Host-based formation of fauna of lung helminths, its biological and taxonomic classification Текст научной статьи по специальности «Биологические науки»

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ЭПИЗООТОЛОГИЯ, ЭПИДЕМИОЛОГИЯ И МОНИТОРИНГ

ПАРАЗИТАРНЫХ БОЛЕЗНЕЙ

Поступила в редакцию 12.03.2016 Принята в печать 20.08.2016

УДК 619:616.995.132-079.4 DOI: 10.12737/21659

Для цитирования:

Мовсесян С.О., Панайотова-Пенчева М.С., Демиаскевич А.В., Воронин М.В. Фауна легочных гельминтов в организме хозяина, ее биологическая и таксономическая классификация //Российский паразитологический журнал. — М., 2016. — Т. 37. — Вып. 3. — С 345-369

For citation:

Movsesyan S.O., Panayotova-Pencheva M.S., Demiaszkiewiz A.W., Voronin M.V. Host-based formation of fauna of lung helminths, its biological and taxonomic classification. Russian journal of parasitology, 2016, V. 37, Iss. 3., pp. 345-369

ФАУНА ЛЕГОЧНЫХ ГЕЛЬМИНТОВ В ОРГАНИЗМЕ ХОЗЯИНА, ЕЕ БИОЛОГИЧЕСКАЯ И ТАКСОНОМИЧЕСКАЯ

КЛАССИФИКАЦИЯ

Мовсесян С.О.1'2, Панайотова-Пенчева М.С.3, Демиаскевич A.B.4, Воронин М.В.1

1Центр паразитологии ИПЭЭ им. А.Н. Северцова РАН, Москва, Россия, e-mail: [email protected] Институт зоологии Научного Центра Зоологии и Гидроэкологии АН Республики Армения, Ереван, Армения.

Институт экспериментальной морфологии, патологии и антропологии и музей (ИЕМПАМ) Болгарской Академии Наук, София, ул. Акад. Г. Бончева, 25, e-mail: [email protected]

4Институт Паразитологии им. В. Стефански при Польской Академии Наук, Польша, 00-818 Варшава, ул. Тварда 51/55.

Цель исследования: Провести изучение различных групп легочных гельминтов; разработать биологическую и таксономическую классификацию данного вида гельминтов.

Материалы и методы: Проведены исследования 16 видов гельминтов семейств Cervidae, Bovidae, Leporidae, а также легочных гельминтов человека на территории России (Юг и центральные районы), Армении, Болгарии, Польши. Обнаруженные гельминты были изучены с использованием традиционных и новых методов гельминтологического исследования.

Результаты и обсуждение: В легких у исследованных млекопитающих, найдено 23 вида гельминтов, включая 1 Taeniidae (Echinococcus granulosus), 4 Dictyocaulidae и 18 Protostrongylidae. Мы разделили все эти легочные гельминты натри биологические группы.

В первую группу (геогельминты) вошли нематоды семейства Dictyocaulidae. Жизненный цикл данного вида гельминтов моноксенический, осуществляется прямым путём, без промежуточных хозяев

Вторая группа (биогельминты) включала в себя гельминты семейства Protostrongylidae. Характерным признаком является участие в их биологическом цикле промежуточных хозяев — наземных моллюсков.

Ктретьей группе были отнесены возбудители довольно опасного зооноза — Echinococcus granulosis larvae. Эти цестоды развиваются со сменой хозяев, но их промежуточными хозяевами являются позвоночные млекопитающие, имеющие окончательных хозяев —также позвоночных, в основном, плотоядных животных.

Нами также предложена таксономическая классификация семейства Protostrongylidae haelminths.

Ключевые слова: биологическое разнообразие, легочные гельминты, окончательные хозяева, промежуточные хозяева, географическое распределение, зоонозы.

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Russian Journal of Parasitology, 2016, V. 37, Iss. 3

DOI: 10.12737/21659 Received: 12.03.2016 Accepted: 20.08.2016

HOST-BASED FORMATION OF FAUNA OF LUNG HELMINTHS, ITS BIOLOGICAL AND TAXONOMIC CLASSIFICATION

Movsesyan S.O.12, Panayotova-Pencheva M.S.3, Demiaszkiewiz A.W.4, Voronin M.V.1

1Center of Parasitology, A.N. Severtsov's Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia, e-mail: [email protected]

Institute of Zoology of Scientific Center for Zoology and Hydroecology, NAS of Republic of Armenia, Yerevan, Armenia.

Institute of Experimental Morphology, Pathology and Anthropology with Museum, Bulgarian Academy of Sciences, Sofia, Acad. G. BonchevStr., 25, e-mail: [email protected]

4W. Stefansky Institute of Parasitology, PAS, 00-818, Warsaw, Twarda str. 51/55, Poland

Object of study: Studies of lung helminths from various groups were performed. Elaboration of biological and taxonomic classification of these species has been proposed.

Materials and methods: 16 species from families Cervidae, Bovidae, Leporidae and humans were studied for lung helminths in Russia (South and central), Armenia, Bulgaria, Poland. The helminths found were studied using a scope of traditional and elaborated helminthological methods.

Results and discussion: In lungs of mammals studied 23 helminth species have been found including 1 of Taeniidae (Echinococcus granulosus), 4 of Dictyocaulidae and 18 of Protostrongylidae.

We have divided species composition of these lung helminths into three biological groups.

The first biological group included nematodes from Dictyocaulidae family. Life cycles of those helminths are monoxenous (they are geohelminths). The second group includes helminths from family Protostrongylidae. Their life cycles include intermediate hosts — land snails and so they are dixenous (biohelminths). The third group includes an agent of a quite dangerous zoonosis — Echinococcus granulosis larvae. These cestodes also develop per dixenous type, but their intermediate hosts are vertebrates with definitive hosts also vertebrate, mostly carnivores.

Taxonomic classification for family Protostrongylidae haelminths is also proposed.

Keywords: biological diversity, lung helminths, definitive hosts, intermediate hosts, geographical distributions, zoonoses.

The results ofourstudies on biological diversity ofanimal (and human) lung helminths had been partially published in articles presenting some fragments on biological diversity of lung helminths and helminthoses. E.g., the article (Movsesyan et al., 2014) gives data on a character of sheep infections with Protostrongylidae in Armenia depending on natural landscape zones, results of these studies has also been presented at BIT's 5th Annual World Congress of Microbes — 2015 (Shanghai, China) and published as abstract in the Congress' Proceedings (Movsesyan, 2015).

It had been established that protostrongylosis, mulleriosis, cystocaulosis are widely distributed in Armenia and are registered at all natural landscape zones in animals of all ages. In 20-25% of cases protostrongyloidoses cause associated lung infections (Movsesyan et al., 2009).

Material on biological development cycles of Protostrongylidae had been presented in works (Movsesyan et al., 2010; Panayotova-Pencheva, Movsesyan, 2012) which show many land mollusk species serving as intermediate hosts for these nematodes.

Development cycles, distribution and epizootology of animal Protostrongylidae were given in the article by Panayotova-Pencheva et al. (2012). It shows part various vertebrate and invertebrate species play as definitive and intermediate hosts, respectively.

Abstract:

Introduction

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Here we publish the full results of our studies of biodiversity of lung helminths of animals and humans for the first time.

Material and methods

Helminthological material has been obtained from mammals of families Bovidae, Cervidae, Leporidae at Armenia, Bulgaria, Poland and southern regions of Russia (Fig. 1).

Methods

The helminthological material obtained was taken through cameral processing to establish species identity.

The methods used are given below in short and may be found in more detail in the monograph Diagnosis of Parasitical diseases (2004) edited by S.O. Movsesyan.

Intravital diagnostics of lung nematodes was performed using methods of Weid, Berman, Boyakhchyan, Kotelnikov, Korchagin, Khrenov. For postmortem diagnostics we used methods of partial dissection of organs in question per Skrjabin to obtain helminths from lungs, liver, kidneys and other organs.

Basics of these methods are given below:

Method of Weid — several fresh (no more than 6 hours) faecal pellets were placed into a Petri dish or clock glass, water was added, and after 5-10 minutes the pellets were taken from the dish while the liquid left placed under microscope to search for lung nematode larvae.

Method of Berman — used a cone with thin end up to 15 cm, on which rubber tube up to 20 cm was put. A thin test tube was placed into its free end. Fresh faeces (no more than 6-7 hr, 19-20 g) were put on wire sieve or gauze and placed into the cones with warm — up to 40 °C — water. After an hour long exposition the test tube was taken from the rubber tube, liquid poured out to the sediment's level, sediment was shaken then taken to a slide and studied under microscope for nematode larvae.

Method of Kotelnikov. Korchagin and Khrenov — animal faeces were placed into centrifugal tubes, filled with water at 25-26 °C and centrifuged at 1000-1500 rotations/minute for 2 min. After that faeces were taken from tubes using pincers, water poured out to sediment level and sediment shaken then taken to slides and studied under microscope.

Method of partial helminthological dissection per Skrvabin—to obtain nematodes from lungs the latter were torn into small fragments and placed into a container with water. After 10-15 minutes lung fragments were rinsed and then discarded while water kept until sedimentation. The sediment was then studied under microscope for nematode larvae. The larvae found were placed into 3% formaldehyde solution for subsequent cameral processing.

Method of boiling abnormal lung tissue in lactic acid (Panavotova-Pencheva, 2011) — This method was used to find small, hardly visible worms located in the bronchioli and alveoli. The abnormal lung tissues were examined as follows: 1-2 cm fragments from the lung lesions were taken and boiled in 40 percent lactic acid in a water bath at 100 °C for 1.5 hour. After that small (2-3 mm) pieces were compressed between slides and observed under a light microscope at magnification of 63, 160 and 400x to visualize sexual structures such as the spicules and gubernaculum.

Method of Boyakhchyan (Boyakhchyan. 2007) — faeces were taken from animals individually (3-4 balls), placed into small (20-30 cm ) glass or plastic flagons, filled with water and closed. The flagons with probes were exposed so for 3 hours without shaking. During this time lung nematodes' larvae exited into water from faeces. To conserve the larvae liquid from the flagon was moved into a similar one containing 5-10 ml of 10% formaldehyde and faeces discarded. The flagons were tightly closed. In such manner they may be retained for a long time. So they were taken to a laboratory for microscopic studies.

Echinococcus larvae could be easily found during dissection of infected organs (lungs, liver, etc.) through presence of vesicles — cysts of Echinococcus.

To find out species composition of Protostrongylidae obtained, monograph of S.N. Boev(1975) was used. Larval forms of Echinococcus were established according to K.I. Abuladze (1964).

For mollusk species composition fundamental monographs (Akramovsky, 1976; Likharev,

Rammelmeier, 1952; Damianov S.G., Likharev I.M., 1975; Sysoev, Schileiko, 2009) were used. _

All-Russian Scientific Research Institute of Fundamental and Applied Parasitology of Animals and Plants named after K.I. Skryabin 117218, Russia, Moscow, Bolshaya Cheremushkinskaya str., 28

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Table 1

A list of definitive host species of lung nematodes

Animal species Russia Armenia Bulgaria Poland Nematode species

Order Artiodactyla Suborder Ruminantia Family Cervidae

Dama dama - Varestrongylus sagittatus; D. filaria; D. viviparus; D eckerti

Cervus nippon - - - E. cervi] V. sagittatus; D. filaria; D. viviparus; M. capillaris

C. elaphus - V. sagittatus; E. cervi] Dictyocaulus eckerti\ D. filaria; D. viviparus

C. elaphus sibiricus - - - Varestrongylus capreoli; V. sagittatus; E. cervi

Capreolus capreolus - - Varestrongylus capreoli; Muellerius capillaris; Dictyocaulus capreolus; D. viviparus

Alces alces - - E. cervi; E. aids, V. capreoli; Muellerius capillaris; D. capreolus; D. filaria; D. viviparus

Fam. Bovidae

Bison bonasus - - - Dictyocaulus viviparus

Bos taurus - Dictyocaulus viviparus

Rupicapra rupicapra - - P. hobmaieri; P. rupicaprae; M. capillaris; M. tenuispiculatus; N. linearis

Capra aegagrus - - P. muraschkinzewi; P. rufescens; M. capillaris; C. ocreatus

Ovis ammon - - P. davtiani; P. hobmaieri; P. raillieti; C. ocreatus

Ovis musimon / Mouflon musimon - - P. davtiani; P. hobmaieri; P. raillieti; P. rufescens; M. capillaris; V. capreoli

Ovis ophion armeniana - - - P. davtiani; P. muraschkinzewi; C. ocreatus

Ovis an es/ Ovis amm on. dorn. M. capillaris; C. ocreatus; N. linearis; P. brevispiculum; P. rufescens; P. hobmaieri; D. filaria

Capra hircus M. capillaris; N. linearis; P. rufescens; P. hobmaieri; D. filaria

Order Lagomorpha Family Leporidae

Lepus europeus + - -

Total animal species 16 13 6 9

Our analysis of character of lung helminths life cycles was based on concept proposed by Leickart at 1879 (cited through Petrochenko (1967)) that helminths may develop in more than one host. This concept provided basis for intensive studies of helminths' life cycles. As a result, the following concepts had been formulated for helminths' life cycles:

Monoxenous, dixenous and polyxenous types of development — terms were based on a Greek word 'xenos'—i.e. host.

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Later K.I. Skrjabin and R.S. Schultz (1940) proposed a new classification of character of life cycles of helminth development dividing them into categories of geohelminths development of which takes place without intermediate hosts and biohelminths where intermediate hosts do take

Results and Discussion

Species composition of Protostrongylidae-infected animals can be seen from Table 1 showing that totally 16 animal species were tested, with 13 in Russia, 7 in Bulgaria, 9 in Poland and 6 in Armenia. Ruminants from Bovidae and Cervidae families were mostly mixed infected (with several of the nematode species at the same time). This fact shows a broad receptivity of ruminants to Protostrongylidae. At the same time, regimen of maintenance and nutrition — grazing, watering, contacts with infection foci at natural conditions — also contribute to these animals infection. As for other studied mammals — from family Leporidae — they were found infected with only a single helminth species: Protostrongylus tauricus.

According to literature data, the following lung helminth species had been found in wild ungulates by Fertikov et al. (1999):

in Alces alces — Dictyocaulus filaría, D. viviparus, Muellerius capillaris, Elaphostrongylus cervi, E. alcis, Varestrongylus capreolr,

in Cervus dama — D. filaría, D. viviparus, Varestrongylus saggittatus]

in Cervus nippon — D. filaría, D. viviparus, E. cervi, V. saggittatus;

in Capreolus capreolus — D. viviparus, Muellerius capillaris, Varestrongylus capreolr,

in Cervus elaphus — D. viviparus, E. cervi, V. capreoli, V. saggittatus.

Samojlovaskaya (2010) had found the following species of lung nematodes in wild ungulates:

in Alces alces — D. filaría, V. capreoli;

in Cervus nippon — D. filaría, M. capillaris.

In addition to Protostrongylidae we had also found 4 nematode species from family Dictyocaulidae (Díctyocaulus filaría, D. viviparus, D. eckertí, D. capreolus) and one Taeniidae cestode species (Echinococcus granulosus).

According to their life cycles, helminth species found were divided into three biological groups (Movsesyan et al., 2014) (Fig. 2 (a, b, c)):

Geohelminths (monoxenous) — Dictyocaulidae;

Biohelminths (dixenous) with invertebrate intermediate hosts — Protostrongylidae; Biohelminths (dixenous) with vertebrate intermediate hosts — Taeniidae.

I Biological group:

Monoxenous life cycles were characteristic of nematodes from family Dictyocaulidae a(Fig. 3), including Díctyocaulus filaría from lungs of small ruminants (sheep, goats, moufflon, Bezoar goat), D. viviparus from lungs of cattle and D. eckerty from Red deer and Fallow deer.

There were 4 Dictyocaulus species found in Poland: D. viviparus from cattle and European bison, D. filaría from sheep, D. eckerty from Red deer, and D. capreolus from elk and Roe deer (Demiaszkiewicz et al., 2009 a; Demiaszkiewicz et al., 2009 b; Pyziel et al., 2015).

In Bulgaria, D. eckertí was found in Red deer Cervus elaphus and Fallow deer Dama dama (Panayotova-Pencheva, 2012).

For sheep of Armenia, dictyocaulosis is distributed throughout all 5 ecological zones studied. Also, the highest infection rate (60%) with D. filaría has been found in lambs at subalpine meadows and the lowest — in lambs from dry Subtropics (Fig. 4).

II Biological group:

The second biological group of lung helminths are those development cycles of which pass through invertebrates, specifically land mollusks. Such are Protostrongylidae nematodes. The main diagnostic criteria of their morphology are shown at fig. 5 a, b.

In regions studied we have found 18 Protostrongylidae species, including 18 in Russia, 11 in Bulgaria, 10 in Poland and 7 in Armenia. The species common for all region was Muellerius capillaris. A list of species is given in Table 2.

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Table 2

A list of Nematoda species studied

е es Russia* Armenia Bulgaria Poland

Dictyocaulidae

Dictyocaulus filaria (Rudolphi, 1809) -

D. viviparus (Bloch, 1782) -

D. capreolus Gibbons, Höglund, 2002 -

D. eckerti Skrjabin - -

Total Dictyocaulidae 4 species

Protostrongylidae (Leiper, 1926) Boev et Schulz, 1950

Cystocaulus nigrescens (Jerke, 1911) Gebauer, 1932 - -

C. ocreatus (Railliet et Henry, 1907) Mikacic, 1939 -

Elaphostrongylus aleis Sten 1990 - -

E. cem Cameron, 1931 -

Muellerius capillaris (Mueller, 1889) Cameron, 1927

M. tenuispiculatus Gebauer, 1932 -

Neostrongylus linearis (Marotel, 1913) Gebauer, 1932 -

Protostrongylus brevispiculatum Mikacic, 1940 - -

P. davtiani (Savina, 1940) Davtian, 1949 -

P. hobmaieri (Schulz, Orlow et Kutass, 1933) Cameron, 1934

P. kochi (Schulz, Orloff et Kutass, 1933) - -

P. muraschkinzewi (Davtian, 1940) Dougherty, 1951 - -

P. raillieti (Schulz, Orlow et Kutass, 1933) Cameron, 1934 -

P. rufescens (Leuckart, 1865 Kamensky, 1905 -

P. rupicaprae Gebauer, 1932 -

P. tauricus Schulz et Kadenazii, 1949 - -

Varestrongylus capreoli (Stroh et Schmid, 1938) - -

V. sagittatus (Mueller, 1890) Dougherty, 1945 -

Total Protostrongylidae 18 species 18 11 13

'Russia — here means south and central regions

Currently world fauna of Protostrongylidae includes about 60 species of 6 subfamilies and 12 genera. Their systematics are given at fig. 6.

According to Gadaev (2015) the following Protostrogylidae species were dominant in wild animals of Chechen Republic of Russian Federation:

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in Capreolus capreolus — P. davtiani, P. skrjabini, P. hobmaieri, M. capillaris;

in Capra cylindricornis — P. kochi, P. hobmaieri, M. capillaris, C. nigrescens;

in Capra aegagrus — M. capillaris, P. davtiani;

in Rupicapra rupicapra — M. capillaris.

Taking into account all the regions, the Protostrongylidae species most widely distributed were: Muellerius capillaris, Cystocaulus nigrescens, Protostrongylus muraschkinzewi, P. hobmaeri, P. kochi, P. davtiani. Some pictures of widely distributed lung helminths are presented on fig. 7.

As for intermediate hosts of Protostrongylidae, 77 species were found. 50 of them were present in Russia, 39 in Armenia, 20 in Bulgaria, 12 in Poland. Studies in Armenia conditions have shown that there are 9 most commonly infected mollusk species (Fig. 8), with Helicella derbentina, Napaeopsis hohenackeri playing the greatest part.

These mollusks in conditions of Armenia high-and lowlands were infected with Protostrongylidae larvae (Fig. 9) at 3,0-13,0% at spring and 17,2-22,2% at summer-autumn period.

In Bulgaria natural infection of mollusks with protostrongylids was studied in Veliko Tarnovo region. It was found that 3 species were infected. These were Helicella obvia, Monacha cartusiana and Bradybaena fruticum. Season dynamics of the infection intensity and prevalence of protostrongylid larvae in the snails were investigated. The prevalence was highest during summer — between 30% and 35%, comparatively high at spring —24% and lowest at autumn — 8.6%. Similar dynamics have been observed for parasite load but in this case a peak month was August after which it smoothly decreased (Panayotova-Pencheva, 2005).

There are 12 species of land mollusks in Poland which are Protostronhylidae intermediate hosts: Arion subfuscus, Bradydaena fruticum, Cepaea nemoralis, C. vindobonensis, Helicella obvia, Helix pomatia, Helicigona arbustorum, Perforatella bidens, Succinea putris, Zonitoides nitidus, S. oblonga, Trocholus hispidus (Movsesyan et al., 2010).

A scheme of Protostrongylidae life cycle is given at Fig. 10.

Dynamics of infection of sheep and goats from various age groups and ecological zones in Armenia with Protostrongylus are shown as graphs (Fig. 11 a, b) demonstrating the infection appearing in all climate zones but with highest occurrence at mountain meadow-steppes and mountain steppes.

Studies of three sheep age groups (lambs, young, adult) at four natural landscape zones (dry Subtropics, semi-deserts, mountain steppes and mountain meadow-steppes) have shown that the highest rate of infection with Muellerius and Protostrongylus (about 35%) can be seen in adults at mountain steppes and mountain meadow-steppes. At the same zones infection with Cystocaulus reached more than 45%.

Ill Biological group:

The third group of lung helminths, with development cycle using vertebrate intermediate hosts (also dixenous type) includes a causative agent of a dangerous zoonosis Echinococcus granulosus (Batsch, 1786) Rudolphi, 1801 (Fig. 12). Its definitive hosts are many vertebrate species, especially carnivores. A scheme of its life cycle is shown at fig. 13.

A wide distribution of larval echinococcosis in Armenia according to H. Gevorgian (2006) is given in Table 3.

Table 3

Distribution of larval echinococcosis in Armenia. Comparative data on infection level of animals at butcheries

Animals u e Infected Infection level, %

Cattle 1872 913 49±1,16 p<0,001

Sheep and goats 562 125 22±1,75 p<0,001

Pigs 726 107 15±1,32 p<0,001

Total 3160 1145

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So, degree of infection of cattle with this disease reaches almost 50% (Fig. 14 — affected animal organs) with 22% infection rate of sheep and goats and 15% of swine.

Studies of human population in Armenia have shown the infection in all age groups with the highest degree in people of 30-35 age. Echinococcus cysts were found in all organs (fig. 15), but lungs and liver were most commonly infected (42-43%; Fig. 16).

Helminth material was collected from wild and domesticated mammals from Russia South and central regions, Armenia, Bulgaria, Poland. At all 16 animal species were studied, including domestic sheep and goats, and also 13 species of wild mammals from families Cervidae, Bovidae, Leporidae. Numbers of species studied from Russia — 15, from Armenia — 6, from Bulgaria — 7, from Poland — 9.

In these animal species, 23 lung helminth species were found, from families Dictyocaulidae, Protostrongylidae, Taeniidae.

Numbers of lung helminth species per region were as follows: South and central Russia — 18, Armenia — 7, Bulgaria — 14, Poland — 10. The following species were found to be common for all regions studied: Echinococcus granulosus, Dictyocaulus fílaria, D. viviparus, Muellerius capillaris. Based on the analysis of life cycles, the biological classification of lung helminths into three types has been proposed:

1 — Monoxenous, or geohelminths — direct type of development. This biological type includes life cycle of fam. Dictyocaulidae nematodes.

2 — Dixenous, or biohelminths, development of which includes invertebrates as intermediate hosts — mainly land mollusks of 77 species. 50 mollusk species take part in life cycles of these helminths in Russia, 39 — in Armenia, 20 — in Bulgaria, 12 — in Poland. The species most commonly infected with nematode larvae were Helicella derbentina, Napaeopsis hohenackeri, Monacha cartusiana, Bradybaena fruticum. This type includes life cycle of fam. Protostrongylidae nematodes.

3 — Also dixenous, but using vertebrates as intermediate hosts. This includes life cycle of cestode Echinococcus granulosus.

Acknowledgements:

The work was performed in cooperation of Academies of Sciences of Russia, Armenia, Bulgaria, Poland.

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3. Boev S.N., 1975. Principles of nematodology. Vol. 25: Protostrongylidae. Moscow: "Nauka", 268 pp. [in Russian].

4. Boyakhchyan G.A., 2007. Methodics of intravital diagnostics of sheep and goat lung helminthoses. // Russian Parasitological Journal, #2, 122-124. [in Russian, abstract English].

5. Damianov S.G., Likharev I.M., 1975. Gastropoda terrestrial. Fauna of Bulgaria, Vol.4, Sofia, Publishing house BAS, 426 pp. [in Bulgarian]

6. Demiaszkiewicz A.W., Pyziel A.M., Lachowicz J. 2009 a. Abomasum and lung nematodes of red deer in Strzatowo Forest District. Sylwan, 153, 57-61.

7. Demiaszkiewicz A.W., Pyziel A.M., Kuligowska J., Lachowicz J. 2009 b. Dictyocaulosis of European bison in Biatowieza Forest. European Bison Conservation Newsletter, 2, 112-118.

8. Fertikov V.I., Sonin M.D., Rykovsky A.S., Egorov A.N., 1999. Helminths of wild ruminants of National Park Zavidovo and forest zone of Russia [Gelminty dikikh kopytnykh Natzionalnongo Parka Zavidovo I lesnoj zony Rossii], pp. 46-53. [in Russian]

9. Gadaev H.H., 2015. Pulmonary strongylata in wild ruminants in the Chechen Republic. // in: Proceedings: Theory and practice of fighting parasitic diseases, Issue 15, Moscow, pp. 92-94. [in Russian, abstract English]

10. Gevorgyan A.Sh, 2006. Peculiarities of distribution and biology of cystic Echinococcosis pathogen (Echinococcus granulosis Batsch, 1786), Dissertation, Yerevan.

Conclusion.

References:

\

РОССИИСКИИ ПАРАЗИТ СШОГИЧЕСКИИ Ж У

11. Likharev I.M., Rammelmeier E.S., 1952. Land Mollusks of USSR Fauna. Moscow-Leningrad, "AS USSR". 512 pp. [in Russian]

12. Movsesyan D., Boyakhchian G., Arutyunova L., Chubarian F., Petrosyan R., Nikogosyan M., 2009. Protostrongylidosis (Protostrongylidae) and caused by them helminthosis of sheep of Armenia. // Russian Parasitological Journal, #4, 10-29. [in Russian, abstract English].

13. Movsesyan D., Boyakhchian G., Chubarian F., Nikogosyan M., Petrosyan R., Arutyunova L., Gevorgyan H., Panayotova-Pencheva M., Demiaszkiewicz A., Voronin M., 2014. Biological classification of life cycles of lung helminths // Proceedings of the International Conference "Biological Diversity and Conservation Problems of the Fauna of the Caucasus — 2", September 23-26,Yerevan, Armenia, pp. 259-264. [in English]

14. Movsesyan S., 2015. Lung helminths and helminthoses. // BIT's 5th Annual World Congress of Microbes, July 31 — August 2, Shanghai, China, p. 123.

15. Movsesyan S.O. (Ed.), 2004. Diagnosis of Parasitical diseases. // in: Parasite infections diseases of farm animals in Nagorno-Kharabakh Republic, Stepanakert, "Sona", 32-48. [in Russian]

16. Movsesyan S.O., Boyakhchian G.A., Chubarian F.A., Petrosian R.A., Nikogosian M.A., Arutyunova L.D., Panayotova-Pencheva M.S., Bankov J., Demiaszkiewicz A.W., Malczewski A., 2010. The role of snails in formation of biodiversity of pulmonary nematodes (Protostrongylidae) of animals. // Russian Parasitol. J., #3, pp. 43-60. [in Russian, abstract in English].

17. Panayotova-Pencheva M. 2005. Epidemiological studies on helminthoses in goats and sheep caused by Protostrongylidae Leiper, 1926. Veterinarski glasnik — Beograd, 5/6, 619-633. ISSN: 0350-2457.

18. Panayotova-Pencheva M. 2011. Species composition and morphology of protostrongylids (Nematoda: Protostrongylidae) in ruminants from Bulgaria. Parasitology Research, 109 (4), 1015-1020.

19. Panayotova-Pencheva M., 2012. Morphological data on Dictyocaulus eckerti (Nematoda: Trichostrongyloidea) in materials from Bulgaria. Comptes Rendus de l'Academie Bulgare des Science , 65 (9), 1225-1232.

20. Panayotova-Pencheva M.S., Boyakhchian G.A., Baycheva O., Movsesyan S.O., 2012. Protostrongylides (biological cycles, distribution, epizootology of animal protostrongylidoses). // Transactions of Center of Parasitology Vol. XLVII: Morphology, Systematics and Ecology of Parasites, 156-176, Moscow: Nauka. [in Russian, abstract English].

21. Panayotova-Pencheva M.S., Movsesyan S.O., 2012. Experimental models and methods in studies of Protostrongylides life cycles. // in: Modern Problems of General Parasitology, Moscow, 234-258. [in Russian, abstract English]

22. Petrochenko V.I., 1967. Formation of invertebrate and vertebrate hosts of trematodes in phylogenesis [Stanovlenie bespozvonochnykh i pozvonochnykh zhivotnykh khozyaevami trematod v filogeneze] // Russian zoological journal, v. 46, # 3, pp. 317-326. [in Russian].

23. Pyziel A.M., Laskowski Z., Hoglund J. 2015. Development of multiplex PCR for identification of Dictyocaulus lungworms in domestic and wild ruminants. Parasitology Research, 114, 3923-3926.

24. Samoylovskaya N.A., 2010. Ecologicand epizootologic analysis of parasitic diseases of wild ruminants in National Park "Losiny Ostrov" (Moscow Region) [Ecologo-epizootologitcheskij analiz parazitarhykh boleznej dikikh zhvachnykh v natsional'nom parke "Losinyj ostrov"], Dissertation autoreferate, Moscow, 22 pp. [in Russian]

25. Skryabin K.I., Schulz R.S., 1940. Principles of general helminthology. M.: "Selkhozgiz", pp. 191-196.

26. Sysoev A., Schileiko A., 2009. Land snails and slugs of Russia and adjacent countries. Sofia-Moscow, "Pensoft", 312 pp.

Литература

1. Абуладзе К.И., 1964. Принципы Цестодологии, том. 4. Подотряда Taeniata, Москва: "Наука", С. 312-340.

2. Акрамовский Н.Н., 1976. Фауна Армении: моллюски. Ереван, Издательство: Академии наук Армении, 268 с.

3. Боев С.Н., 1975. Принципы нематодологии. Вып. 25: Protostrongylidae. Москва: "Наука", 268 с.

4. Боякчан А.Г. 2007,. Методика прижизненной диагностики гельминтов легких овец и коз. // Российский Паразитологический Журнал, В. 2. С. 122-124.

5. Дамиановский Г.С., Лихарев И. М., 1975. Наземные брюхоногие моллюски. Фауна Болгария, Объ-ем.4, София, Издательство BAS 426 с.

6. Demiaszkiewicz A.W., Pyziel A.M., Lachowicz J. 2009. . Abomasum and lung nematodes of red deer in Strzatowo Forest District. Sylwan, 153, 57-61.

7. Demiaszkiewicz A.W., Pyziel A.M., Kuligowska J., Lachowicz J. 2009. Диктиокаулезы зубров в Беловежской пуще. Бюллетень Европейского Сохранению Зубров, 2, 112-118.

8. Фертиков В.И., Сонин Д.М., Рыковский А.С., Егоров А.Н., 1999. Гельминты диких жвачных в национальном парке Завидово и лесной зоны России, С. 46-53.

jssshai ет тдзуюттзгог

Том 37 Выпуск 3/2016

9. Гадаев Х.Х., 2015. Легочные стронгиляты в диких жвачных животных в Чеченской Республике. // труды: Теория и практика борьбы с паразитарными болезнями, выпуск 15, с. 92-94.

10. Геворгян А.Ш. 2006,. Особенности распределения и биологии возбудителя цистного эхинокок-коза, диссертация, Ереван.

11. Лихарев И.М., Раммельмеер Е.С. 1952,. Наземные моллюски фауны СССР Москва-Ленинград, 512 с.

12. Мовсесян Д., Боякчан Г., Арутюнова Л.Ф., Чубарьян Ф.А., Петросян Р., Никогосян М., 2009. Protostrongylidosis (Protostrongylidae) и вызываемые ими гельминтозы овец Армении // Российский па-разитологический журнал, В4, 10-29.

13. Мовсесян Д., Боякчан Г., Чубарян Ф.А., Никогосян М.А., Петросян Р., Арутюнова Л., Геворкян X., Рапауо^а-Пенчева М. А., Demiaszkiewicz, Воронин М., 2014. Биологическая классификация жизненных циклов гельминтов легких // Материалы международной конференции "биологическое разнообразие и проблемы охраны фауны Кавказа — 2", 23-26 сентября,Ереван, Армения, с. 259-264.

14. Мовсесян С., 2015. Гельминты и гельминтозы легких. 5-й ежегодный // Всемирный Конгресс, 31 июля — 2 августа, Шанхай, Китай, С.123.

15. Мовсесян С.О. (Ред.), 2004. Диагностика паразитарных заболеваний. // в: инфекционные болезни сельскохозяйственных животных в Нагорно-Карабахской Республики, в Степанакерте, «Сона»,

16. Мовсесян С.О., Боякчан А., Чубарян Ф.А., Петросян РА., Никогосян М.А., Арутюнова Л.Д, Panayotova-Пенчева С.М., Банков Ж., Demiaszkiewicz, Мальчевский А., 2010. Роль улиток в формировании биоразнообразия легочных нематод (Protostrongylidae) животных. // Российский паразитологиче-ский журнал, В.З, С. 43-60.

17. Panayotova-Пенчева М. 2005. Эпидемиологические исследования на гельминтозы в козочек и овец, вызванного Protostrongylidae Leiper, 1926. Veterinarski glasnik — Београд, 5/6, 619-633. Номер ISSN: 0350-2457.

18. Panayotova-Пенчева М. 2011. Видовой состав и морфология protostrongylids (Нематоды: Protostrongylidae) жвачных животных из Болгарии. Паразитология Исследования, 109 (4), С.1015-1020.

19. Panayotova-Пенчева М., 2012. Морфологические сведения о Dictyocaulus eckerti (Нематоды: Trichostrongyloidea) материалы из Болгарии. Конт Rendus де L"Academie Болгар. дес науки , 65 (9), 1225-1232.

20. Panayotova-Пенчева С.М., Боякчан А.Г., Baycheva О., Мовсесян С.О., 2012. Protostrongylides (биологических циклов, распределение, эпизоотологии протостронгилидозы животных) // Труды центра Паразитологии Объем. XLVII: Морфология, систематика и экология паразитов, 156-176, Москва: Наука.

21. Panayotova-Пенчева С.М., Мовсесян С. О., 2012. Экспериментальные модели и методы исследований жизненных циклов Protostrongylides. // Современные проблемы общей Паразитологии, Москва, 234-258.

22. Петроченко В.И., 1967. Формирование беспозвоночных и позвоночных хозяев трематод в филогенезе [Становление беспозвоночного я pozvonochnykh животных khozyaevami трематод филогенезе в] // Русский зоологический журнал, том 46, В.З, С. 317-326.

23. A. Pyziel М., Лесковский 3., Хеглунд Ю. 2015. Разработка мультиплексной ПЦР для идентификации Dictyocaulus легочной нематоды у домашних и диких жвачных животных. Паразитология Исследования, 114, 3923-3926.

24. Самойловская H.A. Эколого-эпизоотологический анализ паразитарных болезней диких жвачных в национальном парке «Лосиный остров» (Московская область), автореф.канд.диссертации, Москва, 2010, 22 с.

25. Скрябин К.И., Шульц Р.С., 1940. Основы общей гельминтологии. М: «Сельхозгиз», с. 191-196.

26. Сысоев А., Шилейко А. 2009,. Улитки и слизни России и сопредельных стран. София-Москва, "Pensoft", 312 с.

С.32-48.

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PPÇÇ'flWCK'fl'fl IUIPA3NT0niirilHECKIIII 3K7! 233SSKÎ3 J3333EM1 33? P5MS3T3313333V

Volume 37 Issue 3/2016

List of illustrations:

№i_____ _ _

Fig. 1. Map of regions studied (Russia south, Armenia, Bulgaria, Poland).

Fig. 2. Helminths of different types of life cycles: a — Dictyocaulidae — geohelminths, monoxenous type; b — Protostrogylidae — biohelminths, or dixenous type with invertebrate intermediate hosts; c — Taeniidae (Echinococcus) — dixenous type with vertebrate intermediate hosts.

All-Russian Scientific Research Institute of Fundamental and Applied Parasitology of Animals and Plants named after K.I. Skryabin 117218,Russia, Mo—ow,

Том 37 Выпуск 3/2016

/

Fig. 3. A scheme of life cycle of Dictyocaulidae nematodes — geohelminths, i.e., no intermediate hosts by Eckert, 2001, modified by Movsesyan: 1 — host (moufflon); 2 — Dictyocaulus adult male and female; 3 — egg with larva; 4; 5; 6 — larvae of different stages; 7 — grass.

lambs " young adult

Fig. 4. Distribution of dictyocaulosis (caused by D. filaria) in various age groups of sheep in various

landscape zones of Armenia.

ЩИ

PdOCMNCKHM IUIPA3NT0niirilHECKIIII JK7! HSJSSMM J3333EM1 33? P5MS3T3313333V

Volume 37 Issue 3/2016

1 - head end

2- Protostrongytus

3- MueUertus

4- Neostrongytus

5- Skriabtnocaulos

6- Elaphostrongytus

V

1- Proto%trongylui U- Mutldrim 3 ■ Hfcttrongylus 4- Elaphoftmngylui

Fig. 5. Diagnostic criteria of morphology of various Protostrongylidae: a — head end and bursae; b — spiculae.

Subfamilies

Protostrongyllnae Kamensky, 1905

Spiculocaulus Schulz, Orlov et Kutass, 1933

Protostrongylus Kamensky, 1905

Muellerinae Skrjabin, 1933

Varestrongylinae Boev, 1968

Muelleriu s Camera n.1927

Cystocaulus Schulz, Orlov et Kutass, 1933

Neostrongylinae Boev et Schultz. 1950

Genera

Varestrongylus Bhalerao, 1933

Pneumocaulus Schulz et Andreeva. 1948

Skrjablnocaullnae Boev et Sullmov, 1963

Neostrongylus Gebauer, 1932

Ypm

L_

Pneumostrongylus Mönnig, 1932

Elaphostrangylina e Boev et Schultz, 1950

Skrjabmocaulus Boev et Sulimov, 1963

Etaphostrongylu s Cameron, 1931

Orlhoslrongylus Dougherty et Goble, 1946

Parelaphostrongylus Boev et Shultz,

Fig. 6. Systematics of nematodes from fam. Protostrongylidae.

to, H.A. © ......... H.A.

All-Russian Scientific Research Institute of Fundamental and Applied Parasitology of Animals and Plants named after K.I. Skryabin 117218, Russia, Moscow, Bolshaya Cheremushkinskaya str., 28

Fig. 7. Structures of some widely distributed lung helminths

ОВСКаЯнА © Муравьева Л.А.Ц © Samoylovskay N. © IWva L.

Всероссийский научно-исследовательский институт фундаментальной и прикладной паразитологии животных и растений имени К.И. Скрябина

117218, Россия, г Москва, ул. Б. Черемушкинская, 28, e-mail: [email protected] ос-о © «Российский паразитологический журнал»

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d

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Fig. 7. Structures of some widely distributed lung helminths

All-Russian Scientific Research Institute of Fundamental and Applied Parasitology of Animals and Plants named after K.I. Skryabin 117218, Russia, Moscow, Bolshaya Cheremushkinskaya str., 28

h

Fig. 7. Structures of some widely distributed lung helminths

© Samoylovskaya N. © Mu^va L.

Всероссийский научно-исследовательский институт фундаментальной и прикладной паразитологии животных и растений имени К.И. Скрябина

117218, Россия, г Москва, ул. Б. Черемушкинская, 28, e-mail: [email protected] ^gQ © «Российский паразитологический журнал»

i

Fig. 7. Structures of some widely distributed lung helminths (original pictures by Panayotova-Pencheva):

a — Muellerius capillaris, b — Cystocaulus ocreatus, c — Protostrongylus rufescens, d — Protostrongylus rupicaprae, e — Protostrongylus tauricus, f — Protostrongylus hobmaieri, g — Protostrongylus brevispiculum, h — Muellerius tenuispiculatus, i — Dictyocaulus eckerti, j — Neostrongylus linearis, k — Varestrongylus sagittatus.

tan HA © .....i:..H.Â.

Fig. 8. Land snails of Armenia most commonly infected with Protostrongylidae.

1 — Pupilla muscorum;

2 — Chondrula tridens\

3 — Napaeopsis hohenackeri\ 4 — Succinea putris\ 5 — Helicella derbentina;

6 — Hesseola solidior, 7 — Vitrinoides monticola; 8 — Deroceras caucasicum\ 9 — Helix lucorum.

Всероссийский научно-исследовательский институт фундаментальной и прикладной паразитологии животных и растений имени К.И. Скрябина 117218, Россия, г Москва, ул. Б. Черемушкинская, 28, e-mail: [email protected]

e

Fig. 9. Protostrongylidae larvae from mollusks of Armenia.

a. Protosrongylidae spp. from Helicella derbentina

b. Protosrongylidae sp. from Vitrinoides monticola c. Protosrongylidae spp. in Napaeopsis hohenackeri

d. Cystocaulus nigrescens from Napaeopsis hohenackeri e. Protostrongylus sp. from Helicella derbentina

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Fig. 10. Life cycle of Protostrongylidae (dixenous) by Eckert, 2001, modified by Movsesyan. 1 — definitive host; 2 — 1st stage larva; 3 — 2nd and 3rd stages larvae; 4; 5 — intermediate host (mollusk).

Всероссийский научно-исследовательский институт фундаментальной и прикладной паразитологии животных и растений имени К.И. Скрябина 117218, Россия, г Москва, ул. Б. Черемушкинская, 28, e-mail: [email protected]

Prevalence of sheep protostrongylosys, %

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Fig. 12. Adult Echinococcus granulosus.

Carnivora hoste become infected of rar eoring viscero containing hydatid cysts

Adult Echinococcus granulosus tapeworm (4-$mm) in tmail intestine of carnivore

DEFINITIVE (carnivore) HOSTS

Section through hydatid cyit with brood capsules containing orotoscoricsi

INTERMEDIATE (usually harbivore) HOSTS ^..........'

Eggs (30-40^.) or« passed in feces of infected carnivore and ingested by herbivore host i

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Eggs hotch in intestine, penetrats through intestinal wall into circulatory system and are carried to liver and lungs where , they develop into hydatid cysts

Humans moy ingest ova accidentally

Fig. 13. Life cycle of Echinococcus granulosus by Eckert, 2001.

All-Russian Scientific Research Institute of Fundamental and Applied Parasitology of Animals and Plants named after K.I. Skryabin 117218, Russia, Moscow, Bolshaya Cheremushkinskaya str., 28

Fig. 14. Liver and lung affected by E. granulosus infection — Gevorgyan, 2011, Armenia.

Fig. 15. Characteristics of human infection with E. granulosus distribution between age categories

(Gevorgyan, 2011).

Всероссийский научно-исследовательский институт фундаментальной и прикладной паразитологии животных и растений имени К.И. Скрябина

117218, Россия, г Москва, ул. Б. Черемушкинская, 28, e-mail: [email protected]

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Fig. 16. Distribution of E. granulosus cycts between organs in humans in Armenia.

© 2016 The Author(s). Published by All-Russian Scientific Research Institute of Fundamental and Applied Parasitology of Animals and Plants named after K.I. Skryabin. This is an open access article under the Agreement of 02.07.2014 (Russian Science Citation Index (RSCI)http://elibrary.ru/projects/citation/cit_index. asp) and the Agreement of 12.06.2014 (CA-BI.org/Human Sciences section: http://www.cabi.org/Uploads/ CABI/publishing/fulltext-products/cabi-fulltext-material-from-journals-by-subject-area.pdf)

All-Russian Scientific Research Institute of Fundamental and Applied Parasitology of Animals and Plants named after K.I. Skryabin 117218, Russia, Moscow, Bolshaya Cheremushkinskaya str., 28