A Serological Survey About Zoonoses in the Verkhoyansk Area,Northeastern Siberia (Sakha Republic,Russian Federation)

Introduction

Whatever their status, worldwide or restricted to particular areas on the planet, zoonoses are recognized as an important source of disease (van Doorn 2014) and an increasing major threat for human health in the future (Learner 2013). Zoonoses are often acquired by contact with either domestic or pet animals or with wildlife, and this feature is enhanced by the permanently growing need of resources that leads humans to increase the pressure on the environment (Karesh et al. 2012). Moreover, climate change may participate in the modification of natural foci of zoonotic diseases (Revich et al. 2008). This epidemiological situation prevails in Arctic and subarctic regions (Jenkins et al. 2013), including Siberia.

In 2007, a survey about the seroepidemiology of nine zoonoses was conducted in Vilûjsk, Yakutia, by researchers from the Northeastern Federal University in Yakutsk and from University Toulouse III/CNRS UMR 5288 (Magnaval et al. 2011). The results from this field work prompted French and Russian scientific authorities to include research on zoonoses in a larger program entitled COSIE (Coevolution of Man and environment in Eastern Siberia). The Vilûjsk survey had been carried out in a subarctic area, ∼325 km south of the Arctic Circle. Therefore, future investigations were intended to concern a more boreal zone and be performed in the administrative region of Verkhoyansk (latitude: 67°33′13.9″ [67.5539°] North—longitude: 133°23′23.1″ [133.3898°] East). Field information provided by archeologists also working inside the COSIE program selected two villages, Suordakh (latitude: 66°40′34.5″ [66.6762°] North—longitude: 131°46′16.4″ [131.7712°] East—elevation: 216 meters—325 inhabitants) and Tomtor (latitude: 67°12′17.9″ [67.205°] North—longitude: 132°8′10.4″ [132.1362°] East—elevation: 177 meters—282 inhabitants). Both villages are located on the Dulgalakh River on the eastern rim of the Khrebet Orulgan Mountains that are part of the Verkhoyansk Range. Climatic conditions are the harshest in the Northern Hemisphere, and Verkhoyansk has been nicknamed the Pole of Cold. According to the Climats™ database provided by Meteo France (Toulouse, France), data concerning the Verkhoyansk weather station (elevation: 136 meters) indicate that the mean annual temperature is −15.9°C, the annual thermal amplitude ranges on average from −55°C in January to +20°C in July, and the average number of days with freeze is 285 a year.

The present article reports the results from a survey that was conducted from 27 March, 2012, to 4 April, 2012, in Suordakh and Tomtor villages to determine the seroprevalence of 10 agents of zoonoses and to identify possible risk factors for seropositivity. It should be recalled that such serological investigations detect only a contact with a given infectious agent, and not the related disease. However, the names of the zoonoses were used throughout the text due to a better convenience.

Materials and Methods

Results

The demographic and occupational characteristics of the study subjects are displayed in Table 2, and Table 3 shows the environmental features and the food habits of the surveyed population. Because of a similar environment and way of life in both villages, the criterion, place of residence, was not entered.

Table 4 shows the results of the serological investigations. No positive result was observed for cysticercosis, CE, toxocariasis, trichinellosis, and both arboviral zoonoses. The positivity rate was 10.4% for Lyme borreliosis, 5.2% for toxoplasmosis (only specific IgG were detected), 2.6% for recently acquired Q fever, and 1.3% for AE. All patients' sera exhibiting a positive result for Lyme serology tested negative by Treponema TPHA.

Bivariate analysis of the data set using χ², Fisher's, and Mann–Whitney tests did not find any correlation between the outcome variables, namely the serology results stratified as positive or negative, and the possible exposure variables listed in Tables 2 and 3. No correlation was found between age and serology results considered as continuous variables (Spearman's test).

Discussion

First, the study population was essentially a convenience sample rather than representative of the entire population of Suordakh and Tomtor villages, so results concerning the observed diseases must be cautiously considered. Then, Russian literature was used when the articles were written in English and available through Internet.

A prominent finding concerning bacterial zoonoses was a 10.4% seroprevalence rate for Lyme borreliosis. Although Lyme disease in western Siberia may be caused by B. afzelii or Borrelia garinii (Rar et al. 2005), ELISA using VlsE recombinant antigen can detect antibodies directed against these species belonging to the B. burgdorferi sensu lato complex (Wilske 2005). According to Russian sources, northeastern Siberia was considered as free of Lyme borreliosis (Malkhazova et al. 2014). However, specimens of the tick Ixodes persulcatus, specifically the vector for B. burgdorferi s.l. in Siberia (Eisen and Lane 2002), have been recently found in Yakutia (Revich et al. 2012). Moreover, during the 2007 Vilûjsk survey, Lyme serology using indirect immunofluorescence detected 9 positive results in 90 subjects (Magnaval et al. 2011), and a survey carried out among 41 rural volunteers from the same Vilûjsk area found a 19.5% positivity rate using ELISA, followed by WB (Storch et al. 2008). These findings suggest that infection by B. burgdorferi s.l. would have spread to the Arctic areas of the Sakha Republic from not officially recognized foci that pre-existed in subarctic Yakutia. This could be due to climate change, since the level of ambient temperature regulates tick density, and the periods of the year that ticks are active (Eisen and Lane 2002); in Yakutia, the annual average temperature has increased by 1.1°C between 1955 and 2000 (Revich et al. 2008).

A similar discrepancy between available data and the results from the present survey arose about Q fever. Human cases were reported from eastern Siberia during the USSR era (Revich et al. 2012), but more recent epidemiological information from this area is not currently available in the English literature. The presence of IgG antibodies against Phase II antigens is evocative of an acute or recent infection, so the finding of two positive results (2.6%) suggests that Q fever has a rather high incidence rate in the studied rural population. An analysis of the official Russian statistics for the period 1985–2005 yielded a mean annual incidence in Russia of ∼1 case per million of population (Tokarevich et al. 2006), but it was stated that Q fever was obviously underdiagnosed.

Among parasitic zoonoses, specific immunodiagnoses tested negative for cysticercosis, toxocariasis, and trichinellosis. Concerning toxocariasis, the Vilûjsk survey (Magnaval et al. 2011), which also used WB, found a 4.4% seroprevalence rate among 90 subjects, a result which was not significantly different from the 0% recorded in this study (Fisher's exact test). In Canada, in the Arctic region of Nunavik, which extends from 55° N to 62° N, the seroprevalence rate by ELISA was 1.7% among 2213 volunteers (Goyette et al. 2014). According to Russian official statistics, the incidence rate for toxocariasis would be very low, ranging from 0.26 per 100,000 in the Sakha Republic to 0.44 per 100,000 in the Arctic district of Arkhangelsk (Dudarev et al. 2013). However, the assessment of the incidence rate is not appropriate to study the epidemiology of this long-standing zoonosis—because it is quite difficult to distinguish between current and past infections (Smith et al. 2009)—and was actually never used (Lee et al. 2014). Undoubtedly, the harsh Arctic climate destroyed Toxocara sp. eggs in the soil and therefore dampened the diffusion of this mostly soil-transmitted helminthozoonosis.

For cysticercosis, the international literature did not provide any information about the prevalence of this helminthiasis in Arctic areas in America or Europe or in Siberia (Dudarev et al. 2013). In the present study, where no positive result was observed, only 48.1% of the subjects reported a food habit of pork meat that was always well cooked. This factor was further circumstantial evidence that any human infection with the adult form of T. solium was absent.

The food-borne route, through ingestion of meat from various domestic or wild carnivorous or omnivorous mammals, and also from horses, is the major way of contamination for human trichinellosis. The absence of any positive serological result in a population that has a food habit of meat from hunted bears or from locally slaughtered horses (Table 3) was therefore surprising. In Vilûsjk (Magnaval et al. 2011), the seroprevalence was 4.4%, but did not significantly differ from the 0% rate found in the present survey (Fisher's exact test). In Alaska, only sporadic cases or small epidemics have been reported (Jenkins et al. 2013). In Nunavik, the seroprevalence of trichinellosis in the Inuit population was as high as 18.6% (Goyette et al. 2014), but the prominent risk factor was a food habit of raw meat from freshly killed walruses (Larrat et al. 2012), a culinary tradition, which is unknown in the Verkhoyansk area. Russian official statistics reported not only a 0.31 per 100,000 incidence rate for trichinellosis in the entire Sakha Republic but also very low incidence values from Arctic Russia, ranging from nil in the Murmansk district to 0.01 per 100,000 in the Arkhangelsk district (Dudarev et al. 2013), all facts which were in accordance with the zero seroprevalence found in the Verkhoyansk area. Explanation of this result could have a climatic origin: in the Arctic or subarctic areas of Yakutia, people used to store meat from game or domestic animals outside the home for weeks, in pantries that are therefore exposed for at least 8 months a year to temperatures under −20°C, and this storage habit could achieve natural sanitization.

Concerning echinococcoses, seroprevalence was found to be zero for CE, similar to the Vilûjsk survey (Magnaval et al. 2011), but one AE case was detected (1.3%). In Alaska, only 13 CE human cases have been diagnosed by imaging and/or surgery between 1987 and 2009 (Jenkins et al. 2013) among a population that had grown from 540,000 up to 700,000 residents. In Nunavik, the seroprevalence, as assessed by a commercial ELISA kit using a crude antigenic extract of E. granulosus, was 6.3% among 2213 subjects (Goyette et al. 2014). For AE, the presence of only one positive result of 77 should be cautiously considered because reliable elements of comparison with other Arctic areas are lacking. In western Alaska, the seroprevalence ranged in 1980 from <1% to 1.6% in the villages located on the Alaskan shore of the Chukchi Sea or on the small islands in the Bering Strait (Jenkins et al. 2013). However, the sensitivity and the specificity of the immunodiagnostic methods used in the late 1970s are questionable. No data are available for Nunavik, and concerning Europe, AE in humans has not been detected in northern Scandinavia (Wahlström et al. 2012). The combination of these facts with the finding of this single Yakutian-positive result suggests that AE transmission would occur at a low level in Arctic Yakutia. Unfortunately, the Russian official statistics do not distinguish between AE and CE and report only the incidence for echinococcoses, which ranged from 0.04 per 100,000 to 1.21 per 100,000 (Dudarev et al. 2013). Because Echinocococcus sp. eggs that would be spread in a humid soil are then extremely resistant to extreme temperatures (Jenkins et al. 2013), the Arctic environment cannot explain such a low level of seroprevalence for CE and AE, and therefore this finding requires further investigation.

For toxoplasmosis, the 5.2% seroprevalence found in the present study did not significantly differ from the 8.9% rate reported from Vilûjsk (Magnaval et al. 2011). In Alaska, a 16% seroprevalence rate was found in 1975 from 1572 natives (Peterson et al. 1974). However, the expression of the serology results in dilution, and not in international units, made any comparison with the current result from Yakutia impossible. In Nunavik, a 27.2% seroprevalence was found among 2209 Inuit subjects, a result that significantly differed (Fisher's exact test: 0.000001, p = 0.000002) from the 5.2% rate found in the Verkhoyansk area. Consumption of meat from marine mammals, a food habit that was absent in the Verkhoyansk area, was identified as the only risk factor in Nunavik (Goyette et al. 2014). In the studied Yakutian communities, classical risk factors for toxoplasmosis transmission, namely the presence of domestic cats at home (42.9%) and the food habit of raw horse meat (92.2%), were prominent. These facts made the observed 5.2% seroprevalence surprising. Again, the rough climatic conditions can be suspected to play a major role in the reduction of toxoplasmosis transmission. The long Siberian cold season with a deep freeze certainly affects the survival of oocysts in the environment and therefore the infection rate in meat-producing animals (Hill and Dubey 2002). Moreover, freeze sanitizes meat by destruction of the cysts containing bradyzoites. For example, tissue cysts in pork meat were rendered nonviable following exposure at −12°C for 3 days (Dubey 1988). Similar to trichinellosis, the local habit of storing meat in external pantries during the cold season or, during summer, in cellars deeply dug in the permafrost certainly drastically lowers toxoplasmosis transmission in Arctic Yakutia.

No seroprevalence was recorded for TBE and WNV infections, and the difference with the results from the Vilûjsk survey (Magnaval et al. 2011) was not significant (Fisher's exact test). Currently, the main endemic area of TBE is a belt extending from eastern Europe to China and Japan (Lindquist and Vapalahti 2014) with the 60° N parallel as the northern limit (Estrada-Peña and de la Fuente 2014). However, due to a patchy distribution of active foci and also to the climate change, this zoonosis has to be considered outside this traditional North border (Revich et al. 2008). In the Arctic Russia, TBE has been reported on a regular basis, for example, from the Arkhangelsk district or from the northern part of the Komi Republic (Revich et al. 2008). This epidemiological fact, combined with the likely presence of I. persulcatus ticks in the Verkhoyansk area, as suspected from the Lyme seroprevalence found in the present study, suggests that foci of TBE could exist in northern Yakutia. Further surveys, including a molecular-based search of TBE viruses in ticks, should therefore be envisaged. WNV infection occurs mostly in temperate climates, but several strains of WNV have been isolated from ticks, birds, and mosquitoes in the southern area of European Russia and western Siberia (Platonov 2001), and occasional foci of human infection have been reported in northern Europe and Siberia (Platonov et al. 2014). These findings indicate that the lack of positive results in the present study should be considered similarly to TBE.

In conclusion, in the Verkhoyansk district, Lyme borreliosis and Q fever appeared to be transmitted to humans on a regular basis. In the case of a possible presence outside this area, these zoonoses would represent a major threat to the health of people living, sporting, or working in Arctic Yakutia. The epidemiological situation of AE and CE in the Verkkoyanksh region has to be clarified. Climate change can be incriminated in the spreading of Lyme borreliosis in Yakutia and particularly toward upper latitudes in this country (Revich et al. 2012), whereas the recognized epidemiology of AE and Q fever suggests that both zoonoses have been present in Arctic Yakutia for a long time.