Helminth infections in domestic dogs from Russia

Dogs are the hosts for a wide helminth spectrum including tapeworms, flatworms, and nematodes. These parasites affect the dog health and cause morbidity and mortality, especially in young and old animals. Some species, as Toxocara canis, Ancylostoma caninum, Dipylidium caninum, and Echinococcus spp. are well-known zoonotic parasites worldwide, resulting in high public health risks. Poor data about canine helminth species and prevalence are available in Russia, mainly due to the absence of official guidelines for the control of dog parasites. Moreover, the consequent low quality of veterinary monitoring and use of preventive measures, the high rate of environmental contamination by dog feces and the increase of stray dog populations, make the control of the environmental contamination by dog helminths very difficult in this country. This paper reviews the knowledge on canine helminth fauna and prevalence in Russia. Practical aspects related to diagnosis, treatment, and control of parasitic diseases of dogs in Russia are discussed.


Introduction
Dogs are the most popular pets worldwide and are infested with many parasites, which may represent a health risk for humans, especially children, the elderly and the immune-compromised [1][2][3]. For instance, Dipylidium caninum, Echinococcus granulosus, Ancylostoma spp., and Toxocara canis are common parasites of dogs that can affect humans in different countries around the world. Knowledge about parasite species in domestic dogs, prevalence and intensity of helminth infestations in dog populations, transmission of canine parasites and the seasonal dynamics of parasite infestations are essential for control and prevention of helminthosis in domestic animals and humans.
Investigation of free-roaming dog populations as part of urban ecology is a major key for the solution of many ecological problems in industrial ecosystems [4,5].
In Russia, 40-50% of household owners keep a dog, and the total dog population amounts to 30 million [6]. Therefore, the growing number of owned dogs in urban areas in Russia has also been accompanied by substantial increases in the stray dog population. For example, the stray dog population amounts to 12,300 specimens in Kazan [7], 9500 in Novosibirsk (http://laboratorium.narod.ru/gelm.html) and 10,000 in Omsk [8]. Stray dogs do not receive medical attention and never, or rarely, receive anti-parasitic treatments. Thus, they represent a major source of spread of gastrointestinal helminth eggs, which are harmful for people [9,10]. This article is a compendium on helminth infestations in dogs in the Russian Federation, with particular focus on zoonoses.

The Russian Federation
The Russian Federation is the largest country in the world, covering 7,125,200 km 2 (6,612,100 sq. miles). Russia consists of seven basic climate zones. The humid continental climate predominates in all parts of the country: European Russia, in the south of West Siberia and in the south of the Russian Far East, including the cities of Moscow and Saint Petersburg, except for the tundra and the extreme southeast.

Diagnosis of Canine Helminth Parasites
The diagnosis of helminth parasites affecting dogs is made by coprological examination methods, Strongyloides larva detection techniques and post-mortem examination. Helminth eggs are usually detected in feces by ordinary coprologycal techniques such as Fulleborn's method and Darling's method; these methods are present low sensitivity for some helminth species and result in the underestimation of the real prevalence of some parasites [36][37][38]. Some flotation and sedimentation techniques are used only in Russia. For instance, Kotelnikov-Varenichev's and Kotelnikov-Chrenov's methods are centrifugal flotation techniques, which have high sensitivity for many helminth species [39][40][41][42]. Goryachev's sedimentation technique proposed for detecting Opisthorchis eggs is also use in some studies (Table-4) [43]. However, other coprological examination methods using worldwide are not used in Russia. For example, TF-test ® designed for detecting human gastrointestinal parasites [44] is frequency used for detecting helminth eggs in canine feces [45]. Some comparative study showed that the centrifugal flotation technique was more sensitive than centrifugal sedimentation and TF-test ® for recovery Ancylostoma spp., T. canis, Trichuris vulpis eggs in canine feces [45]. Another method is Willis technique has high sensitivity for T. canis eggs in canine feces [46]. Moreover, recent study showed that this method performed better than the centrifugal flotation techniques and Hoffman-Pons-Janer technique for detecting Ancylostoma spp. in dog feces [47].
Traditional Baermann's and modified Baermann-Orlov's methods are used for S. stercoralis larva detection from canine feces [48,49]. Zink sulfate flotation technique which is sensitive for S. stercoralis larva is not used in Russia [50].
Necropsy examination is performed according to the standard procedures [49,51]; methods of total and part helminthological examination suggested by Skrjabin [52] used in parasitological study.

Prevalence of Helminth Infections in Dogs in Russia
Data obtained from reports in different regions showed broad prevalence rate fluctuations. The prevalence depends on climate, living conditions, and quality of veterinary care [53,54]. Many reports did not include data about the total prevalence of gastrointestinal parasites in dogs. However, individual prevalence rates for different parasites were greater than 50% in 37% of studies. High prevalence rates and a broad parasite spectrum were found in studies using the necropsy method (Table-2).
Overall, nine parasites species were found in studies using coproscopic examination methods. Some species, such as M. xanthosomus, M. bilis, S. stercolaris, M. lineatus and D. latum, were not found on fecal examination. In some cases, it was also difficult to distinguish species of eggs Opisthorchiidae family [55] and eggs genus Taenia based only on morphological characters [56]. The most common species in Russia was T. canis, followed by D. caninum, T. leonina, and Uncinaria stenocephala (Tables-2 and 3). A. caninum was found in 52.3% of studies conducted in areas with a continental or temperate climate, where there are warm summers and high humidity, as these conditions are optimal for A. caninum larval development [57].
Flatworms of the genus Metorchis (Looss, 1899) are worldwide parasites of Cyprinidae fishes, and infest fish-eating mammals. In Russia, M. xanthosomus was found in Dagestan and Kabardino-Balkaria Republic, while M. bilis was found in Caucasian Minerals Water (Table-2). It is interesting that these species were found separately in different regions since both species have common intermediate hosts.
The first host is the mollusk Bithynia tentaculata L. 1758 living in the Palearctic zone, except the North zone [58]. The second hosts are Cyprinidae fishes [59].
The cestode M. lineatus has a worldwide distribution. It has been found in Europe [60], the Middle East [61], Africa [62], North, and South America [63]. Adult worms live in small intestine of carnivorous mammals including fox, wolves, dogs, cats, coyotes, raccoons, and lynxes [64]. One case of the peritoneal larval stage was recorded in dogs from Germany [65]. This species spreads proglottids via the feces so it cannot be found with flotation methods. In Russia, dogs infested with M. lineatus were found in Dagestan with a low prevalence rate [16].

Dogs and People: Problem of Parasite Zoonoses
Most parasites species found in dogs from Russia have zoonotic potential. T. canis is the most common canine intestinal endoparasites worldwide. Humans are infected by Toxocara via ingestion of embryonated eggs in contaminated soil [66]; however, pet hair can also contain embryonated eggs [67]. The first importance reports about human toxocariasis in Russia were published in 1961-1962 [68,69]. Only in 1988 did the connection between the source of toxocariasis in dogs and nosoareal of toxocariasis in humans appear [70]. Recently, the problem of toxocariasis in humans and dogs has been highlighted worldwide. In the Russian Federation, toxocariasis has frequency appeared in children, especially in children with allergic diseases (31-47% of children with allergic diseases) [71]. Ocular toxocariasis is frequently recorded in children, whereas visceral toxocariasis is more frequently recorded in adults. Since 1991, Toxocara infestation rates in people have increased. For example, Toxocara infestation was recorded in 0.03 per 100,000 people in 1991 and in 2.32 per 100,000 people in 2012. However, toxocariasis was recorded in 2.1 per 100,000 people from 2008 to 2012 [72]. Infestation rates are broadly variable in different regions and in people of different age groups. Toxocara prevalence in people from Russia is 5.4% in Moscow and Tula, 7.4% in Dagestan and 6% in the Irkutsk District [73]. The Toxocara prevalence was 16.7% in children from the Altay Region, whereas toxocariasis was recorded 6 times more frequently in adults from the Krasnodar region. E. granulosus is a widespread parasite, which has a major medical, veterinarian and socioeconomic cost. The adult parasite stage occurs in the canine small intestine, and people are infested by ingestion of contaminated food [74] or by direct contact with contaminated dogs that retain eggs on their coats [75]. Echinococcosis in humans is the most serious parasitic disease, as a fatal outcome is recorded in 2-23% of cases [76]. Higher prevalence rates appear in China, western and southern Russia, Southwestern Europe, South Africa and Central and South America [76]. The Orenburgskii Region is the most problematic territory in Russia, as echinococcosis was registered in 3.4±0.4 per 100,000 people [77]. Recently, DNA-based studies showed that E. granulosus comprise 10 genotipes which have been distinguished in different species [78]. E. granulosus s. s. (G1-G3), E. canadensis (G6, G8 and G10) were found in Russia [79].
Liver flukes of the genera Clonorchis Loos, 1907, Metorchis, and Opisthorchis Blanchard 1895, in the family Opisthorchiidae, exploit freshwater snails and fish as the first and second intermediate hosts, respectively. The final hosts, fish-eating birds and mammals, including dogs and humans, are infected by eating fish harboring infective metacercariae [85]. Feces of dogs infested with Opisthorchis felineus and Metorchis spp. are major sources of water contamination [86]. The largest infestation center is located in the Ob-Irtysh basin and includes 10 regions of Russia and Kazachstan. The infestation rate is 51-82% in humans. The other intensive infestation center is Chulym River in the Krasnoyarsk region; the prevalence of O. felineus in people is 70-80% [87].
M. bilis is also found in fish from the Ob-Irtysh basin. The prevalence rate in people from West Siberia is 28.1% [88].
The flatworm C. sinensis is endemic to the Far Eastern region and it was also found in dogs and people from China and Korea [86,89]. C. sinensis is frequently found in people from the Russian Far East [90].
The tapeworm M. lineatus has major veterinary importance, and occasionally, it has been found in people [91]. In Russia, cases of M. lineatus infestation in humans have not been reported, however dog feces containing proglottids are major sources of environmental contamination.
D. latum is a common parasite of fish-eating mammals. Fecal contamination of water is a source of D. latum spread. In the last 10 years, only one report regarding canine infestation from Ivanovo was published. A big center of infestation located in Russia is Baikal Lake. Infestation rates in humans from the Irkutsk Region were 9.6 cases per 100,000 people [92].
Another flatworm, Alaria alata, has specific veterinary importance [93], however, several reports about human larval alariosis were published since 1973 [94,95]. In Russia, A. alata was found in dogs, foxes, wolves and badgers in the Vladimir, Ivanovo and Moscow regions, and in the Volgograd and Astrachan regions, in the North Caucasian District. Prevalence rates were 38.4-48.6% in farm dogs, 46.1-59.3% in stray dogs and 100% in wolves and foxes [96].

Control and Prevention
Zoonosis is the major veterinary and medical problem. Zoonotic infestations include well-known parasite species such as T. canis [97].
Parasitology monitoring is provided irregularly. Poor living conditions and lack of anti-parasitic medication causes environmental contamination with helminth eggs [98]. Environmental contamination of helminth eggs is a big problem in many urban and rural areas in Russia, especially in agricultural areas, where feces are used for fertilizing. Currently, basic methods for dog helminth infections prevention include regular deworming of domestic animals, control of environmental contamination (avoid contamination of canine feces in public places), and spread of information about zoonotic parasites [99]. Moreover, control of food quality and pet diets help to prevent parasite infestations. For example, to prevent C. sinensis and O. felineus infestation in dogs, it is recommend to avoid the feeding of fresh cyprinid fishes [99].
Many dog owners cannot afford preventive measures and will act only when a life-threatening problem is affecting their animals. Furthermore, there are a large number of free-roaming dogs populations in the Russian cities. Government is not able to manage these animals due to the lack of adequate infrastructure and trained personnel to conduct an effective long-term population control program. As a result, pet dogs and cats are usually endangered by a wide range of parasites that may cause disease in them and eventually in their human counterpart.

Conclusions
The close contact between pets and humans may involuntarily represent a hazard for humans. Therefore, to avoid the potential risks associated with owning a pet, it is fundamental to maintain pets in good health and protect them from zoonotic pathogens. Therefore, veterinary practitioners and medical physicians should work together toward improving the well-being and general health of both animals and humans.

Authors' Contributions
MTV and AVE participated in the draft and revision of the manuscript. Both authors read and approved the final manuscript.