). During coproscopy of feces of 55 dogs, whipworm eggs were found in 25 animals (45.5%). Males and females of Toxocara canis were found in the intestines during autopsy of 5 animals (EI 22%, AI 2–4 copies). Eggs Toxocara coproscopy found in the feces of dogs 9 out of 55 (16.4 percent). The EI of the nematode Toxascaris leonina averaged 14.0%. AI 1–3 copies. The nematode Pterygodermatites (Rictularia) affinis was found in the singular (male) in the duodenum of one dissected dog.

CONCLUSIONS: In domestic and neglected dogs living in the territory of Samarkand and the Samarkand region, it was possible to establish the presence of 8 species of intestinal helminths, of which three species are dangerous to humans and have important epidemiological significance: E. granulosus, D. caninum and T. canis.

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In the history of the development of human civilization, dogs occupy an important place. According to modern historical data, these animals were domesticated about 15 thousand years ago and all the subsequent time were in close contact with humans. It is for this reason that some pathogens of dog diseases, including parasitic ones, have become more likely to enter the human body and use it as an intermediate or final host. The relationship between a man and a dog was formed in different peoples and social groups of human civilization in different ways, and in many ways depended on national, cultural, religious, etc. features. In some cases, the dog served as a decorative pet, which was constantly in close contact with the owner. In others , it was used exclusively for performing official functions: security, hunting, etc. The probability of transmission of pathogens from dogs to humans and other pets depends largely on the closeness of contact with them in space and time.
Uzbekistan has traditionally developed pastoral animal husbandry, mainly of small cattle. For grazing livestock local breeders employ a large number primarnih dogs. In addition, dogs are often kept in private households on a chain leash, performing security functions.
Samarkand is one of the major cities of Uzbekistan, which is the pearl of this country with a rich history, which is visited annually by hundreds of thousands of tourists from all over the world. As in any other major city, there is a problem of a high number of stray dogs in Samarkand. This problem is especially acute on the outskirts of the city, where stray dogs come into contact with other wild animals of the canine family (jackals and foxes-korsaks), which contributes to the effective exchange of various infectious agents between them. In this regard, the study of the parasitofauna of dogs, both domestic and neglected, allows us to establish the species composition of parasitic animals and assess their danger to humans as a source of infection.

The aim of the study: To study the intestinal helminth fauna of domestic and neglected dogs living in the city of Samarkand and the surrounding areas of the Samarkand region and to assess their epidemiological significance.

Methods
The research was conducted in 2016-19 on the basis of the L. M. Isaev Research Institute of Medical Parasitology (Samarkand, Republic of Uzbekistan).
The material for this work was the results of parasitological studies conducted in 112 dogs of various breeds and mongrels from Samarkand and the immediate vicinity. Methods of both intravital and postmortem study were used. The method of incomplete helminthological autopsy was used to examine 45 animals of different ages that died for various reasons. The detected helminths were preserved in saline solution, partially fixed in 70% alcohol and Barbagallo liquid. All materials were not labelled. The species identity of the detected helminths after cameral treatment was established according to the appropriate determinants [1]. Diagnostic deworming was performed on 12 priotarny dogs. For this purpose, arecoline bromide was used at a dose of 4 mg/kg of animal body weight. The drug was administered with water forcibly. After 30-40 minutes, the fecal secretions were examined by sequential washing (decantation) to detect helminths. A microscopic examination of the feces of 23 animals was carried out in the temporary detention center for stray dogs. In addition, helmintho-endoscopic studies of the feces of 32 yard dogs of different ages from various households in the city of Samarkand and the region were carried out. At the same time, the Fulleborn flotation method was used. Smear microscopy was performed at low and high magnification with the Olympus microscope. According to the results of the studies, the intensity of invasion (AI) and the extent of invasion (EI) were determined. All calculations were performed using the Microsoft Excel 2016 program.
Results
Main results of the study
The conducted parasitological studies allowed us to establish that almost all the examined dogs were infected with helminths. Helminthofauna was represented by 8 species - 4 species of cestodes and 4 nematodes.
When conducting an incomplete helminthological autopsy in dogs (45 individuals), the most frequently detected canine (pumpkin - shaped) tapeworm-Dipylidium caninum (Linnaeus, 1758), which was localized in the small intestine. The extent of infestation was 80%, with AI ranging from 5 to 56 specimens per animal. Such a high level of infection with canine tapeworm was associated with the fact that the intermediate hosts of this helminth – fleas – were present on absolutely all animals and in significant numbers.
During the preventive deworming of 12 priotarny dogs, dipilidium was found in the feces of every second animal (50%). The AI ranged from 2 to 12 copies. Thus, when examining dogs from both groups (autopsy and deworming), the AI was 73.7%.
It is worth noting that only direct methods of detecting sexually mature individuals in the intestines of dogs can assess the frequency and degree of infection with this helminthiasis. Since this parasite has a closed uterus, the eggs do not leave the limits of the segment, and, consequently, microscopic methods of examining feces are uninformative, giving a negative result even in deliberately invasive animals.
Human infection with D. caninum by local health authorities of the Republic of Uzbekistan is rarely registered, more often children, residents of rural areas, who are infected by accidental ingestion of fleas containing helminth cysticercoids. As a rule, this happens in close contact with domestic dogs. The disease in humans often proceeds latently, and the only sign is the detection of segments of this helminth in the feces, which outwardly resemble cucumber seed, and have mobility [2].
Tapeworm Taenia hydatigena (Pallas, 1766) was detected during preventive deworming in 5 animals out of 12 (41.7%), and at autopsy in 18 dogs out of 45 (40%), with the intensity of invasion ranging from 1 to 4 specimens. The intermediate hosts of the tapeworm are small ungulates, on the serous covers of the abdominal organs of which larvae (larvocysts - Cysticercus tennuicollis) are formed about the size of a chicken egg or more. Conducted a survey of butchers from private slaughterhouses in Moscow Samarkand and Samarkand region has allowed to establish that such education is often found on the gland of the abdomen of the sheep. Infected with the parasite, the omentum is either thrown away, and it becomes easy prey for stray dogs, or fed to their yard dogs, which are kept in slaughterhouses for protection. All this contributes to maintaining a high level of infection of both the final hosts (dogs) and intermediate ones (sheep). In some cases, cysticerci of this type of helminth can also parasitize humans [3,4.].
Sexually mature individuals of Echinococcus granulosus (Batsch, 1786) were found only in one individual out of 45 dissected (EI was 4.4%). Their number was more than 350 copies.
The circulation of this parasite, which is dangerous for humans, is carried out between representatives of the canid family and various herbivores. In the conditions of Uzbekistan, this most often happens with the participation of small cattle. When slaughtering animals and butchering carcasses, larvocist-affected liver and lungs are not properly disposed of, but, as in the case of Taenia hydatigena, are usually fed to dogs, or thrown into the trash. Methods of in vivo diagnosis in dogs, based on coproovoscopy, are uninformative, since this helminth has a closed uterus and there are practically no parasite eggs in the feces. In addition, morphologically, the eggs of Echinococcus are almost indistinguishable from those of other cestodes of the family Taenidae.
The low EI of echinococcus among the dogs we examined does not reflect their true infection, which is undoubtedly much higher. Most likely, most of the infected animals live in the vicinity of the city, where there is often a domestic slaughter of animals without proper veterinary and sanitary supervision. In addition, the high level of echinococcosis infection in the population (6-9 per 100,000 people), which has not been declining for many years, indicates a high proportion of infected animals among domestic and stray dogs. Every year in Uzbekistan, from 1.5 thousand to 4.5 thousand operations are performed for echinococcosis [5].
Mesocestoides lineatus (Goeze, 1782) cestodes were found at autopsy in 3 dogs out of 45 (6.7%) with an AI index of 1-2 specimens. Mesocestoides infected animals were from the suburbs of Samarkand, where a well-developed irrigation horticulture and agriculture. In these places, favorable conditions are created for the habitat and reproduction of intermediate hosts of this parasite. The first intermediate host is free – living soil mites, and the second is many rodent species. This helminth has no practical medical significance. Parasitization of these cestodes in the human body is extremely rare and has not been registered in Uzbekistan. [6]
Whipworms-Trichuris (=Trichocephalus) vulpis (Froelich, 1789) were found in the caecum of 20 dissected animals (88%) with an invasion intensity of 5 to 23 specimens. During diagnostic deworming of dogs, they were not detected in the feces. This is due to the peculiarity of the fixation of helminths, which are embedded in the submucosal layer of the intestine with their anterior end, which prevents their expulsion when exposed to arecoline bromide.
Coproscopy of the feces of domestic and dogs from the temporary detention center (a total of 55 individuals allowed to detect T. vulpis eggs in 25 animals (45.5%). This type of helminth in humans is not parasitic.

Toxocara canis (Werner, 1782) - canine ascariids, were found in the small intestine of 5 dogs during an incomplete helminthological autopsy (22%). The number of helminths in one organism ranged from 2 to 4 individuals. In all cases, both females and males were present. In diagnostic deworming 12 primarnih dogs Toxocara was not detected in any case.
Conducting coproscopic studies of domestic dogs (32 individuals) and dogs from a temporary holding kennel (23 individuals), toxocar eggs were found only in 9 young animals under the age of one year (16.4%). Such selective parasitism only in young animals is associated with the presence of a tissue migration stage in the development cycle of the parasite, during which the larvae of this helminth are in the organs and tissues of the animal for a long time. With numerous repeated infections, with age, the final host forms a sufficient immune response that prevents the complete completion of the helminth development cycle in the body, as a result of which the larvae that have again entered the blood die [7]. A similar situation is also known in humans in highly intense foci of hookworm and ascariasis, when the adult local population is less affected than visitors and children, and the invasion is much easier for them, and in some cases [8].
Toxocarosis-zoonosis, the incidence rate of people (according to serological epidemiological survey) varies from 2.6% in Belgium, 3.6% in Japan, 6.1% in the Netherlands to 51.0% in Taiwan, 68.2% in Colombia and about 80% in the Caribbean Islands [9].
There are currently no data on the incidence of toxocarosis in the Republic of Uzbekistan, since no such studies have been conducted.
Sexually mature nematodes Toxascaris leonina (Linstow 1902) were found in the small intestine of 5 out of 45 dissected animals (11.1%). Their number was small-1-3 individuals. Microscopy of feces from 32 domestic dogs revealed the eggs of these helminths in 4 samples (12.4%), and in 5 of 23 (21.7%) dogs that were in the temporary detention center of stray dogs. The average EI of T. leonina in all the examined animals was 14.0%.
Parasitism of toxascaris, in contrast to toxocars, was observed in dogs of different ages, which is typical for helminths, in the development cycle of which there is no migration phase. T. leonine has no medical significance
The nematode Pterygodermatites (=Rictularia) affinis (Jägerskiöld, 1909) was found in the singular (male) in the duodenum of one dissected dog. This is a biohelminth, whose intermediate hosts are various insects [7]. This type of medical value does not matter.

Limitations of the study
The obtained helminthoscopy data reflected the results of only a single study of dog feces. In this regard, the true EI indicators may be slightly higher.
Conclusion
Thus, in dogs, both domestic and unsupervised, living in the territory of Samarkand and the Samarkand region, it was possible to establish the presence of 8 species of intestinal helminths, of which three species are dangerous to humans and have important epidemiological significance. Of the cestodes, these are Echinicoccus granulosus and Dipylidium caninum, and of the nematodes, Toxocara canis.

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About the authors

Vladimir S. Turitsin

Saint-Petersburg State Agrarian University; Military medical academy of S.M. Kirov

Email: turicin_spb@mail.ru
ORCID iD: 0000-0001-9066-0026
SPIN-code: 2022-1869

Cand. Sci. (Biol.), Assistant Professor, Department of infectious diseases, with a course in medical Parasitology and tropical diseases

Russian Federation, 2 Peterburgskoe shosse, Pushkin, St. Petersburg, 196601; Saint Petersburg

Sergei S. Kozlov

Military medical academy of S.M. Kirov; Saint-Petersburg State Pediatric Medical University

Email: infectology@mail.ru
ORCID iD: 0000-0003-0632-7306
SPIN-code: 5519-6057

MD, Dr. Sci. (Med.), Professor

Russian Federation, 6, Acad. Lebedeva street, 194044 Saint Petersburg; Saint Petersburg

Olesya D. Achilova

L.M. Isaev Research Institute of Medical Parasitology

Author for correspondence.
Email: aleska-9090@inbox.ru
ORCID iD: 0000-0001-6045-2445
SPIN-code: 9664-0413

Junior research fellow

Uzbekistan, 38 Isayev str., Samarkand, 140105

References

  1. Kozlov DP. Determinant of helminths of predatory mammals of the USSR. Moscow : Nauka; 1977. 257 p. (In Russ).
  2. Parasitic diseases of humans (protozoans and helminthiasis): Handbook for doctors. Ed. by V.P. Sergiev, Yu.V. Lobzin, S.S. Kozlov. Saint-Petersburg : Folio; 2016. 640 p. (In Russ).
  3. Podyapolskaya VP, Kapustin VF. Helminthic diseases of man. Moscow : Medgiz; 1958. 663 p. (In Russ).
  4. Kufs H. Cysticercus tenuicollis and surgical therapy of cysticercosis cerbri [In Undetermined language]. Psychiatr Neurol Med Psychol (Leipz). 1953;5(1-2):13–15.
  5. Ilkhamov FA. Improvement of traditional and development of new methods of surgical treatment of echinococcosis of the liver [Sovershenstvovanie traditsionnykh i razrabotka novykh metodov khirurgicheskogo lecheniya ehkhinokokkoza pecheni] [dissertation abstract]. Tashkent; 2005. 32 p. (In Russ).
  6. DPDx ― Laboratory Identification of Parasites of Public Health Concern. Mesocestoidiasis. [Internet]. Available from: https://www.cdc.gov/dpdx/mesocestoidiasis/index.html
  7. Shulyak BF, Arkhipov IA. Nematodoses of dogs (zoonoses and zooanthroponoses). Moscow : ConsoMed; 2010. 495 p. (In Russ).
  8. Leikina ES. Main achievements in the study of helminthiasis immunology. Parasitology. 1976;10(2):115–124. (In Russ).
  9. Erofeeva VV. Ecological and epidemiological problems of toxocarosis in Russia. International Research Journal. 2017;(6):15–19. (In Russ). doi: 10.23670/IRJ.2017.60.005

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