The World Largest Focus of the Opisthorchiasis in the Ob-Irtysh Basin, Russia, Caused by *Opisthorchis felineus*

*Anastasia V. Simakova, Natalya V. Poltoratskaya, Irina B. Babkina, Tatyana N. Poltoratskaya, Alexander V. Shikhin and Tatyana M. Pankina*

#### **Abstract**

The world's largest focus of opisthorchiasis caused by cat fluke *Opisthorchis felineus* Rivolta, 1884, is associated with the Ob-Irtysh basin (Russia). The chapter provides data on the history of discovery and the study of opisthorchiasis. Features of the morphology and life cycle of *O. felineus* are described. Data on the infection of intermediate hosts (mollusks and cyprinids fish) are provided. Species of fish that have important epizootological significance are indicated. The incidence of opisthorchiasis in the people of different age and social groups, clinical manifestations, pathogenesis, and complications is discussed. The climatic and social factors that contribute to maintaining the focus of opisthorchiasis are described. The measures of personal and social prevention of the people are given.

**Keywords:** *Opisthorchis felineus*, history and study, intermediate hosts, important epizootological significance, epizootology and epidemiology, personal and social prevention

#### **1. Introduction**

The goal of this work was to assess the current epidemiological and epizootological situations in the world largest focus of opisthorchiasis; to clarify the specific features in its clinical course, pathogenesis, and complications; to determine the natural, climatic, and social factors that enhance preservation of this focus; and to propose an algorithm for preventive activities.

The tasks of this research are to study the epizootological situation and features of the circulation of *Opisthorchis felineus* in the Ob-Irtysh basin, assess the epidemiological situation of opisthorchiasis in Russia, and give recommendations on measures to prevent the disease.

The concept of sustainable development [1] sets the control of unattended diseases as one of the global goals in the area of public health care; these diseases include the helminthic invasions in hyperendemic foci. The ongoing changes in

all spheres of production and sale of raw materials and goods have led to serious violations of sanitary rules and norms, which deteriorate the epizootic situation for parasitic invasions in the world.

Opisthorchiasis, the trematodiasis caused by *O. felineus* Rivolta, 1884, is one of the relevant problems in both Russia (with its world largest Ob-Irtysh natural focus) and worldwide despite the implemented prevention measures. The relevance of this problem is determined by both its high incidence among adults and children, severity of the resulting pathology, and its chronic course.

The socioeconomic factors, such as active migration of population, unawareness of opisthorchiasis among the newcomers to the region, poor knowledge about the rules for disinfection of local population, all-year-round consumption of fish, and homemade fish products, increase in the number of amateur fishermen and poachers, and vending of fish and fish products on unauthorized markets creates the conditions for the stable preservation of opisthorchiasis.

One of the major factors that influence the level of *O. felineus* liver fluke invasion is a high rate of fish invasion by its metacercariae. The natural and climatic conditions that have established in the Ob-Irtysh basin support the active opisthorchiasis focus there.

A vast floodplain of the Ob-Irtysh basin, rich in lakes and meadows, and a developed network of first- and second-order tributaries enhance the maintenance of the Bithyniidae mollusks at a high level.

Close coexistence and cohabitation of the first intermediate host and cyprinid fish (second intermediate host) in the same habitats provide the implementation of liver fluke life cycle. In their abundance and species diversity, the cyprinid fish are the leader group in the Ob-Irtysh basin. A high infection rate of the prevalent fish species, which are of important commercial value, with *O. felineus* metacercariae is a major risk factor, influencing the incidence of this disease among local population.

#### **2. Brief history of opisthorchiasis discovery and research**

The liver fluke was for the first time described in 1884 by Sebastiano Rivolta, an Italian scientist. He isolated the parasite from the liver of a cat and a dog and named it the liver fluke, *O. felineus*, and the corresponding disease, opisthorchiasis. K.N. Vinogradov, a professor at the Tomsk University, discovered the liver fluke in the human liver in 1891. After the discovery by Vinogradov, human cases of opisthorchiasis were repeatedly recorded in 1892–1929 in Tomsk, Biysk, Novosibirsk, Tyumen oblast, Kuznetsk raion, and other localities. During WWII, a Russian soldier from Siberia died in one of the fascist concentration camps; his autopsy demonstrated 42,000 liver flukes in his liver and pancreas.

As has been observed, the liver fluke is not met far and wide but rather near freshwater bodies. Brown in 1893 assumed that fish consumption is the source of liver fluke infection, which was later (1904) experimentally confirmed by M. Askanazy (Germany). In 1891, Vinogradov postulated the first intermediate host of liver fluke, which was experimentally confirmed by H. Vogel (Germany): he demonstrated that the first intermediate host was the mollusk *Bithynia leachii* (Sheppard, 1823).

The study of opisthorchiasis commences in 1929 after publication of the information that 100 opisthorchiasis patients were admitted to the Tobolsk hospital over 6 months. This initiated organization of specialized helminthological expeditions to the Ob-Irtysh basin, headed by K.I. Skryabin. Numerous experiments have demonstrated that this region houses the largest opisthorchiasis focus. Russian

*The World Largest Focus of the Opisthorchiasis in the Ob-Irtysh Basin, Russia, Caused… DOI: http://dx.doi.org/10.5772/intechopen.91634*

helminthologists under the guidance of Skryabin paid significant attention to the study of *O. felineus* (1927–1929). The liver fluke larvae were for the first time discovered in the muscle of fish individuals inhabiting Siberian water bodies by N.N. Plotnikov and L.K. Zerchaninov in 1932.

All these efforts allowed for discovery of a considerable incidence of opisthorchiasis among people, cats, and dogs along the Irtysh and Ob rivers up to the polar circle. In 1973, a cat was autopsied by an expedition organized by Skryabin in the north of the Tomsk oblast; eight cysts containing liver flukes were found in its liver; one of the cysts, medium in its size (similar to a walnut), contained 654 parasites.

The following scientists contributed to the studies of the epidemic situation of opisthorchiasis: S.D. Titova (publications of 1946–1980), V.S. Myasoedov (publications of 1953, 1959, and 1960), M.P. Miroshnichenko (1954, 1955, and 1956), T.A. Bocharova (1971–2005), G.I. Golovko (1981–1986), and so on. The population migration to the oil and gas areas in the north of the Tomsk oblast increased the attention to this disease [3, 18–22, 24, 43].

#### **3. Life cycle of** *O. felineus*

The liver fluke *O. felineus* has an intricate life cycle, which involves three hosts: the definitive host and two intermediate hosts; the life cycle comprises two freeliving stages, the egg and cercaria (**Figure 1**).

Infected domestic and wild animals that fed on fish and infected people, which are the definitive host of the liver fluke, are the sources of invasion. One trematode lays approximately 2000 eggs per day. The eggs are not viable when dry and are rapidly killed by sunlight but retain their viability for 15 months in a water body at a temperature of 4–7°C; all eggs die after 29 months [2].

When entering water with human and animal feces, the liver fluke eggs can be ingested with detritus by the first intermediate host, a Bithyniidae (genera *Codiella* and *Opisthorchophorus*) mollusk [2].

In the Ob-Irtysh basin, the mollusks susceptible to the invasion inhabit only standing perennial silt water bodies. The mollusks are unable to migrate for a long distance and form local clusters. Presumably, the infection rate of mollusks depends on the population density and the distance from human dwellings [3].

The infection rate of Bithyniidae mollusks in the upper reaches of Ob and Irtysh rivers within the Altai Krai is 2%, amounts to 6.1% within the Novosibirsk oblast, and varies in the range of 0.3–20.2% in the Irtysh basin in the Omsk oblast [4, 5]. The density of the mollusk population in the floodplain water bodies in the Tomsk oblast is 8100 individuals/m3 ; however, the prevalence of invasion is extremely low (3.7%), and the intensity is very high (on the average, 8130 ± 470 cercariae/mollusk). Coinvasions are extremely rare [6]. The infection rate of mollusks in the Tura and Pyshma river floodplains varies from 4 to 9%; the infection characteristics in the Khanty-Mansiysk Autonomous Okrug are also low, to 6.7% [7].

In the mollusk gut, miracidia, free-swimming larvae, hatch from the eggs (**Figure 1**). A miracidium hatched from the egg enters the mollusk body cavity by passing through the gut wall to undergo a regressive metamorphosis there. It loses its larval organs (glands, epidermal plates, cilia, etc.) preserving only the germline cells and protonephridia to change into a mother sporocyst with a length up to 2 mm [2].

Young sporocysts are transversely constricted to give smaller sporocysts, which propagate and form rediae. Rediae are sack-like structures with a large mouth and gut. When leaving the mother sporocyst, rediae migrate to the liver of mollusk to parthenogenetically reproduce.

**Figure 1.** *Life cycle of* O. felineus*.*

In the redia, tailed motile larvae—cercariae—are formed of the germ balls. The developmental stage in the mollusk takes 2–2.5 months (**Figure 1**) [2].

With the maturation, cercariae leave the redia through the pore to migrate in the mollusk body leaving it for water, where they swim for 30–50 h. Up to 3500 cercariae can leave the mollusk during 24 h. The release of cercariae has two peaks, namely a pronounced midsummer peak and a flat spring one [2].

When encountering a cyprinid fish (ide, dace, roach, bream, Siberian roach, Caspian roach, tench, common rudd, common carp, asp, common bleak, etc.), the cercaria attaches to it; detaches its tail; loses its eyes and sensory organs; and penetrates into the muscles to form the inner and outer (a capsule of connective tissue) membranes and to transform into the next phase, metacercaria (**Figure 1**).

The metacercariae have a size of 0.23–0.38 × 0.18–0.28 mm and are very survivable. The metacercariae become invasive 3–6 weeks after entering the fish and now are able to infect the definitive hosts—domestic and wild carnivores and omnivorous animals and humans. Metacercariae retain their viability in the fish body for 1–3 years and even to 9 years according to some data [8].

#### *The World Largest Focus of the Opisthorchiasis in the Ob-Irtysh Basin, Russia, Caused… DOI: http://dx.doi.org/10.5772/intechopen.91634*

As is known, only cyprinid species are suitable intermediate hosts for the metacercariae. Approximately 20 species of both aboriginal and alien cyprinid species of commercial or noncommercial value inhabit the rivers and lakes of the Ob-Irtysh basin, the most important fish species of commercial significance are the ide, bream, crucian carp, roach, and, to a lesser degree, dace [2].

The rate of the fish infection by liver fluke metacercariae has been studied with different intensities in different periods. A large volume of data on the prevalence of fish infection in the Ob-Irtysh basin was accumulated in the 1990s to 2000s. Our data and the earlier results suggest high rates of infection of the ide, dace, and roach. The prevalence of ide and dace infection amounted to 20–100% and of roach, 2–80% with the intensity of infection of 1–1780 metacercariae per individual. These fish species are among the major carriers of *O. felineus* metacercariae and significantly contribute to the preservation of the opisthorchiasis focus. In addition, the bream and common bleak, alien species for this region, also appeared to be susceptible to the infection by liver fluke metacercariae and, correspondingly, have been involved in the maintenance and spreading of opisthorchiasis in Western Siberia [8–25].

The definitive hosts are infected orally by consuming the cyprinid fish muscles infected by liver fluke. The metacercarial membrane is finally destroyed in the host stomach, and the young helminth migrates along bile ducts to the liver and gall bladder to reach the sexual maturity in 20–25 days (**Figure 1**) [2].

The intensity of invasion of definitive hosts and their role in maintaining the strength of opisthorchiasis focus are different. As is assumed, in addition to humans who account for 56.6% of the invasion, cats (15.8%), dogs (3.6%), and pigs (to 0.9%) are also significant contributors to opisthorchiasis [26]. The total prevalence of cat invasion in the opisthorchiasis focus of the Khanty-Mansiysk Autonomous Okrug in the 2000s amounted to 48.2% (males were more frequently affected than females). The prevalence of dog invasion was lower, amounting to 17.14% [27]. An analogous study in Novosibirsk demonstrated the total prevalence of cat invasion of 7.9% with the intensity of 69.9 flukes and of dog invasion of 3.4% with the intensity of 23.8 flukes. Males appeared more affected among cats and females among dogs. The invasion parameters increase with animal age [28].

In addition to domestic carnivores, wild carnivores (common fox, wolf, brown bear, lynx, polecat, sable, mink, muskrat, bank vole, and others) also contribute to the liver fluke circulation in natural foci. These animals play different roles in the epizootic process in opisthorchiasis: the animals living in the floodplain and constantly "supplying" the infectious material to the biotopes of the first intermediate host are actual players of the opisthorchiasis circulation in the Ob-Irtysh basin, whereas the remaining animals are potential sources of invasion. In general, foxes and muskrats account for the largest number of invaded wild animals. The rate of invasion in the floodplain of Ob river and its tributaries reaches 77% on the background of a growth in the prevalence characteristics from the upper to lower reaches. The intensity of invasion amounts to 10–500 liver flukes per individual. The invasion of the muskrat in Western Siberia reaches 33% [29]; however, this issue requires further studies.

Thus, a complex multihost life cycle of this parasite enhances its long-term retention in wildlife and preservation of the natural opisthorchiasis focus in the Ob-Irtysh basin.

#### **4. Epidemiology of opisthorchiasis in Russia**

Opisthorchiasis is an important social problem in Russia. Two-thirds of the world distribution range of this pathogen concentrates in this country [30]. Opisthorchiasis accounts for approximately 80% of all helminthic diseases. According to the official statistical data, up to 26,000 cases are annually recorded. The actual number of opisthorchiasis patients taking into account the correction factor is 15-fold higher [31].

In total, 106,362 cases of invasion were detected in 2014–2018. The maximum number of cases was recorded in 2014 (25,545 cases) and minimum, in 2017 (18,755 cases). The incidence rate of opisthorchiasis among population in 2018 decreased by 25.3% as compared with 2014, varying from 12.79 to 17.51 per 100,000 population (**Table 1**).

The natural foci of opisthorchiasis are adjacent to the Ob, Irtysh, Ural, Volga, Kama, Don, Dnepr, Severnaya Dvina, and Biryusa rivers [32–42].

Approximately 80% of the opisthorchiasis cases are recorded in the territories adjacent to the Ob, Irtysh, and Tom river basins and their tributaries [43], housing the administrative centers of the Omsk, Novosibirsk, Tyumen, Tomsk, and Kemerovo oblasts and Khanty-Mansiysk and Yamalo-Nenets Autonomous Okrugs. Most part of the local population is affected (80–95%) [44–46]. The total incidence rate over 2014–2018 was 84,331 opisthorchiasis cases, accounting for 79.3% of the total cases in the Russian Federation.

The Khanty-Mansiysk Autonomous Okrug heads the list of percentage of opisthorchiasis incidence (2.6–4.6) followed by Yamalo-Nenets Autonomous Okrug (1.2–2.3%), Novosibirsk oblast (1.1–1.5%), Tomsk oblast (1.0–1.6%), Tyumen oblast (0.9–1.3%), Omsk oblast (0.7–1.0%), Kemerovo oblast (0.5–0.7%), and Altai Krai (0.3–0.5%) [47–51].

The incidence rate of opisthorchiasis in the analyzed regions varies, with the maximum exceeding 1.3–1.8-fold the minimal value. The highest incidence rates are recorded in the hyperendemic regions of Yamalo-Nenets (124.2–226.7) and Khanty-Mansiysk (259.2–461.5) Autonomous Okrugs, Tyumen oblast (90.7–132.2), Tomsk oblast (104.7–158.4), Novosibirsk oblast (112.2–148.8), and Omsk oblast (72.8–103.3). The Kemerovo oblast (49.8–66.23) and Altai Krai (33.09–45.48) are the regions with a high level of invasion. The incidence of opisthorchiasis in these regions severalfold exceeds the mean level for the Russian Federation with the Khanty-Mansiysk Autonomous Okrug heading the list (19–26-fold) followed by Yamalo-Nenets Autonomous Okrug (9–13-fold), Tomsk and Novosibirsk oblasts (7–10-fold), Omsk and Tyumen oblasts (5–8-fold), Kemerovo oblast (3–5-fold), and Altai Krai (2–3-fold).

According to the statistical data for 2014–2018, a decrease in the absolute characteristics and incidence rate was in general observed in all hyperendemic regions, which is explainable by inadequate diagnosing, registration, and recording of the cases as a result of decreased attention to the problem of opisthorchiasis.

Opisthorchiasis is mainly diagnosed among the adult population (over 90% cases in people aged 39–59); however, the level of child morbidity is rather high. Opisthorchiasis has been recorded in all age cohorts of children up to 17 years, with the age cohort of 7–14 years accounting for 60–80% of all cases recorded in children. In the Tomsk oblast, the children to 17 years old are the most affected as compared with other regions (29.7% in 2014–40.8% in 2018). In the mid-Ob river region, opisthorchiasis is detectable in children starting from 3 years (25–30%) with an increase at the age of 12–14 years (50–60%) to 100% in the adults [52]. In the child population of the city of Urai (Khanty-Mansiysk Autonomous Okrug), the most affected cohort is 7–14 (38%) and 14–17 (34%) years old versus 23 and 5% for the cohorts of 3–6 and 2–2 years [53]. An increase in the prevalence of infection among the children of 1–2 years (from 3.8 to 6.1%) is observed in the Tomsk oblast. Cases of opisthorchiasis in the children under 1 year have been recorded in Khanty-Mansiysk Autonomous Okrug (six cases in 2017).

