Genetic Diversity of an Avian Nasal Schistosome Causing Cercarial Dermatitis in the Black Sea-Mediterranean Migratory Route
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Parasitology Research https://doi.org/10.1007/s00436-018-6087-0 ORIGINAL PAPER Genetic diversity of an avian nasal schistosome causing cercarial dermatitis in the Black Sea-Mediterranean migratory route Keyhan Ashrafi1,2 & Alireza Nouroosta3 & Meysam Sharifdini1 & Mohammad Reza Mahmoudi1 & Behnaz Rahmati1 & Sara V. Brant4 Received: 30 July 2018 /Accepted: 11 September 2018 # Springer-Verlag GmbH Germany, part of Springer Nature 2018 Abstract This study is part of an effort to document the diversity of avian schistosomes in ducks and snails in Northern Iran, a major flyway (Black Sea/Mediterranean) for migratory birds and where cercarial dermatitis (CD) is prevalent in rice growing areas. CD is an allergic skin reaction from schistosome trematodes that emerge from aquatic snails. Most CD cases are reported from recreational swimmers or aquaculture farmers. Much of the work on the epidemiology of CD has focused in recreational waters in the Americas and Europe, with fewer studies in aquaculture, particularly in Iran. The artificial environment at aquaculture sites support dense populations of snails that are hosts to schistosomes, as well as domestic ducks. Thus, are domestic ducks reservoir hosts of species of Trichobilharzia, one of the main etiological agents of CD in Northern Iran? This study focused on a survey of domestic ducks for the presence of the nasal schistosome, T. regenti, that has been reported widely in Europe. Trichobilharzia regenti were found in domestic ducks in the Guilan Province of Iran based on morphological and molecular analyses. The presence of this species in Northern Iran indicates that the domestic duck can serve as a reservoir host for this species and that one of the local snail species is likely the intermediate host. The continued study and surveillance of this species is important because it is a neuropathic schistosome that can use a diversity of bird definitive hosts and Radix snails that are widespread across Eurasia. Keywords Cercarial dermatitis . Schistosome . Schistosomatidae . Trichobilharzia regenti . Iran Introduction except Antarctica, in mammals or birds as definitive hosts and either freshwater or marine aquatic gastropods as intermediate Cercarial dermatitis (CD) is an allergic skin reaction at the hosts. Most cases of CD are reported from recreational swim- penetration site of larval schistosome trematodes (Digenea: mers, such as at beaches, or aquaculture farmers, such as rice Schistosomatidae) that emerge from aquatic snails in the sum- farms. Much of the work to understand the epidemiology of mer months in temperate latitudes, and likely year-round in CD has been focused in recreational waters in the Americas tropical latitudes. Schistosomes are found on all continents, and Europe (see references in review Horak et al. 2015), but fewer studies in aquaculture sites. Areas of aquaculture are Section Editor: Ramaswamy Kalyanasundaram where people and animals have prolonged contact with the water, particularly countries in Asia that have some of the * Sara V. Brant highest rice production (International Rice Research Institute [email protected] 2009). Rice producing countries in the Middle East have re- cently been taking notice of the prevalence of CD in their 1 Department of Medical Parasitology and Mycology, School of countries (e.g., Farahnak and Essalat 2003;Atharietal. Medicine, Guilan University of Medical Sciences, Rasht, Iran 2006; Al-Khuzaee 2009; Schuster et al. 2014; Omar et al. 2 Cellular and Molecular Research Center, School of Medicine, Guilan 2016). University of Medical Sciences, Rasht, Iran The last decade has seen an increase in reports 3 Student Research Committee, Guilan University of Medical documenting cases and the etiological agents of CD, particu- Sciences, Rasht, Iran larly in Iran (Farahnak and Essalat 2003; Athari et al. 2006; 4 Museum of Southwestern Biology, Division of Parasites, Department Karamian et al. 2011; Gohardehi et al. 2013; Maleki et al. of Biology, University of New Mexico, 1 University of New Mexico 2012; Mahdavi et al. 2013a, b; Imani-Baran et al. 2013; MSC03 2020, Albuquerque, New Mexico 87131, USA Parasitol Res Ghobaditara et al. 2015; Fakhar et al. 2016; Yakhchali et al. Province includes 238,000 acre of rice fields and produce 2016). The artificial environment of, for example, a rice field, about 40% of rice product of the country. After rice harvesting supports populations of snails that are hosts to schistosomes, from early August to late September, the rice paddies, espe- as well as domestic ducks, which also host avian schisto- cially those located near the farmer’s houses, become appro- somes. Thus, an important question in the epidemiology of priate places for livestock grazing, domestic ducks breeding CD, particularly in aquaculture is, are domestic ducks reser- and snail intermediate hosts reproduction. The domestic ducks voir hosts of one or more species of Trichobilharzia,oneof constitute an important part of the diet of indigenous popula- the main etiological agents of CD (Horak et al. 2015)? Wild tion, so they are sold in weekly local markets. Late fall also ducks, geese, and swans are well known hosts of avian schis- coincides with the start of the rainy season in Guilan and when tosomes and because these hosts can migrate long distances, the rice fields receive large amounts of water. These paddies so too can their parasites, or can they? Can they migrate and then become a suitable environment to establish and sustain maintain local life cycles? Discovering the species of schisto- the snail intermediate hosts and ducks feeding, including the some and host use diversity and source populations is a foun- many water collections and small streams around Guilan vil- dational step to initiating a targeted control program (Horak lages, all of which facilitate the schistosome life cycle. See et al. 2015). This study is part of a larger effort to document Table 1 and Fig. 1 for the collection localities and locality the diversity of avian schistosomes in ducks and local snails in descriptions. Northern Iran where CD is prevalent in aquaculture areas. This study focused on a survey of domestic ducks in Guilan Parasite collection Province as reservoir hosts for the presence of the nasal schis- tosome that has been reported widely in Europe (Horak et al. Domestic ducks, Anas platyrhynchos domesticus,werepur- 1998; Picard and Jousson 2001; Dvorak et al. 2002; chased directly from villager’s houses surrounded by rice Rudolfova et al. 2007; Jouet et al. 2008, 2010a, 2010b; fields where the ducks were feeding (Fig. 1). Locality data Skirnisson et al. 2012;Christiansenetal.2016) and in some were determined by GPS (Table 1). The ducks were trans- localities in Northern Iran (Gohardehi et al. 2013;Malekietal. ferred to the parasitology laboratory at the Guilan University 2012; Mahdavi et al. 2013a, b;Fakharetal.2016). The con- of Medical Sciences and decapitated to examine for presence tinued study and surveillance of this species is important be- of nasal schistosomes. The following procedure was used for cause it is a neuropathogenic schistosome that can use a di- all duck heads: (a) two longitudinal incisions through the bird versity of bird definitive hosts and Radix snails that are wide- nostrils along the beak and then a transverse cut to connect the spread across Eurasia (Leontovyc et al. 2016). longitudinal incisions were made, (b) the nasal mucosa was cut open and surrounding vascular tissues were removed, (c) Materials and methods the mucosa and tissue were then transferred into two Petri dishes, one with water and the other with saline to obtain intact eggs and miracidia, and (d) the nasal mucosa were teased apart Study area gently to look for adult worms. Guilan Province has an area of 14,042 km2 (38°28′ 58″ N, 50° 35′ 59″ E) and is situated at the western shores of the Caspian Morphological and genetic analyses Sea. Guilan Province contains 16 districts located at different geographical zones, for example, coastal plain lowlands that For morphological studies, some of the eggs were transferred are below sea level in some regions, foothills, and forested onto a glass slide and coverslip and measured under a micro- mountainous areas. This province has a humid subtropical scope (Olympus BX50) equipped with digital camera climate with the heaviest rainfall in Iran reaching as high as (TrucChrome Metrics, China) and Nomarski Piece (U-DICT, 1900 mm in some regions. Mean rainfall in Guilan Province is Olympus, Japan). The length and width of the eggs were mea- about 1500 mm which is four to six times more than mean sured, and the data analyzed in SPSS Ver. 22 (minimum, max- annual rainfall in Iran. Humidity is very high because of the imum, average, and SD). The remaining eggs, miracidia, and marshy character of the coastal plains and can reach 90% in worm fragments, if any, were transferred to microtubes con- summer with temperature of over 26 °C. The coastal plain taining 96% alcohol for molecular studies. Some of the col- along the Caspian Sea is similar to that of Mazandaran (area lected samples were also kept in labeled microtubes in 90% also reports CD) that is mainly used for rice paddies. These alcohol in the Department of Parasitology and Mycology of areas have altitudes ranging from − 27 m below sea level (b.s. the Guilan University of Medical Sciences as a permanent l) to 300 m above sea level (a.s.l), where 60% of the land- museum voucher. It is critical for the evolutionary character- cover consists of wetlands,