Helminth Parasites of Eastern European Hedgehog (Erinaceus concolor) in Northern Iran.

BACKGROUND: Recently there is a high tendency among exotic pet owners for keeping hedgehogs. This mammal can transfer some significant zoonotic pathogens to human. Hence, the present study was conducted for the first time to prepare a list of helminth parasites of hedgehogs (Erinaceus concolor) in North of Iran.
METHODS: Ten (four males and six females) road killed hedgehogs were collected during April to January 2011 in rural areas of Babol city, Mazandaran province, Iran. All of internal organs were scrutinized for helminth burden. The extracted specimens were fixed and preserved in 70% ethanol and then cleared in Lacto-phenol solution. Helminth identification was carried out according to available systematic keys.
RESULTS: All the examined hedgehogs (100%) were infected with parasitic helminth as following: two hedgehogs (20%) were infected with Crenosoma striatum, four hedgehogs (40%) harbored Physaloptera clausa, one (10%) host had Hymenolepis erinacei and three (30%) of them were infected with Nephridiacanthus major.
CONCLUSION: This is noteworthy that the current survey is the first report of helminth parasites fauna of Eastern European Hedgehog in Iran. Since, this is the first such investigation in our country, more researches are required to perform on unexplored areas of Iran in order to increase our knowledge regarding hedgehog parasitic diseases.

Introduction

Hedgehogs are minute mammals of Erinaceidae family. These exotic pets are nocturnal and their body is coated with spiny-like niddles. Recently they are receiving a great attention among pet owners (1, 2). These animals have become increasingly popular as an exotic household pet due to being unique, cute, low and easy maintenance pets. It is estimated that there are more than 40,000 in houses of people in the United States (3, 4). Though hedgehogs traditionally categorized in the now abandoned order of Insectivora, these animals not exclusively insectivores but are nearly considered omnivorous. Hedgehogs feed on insects, snails, frogs, snakes, carrion and mushroom grass roots (5).

This animal can interfere in some zoonotic pathogens such as, Capillaria aerophila, Salmonella spp. and Herpes virus. This rodent can be considered as an appropriate host for a wide variety of parasites, bacteria, viruses and fungi both in medical and veterinary fields (6, 7).

Biogeographically E. concolor is considered temperate Eurasian species that is the hedgehog of the well-watered forest, agricultural areas and shrub-land of northwestern and northern Iran through to the Alborz region (8).

To the best of our knowledge, there is no published work on helminthic infection of hedgehogs in Iran though hedgehogs have a cosmopolitan distribution in our country particularly in North of Iran. Thus, the primary objective of the current investigation was to prepare a list of parasitic helminthes of hedge-hogs in North of Iran.

Materials and methods

Sampling

An investigation was performed on ten (four males and six females) dead hedgehogs due to road casualties that were hit by cars from April to January 2011 in rural areas of Babol City (36°32’ 39” N, 52°40’ 44” E) Mazandaran Province, Iran. All of bodies were transferred to Parasitology Laboratory of Islamic Azad University of Babol for precise examination and identification.

Necropsy

Firstly, individual data of dead hedgehog including site of death, date of collection and gender were recorded precisely. Secondly, at the necropsy process of hedgehog corpses, the abdominal and thoracic cavities were incised and the viscera were removed. The following internal organs were dissected and washed carefully: The lungs, trachea, heart and liver were dissected and rinsed after macroscopic examination for the presence of helminth. Afterwards, the digestive tract (stomach, small intestine and large intestine) were separated and opened up along its entire and frequently rinsed in order to gather the whole contents. The contents of each organ separately were screened by aid of Mesh 70 and in the next step the remnants was sieved and transferred to Petri dishes for more investigation. For the purpose of collecting tiny helminthes which probably are attaching to mucosal layer of the stomach and intestinal tract a stereomicroscope was used (9). All of the isolated specimens from each part of the body were counted, removed, fixed and preserved in 70% ethanol. In the next stage, they were cleared in Lacto phenol and studied in temporary mou-nts by means of light microscope. The parasites identifications were performed according to available systematic keys including (10-12)

Results

All examined hedgehogs had 100% helminthic infection. From ten examined hedgehogs the following helminthes were obtained: two nematodes, one cestode and one acanthocephalan including Crenosoma striatum (Crenosomatidae, Fig. 1) (10), Physaloptera clausa (Physalopteridae, Fig. 2) (10), Hymenolepis erinacei (Hymenolepididae, Fig. 3) (11) and Nephridiacanthus major (Oligacanthorhynchidae) (12), respectively.

Fig 1

Head and tail of C. striatum obtained from Hedgehog lung (Photograph by Mohammad Reza Youssefi)

Fig 2

Head and tail of Physaloptera clausa obtained from Hedgehog stomach (Photograph by M.R. Youssefi)

Fig 3

Scolex of Hymenolepis erinacei obtained from Hedgehog small intestine (Photograph by M.R. Youssefi)

From ten hedgehogs, two (20%) of them were infected with C. striatum, four hedgehogs (40%) harbored Physaloptera clausa, one (10%) had Hymenolepis erinacei and three (30%) of them were infected with Nephridiacanthus major. The localization, prevalence, intensity, abundance, range and median of helminth species in hedgehogs were analyzed and presented in Table 1.

Table 1

Localization and infection rate of extracted helminth from hedgehogs (N: 10)

Parasites	Localisation	Infection %	Hedgehogs♀	Hedgehogs ♂
C. striatum	Lungs	2(20)	1	1
P. clausa	Stomach	4(40)	2	2
N. major	Small intestine	3(30)	2	1
H. erinacei	Small intestine	1(10)	1	0
Total		10(100)	6	4

Discussion

In the current survey the following helminthes were collected: C. striatum from Lung, P. clausa in Stomach and N. major and H. erinacei from Small intestine. The general prevalence of present study noticeably was high (100%) which corresponds to other investigations results (13, 14).

This is the first published wide study on hedgehog helminthes in Iran. However, there are two separate studies on two of hedgehogs helminthes in Iran before this study, brief report of C. striatum in Urmia (north eastern Iran), although the prevalence (in 10 checked hedgehogs) and the genus and species of hedgehogs are not mentioned (15).

And in the second study, Nephridiacanthus major was found in one (of two checked, intensity 2) Erinaceus concolor from Mazandaran province and one Hemiechinus auritus from Golestan province (intensity 35), acanthocephalan samples were studied morphologically with Light Microscope and Scanning Electron Microscope (for the first time), also histopathology study was done that showed extensive damage of this acanthocephalan to the infected hosts (16). This is worthwhile to clarify that some surveys have proven the major role of hedgehogs as a reservoir and carrier host in urban, peri-urban and rural environments (17). Poglayen et al. observed Dicrocoelium dendriticum and Haemonchus contortus in E. europaeus. In addition classical ruminant helminthes were reported also from Atelerix albiventris (West African Hedgehog) (18, 19). Cirak studied on 18 E. concolor (10 females, 8 males) and introduced the following helminth and parasitic burden: P. clausa (72.2%), C. striatum (55.5%), A. erinacei (55.5%), H. erinacei (55.5%), N. major (50%) and E. aerophilus (22.2%) (9). Based on Gaglio investigation on European hedgehogs (E. europaeus) by dissection, 91% of studied animals had parasitic helminth infection. Besides, six helminth species were collected including five nematodes (C. striatum, E. aerophilus, Capillaria erinacei, C. ovoreticulata and Capillaria spp.), one trematode (Brachylaemus erinacei) and merely one acanthocephalan (Oliganthorhynchus erinacei) (13).

In an elaborate survey on two hedgehogs comprising Atelerix algirus and Paraechinus aethiopicus in Algeria these helminth species were recognized: One cestodes, Mathevotaenia erinacei, eight species of nematodes: Aonchotheca erinacei in the lumen, spirurids in the intestine, C. striatum in the lungs, Gongylonema mucronatum (in oesophagus, P. clausa in the stomach, Physaloptera sp. larvae in the mesentery, Pterygodermatites plagiostoma in the stomach, Spirura rytipleurites seurati in the intestine; and one acanthocephalan,Moniliformis moniliformis in the lumen. The most prevalent species both in A. algirus and P. aethiopicus was P. clausa 64.0% and 64.7%, respectively (14).

As a matter of fact, hedgehogs are primarily insectivores. However, they have a flexible diet, feed on a variety of vertebrate, invertebrate animals as well as carrion and plant matter when accessible. Therefore, they have an immense potential ability about transferring causative agents of diseases owing to having a wide variety of food choices. Nowadays pets have a significant role in societies throughout the world. They are considered as an important companion in many households, contributing in activities such as physical, emotional and social development of children and the well-being of their owners, particularly in the elderly individuals. Despite of this fact that pets offer noticeable benefits, potential treats are associated with pet ownership should not be neglected. Exotic animals are remarkably being invited into homes as pets. Nonetheless, neither pet owners nor veterinary healthcare providers are enough knowledgeable concerning the potential of many of these animals to transfer zoonotic diseases (20).

The following zoonotic helminth parasites were recorded from hedgehog: Capillaria hepatica from Switzerland (21), Moniliformis moniliformis and Mathevotaenia from Algeria (22).

Conclusion

Considering aforementioned facts, it is crystal clear that two major groups including pet owners and veterinary surgeons are more at the risk of zoonose diseases owing to close contact with exotic animals. Control and prevention of zoonotic diseases is associated with breaking the cycle of transmission, and there is no shadow of doubt that education is the major key to control (20). Thus, further precise helminthological investigations are required due to noticeable unexplored area of our country in order to ascend our knowledge concerning helminthic parasites of hedgehogs and probable zoonoses and veterinary diseases.