Phylogenetic analysis of nasal avian schistosomes (Trichobilharzia) from aquatic birds in Mazandaran Province, northern Iran

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Highlights

  • Report of the first molecular phylogenetic data for a nasal Trichobilharzia in Iran

  • Our isolates were homologous with unique haplotypes of putative T. regenti in France, Poland and Czech Republic.

  • Anas clypeata seems to be the main final host of this nasal schistosome in Northern Iran.

  • This may be one of the major species causing cercarial dermatitis, particularly in rice fields.

Abstract

Nasal schistosomes are trematodes in the family Schistosomatidae, many members of which are causative agents of human cercarial dermatitis (HCD). Little is known about the species diversity and distribution of nasal dwelling schistosomes of water birds, particularly in countries outside of Europe; even less is known in countries like Iran. Nasal schistosomes are of particular interest since these species migrate via the central nervous system to the nasal cavity once they penetrate their host. Thus, there must be efforts to determine the incidence of HCD due to nasal schistosomes. HCD outbreaks are reported seasonally in Mazandaran Province, northern Iran, an area well known for rice cultivation leading to increased person contact with water and infected snails. Such places include favorable habitat for both domestic ducks year round, and wild migratory ducks in the winter through spring. Recent reports have detected the presence of both nasal and visceral schistosomes in ducks in this area but with little species characterization. In this study, we examine a diversity of aquatic birds to determine the distribution, prevalence and bird host use of nasal schistosomes. We apply for the first time a molecular identification and phylogenetic analysis of these schistosomes. From 2012 to 2014, the nasal cavity of 508 aquatic birds from Mazandaran Province were examined that included species in Anseriformes, Gruiformes, Charadriiformes and Phoenicopteriformes. Nasal schistosomes were found in 45 (8.9%) birds belonging to Anseriformes (Anas platyrhynchos and Anas clypeata). Phylogenetic analysis of the nuclear internal transcribed spacer 1 rDNA and the mitochondrial cytochrome oxidase1 gene of isolated eggs revealed that all samples grouped in a sister clade to the European Trichobilharzia regenti. However, Trichobilharzia from this study were more similar to a unique haplotype of Trichobilharzia, isolated from the nasals of an A. clypeata in France. The genetic and phenotypic differences between the species found herein and T. regenti from Europe, may prove with additional data to be a distinct species of Trichobilharzia.

Introduction

Schistosomes (Schistosomatidae) are blood trematodes that infect aquatic snails as intermediate hosts and birds and mammals as definitive hosts. Mammalian species are well known for causing the most devastating helminth disease in people, schistosomiasis (WHO 2013). Most of the species diversity within Schistosomatidae is found in avian definitive hosts and much of that diversity is found the venous system (liver, mesenteric veins), and less commonly in the nasal tissue and arterial system habitat of their hosts [1]. Though avian schistosomes are distributed globally, species inhabiting in the nasal cavity have been found only in the Eastern Hemisphere.

Within the avian schistosomes, there are 8 described species known to occur in the nasal tissue, 5 from Africa, 2 from Australia, and one from Eurasia. Trichobilharzia regenti [2], [3] is the only nasal species for which there are well described morphological, genetic, pathological, and life cycle features. The life cycle of the nasal schistosomes in Australia have been detailed [4], [5], and the species in Africa have been reported once to a few times [6], [7]. However, in the absence of substantiating genetic data, it is difficult to know the species and phylogenetic relationships among them. This question of relationships is of interest since these regions are connected by the migratory flyways of the avian hosts. Other than Western Europe, limited investigations have included avian schistosomes in Eurasia, most of it conducted in China and Russia [8], [9], [10], [11], [12].

Both mammalian and avian schistosomes are the causative agents of human cercarial dermatitis (HCD), but avian schistosomes species are most often implicated [13]. HCD is an allergic skin reaction at the penetration site of the larvae or schistosome cercariae [13] in both freshwater and marine environments. These cercariae do not mature and usually die in the skin. Studies on the pathology of an avian nasal schistosome, T. regenti, have shown that the larvae migrate via the central nervous system to reach the nasal tissue [14]. In a mammalian host, mice infected experimentally with T. regenti have shown that the worms attack the central nervous system and create neuromotor disorders such as leg paralysis [14], [15]. The potential for similar neurological symptoms occurring in humans, particularly the young and immunocompromised, cannot be ignored. Thus, there is a need to know if there are nasal schistosomes responsible for outbreaks of HCD, particularly in areas where people spend a majority of their time in water in contact with these parasites. Thus our broader goal is to describe the species and life cycles of schistosomes causing HCD in northern Iran, and this paper will focus on defining a species found in nasal cavities of birds [16].

Until recently, almost nothing was known about avian schistosomes and HCD in the Middle East, much of which includes areas at high risk of HCD. Only recent investigations in Iran have contributed much of what we know today [17], [18], [19], [20]. In a study in northern Iran, Mazandaran Province, where HCD has been well established [21], infections with a nasal species of Trichobilharzia in the duck Anas clypeata was confirmed by molecular methods [19]. That work motivated this study to include a more rigorous survey of nasal schistosome occurrence. Northern Iran remains a place of interest for HCD, as it is a major stopover for migratory birds and has a high incidence of HCD, particularly in rice fields [22]. Investigations continue to establish the prevalence and species of mammalian (domestic animals used for aquiculture) versus avian (large populations of migratory birds) schistosomes, since both hosts are present and cause HCD [22]. In the present study, efforts were made to determine the prevalence and distribution of nasal avian schistosomiasis in Mazandaran Province in species of wild migratory aquatic birds.

Section snippets

Study area and sampling

The study was conducted in two main wintering areas for migratory birds in Mazandaran province (Sari and Fereydun kenar; 36.6544 N; 52.4928 E) in northern Iran to determine the distribution of nasal schistosomes in bird hosts. From December 2012 to February 2014, a total of 508 heads of aquatic birds were collected. The birds belonged to 10 species from four orders (see Table 1): Anseriformes—Anas platyrhynchos (mallard), A. clypeata (northern shoveler), Anas crecca (common teal), Anas acuta

Results

The number of birds examined and the prevalence of infection by nasal schistosomes for each species are presented in Table 1. Nasal schistosomes (eggs and/or adult fragments) were found in 45 out of 508 (8.9%) heads of aquatic birds, which represented only two anseriform species (A. clypeata, A. platyrhynchos) out of the 10 aquatic birds examined. Worms were found in 29/89 (32.6%) A. clypeata and 16/186 (8.6%) A. platyrhynchos (Table 1). Interestingly, among these two bird species, the

Discussion

The data presented herein are part of the larger goal to understand the epidemiology of HCD as an endemic parasitic disease in northern Iran [19]. The initial steps to realizing this goal are to systematically survey and identify the hosts and their schistosomes to make the critical life cycle connections. In addition to very little survey data, few molecular studies had been undertaken to identify the species of schistosomes and hosts, particularly in the Middle East regions. The northern

Conclusions

The results herein delineated and confirmed a clade of samples closely related to the nasal schistosome T. regenti that suggest they are a distinct species. Because the samples found in our study form a sister clade to T. regenti, it is hypothesized that Trichobilharzia cf. regenti has a focal point in this geographic area, including northern Iran. Until this study, there were no sequences of Trichobilharzia cf. regenti except those from France and Poland, even after a decade or more of

Acknowledgments

The authors would like to thank Mr. AbdolSattar Pagheh from the Mazandaran University of Medical Sciences, Sari, Iran, for his kind help; as well as the Deputy of Research and Technology of Mazandaran University of Medical Sciences for generous support of this study. This study has been supported by the Mazandaran University of Medical Sciences (project No. 143-92).

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