The current situation of echinococcosis in the Far East and South of Russia

Introduction

Echinococcosis holds a special place in the structure of parasitic pathology due to its widespread distribution and a distinct tendency to a long asymptomatic latent course with clinical manifestation usually in the late stages of the disease [1][2]. The relevance of this problem is related to the potentiality of the development of severe clinical forms of the disease with various visceral lesions, leading to fatal outcomes in some cases [3]. Most often, Echinococcus affects the liver and lungs [4]. However, literature data and the authors’ own experience attest that approximately 5–6% of cases are associated with rare localizations of the pathogen including the kidneys, heart, brain, and spinal cord membranes [5].

Currently, taxonomic validity has been proven for 4 species of the genus Echinococcus. These include E. granulosus, E. multilocularis, E. oligarthrus, and E. vogelli with intraspecific varieties, whose taxonomic status has not yet been established [6]. In certain territories, as throughout Russia, echinococcosis caused by E. granulosus is the predominant form while E. multilocularis as a causative agent of the disease is registered significantly less frequently [7].

In recent years, the leading positions in terms of echinococcosis incidence rates have been held by the Far Eastern Federal District (FEFD) and the territories of the South of Russia, where in the pre-COVID period the annual augmentation amounted to 5–10 cases per 100 thousand population [7][8]. This situation is quite natural since a high epizootic activity of E. granulosus is recorded in these regions. In particular, according to Kabardieva et al. (2021), upon helminthological investigations of feces samples from dogs in 7 regions of the North Caucasus, the average incidence index of echinococcosis reached the level of 85.07%; and the rate of detection of E. granulosus eggs in the soil in the areas of the South of Russia varied from 65.8% in the Stavropol Territory to 88.2% in the Republic of Ingushetia [9]. A similar situation has developed in various territories of the FEFD, where high rates of infestation are recorded in numerous species of game animals, which belong to the definitive and intermediate hosts of E. granulosus and E. multilocularis [10].

Considering the abovementioned, an integrated approach to epidemiological surveillance on echinococcosis should be introduced in the endemic territories of the FEFD and the South of Russia involving analysis of the long-term dynamics of infestation by pathogens among the population in these subjects, along with seroepidemiological monitoring and assessment of the epizootic situation.

The purpose of the study is to assess the epidemic situation of echinococcosis in the endemic territories of the FEFD and the South of Russia in the period from 2012 to 2022.

Materials and methods

The assessment of the epidemic situation of echinococcosis in the territories of the FEFD and the South of Russia was carried out on the basis of an analysis of long-term dynamics of incidence and seroepidemiological monitoring, as well as sanitary and parasitological examining of environmental objects. The study involved specialists from two institutions, namely the Khabarovsk Research Institute of Epidemiology and Microbiology and the Rostov Research Institute of Microbiology and Parasitology; both institutes are included in the Federal Service for Supervision of Consumer Rights Protection and Human Welfare (Rospotrebnadzor).

The study used data from annual statistical reporting forms No. 2 “Information on infectious and parasitic diseases”, and data from the Reference Center for Monitoring Larval Helminthiases of the Rostov Research Institute of Microbiology and Parasitology of Rospotrebnadzor. Data from 799 epidemiological survey cards of cases of echinococcosis and alveococcosis were examined.

Seroepidemiological investigations among a relatively healthy population were carried out in 6,406 people permanently residing in the FEFD, and 6,782 people permanently residing in the Southern Federal District (SFD) and the North Caucasus Federal District (NCFD). A total of 13,108 blood serum samples were examined. To detect class G immunoglobulins to E. granulosus antigens by ELISA, the diagnostic kit “Echinococcus-IgG-ELISA-BEST” (public company “Vector-Best”, Novosibirsk) was used.

The study design (Fig. 1) was developed considering modern methodological approaches to conducting epidemiological monitoring of larval helminthiases.

Statistical processing of the obtained data was carried out using Microsoft Office Excel 2010 and the Statistica 10.0 for Windows software package. In descriptive statistics, the following indices were calculated: the arithmetic mean, standard error of the mean, confidence interval, and median; the indices of comparative statistics included Student's test and Spearman's rank correlation coefficient. Differences between comparison groups were considered significant at p<0.05.

Results

The conducted examination showed that cases of echinococcosis in the FEFD were registered annually (Fig. 2) through the period from 2012 to 2022 in 10 out of 11 subjects of the region.

In particular, cases of echinococcosis were registered every year in the Republic of Sakha (Yakutia) and the Trans-Baikal Territory. Only on the territory of the Jewish Autonomous Region no registered cases of echinococcosis were revealed during the examined period (Table 1).

The incidence of echinococcosis among the population of the Republic of Sakha (Yakutia) was registered in all 34 administrative districts of the republic. The most unfavorable situation was observed in the Olekminsky, Kobyaisky, Verkhnevilyuysky, and Namsky districts. A significant number of cases were also identified in the regional capital, Yakutsk, which was, presumably, related to the greater availability of medical services for the urban population and, accordingly, higher rates of examination coverage of the subject populations.

In the Trans-Baikal Territory for the period from 2012 to 2022, 53 cases of echinococcosis were registered (Table 1), including children under 17 years of age. The largest number of cases was registered in the Krasnochikoysky, Nerchinsko-Zavodsky, and Tungokochensky districts and in the city of Chita. Cases of echinococcosis were revealed in families of hunters with long-term experience. They had hunting dogs, which were kept freely, and deworming measures were carried out untimely or were absent completely.

Through the period of 2012–2022 in the Chukotka Autonomous Area, 20 cases of echinococcosis were found, mainly among rural residents belonging to representatives of indigenous peoples of the North. It is important to note that sledding, reindeer herding, and hunting dogs are widely used by the population in these areas. As of January 1, 2022, 49 patients with echinococcosis and alveococcosis, and 142 people with suspected cystic echinococcosis and alveococcosis were registered at the dispensary. It is also worthy of note that since 2005 there has been a stable downward trend in incidence that was associated with ongoing preventive measures.

A comparative analysis of the epidemic situation in different federal districts revealed that the NCFD held the leading position in terms of the incidence of echinococcosis. In particular, throughout the entire examining period, the incidence rates of echinococcosis in the NCFD exceeded the average statistical indicators for Russia and were higher than those in the SFD and FEFD.

Throughout the period of 2012–2015, an extremely unfavorable epidemic situation of echinococcosis was observed in the Karachayevo-Circassian Republic with annual registration of more than 400 cases of the disease. Moreover, incidence rates averaged 1.5–2.0 per 100 thousand population. However, through the 2020–2022 period, due to the implementation of the republican program for the prevention and control of echinococcosis, no cases of this disease were revealed.

Despite the fact that through the 2012–2022 period, the incidence rates of echinococcosis in the SFD did not exceed the average statistical indicators for Russia with the exception of the 2018–2019 period, in certain areas, from 5 to 11 cases of the disease were recorded annually.

The data presented in Table 2 attest that through the 2012–2022 period, the Republic of Kalmykia with a rate of 0.74–2.19 per 100 thousand population and the Astrakhan Region with a rate of 0.49–1.87 per 100 thousand population were attributed to the territories of the SFD with high incidence rates of echinococcosis. The incidence rates in other territories of the district during this period did not exceed average statistical indicators for Russia. Regrettably, cases of involving children in the epidemic process were registered. In particular, in 2018, out of 59 cases of echinococcosis in the SFD, there were 6 children including 5 cases in the Republic of Kalmykia and 1 case in the Republic of Adygea. In 2022, among revealed cases, there were 3 children including 1 case in the Republic of Adygea and by 1 case each in the Rostov and Astrakhan Regions. In one case, echinococcosis was diagnosed in a child aged 3 years. In general, through the 2017–2022 period, the proportion of children with cystic echinococcosis was 12.3%.

When analyzing epidemiological survey cards, it was found that the gender structure of cases was specified by the ratio of men and women as almost equal, namely 51.6% women and 48.4% men. Among patients with echinococcosis in the SFD, residents of rural areas absolutely dominated (98.4%). Contact with domestic and stray dogs was noted by 84.1% of the patients.

Furthermore, an important section of the work was conducting seroepidemiological monitoring. Examining relatively healthy individuals revealed 374 people with seropositive tests in relation to E. granulosus antigens in the FEFD; the rate of positive samples amounted to 5.8% (95% CI: 5.55–6.13%) (Table 3).

The high frequency of detection of antibodies (26.3%) among the relatively healthy population in the Jewish Autonomous Region is noteworthy, since through the 2012–2022 period, no case of echinococcosis was registered in this subject. It is not excluded that the identified discrepancy between the number of seropositive individuals and the incidence rates of echinococcosis is stipulated by an insufficient level of clinical diagnostics.

Seroepidemiological examinations in the SFD revealed that the average rate of seropositivity to E. granulosus antigens over the comparable period was 2 times lower than in the FEFD and amounted to 2.6% (95% CI: 2.31–3.11%) (Table 4).

It should be noted that the rather low rate of seropositivity (1.3%) to E. granulosus antigens in the Karachayevo-Circassian Republic, combined with a decrease in the incidence of cystic echinococcosis registered through the 2020–2022 period indicates a low frequency of contact of the population with this pathogen and, consequently, reducing its circulation in the region. Along with this, the frequency of detection of class G immunoglobulins to E. granulosus antigens in the Rostov Region and the Republic of Adygea was 3.4% and 2.8%, respectively, which directly correlates with the incidence rate in these areas of the South of Russia (p < 0.05; r = 0.51).

In the authors’ opinion, these indices of seropositivity to E. granulosus antigens among a relatively healthy population may indicate, to a certain extent, the stabilization of the epidemiological situation in these areas of the South of Russia.

One of the objectives of this study was related to conducting sanitary and parasitological monitoring of echinococcosis. In particular, 736 samples of soil and sand were taken in various areas of the Rostov region Including the city of Rostov-on-Don and the town of Starocherkassk, as well as pastures of farm animals in the Neklinovsky and Azovsky districts. As a result of examinations, taeniid oncospheres were found in 19 samples (2.6%), which can be considered indirect evidence of a low level of circulation of echinococcosis pathogens in the Rostov Region.

Discussion

The territory of the FEFD is characterized by a tense epizootic situation. Among the social factors determining the high risk of invasion by echinococcosis pathogens, the leading role belongs to the widespread development of commercial hunting and animal husbandry with economically useful dogs, as well as the peculiarities of wildlife management, in particular collecting wild-growing medicinal plants, berries, and mushrooms. The high rates of infestation of different animal species with E. granulosus and E. multilocularis, revealed over the years, indicate the active circulation of these pathogens on the territory of the FEFD. The epidemiological prerequisite for the spread of echinococcosis in the south of Russia is free-range animal husbandry.

The results obtained in this study confirm the data of other authors on the widespread distribution of echinococcosis in the Russian Federation¹ [11]. Indicatively, in a number of territories of the FEFD and the South of Russia, a high incidence level of echinococcosis continues to be recorded without a clear tendency to the stabilization of the epidemic situation. These include the Republic of Sakha and the Republic of Kalmykia, which indicates a pronounced territorial unevenness in terms of the incidence of echinococcosis in different areas.

Of particular concern is the registration of cases of echinococcosis among children. In this study, the proportion of children in the structure of cases amounted to 12.3%.

The main challenge related to echinococcosis is the untimely diagnosis of the disease. Moreover, echinococcal cysts are usually revealed during a random examination. One possible solution to this problem is a wider clinical and instrumental examination of the population belonging to the risk group, which includes hunters and members of their families; persons engaged in livestock farming; as well as masters of processing and manufacturing of fur products.

Concurrently, the implementation of seroepidemiological monitoring is quite an evident measure that allows for the selection of individuals for further in-depth clinical, laboratory, and instrumental examination. This is especially important for areas where echinococcosis is endemic.

In regard to the predictability of the development of the epidemic situation of echinococcosis, including short-term and long-term forecasts, experts should consider, first of all, the most significant risk factors that pose a threat to the sanitary and epidemiological safety of the population. These include the frequency of detecting infestation in wild and farm animals, the peculiarities of wildlife management accounting for the regional specificity of the population, improper maintenance of dogs, and violation of the schedule of deworming, as well as the number of stray animals.

In the authors’ opinion, one of the most prospective directions for further scientific research is the development of methods for predicting changes in the epidemic situation of echinococcosis in endemic areas based on geographic and informational technologies.

Conclusions

1. During the 2012–2022 period, the highest incidence rates of echinococcosis were recorded in the Republic of Sakha (Yakutia) and the Republic of Kalmykia.
2. Residents of rural areas predominated in the structure of cases (98.4%).
3. Individuals seropositive for granulosus were identified in all examined areas. In the FEFD, the proportion of seropositive individuals was 5.8% (95% CI: 5.55–6.13%); in the examined territories of the south of Russia, the rate was 2.6% (95% CI: 2.31–3.11%).
4. The data obtained indicate the relevance of the problem of echinococcosis for the territories of the FEFD and the South of Russia and the demand for improving the epidemiological surveillance of these diseases.