A survey On endoparasites and ectoparasites In domestic dogs and cats In Vladivostok, Russia 2014 T.V. Moskvina, L.V. Zheleznova PII: DOI: Reference:
S2405-9390(15)30016-2 doi: 10.1016/j.vprsr.2016.02.005 VPRSR 6
To appear in: Received date: Revised date: Accepted date:
11 November 2015 5 February 2016 19 February 2016
Please cite this article as: Moskvina, T.V., Zheleznova, L.V., A survey On endoparasites and ectoparasites In domestic dogs and cats In Vladivostok, Russia 2014, (2016), doi: 10.1016/j.vprsr.2016.02.005
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ACCEPTED MANUSCRIPT A Survey On Endoparasites And Ectoparasites In Domestic Dogs And Cats In Vladivostok, Russia 2014
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Moskvina T. V., Zheleznova L. V.
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School of Natural Sciences, Far Eastern Federal University
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Vladivostok, 8 Suhanova str.
phone. (423)2433472; e-mail:
[email protected]
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Moskvina Tatyana Vladimirovna is a postgraduate student; e-mail:
[email protected] Zheleznova Ludmila Valeryevna holds a PhD in biological sciences, and is an assistant professor ;
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e-mail:
[email protected] Abstract: The present survey aims to establish the prevalence of ecto- and endoparasitic
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infestations in dogs and cats in Vladivostok city in 2014. Between December 2013 and
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December 2014, 157 dogs (68 females and 89 males) and 80 cats (29 females and 51
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males) were included in a study conducted in the School of Natural Sciences, Far Eastern Federal University and veterinarian hospitals in Vladivostok. For each animal, ectoparasites and Demodex spp. were identified with the help of cerumen and epidermis
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samples microscopy. Endoparasites were identified through standard coproscopical examinations of fresh faecal samples using the sedimentation-flotation methods. Endoparasites, including gastro-intestinal helminths and protozoans, were identified in 51 % of the cats, Toxascaris leonina being the most commonly diagnosed (7.8%). As for ectoparasites in the cats, Otodectes cynotis only was identified (75%). Endoparasites were identified in 26.8 % of the dogs, the most common endoparasite diagnosed being Ancylostoma caninum (10.3 %). Dogs in the age groups 13 to 36 months and cats over 3 years of age showed significantly higher infection rates – 33.3% and 46.6 %, respectively. In 97 dog faecal samples examined, only one type of parasite was found. In 51 cat fecal samples examined, only one type of endoparasite was found in 50 cats (94.7%) and 1
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ACCEPTED MANUSCRIPT sample (5.3%) contained 2 different endoparasites. As for canine ectoparasitism, Otodectes cynotis (Acari: Psoroptidae Conoor, 1984) (29.4 %), and Сheyletiella yasguri (Acari:Cheyletidae Leach, 1815) (2.1 %) were identified. Prevalence of Demodex canis
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(Acari: Demodicidae Nicolet, 1855) amounted to 6.25 %.
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Conclusions: This survey demonstrates that parasitism is far from being rare among
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Vladivostok’s cats and dogs populations.
Key words: prevalence, ectoparasites, endoparasites, cat, dog
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1. Introduction
Dogs and cats are by far the most common household animals worldwide, including Russia. In Russia, 60 % household owners keep a cat or a dog (Intesco Research Group, 2013). In
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Vladivostok, the dog population has been estimated at 60, 000. No data on the size of the cat population is available. Domestic animals cohabitating with humans can be responsible for
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spreading a wide spectrum of zoonotic diseases. Moreover, parasites damage other domestic animal’s health. Intestinal parasites can cause anorexia, diarrhea, anemia and intestinal disorders,
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with the greatest mortality in young and immunocompromised animals (Neves et al., 2014). Parasite communities and prevalence of parasites can vary due to the season of the year, climate, geographical region, veterinary care quality and frequency, and animals’ living conditions (stray/household) (Mircean et al., 2010). The aim of our study is to investigate prevalence of ecto- and endoparasites in cats and dogs in Vladivostok.
2. Materials and methods
Materials, including faecal samples, skin scrapings and cerumen samples, were taken from household dogs and cats in Vladivostok. Materials were analyzed in veterinary clinics in Vladivostok and in the parasitology laboratory, School of Natural Sciences, Far Eastern Federal 2
ACCEPTED MANUSCRIPT University, Vladivostok. The research was conducted from December 2013 to December 2014. The total number of the animals investigated amounted to 237- 156 dogs (68 females and 89 males) aged from 1.5 months to 12.5 years old and 80 cats (29 females and 51 males) aged from
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1 month to 18 years old (Tables 1, 2). All of the animals had been kept in apartments or detached
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houses in Vladivostok. Faecal samples for detecting protozoan parasites, helminthes, helminthes’
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eggs and cestode proglottids were taken from animals with gastrointestinal disorders symptoms as well as from healthy animals brought in for veterinary preventive checkups. Cerumen samples
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were taken for otodectosis identification from animals suffering from otitis; cats were the most common patients. Skin scrapings were taken from animals with skin lesions symptoms; include
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alopecia, pruritus and hyperemia.
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2.1 Characterization of researched locality
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Vladivostok is the largest city in the Far Eastern Region (43°06′20 ″ N, 131°52′24 ″ E), and
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capital of Primorskiy region. It is situated on the coast of Sea of Japan, an area characterized by a monsoonal climate, with cold and snowy winters and warm and rainy summers. The average maximum and minimum temperatures over 2009 to 2014 were -23.9 °C and 30 °C respectively.
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Humidity levels for Vladivostok are 57-60 % per year. Average amount of snowfall in the winter is 47 cm. The Vladivostok population is approximately 600000. 2.2 Faecal examination
Most samples were sent to the laboratory and were examined on the same day; some samples were stored before examination at 6 Cº for 2-3 days. Every faecal sample was examined using Fulleborn’s method (Połozowski et al, 2006, Vjatkina, 2015) and for flatworm’s eggs identification using a sedimentation method (Kaufmann, 1996). Fulleborn’s method uses saturated NaCl solution (400 g NaCl per 1 l water). Fecal samples of 3-5 g were placed in 10 ml glass jar with a saturated NaCl solution and mixed thoroughly using a glass rod, samples were
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ACCEPTED MANUSCRIPT stored in salt solution for 30-40 min. Then surfaced helminthes eggs and protozoan cysts were collected using a copper loop and placed on the slide with some drop of glycerol added.
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2.3 Ectoparasites and Demodex mites’ examination
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Common diagnostic methods used to detect ectoparasites including Notoedris cati, Сheyletiella
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yasguri. and Demodex mites are based on microscopic analysis of skin scrapings. A modified deep skin scraping technique was used: the scrapings were performed on the boundary of healthy
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and affected areas avoiding capillary bleeding. For lightening, the skin scrapings were placed on the slide with some drops of 10 % NaOH solution added and placed into an incubator at 25 °C
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for 40 min. Fleas and ticks were detected with the help of a fine-toothed comb. Otoscopic evaluation was used for Otodectes cynotis identification. Cerumen samples were collected and
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microscopic examinations were performed.
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2.4 Statistical analyses
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The prevalence was calculated for each parasite. Correlation between parasitism and sex and
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between parasitism and age was made using the Pearson chi-squared test with Yates correction
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r
c
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( Oij Eij 0.5) Eij
i 1 j 1
, i being line number, j – column number, Oij – the
actual number of observations in a cell ij, Eij – the expected number of observations in a cell ij For samples, where the quantitative value of at least the 1st criterion was less than 5, we used Fisher exact test:
~ 2
F
~ 2
~ being sampling distribution , 2
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ACCEPTED MANUSCRIPT 3. Results
3.1 Faecal samples examination results
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Faecal samples from 97 household dogs and 54 cats were examined for endoparasitic
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infestations. The faecal examination showed that 26 dogs (26.8 %) and 20 cats (51.2 %) were
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positive for parasitic infestation. Helminthes were found in 19 dogs’ faecal samples (19.5 %) which included Taenia sp., Dipylidium caninum and 3 species of nematodes, the most common
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being Ancylostoma caninum (10.3 %) (Table 3). High infestation rates of A. caninum depend on environmental conditions. A. caninum larvae development is favored by a wet and warm
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climate(Croese, 1995).Helminthes were also found in 13 cats’ faecal samples, which included D. caninum, Hymenolepis diminuta, Toxascaris leonina and Uncinaria stenocephala. The most
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common parasite found was T. leonina (Table 3). Cystoisospora spp. were found in 7 dogs’
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faecal samples and 7 cats’ faecal samples; (Table 3). In 97 faecal samples from dogs only one
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type of parasites was found. In 51 faecal samples from cats examined 94.7 % contained only one type of parasites, and 5.3 % contained two different species (Table 3).
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3.2 Correlation between age/sex and intestinal parasitism No correlation between age and parasitic infestation in cats and dogs was found (p>0.05). Intestinal parasites were found in dogs aged between 2 months and 7 years and in cats aged between 1 month and 17 years. Prevalence in dogs aged 13 – 36 months was 33.3%, in dogs under 1 year of age it was 23.5 %, and in dogs over 3 years old it equaled 22 %. Prevalence in cats over 3 years of age was 46.6 %, in cats aged 13-36 months was 42.8 %, and in cats under 1 year of age it amounted to 27.2 % . No correlation between sex and gastrointestinal parasitism in cats and dogs was found (p>0.05). Sex distribution in infested animals was different: among dogs there were 17 infested males
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ACCEPTED MANUSCRIPT (29.8 %) and 8 females (20 %), among cats there were 11 infested males (35.5 %) and 8 females (40 %). 3.3 Skin scrapings and cerumen samples examination results
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Demodex canis was identified in 6.25 % of the dogs (Fig. 4). Ectoparasites were reported in 5
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dogs (29.4 %), ear mites Otodectes cynotis included, Cheyletiella yasguri was found in 1 female
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dog (2.1 %) (Table 4).
Only ear mites Otodectes cynotis were found in cats, the infestation rate being 75 % (Table 4,
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Fig. 5).
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3.4 Correlation between age/sex and O. cynotis infestation rates Correlation was not found between Otodectes cynotis infestation and animal’s age for either cats
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or dogs (p>0.05). Otodectes cynotis were found in 9 cats under 1 year of age (100 %), in 5 cats
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13-36 months (75 %) and in 3 cats over 3 years of age (42.8 %); 44.4% of dogs under 1 year
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were infested by ear mites; and in 1 case otodectosis were found in dogs over 1 year of age. There is no correlation between sex and otodectosis in cats or dogs (p>0.05). Sex distribution in infested animals was different: 3 infested males (37.5%) as compared to 2 females (22.2 %)
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among the dogs, among cats, there were 14 infested males (77.7 %) and 4 females (22.2 %).
3.4 Seasonal dynamics of parasitism in Vladivostok Seasonal dynamics analysis showed that gastrointestinal parasites infestation in dogs appeared throughout the year, except for February. The largest number of infested dogs was noted in October. In winter, the number of infested dogs decreased, while in spring and summer gastrointestinal parasitism among dogs was more frequent. Among cats, gastrointestinal parasites infestations were dissimilar during the year. The largest number of infested cats appeared in December and May, whereas in April and September infested cats were not found (Fig.1).
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ACCEPTED MANUSCRIPT Acariasis in 9 dogs – including demodecosis, cheyletiellosis and otodectosis - were found. Cats were infested by ear mites Otodectes cynotis, the largest number of infested cats was registered
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in November and January, while in July and September infested cats were not found (Fig. 2).
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4. Discussion
In the present survey we used Fulleborn’s method for endoparasiteidentification in faecal
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samples. It is a good method for detection gastrointestinal helminthes and protozoan parasites, but it has a low sensitivity in case of Trichuris vulpis infestation in dogs and for larvae detection
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(Połozowski et al, 2006). However this method is simple and has good sensitivity for Toxocara, Ancylostoma and Cestoda eggs detection and is frequency used in Russia (Vjatkina, 2015). The
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present data do not considerably differ from other Russian investigators’ studies on
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endoparasites in domestic cats and dogs using flotation methods with saturated NaCl solution (Fulleborn’s method and its modification). However, such worldwide cats’ and dogs’ parasites as
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Toxocara cati (syn. T. mystax (Sprent, 1956) и Trichuris vulpis Froelich, 1789, Giardia spp. и Toxoplasma gondii Nicolle & Manceaux, 1908, which were found in other Russian cities, were
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not registered in Vladivostok (Table 5, Fig. 3). In the present study, helminthes and protozoan parasite infestations were frequently found in animals over 1 year of age, although in other reports gastrointestinal parasites were frequently registered in animals under 1 year old. Toxocara canis can be transmitted transplacentally and infection decreases significantly as the animal grows older (Becker et all, 2012; Neves et all, 2014). Contrary to this, only 1 puppy infected by T. canis was found in Vladivostok. The prevalence of gastrointestinal parasites found in this survey is smaller than in Russia’s central regions. Prevalence of Dipylidium caninum in cats amounted to 29.6 % in Ivanovo and 26.4 % in Voronezh. In dogs, prevalence of D. caninum was 60.3 % in Ivanovo and 19.1 % in Voronezh. In dogs, prevalence of T. canis was 37.2 % in Ivanovo and 33.3 % in Voronezh and
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ACCEPTED MANUSCRIPT 33.4% in Moscow (Menyaylova, Gaponov, 2011), whereas in Vladivostok it was 1.03%. In comparing Cystoisospora spp. infestation rates in dogs from Moscow to those from Vladivostok, the higher prevalence of Cystoisospora spp. in Moscow was 85.7 % (Zubov, 2008), with a lower
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prevalence of 9.3% also described (Kurnosova, 2013) , while the present study shows 7.2 %
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(Kurnosova, 2013). Besides, the prevalence of Cystoisospora spp. in cats in Moscow in 2009
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was 3.74% (Kurnosova, 2013), when in Vladivostok it was higher (13.7%) (Table 6, Fig. 3).
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5. Conclusions
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In the present study a low prevalence of endoparasites infections in owned domestic dogs and cats was indicated. This may be due to the fact that these animals receive regular veterinary care
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and anthelmintic treatment. Two endoparasites species Toxocara canis and Ancilostoma caninum
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found in dogs have a zoonotic potential.
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Two ectoparasites species were detected in dogs, and one species was found in cats. Ectoparasites and Demodex canis infestation rates were low in dogs. Otodectes cynotis infestation rates in cats were high, which can be eliminated with appropriate treatment and
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avoiding contacts with stray animals.
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Kozlov, D.P., 1965. Jekologo-faunisticheskoe izuchenie gel'mintov kanid (Mammalia: Canidae) Dal'nego Vostoka i rasshifrovka biologicheskogo cikla nematody Thezalia callipaeda (Railliet et Henry, 1910): vtoref. dis. … kand. biol. nauk. (Ecological - faunistic study of helminths Canidius ( Mammalia : Tsanidae ) from Far East and deciphering the biological cycle of the
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ACCEPTED MANUSCRIPT nematode Thezalia tsallipaeda ( Railliet ET Henry, 1910 ). Abstract of the Dissertation of the candidate of biological sciences, Moskva, 18 pp (In Russian). Kryuchkova, E.N., Abalihin, B.G., Egorov, S.V., Sokolov, E. A., Balandina V.N., Egorov D.S.,
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carnivorous pets of Ivanovo Region''s urban populations). Vestnik KGU im. N.A. Nekrasova. 20,
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ACCEPTED MANUSCRIPT Sprent, J.F.A., 1956. The life history and development of Toxocara cati (Schrank 1788) in the domestic cat. Parasitology. 46, 54-78 Vjatkina, P. (Ed.), 2015 Analizy. Polnyj medicinskij spravochnik. Litres, Moscow, 782 pp.
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Zubov, A., 2008. Vozrastnaja dinamika zarazhennosti sobak kishechnymi parazitami v
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region of Russia (In Russian with English abstract). Rossijskij parazitologicheskij zhurnal. 2,1-4
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ACCEPTED MANUSCRIPT Appendices Tables Table 1. Data of sex distribution of Animals Examined *
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Cerumens examination for identifying O. cynotis
total female male 17 9 8 24 7 17
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Skin scrapings examination for identifying ectoparasites and Demodex spp.mites total female male 48 22 26 5 2 3
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Faecal examination for identifying gastrointestinal parasites total female male 97 40 57 51 20 31
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ACCEPTED MANUSCRIPT Table 2. Data of age distribution of Animals Examined * Skin scrapings examination for identifying ectoparasites and Demodex spp.mites 1-12 13-36 Older 1-12 13-36 Older months months then 36 months months then 36 months. months. 17 30 50 12 14 22 22 14 15 1 4
Cerumens examination for identifying O. cynotis
1-12 months
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13-36 months 5 8
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*faecal samples and skin scrapings were taken from 5 dogs
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dogs cats
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ACCEPTED MANUSCRIPT Table 3. Coproscopically examination results Number of infested animals (n) Dogs (total number of dogs examined n= 97) Helminthes Ancylostoma caninum 10 Dipylidium caninum 2 Toxocara canis 1 Uncinaria stenocephala 4 Taenia sp. 2 Protozoa Cystoisospora rivolta 1 Cystoisospora sp. 6 Cats (total number of cats examined n=51) Helminthes Trematoda g.spp. 4 Dipylidium caninum 2 Hymenolepis diminuta 1 Toxascaris leonina 4 Uncinaria stenocephala 2 Protozoa Cystoisospora sp. 7
Prevalence %
10.3 2.1 1.03 4.1 2.1 1.03 6.2
7.8 3.9 1.9 7.8 3.9 13.7
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ACCEPTED MANUSCRIPT Table 4. Cerumen samples and skin scrapings examination results.
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Parasite Number of infested animals (n) Prevalence (%) Dogs (total number of cerumen samples examination n= 17, total number of skin scrapings examination n= 48) Demodex canis 3 6.25 Ectoparasites Otodectes cynotis 5 29.4 Сheyletiella yasguri 1 2.1 Cats (total number of cerumen samples examination n= 24, total number of skin scrapings examination n= 5) Ectoparasites Otodectes cynotis 18 75
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ACCEPTED MANUSCRIPT Table 5. Distribution of parasites in Cats and Dogs in Russia.
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Voronezh (Menyaylova, Gaponov, 2011) + + + + + + + + + + +
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Zelenograd (Aleksandrova, Safiullin, 2010) + + + +
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Vladivostok (present study) Toxocara canis + Toxocara mystax Toxascaris leonina + Trichuris vulpis Ancylostoma caninum + Uncinaria stenocephala + Taenia sp. + Dipylidium caninum + Diphyllobothrium latum Mesocesdoides lineatus Cystoisospora + Giardia spp. Toxoplasma gondii -
Novosibirsk (Borcova, 2007) + + + + + + + + + -
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ACCEPTED MANUSCRIPT Table 6. Prevalence (%) of endoparasites in cats and dogs in Russia Vladivostok (present study)
Dipylidium caninum Toxocara canis
cats 3.9 dogs 2.1 1.03
Ivanovo Voronezh (Kryuchkova et (Menyaylova, al, 2014) Gaponov, 2011) 29.6 26.4 60.3 19.1 37.2 33.3
Uncinaria stenocephala Ancylostoma caninum Cystoisospora spp.
cats 3.9 dogs 4.1 10.3
1 19.2 5.1
cats 13.7
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dogs 7.2
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33.4(Zubov,2008) 27.25(Zubov,2008) -
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Moscow
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ACCEPTED MANUSCRIPT Figure captions Fig. 1. Seasonal dynamics of gastrointestinal parasites prevalence Fig. 2. Seasonal dynamics of ectoparasites and Demodex mites prevalence
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Fig 3. Map with research localities presented in table 5 and 6
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ACCEPTED MANUSCRIPT Fig. 1.
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ACCEPTED MANUSCRIPT Table 1. Data of sex distribution of Animals Examined *
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total female male 17 9 8 24 7 17
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Skin scrapings examination for identifying ectoparasites and Demodex spp.mites total female male 48 22 26 5 2 3
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Faecal examination for identifying gastrointestinal parasites total female male 97 40 57 51 20 31
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ACCEPTED MANUSCRIPT Table 2. Data of age distribution of Animals Examined * Skin scrapings examination for identifying ectoparasites and Demodex spp.mites 1-12 13-36 Older 1-12 13-36 Older months months then 36 months months then 36 months. months. 17 30 50 12 14 22 22 14 15 1 4
Cerumens examination for identifying O. cynotis
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*faecal samples and skin scrapings were taken from 5 dogs
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ACCEPTED MANUSCRIPT Table 3. Coproscopically examination results Number of infested animals (n) Dogs (total number of dogs examined n= 97) Helminthes Ancylostoma caninum 10 Dipylidium caninum 2 Toxocara canis 1 Uncinaria stenocephala 4 Taenia sp. 2 Protozoa Cystoisospora rivolta 1 Cystoisospora sp. 6 Cats (total number of cats examined n=51) Helminthes Trematoda g.spp. 4 Dipylidium caninum 2 Hymenolepis diminuta 1 Toxascaris leonina 4 Uncinaria stenocephala 2 Protozoa Cystoisospora sp. 7
Prevalence %
10.3 2.1 1.03 4.1 2.1 1.03 6.2
7.8 3.9 1.9 7.8 3.9 13.7
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ACCEPTED MANUSCRIPT Table 4. Cerumen samples and skin scrapings examination results.
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Parasite Number of infested animals (n) Prevalence (%) Dogs (total number of cerumen samples examination n= 17, total number of skin scrapings examination n= 48) Demodex canis 3 6.25 Ectoparasites Otodectes cynotis 5 29.4 Сheyletiella yasguri 1 2.1 Cats (total number of cerumen samples examination n= 24, total number of skin scrapings examination n= 5) Ectoparasites Otodectes cynotis 18 75
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ACCEPTED MANUSCRIPT Table 5. Distribution of parasites in Cats and Dogs in Russia.
CE P
AC
IP
-
SC R
+
+
+
-
+
MA
+ +
+ -
+
+
NU
-
TE
Toxocara canis + Toxocara mystax + Toxascaris leonina + Trichuris vulpis + Ancylostoma caninum Uncinaria stenocephala + Taenia sp. + Dipylidium caninum + Diphyllobothrium latum + Mesocesdoides lineatus Cystoisospora + Giardia spp. Toxoplasma gondii -
Zelenograd Voronezh Novosibirsk (Aleksandrova, (Menyaylova, (Borcova, Safiullin, 2010) Gaponov, 2011) 2007) + +
T
Vladivostok (present study) +
D
Parasite
-
-
-
+
-
+
+
+
-
-
-
-
+
+
-
+
-
-
+
-
+
+
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ACCEPTED MANUSCRIPT Table 6. Prevalence (%) of endoparasites in cats and dogs in Russia Parasite
Vladivostok (present study)
Ivanovo Voronezh (Kryuchkova et (Menyaylova, al, 2014) Gaponov,
Moscow
29.6 60.3 37.2
26.4 19.1 33.3
Uncinaria stenocephala Ancylostoma caninum Cystoisospora spp.
cats 3.9 dogs 4.1 10.3
1 19.2 5.1
cats 13.7
-
dogs 7.2
-
IP
33.4(Zubov,2008)
0.98 19.8 -
27.25(Zubov,2008) -
10.7
3.74
(Kurnosova,
2013) 6.38
(Kurnosova, 2013); 85.7 (Zubov,2008) 9.3
AC
CE P
TE
D
MA
T
cats 3.9 dogs 2.1 1.03
NU
Dipylidium caninum Toxocara canis
SC R
2011)
27
ACCEPTED MANUSCRIPT
AC
CE P
TE
D
MA
NU
SC R
IP
T
HIGHLIGHTS The first report about parasites communities in domestic cats and dogs in Vladivostok 9 different species and 3 not-definable parasites in cats’ and dogs’ faecal samples were found Ectoparasites and Demodex canis infestation rates were low in dogs. Otodectes cynotis infestation rates in cats were high
28