Parasitic zoonoses: Gastrointestinal parasites carried by rodents in the west of Iran in 2017

Introduction

Rodents have a high reproduction rate (Lachhman et al., 2008). They can adapt to different locations and changing environments (Seifollahi et al., 2016). More specifically, they have adapted to human habitats and environmental changes (Chaisiri et al., 2012). The human and animal contacts with rodents occur through feces, urine, hair, and saliva that might be infected (Meerburg, 2010), thereby posing a public health threat (Egbunu and Dada, 2016). Moreover, wild rodents act as definitive and/or intermediate hosts for many endoparasites (Lachhman et al., 2008).

The state of rodents in Iran is no different from that of the rest of the world and has been adequately reported in some cases. Recently, many studies investigated parasites of rodents in different parts of Iran (Pakdel et al., 2013, Yousefi et al., 2014, Arzamani et al., 2017, Rahdar et al., 2017, Ranjbar et al., 2017, Mohebali et al., 2017, Moradpour et al., 2018).

Considering the relatively large size of Iran, its diverse climates, and heterogeneous environmental conditions, a plethora of research is deemed necessary to enhance the public knowledge regarding the parasitic fauna of rodents. The current study aimed to identify the parasites in the alimentary canal of rodents, emphasizing parasitic zoonoses in Lorestan Province in the west of Iran.

Materials and methods

Location

This study took place in Lorestan Province, west of Iran, with geographical coordinates of 46º 50' to 50º 1' E and 32º 40' to 34º 23' N (Figure 1) and tropical, moderate, and cold climates. The average annual precipitation is 420-900 mm. The total area is approximately 28,390 km², of which a substantial amount is predominantly covered by oak forests and, to a lesser extent, elm, maple, walnut, and almond trees.

Rodent samples

In total, 118 rodents were collected from various sites in Lorestan Province in the fall of 2017. The rodents were captured by live traps with roasted almonds as baits and transferred to Lorestan University of Medical Sciences (LUMS) Research Center. Eight species of rodents observed in this study included 59 (50%) Meriones persicus, 23 (19.5%) Mus macedonicus, 17 (14.4%) Meriones tristrami, 10 (8.5%) Microtus qazvinensis, five (4.2%) Arvicola terrestris, two (1.7%) Apodemus sp., one (0.8%) Cricetulus migratorius, and one (0.8%) Meriones libycus.

The rodents were euthanized using chloroform. Morphological characteristics of rodents were recorded. The ethical principles were followed, and the study obtained the approval of the Ethics Committee of LUMS.

Parasite samples

The rodents were cut open and dissected by necropsy. The alimentary canal of each rodent was removed, and a scalpel blade was used to scrape the lining membrane. Staining of rodents’ stool samples was performed with Lugol’s solution and trichrome (Fartest, Isfahan, Iran) to detect protozoan cysts or trophozoites. In addition, the formalin-ether technique was used to examine the stool samples. Afterward, smears were studied microscopically.

In some cases, parts of other organs of the rodent's body were observed during examination in Petri dishes, including the liver. The gastrointestinal contents were examined under a stereomicroscope. The recovered macroscopic worms were maintained in ethanol 70% for future examinations. Subsequently, the worms were transferred to the Iranian National Parasitology Museum, Tehran, Iran, for identification. The helminths were identified using helminthological keys (Satyu, 1961, Simon-Vicente, 1985, Eslami, 1997).

Results

The rate of infection with endoparasites was 50.8%. Besides, 37.3% of the rodents carried one parasite. Simultaneous infection with two parasites and three parasites was 14.4% and 5.1%, respectively. The highest diversity of parasites was found in Meriones persicus (Table 1).

The most common helminths were Hymenolepis nana (13.5%), Trichuris sp. (11%), and Syphacia obvelata (8.5%). Examined Mus macedonicus was infected with Catenotaenia sp. (0.8%). In the mature and gravid portion of Catenotaenia sp., the proglottides are longer than wide and genital pores are in the anterior half of the proglottis margin (Figure 2). Heligmosomum was seen in 0.8% of rodents. The body of Heligmosomum sp. is like a string, delicate, generally spiral, and cuticle with transverse lines (Figure 3). The rate of infection with protozoa was 9.3%. Of 118 fecal samples of rodents, five (4.2%) were infected with Giardia sp. and two (1.7%) with Entamoeba coli. In addition, three rodents carried one of the following: Chilomastix sp. (0.8%), Iodamoeba butschlii (0.8%), and Eimeria sp. (0.8%). Detailed findings are shown in Table 1.

It is important to note that the trematode Notocotylus noyeri is reported in Arvicola terrestris for the first time in Iran. This trematode has 15 distinct ventral papillae in each of the three rows. It has an oral sucker but not a ventral one (Figure 4, 5). All captured Arvicola species were severely infected with Notocotylus (100%). They had diarrhea and dark green, bulky, and foul-smelling stools with severe inflammation of the intestines. In the current study, the captured rodents were infected with helminths four times more than with protozoa.

Discussion

This study is the first of its type reporting gastrointestinal parasites from Meriones persicus, Mus macedonicus, Meriones tristrami, Microtus qazvinensis, Arvicola terrestris, Apodemus sp., Cricetulus migratorius, and Meriones libycus in Lorestan Province, Iran. Overall, 50.8% of the rodents were infected with at least one parasite. In the current study, the most infected rodent was M. persicus, which agrees with a study in Boyer-Ahmad Province (Seifollahi et al., 2016). In the present study, Notocotylus noyeri were found in Arvicola terrestris as the first report in Iran. Another species of Notocotylus (N. neyrai) has already been reported in Arvicola in Zanjan, Iran (Moradpour et al., 2018). Although the two species are different in morphological characteristics (Simon-Vicente et al., 1985), it may render better results if molecular tests are performed on both species found in Iran. The species of Notocotylus were not reported by Fasihi et al. (2016) in Kerman, Iran. It can be attributed to the issue that fresh-water snails are primary, intermediate hosts of trematodes, and the number of snails is not high in desert areas compared to the Lorestan climate (Fasihi Harandi et al., 2016).

Several helminthic and protozoan parasites use rodents as the reservoirs of different zoonotic diseases (Seifollahi et al., 2016). Besides, H. nana and H. diminuta, which are common in rodents, are potentially transmissible to humans. They have been reported in previous studies of rodents in Iran (Gholipoury, et al., 2016, Arzamani. et al., 2017, Rahdar et al., 2017, Moradpour et al., 2018). Also, H. nana is a common infection in Iranian children while individual cases of H. diminuta infection have been reported from Iran and other parts of the world (Abu-Madi et al., 2005, Mowlavi, et al., 2008, Hosseini et al., 2015). In the present study, the most common helminths were H. nana (13.5%). Kia et al. (2001) reported that 12.5% of Rattus norvegicus were infected with H. nana in Ahvaz. Gholami et al. (2002) found that 15% of rodents were infected with H. nana in Sari. About 10.8% of mice were infected with H. nana in Kashan, Iran (Rasti, et al., 2000). Another cestode found in the present study was Catenotaenia sp. Rashidi et al. (2017) reported that 3.6% of trapped rodents in Kurdistan Province were infected with Catenotaenia. The infection rate with S. obvelata in our study was 8.5%. This is in agreement with previous reports (Rahdar et al., 2017, Ranjbar et al., 2017). In a study conducted by Rahdar et al. (2017), 10% of rodents were infected with Physaloptera. Kia et al. (2010) observed that 0.6% of M. persicus were infected with this nematode in Ardabil Province, Iran. In the present study, Physaloptera was seen in 0.8% of rodents. Cockroach serves as an intermediate host for this nematode. Therefore, the life cycle of Physaloptera depends on the distribution of cockroachs (Moradpour et al., 2018). In the present study, one of the nematodes found in Microtus qazvinensis was Heligmosomum sp., with a 0.8% infection rate. This parasite has been reported by Kia et al. (2001) in M. persicus and M. socialis. Recently, this nematode has been reported by Mohammadi et al. (2022) among the rodents in Kurdistan from Iran. We observed Mesocestoides sp. larva (Tetrathyridium) in Meriones persicus (0.8%), similar to other research among rodents in Iran (Kia et al., 2010, Moradpour et al., 2018).

In the current study, the infection rate with Giardia, as a significant intestinal protozoon, was 4.2%. In a study performed in Palestine, Al Hindi and Abu-Haddaf (2013) reported a rate of 14.6% for Giardia infection in rodents. A study conducted in Poland reported an infection rate of 96.3% in Microtus and 48.3% in Apodemus species (Bajer et al., 2002). Studies by Rasti et al. (2000) and Kia et al. (2001) reported 25% and 2.7% infection rates in Kashan and Ahvaz cities of Iran, respectively. The observed difference can be attributed to the effect of climate and the nutritional or habitat preferences of rodents (Seifollahi et al., 2016). In the current study, Entamoeba was observed in the studied rodents (1.7%). The finding agrees with other reports from Iran (Rasti et al., 2000, Kia et al., 2001, Seifollahi et al., 2016, Rahdar et al., 2017).

Conclusions

There is an information gap regarding the transmission of zoonotic parasites to humans, which can be addressed by providing evidence on the rodent parasitic fauna in various zoogeographical regions. Future research should focus on the seasonal prevalence of various parasites and determining the role of paratenic and intermediate hosts in the life cycle of parasites investigated in this study.

The current study revealed that rodents in Lorestan Province are infected with many gastrointestinal parasites. Some of them pose risks for residents and domestic animals. Inappropriate disposal of human waste and fertilizers (human or animal fertilizers) may be the reason for the high prevalence of intestinal protozoan infection in rodents. This study indicates that rodents increase the risk of zoonotic parasite transmission.

As our study proved the infestation of rodents with different zoonotic parasites, particularly Hymenolepis sp., the authors suggest interventions to curb rodent populations. In addition, there should be programs to increase the awareness of the local people about the risks of rodents.

Acknowledgment

This study is part of research work founded by Lorestan University of Medical Sciences, Iran (grant No.A-10-1729-1). We thank the late Prof. Iraj Mobedi for his help.

Ethics approval

The authorization number is LUMS.REC.1395/157 in the Lorestan University of Medical Sciences, Khorramabad, Iran.

Conflict of interest

The authors declare no conflict of interest.