Endoparasites of Wild Rodents in Southeastern Iran.

BACKGROUND: This study was aimed to collect wild rodents for endoparasites determination in some parts of Sistan and Baluchistan Province, southeastern Iran nearby Pakistan and Afghanistan countries.
METHODS: A total of 100 wild rodents were captured alive with cage traps. Various samples were collected from blood and feces, also impression smear prepared from different organs. The samples were prepared by formalin-ether or stained with Giemsa, after that were examined under microscope.
RESULTS: All the caught rodents (47 Tatera indica, 44 Meriones hurriana, 5 Gerbilus nanus and 4 Meriones libycus) were studied for endoparasites emphasizing to their zoonotic aspects. Endoparasites including Spirurida, Hymenolepis diminuta, Hymenolepis nana feraterna, Trichuris trichiura, Skerjabino taenia, Trichostrongylus spp, Entamoeba muris, Chilomastix mesnili and Leishmania spp were parasitologically identified.
CONCLUSION: Among 9 genera or species of the identified parasites at least 5 of them have zoonotic and public health importance.

Introduction

Many infectious diseases classified as zoonotic infections can be caused by parasitic, viral and bacterial agents transmitted to human by different types of animals such as rodents (Etemad 1978, Weiss et al. 2008). Ectoparasites such as fleas, lice and ticks can also transmit some infectious agents from rodents to human (Daniels and Hutchings 2001). Meerburg et al. (2009) showed a large spectrum of rodent borne pathogens. Helminth parasites are a large group of metazoan organisms that infect vast numbers of human and livestock (Anthony 2007). Similarly, some protozoan zoonoses such as Toxoplasma and Leishmania can also affect human and become malignant for those who are positive HIV (Alvar et al. 2008, Naqi et al. 2010).

Metazoan and protozoan zoonoses are responsible for a large number of morbidity and mortality of human around the world (Chai et al. 2005) and induce significant public health and socioeconomic problems.

This study was conducted to collect some informative data about the rodents and relevant parasites in some parts of Sistan and Baluchistan Province in Iran with emphasis on finding worms and protozoan parasites which have medical importance to human.

Materials and Methods

Study areas

The study was performed at the Iranshahr and Nikshahr districts in Sistan and Baluchistan Province, southeastern Iran (Fig. 1). The weather in the districts is hot and dry in summer with usual maximum temperature of 45 ºC but temperate and low humid in winter with usual minimum temperature of 15 ºC. Six sites in each district nearby the inhabitant locations along the rodent's routes were randomly selected for trapping.

Fig. 1

Sistan and Baluchistan Province located at southeastern Iran

: location of the study areas in the province

Rodent collection

A total of 100 rodents were captured alive with cage traps. The traps were collected and transfered to Iranshahr Health Research Station. Tail punctured and thin blood smears were made from all of the rodents and then the animals were anesthetized under chloroform inhalation for careful dissection and preparing impression smears of spleen, liver and lungs. One smear also was made from any papilla on the surface of ears. The smears were stained with Giemsa stain diluted in natural distilled water up to 3% for 30 min. Spots that prepared from dissected brains were also stained as the same method and precisely observed by light microscope with magnification of 1000.

Some amounts of the gastrointestinal tract content were collected for gastrointestinal parasites examination. Ether-chloroform method was applied to identify parasites. Both protozoan and helminthes parasites isolated as well as the rodents were distinguished by skilled persons using a number of valid references (Khalil and Jones 1994, David et al. 2004, Jones et al. 2004, Rodney et al. 2008).

Results

Four species of rodents including Tatera indica (47%), Meriones hurrianae (44%), Gerbilus nanus (5%) and M. libycus (4%) were identified. Classification of the animals was performed according to family (Cricetidae), subfamily (Gerbillinae), genus (Tatera, Meriones, Gerbilus) and species. The maximum and minimum quantities belong to T. indica 47(47%) and M. libycus 4(4%) respectively (Table 1).

Table 1

Distribution of wild rodents caught from Iranshahr and Nikshahr districts in southeastern Iran

Genus/species	Iranshahr	Nikshahr	Total N(%)
Tatera indica	38	9	47 (47)
Meriones hurrianae	0	44	44 (44)
Gerbilus nanus	5	0	5 (5)
Meriones libycus	4	0	4 (4)
Total	47	53	100 (100)

The microscopic examination of gastrointestinal tract contents revealed the presence of Spirurida spp. and Trichostrongylus eggs in seven and two T. indica respectively. The rest helminthes isolated including Hymenolepis diminuta, H.nana feraterna, Trichuris trichiura, Skerjabino taenia and Rictularia were found in adult stages. Moreover protozoan parasites, Entamoeba muris and Chilomastix mesnili were isolated from the feces. In one case of liver tissue Leishmania spp., was identified (Table 2).

Table 2

Frequency of protozoan and helminthes parasites identify captured in 100 wild Nikshahr and Iranshahr districts

Rodents	Parasites		Wild Rodents		Total
	Meriones libycus	Meriones hurrianae	Tatera indica	Gerbilus nanus	N (%)
Hymenolepis diminuta	0	0	11	0	11 (23.4)
Hymenolepis nana feraterna	0	0	8	0	8 (17.0)
Spirurida spp.	0	0	7	0	7 (14.9)
Trichuris trichiura	0	0	6	0	6 (12.7)
Skerjabino taenia spp.	0	0	4	0	4 (8.5)
Trichostrongylus	0	0	2	0	2 (4.2)
Rictularia spp.	0	0	1	0	1 (2.1)
Entamoeba muris	0	2 (%4.2)	2	0	4 (8.5)
Chilomastix mesnili	0	3 (%6.3)	0	0	3 (6.3)
Leishmania spp.	0	0	1	0	1 (2.1)
Total	0	5 (%10.6)	42	0	47 (10)

Discussion

This study was conducted to consider the endoparasites of wild rodents in some parts of southeastern Iran where located nearby western borderline of Pakistan and Afghanistan countries.

Control of zoonotic parasites depends on reliable knowledge of their life-cycles, reservoirs, distribution and transmission patterns in each zoogeographical situation. Many rodents particularly commensal species enable to take place in transmission cycle of parasitic infections as an important reservoir (Ghadirian and Arfaa 1972, Sadighian et al. 1973, Mohebali et al. 1998, 2004, Kia et al. 2001, Mowlavi et al. 2004). Reports released by some authors about rodent borne parasitic infections from some parts of Iran made more obvious the role of rodents as reservoir of many protozoan and helminth parasites (Edrissian et al. 1975, 1976, Yaghoobi-Ershadi 1996, Mohebali 1997, Javadian et al. 1998, Sadjjadi and Massoud 1999 Kia et al. 2001, 2010).

During this study four species of rodents, M. libycus, M. hurrianae, T. indica and G. nanus were identified that the most prevalent species was T. indica with 47% (n= 47). In a zoonotic helminth study conducted in Khuzestan, a Province in southwestern Iran, T. indica was found as the most dominant species (Sadjjadi and Massoud 1999). While in another study performed by Kia et al. (2001) Rattus norvegicus was the most prevalent rodent in Ahvaz, centre of Khuzestan Province. In the present study the samples were collected from rural areas so our results are comparable with those studies that emphasis gerbils are dominant species in the rural areas, while in the urban areas rattus can be usually found more than gerbils. In Kamranrashani et al. study in Maraveh Tappeh, Golestan Province located in northeast of Iran a heavy burden of infectivity with helminth parasites (81.8%) was found in R. opimus (Kamranrashani et al. 2012).

In our study M. hurrianae (n= 44, 44%), G. nanus (n= 5, 5%) and M. libycus (n= 4, 4%) stayed at the second to fourth ranks respectively after T. indica. Tatera indica bore the maximum parasitic infectivity and none of the parasites was isolated from M. libycus and G. nanus (Table 2). In a previous study performed in the leishmaniasis endemic areas of Iran T. indica was accounted the main Leishmania major reservoir in Mehran district of Iran where located nearby eastern borderline of Iraq (Mohebali et al. 2004). Some promastigotes of Leishmania spp. were isolated from Phlebotomous papatasi and Ph. salehi sand flies those were collected from T. indica and M. Hurrianae burrows in Chabahar district located at the south of Iranshahr district (Kasiri and Javadian 2000). In our study Leishmania spp. was isolated from T. indica which is consistent their results.

In addition, examination of gastrointestinal content of this rodent showed infection with Entamoeba muris. Although E. muris is assumed to be a common protozoan parasite of the most rodents, results of this study recorded the parasite only for T. indica and M. hurrianae with equal burden of infection. Chilomastix mesnili as the third protozoan parasitic infection in this study was found among three M. hurrianae. Although C. mesnili has been isolated from a few infected individuals, it is a common parasite among rodents and usually none pathogen for human. A scientific report indicated that 0.6% of adolescent girls from two boarding schools, in southern Benin were carrier of C. mesnili at the time of study (Alaofe et al. 2008). All the identified helminth parasites were isolated only from T. indica in this study. These results pointed to the more activity and prevalence of T. indica and also capability of the rodent for assuming a wide variety of parasitic infections in comparison with the other captured rodents in the studied areas.

Among the parasites isolated from rodents in this study, Hymenolepis diminuta, the rat tapeworm, was the most prevalent helminth species. In Kia et al. study (2010) H. diminuta was the most common parasite that could be found in different species of rodents. Some helminthes such as Trichuris trichiura, H. feraterna, Skerjabino taenia, Trichostrongylus spp., Spirurida and Rictularia spp. are infective to human and deleterious for public health (Keney et al. 1975, Mowlavi et al. 2006, 2008, Ok 2009). Infectivity of H. diminuta for human had been distinguished from long time ago in Iran (Ghadirian and Arfaa 1972). Among eight T. indica that were infected with order of Spirurida one of them was identified as adult Rictularia spp. infection but the others remained at the level of order because the infectivities were distinguished only with presence of the eggs. Some studies performed in Khuzestan Province indicated presence of Rictularia spp. and Gongylonema spp. that were isolated from a number of wild rodents and carnivores (Farahnak 1998, Sadjjadi and Massoud 1999, Kia et al. 2001). Spirurida includes a great number of genera and species which all have invertebrate intermediate hosts. Both Rictularia and Gongylonema have been isolated from human (Urch et al. 2005, Keney et al. 1975).

To our knowledge among nine genera or species of the identified parasites at least five of them have zoonotic and public health importance.

Conclusion

Harboring a wide variety of zoonotic parasites by T. indica particularly when the rodent lives nearby the native population residences represents a potential risk to the health of the population. Although the infection of M. hurrianae was not comparable with T. indica, nevertheless the rodent can be accounted at the second potential risk to the health of human at the studied areas.