Distribution and ecology of Echinococcus multilocularis in Central Asia

Distribution and ecology of Echinococcus multilocularis in Central Asia

Parasitology International 55 (2006) S213 – S219 www.elsevier.com/locate/parint Distribution and ecology of Echinococcus multilocularis in Central As...

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Parasitology International 55 (2006) S213 – S219 www.elsevier.com/locate/parint

Distribution and ecology of Echinococcus multilocularis in Central Asia Blok S. Shaikenov * Institute of Zoology, Ministry of Education and Science Pj, Almaty, Kazakhstan Available online 5 December 2005

Abstract Much of Central Asia is characterized by an arid landscape. Foci of Echinococcus multilocularis have a very patchy distribution. This is due to a significant deficiency of moisture in the superficial layers of the ground and is related to the types of animal colonies. In the plain, the abundance of endemic foci increases in a direction from the sandy deserts to steppe. In mountains the highest levels of infection of animals are observed in the eastern part of region. In arid regions, E. multilocularis is typically located in humid mesophilous biotopes. Here there is sufficient moisture in the spring to promote survival of eggs and there is a close interrelation between the definitive and intermediate hosts. D 2005 Published by Elsevier Ireland Ltd. Keywords: Echinococcus multilocularis; Central Asia; Distribution; Ecology

1. Introduction Echinococcus multilocularis is extensively distributed in Europe, northern Asia and North America as far south as the northern states of the USA. In Siberia, prevalence rates in arctic foxes on the Yamal and Taimyr peninsulas, New Land Island, Yakutia and Chukotka reach 65.1– 80% [1 –5]. On the other hand, Rausch et al. [6] reported prevalence rates of almost 80% of E. multilocularis in arctic foxes in Alaska. To a lesser degree, predators and rodents are infected in the forest-steppe and steppes of Western Siberia. In the Omsk area of the Russian Federation, prevalence rates between 27% and 80% were recorded in red foxes between 1951 and 1962 [7], respectively. Likewise in the Barabinskoi steppe in Novosibirsk district, an average of 43% of the foxes were found to be infected [8], and 24 –33% of foxes in the Tuva steppes [9]. In these regions, the usual intermediate hosts of this cestoda are voles (Microtus agrarius, Microtus oeconomus, and Microtus gregalis), Siberian red voles (Clethrionomys rutilus) and the muskrat (Ondatra zibetica), with infection rates of between 3.6% and 7.79% [8]. High humidity on the superficial ground layer and dense vegetation in tundra, forest forest-steppe and a significant part

* Tel.: +7 3272 723123; fax: +7 3272 61 49 01. E-mail address: [email protected]. 1383-5769/$ - see front matter D 2005 Published by Elsevier Ireland Ltd. doi:10.1016/j.parint.2005.11.033

of the steppe zone in the northern part of Eurasia facilitates the longevity of eggs of E. multilocularis. These regions have optimal environment conditions for E. multilocularis. In arid districts of Kazakhstan and Central Asia, it is necessary to take into account microecological factors that promote transmission in some foci. Field researches of rodents were carried out in 1967– 1972, 1979– 1991 and 1999 –2000 in the desert areas around the Aral Sea, the deserts of Karakum, Kzylkum, Moinkum deserts and deserts south of Lake Balkhash. Research was also undertaken in the mountains of Altai, Tarbagatai, Zhungary, Zailiski, ` alasski Alatau and Turgai. To investigate the characteristics O and distribution of natural endemic foci, a variety of habitats were surveyed including the river valleys, irrigation systems, desert landscapes and places with variable features. The effect of geographical features, flora and fauna were also investigated. In total, about 39 000 rodents of 19 species were investigated in the specified deserts. 2. Structure and formation of foci E. multilocularis in the deserts of Central Asia In western Kazakhstan 13,818 rodents of 15 species were investigated (Fig. 1) [10]. Larval cysts of E. multilocularis was found in each location in great gerbils (Rhombomys opimus) and, on one occasion, in each of the little souslik (Spermophilus pygmaeus), grey hamster (Cricetulus migratorius) and little

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Russia

China Uzbekistan

Wooded steppe

Steppe

Desert

Mountain

Semi-desert Lakes/inland seas

Areas where Echinococcus multilocularis was found in the definitive &/or intermediate hosts at high prevalence (>1%) Areas where Echinococcus multilocularis was found in the definitive &/or intermediate hosts at low prevalence (<1%) Areas where definitive &/or intermediate hosts were examined but Echinococcus multilocularis was not found. Fig. 1. Main ecological zones of Kazakhstan and prevalence of E. multilocularis found in large-scale field studies carried out throughout the country (from [10]).

jerboa (Allactaga elater). High infection rates of great gerbils are seen in the valley of the river of Emba (3.16%). In sandy regions between the Emba and Ural rivers, approximately 1% of great gerbils was infected. In the Big Borsuki Desert, the prevalence rate was lower at 0.21 –0.31% of great gerbils. In the stone deserts to the northeast of the Caspian Sea and on the Ustyurt plateau, cysts of alveolar echinococcus rodents are not found in rodents [11 –13]. In the Aral Sea region, Karakum, Kyzylkum, Moinkum and Betpakdala deserts, 14 933 rodents of 16 species have been investigated. Low prevalence rates of 0.05 –0.1% were found in rodents from the vicinity of the Shalkar – Teniz lakes and the Syrdariya and Chu river valleys. However, despite investigating 14 000 rodents, the parasite was not found in the open sandy and stony deserts. In the sandy desert south of Lake Balkhash, 7694 rodents of 8 species have been investigated. Larvae of alveolar Echinococcus were found only 8 times in the lower reaches of the Ili River, and in the area of the Karatal and Naryn rivers (prevalence rate of 0.1%). In sandy areas, larvae were not found in rodents, but in the Ili River valley, 1.5– 9% of muskrats was infected.

The highest infection rates E. multilocularis in natural populations of rodents in deserts of Kazakhstan is found in the valley of the river of Emba in Western Kazakhstan (Fig. 1). This focus is quite extensive and does not appear to be limited by geomorphological structures and may be due to the humid climate influences of the southern part of the Ural mountains. The analysis of bioecological conditions of endemic foci elsewhere shows that they only occur in arid zones where there is significant ground moisture for at least part of the year. Pavlovsky [14] observed that, in endemic zones of various pathogens, different micro foci represent different transmission risk. Naumov [15,16], Fenjuk [17], Kucheruk [18], Olsufjev and Kucheruk [19] and Maximov [20] have, as a result of studying the natural endemic foci of plague and tularemia, observed that the heterogeneity of foci of infection is related to types of habitat. The analysis of our materials suggests that the occurrence of natural endemic foci of E. multilocularis in arid landscapes of Kazakhstan is also determined by habitat features of intermediate and definitive hosts and the survival rate of parasite eggs in various environmental conditions.

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2.4. Ecological communication between E. multilocularis and definitive hosts

2.1. Relief The development of specific flora, which may promote rodent habitat, is related to the microenvironment and local relief. In general, it is determined by the amount of rainfall and moisture retention of the landscape features. Of particular importance is the ability to accumulate moisture. Significant moisture accumulates on certain slopes, low-lying areas, ravines and channels. In these areas, thickets of trees and bushes grow which also play a role in retaining the moisture. The low-lying sites accumulate fine particles as a result of the activities of wind and water. In addition, they preserve moisture in the superficial layers. 2.2. Soil The superficial substratum depends on moisture preserved and plays significant roles in maintaining infectivity of oncospheres. Sandy and clay grounds are favorable in this respect. In sandy soils, moisture is lost quickly and it heats up quickly on exposure to the sun. 2.3. Types of vegetation There is a relationship between the distribution E. multilocularis and types of vegetation due to the feeding behavior of rodents in the spring. Literature data report that rodents readily eat the young shoots of plants. Research has shown that endemic foci occur in places where there is an abundance of annual meadow plants. It is possible that when the young plants are growing rapidly, eggs are carried upwards off the ground and make them more accessible to intermediate hosts. Rodents’ use of vegetative parts of perennial plants (efemeroides, wormwood, and bushes) excludes contact with infection elements.

Of the three stages in the lifecycle of E. multilocularis, it is the adult stage in the definitive hosts that is the most spatially mobile. It is difficult to define the factors that promote infection within the definitive host and hence play a role in determining the location of endemic foci. The location of fox burrows for more than 5 –6 months of the year is probably important. The location on slopes of hills in the vicinity of water is also important. This allows foxes to visit colonies of rodents and contaminate their environment with parasite eggs. Intense environmental contamination in the spring is probably particularly important. Close interrelationships between predators and the intermediate hosts depend on the characteristics of the rodent habitat. In autumn, predators tend to disperse and over winter may make substantial migration. In desert except for the shores of reservoirs, formation of significant foci of E. multilocularis appears to be an ecological paradox. Nevertheless, the high density of susceptible intermediate and final hosts makes this zone a potential dangerous transmission zones. Transmission in the desert involves the red fox (Vulpes vulpes), corsac fox (Vulpes corsac), a spotty cat (Felis lybica) and rodents: large gerbils (R. opimus) and Libyan jird (Meriones libycus), grey hamster (C. migratorius), little jerboa (A. elater), earth jerboa (Allactaga acantion). Nevertheless, most frequently, endemic centers of E. multilocularis in the desert involve large gerbils. However in different parts of the desert (as well in other landscapes), the rodent fauna varies. It depends on the relief, soil structure, humidity of the superficial soil layers, and vegetation. There are two distinct types of large gerbil colony characterized by their food supply and mobility of individuals and reproductive potential.

Fig. 2. The homogenous type of rodent colonies on the plateau of sandy deserts (from [13]).

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Fig. 3. The ribbon type of natural foci of E. multilocularis in north of the Aral Sea (from [13]).

2.5. The continuous type of colony This is formed in places with a homogeneous landscape. Basically it is found in open sand or leveled clay and clay – stone deserts (Fig. 2) [13]. As previously mentioned, these types of colonies are seen in desert plateaux: north east of the Caspian Sea, in Ustyurt, Aral Sea region, Karakum, Kzylkum, Moinkum and in the sand desert south of Lake Balkhash. In this type of colony, cysts of alveolar echinococcosis have not been seen. This is because: 1) in flat deserts, physical properties of the superficial substratum do not promote moisture retention and hence survival of eggs; 2) in these diffuse colonies, there is a break in ecological contact between definitive and intermediate hosts in the spring which is an important time for parasite transmission; and 3) large gerbils on flat sandy deserts feed on the vegetative parts of efemeroides and bushes which are not contaminated with parasite eggs. The non-uniform or mosaic type of colony is characterized by certain geographical features and microclimate conditions. There are three types of mosaic colony: ribbon, oasis and island.

between ridges, in ravines, dry valleys (Fig. 3) [13]. These types of features often have plentiful moisture in late winter and early spring. This type of landscape is seen in the vicinity of the rivers of Emba, Syr-Darya, Ili, and Karatal in the south of the country and on the shores of lakes (Balkhash and Alakol). The cumulative area of ribbon colonies in Kazakh deserts is large. But favorable conditions are not ubiquitous. However this type of rodent colony plays an important role in formation of endemic foci of alveolar echinococcosis in the West of Kazakhstan, in particular in the valley of the river of Emba. In

2.6. Formation of endemic foci of E. multilocularis in mosaic colonies The natural endemic foci of this cestode in deserts of Kazakhstan are essentially mosaic settlements. The basic feature of these settlements is the presence of a stable and high-density of rodent population. Large populations are supported by favorable soil conditions, vegetation and moisture particularly in the spring. The high population density plays an important role in the contact rate between rodents and predators. Ribbon type of foci of alveolar echinococcosis in deserts of Kazakhstan is the most widespread. These habitats tend to occur

Fig. 4. The oasis type of natural foci of E. multilocularis in Southern Balkhash (from [13]).

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Fig. 5. The island type of natural foci of E. multilocularis in Betpakdala desert (from [13]).

this area, infection rates of large gerbils are 3.1 – 3.6%. Likewise, similar infection rates are seen on the shores of lakes in the south of Kazakhstan [11]. Oases foci of E. multilocularis occur in the deserts of the south of Kazakhstan. They are characterized by deep hollows among sandy and clay deserts (Fig. 4). The retention of subsoil moisture favors the rich development of a grassy cover. On slopes, bushy thickets are numerous and predators find favorable conditions. Surface water is frequently found. However, such oasis colonies are small in number and therefore probably play only a minor role in the epidemiology of transmission of E. multilocularis. Such types of colony have been observed south of Lake Balkhash [12,21]. Island colonies of large gerbils are characterized by separate sandy hills located among saline plains [15,22]. The burrows of large gerbil colonies are usually found at the base of the sandy hills some 1– 3 m above the surrounding plain (Fig. 5).

In saline soils because of the presence of water (such as from thawed snow) in the superficial layer there is always an abundance of efemers and solnetzic (salt plants). In such conditions on the banks of the river Chu, we have found significant infection rates of large gerbils with alveola echinococcosis. 3. Ecological bases of formation of the foci E. multilocularis in mountains In Alpine and sub alpine areas the winters are long and maximal precipitation of 800 –1000 mm or more occurs. Therefore infectious stages can maintain viability for longer periods. There is less variability in rodent fauna in the high mountains. In these areas are found grey marmot (Marmota baibacina), narrow-skulled voles (Microtus gregalis), and red (C. rutilus) and Royle’s vole (Alticola roylei). The former

Fig. 6. The natural foci of E. multilocularis in mountains: (A) in subalpine zones and (B) in grassland-steppe belts (from [13]).

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two species prevail in open habitats (Fig. 6). Marmots make up a considerable portion of the summer diet of foxes. Predators constantly visit marmot habitat. They mark the territory with faeces and this provides the infectious stages for the rodent. Intense endemic foci of alveolar echinococosis in grey marmot colonies in subalpine meadows are found in the upper reaches Zailiiski Alatau and in natural boundaries Shalkydysu and Oi-Karagai. Prevalence rates in rodents have changed from 5% up to 24.5% (our data). In the mountains, there are several habitat types. Foxes regularly visit open meadows where there are high populations of rodents. Royle’s vole and narrow skulled voles predominate in the diet of predators in the Zailiiski and Dzungarian Alatau [23]. Habitats characterized with sparse vegetation, rocky outcrops or fir groves are rarely visited by foxes and hence there is limited opportunity for the dispersion of helminth eggs in these areas. Larvae of E. multilocularis are found in the narrowskulled vole and root vole (Microtus oeconomus) in the Zailiiski and Dzungarian Alatau. High numbers of these animals are found on open meadow subalpine and foreststeppe belts [12,20]. The greatest distribution E. multilocularis among other republics of Central Asia is in Kyrgyzstan where 80% of territory occupies mountains. Abdyjaparov and Kuttubaev [24] observed that the infection rates of rodents in subalpine meadows are 0.3 – 3.9%. On Tian-Shan and Pamire-Alai, E. multilocularis are found at 10 species of rodents. Most frequently, it infects grey and red marmots (Marmota baibacina and Marmota n˜audate) and the narrow-skulled vole (Microtus gregalis). Relatively only a small area of Uzbekistan and Turkmenistan has been investigated. E. multilocularis has been found at foxes (8.6%), corsac and the jackal. Rodent infections have been reported: Ondatra zibethica has been reported to be infected at 0.68%; Rhombomys opimus 1.16% and Meriones meridianus 0.44% in the lower valley and delta of the Amu-Darya River [25]. 4. Occurrence of endemic foci in the steppe The structure of the animal population in the steppes is nonuniform and there is a variable landscape and humidity. The greatest concentration of carnivores and the highest density of rodents are found in river valleys, the shores of lakes and reservoirs, conical-shaped depressions on hillsides, lowland and in wooded areas. Batkaev [26 – 28] and Pleshev [29,30] studied the distribution alveolar echinococcosis in Northern Kazakhstan. Wooded patches, lake shore, meadow in valleys and lowland steppe were the 4 predominant habitats, in which hosts infected with the parasite, were found. In the Pavlodar area, the parasite was found in 3.5% (of 155) of steppe marmots (Marmota bobac), 0.4% of steppe lemmings (Lagurus lagurus), 4.4% (of 805) of red voles, 3.2% (of 900) muskrats (Ondatra zibethica), 3.5% (of 566) of narrow-skulled

voles, 2.3% (of 131) of root voles, 0.4% of field-striped mice (Apodemus agrarius) and 0.3% of wood mice (Apodemus sylvaticus). Similar infection rates were found in rodents in the Ishim River valley [29]. It was reported that 25.9% and 21.7% of 154 and 244 foxes and corsacs, respectively, were infected [27,28]. Fedorov [31] found 30% of corsacs in the Ishim River valley was infected. In the forest-steppe and on northern slopes of low mountains east of a line joining Petropavlovsk – Astana – Karkaralinsk, the annual rainfall is 350 –430 mm. In this area, when the temperature is greater than 10 -C, the surface moisture retained in the spring provides suitable conditions for the parasite. The variable relief of low mountains, accumulation of deposits in depression, small lakes and spring flood meadows is typical of this area. The network of small rivers and the presence of large valleys (of the rivers Ishim, Shiderty and Irtysh) characterize the landscape where endemic foci of E. multilocularis are found. 5. Features of endemic foci along the shores of lakes Intense endemic foci of alveolar echinococcosis in Kazakhstan are associated with large lakes (lakes Balkhash, Alakol, Zaisan, Korgazhin, Saburov) where there are populations of muskrat [32,33]. Infection rates can reach 1.5– 9%. Research undertaken around lakes Zaisan and Balkhash has shown that there is a patchy distribution of the parasite. Infected animals are frequently found in flat shore areas. This may be due to the increased moisture in these areas from changing lake levels, especially in the spring. Rising lake levels in the spring also restrict the available area for muskrats and so may increase their exposure to the eggs of the parasite [34]. 6. Conclusions Landscape and microclimatic conditions affect the location of endemic foci of E. multilocularis in different zones in Central Asia resulting in a very patchy distribution. These features affect the type and structure of definitive and intermediate host populations and their interrelationships and hence transmission of the parasite. In the plains, the intensity of the distribution increases from the sandy desert with the lowest prevalence rates which much higher prevalence rates seen in animals in the steppe. In mountain areas high infection rates are seen in the east of the region. Generally, E. multilocularis is most commonly found in a humid and mezophil biotope. Here there is sufficient moisture to promote survival of therefore living egg stage and sufficient interaction between definitive and intermediate hosts to promote transmission. Acknowledgements The author would like to thank INTAS (03-51-5661) for financial support and Prof. P. R. Torgerson for courtesy reviewing the paper.

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