RODENTS AS A POTENTIAL SOURCE OF SOME ZOONOTIC ENTERIC PARASITES IN BENI-SUEF PROVINCE

RODENTS AS A POTENTIAL SOURCE OF SOME ZOONOTIC ENTERIC PARASITES IN BENI-SUEF PROVINCE

GIHAN, K. ABDEL-LATEF^*and LILIAN NAGY MAHROUS^**

^*Departments of Hygiene, Management and Zoonoses

^**Veterinary Parasitology, Faculty of Veterinary Medicine, Beni-Suef University, Beni-Suef 62515, Egypt.

Email: gehankamal2008@outlook.com                                                                 Assiut University web-site: www.aun.edu.eg

INTRODUCTION

Gastrointestinal protozoon parasites are a major health problem with a high prevalence worldwide (Abd El Bagi et al., 2004). The prevalence of parasitic diseases depends on environmental, social and economic factors to such an extent that the presence of intestinal parasites is an indicator of vast collective ill health. In Egypt, clinical and economic impacts of parasitic zoonoses have been reported by several researchers. School-age children are prone to intestinal parasites because of crowding and behavioral patterns that greatly contribute to the spread of parasitic infection. A high prevalence of parasitic infection in children has been recorded, with levels reaching up to 48% (Banta et al., 1964). In addition, parasitic diseases are prevalent among the residents of rural areas. Previous literature of parasitic infections performed on villages revealed high infection rates of single and multiple gastrointestinal parasitic infections (85%) in small villages (Banta     et al., 2009; Fawzi et al., 2004). Parasitic diseases pose serious public health effects on both immunocompromised and immunocompetent patients (Baiomy et al., 2010; Abdel-Hafeez et al., 2012). Moreover, parasites are considered to be the mainetiologic agent of diarrhea, with prevalence 61% among individuals suffering diarrhea (El-Naggar      et al., 2006; Mousa et al., 2010). In a survey conducted in the Delta region, 67.1% of chronic diarrheic patients were found suffering from parasitic infections. In such work, single infection (54.2% of all patients) and mixed infections (12.9% of total chronic diarrhea patients) were present (Baiomy       et al., 2010).

During the last decades, the presence of Giardia sp. and Entamoeba spp. in the environment, especially water, and in mammals, including humans, has been raised (Tavarez et al., 1991; Fayer et al., 2000). Giardiasis is a major diarrheal disease found worldwide. It has been found that animals are considered as reservoirs for Giardia sp., with G. intestinalis could be detected in wild rats (Abdel-Wahed et al., 1999). Many literatures reported that amoebiasis is the most aggressive protozoal disease that affects the human bowel and is considered as a mandatory cause of death among the parasitic diseases (WHO, 1997). Amoebiasis is a global protozoal disease, with approximately 50 million people are infected annually, with the end result of 100,000 deaths (WHO, 1997; Gatti et al., 2002). It is thought to be more common in areas of poor sanitation and nutrition, particularly in the tropics (Gatti et al., 2002). Zoonotic transmission of E. histolytica has been discussed by Jackson et al. (1984). Experimental infection with E. histolytica occurred in dogs, cats, rats, monkeys and other laboratory animals. These animals might be infected with human strains as a result of close contact with humans. Hymenolepis diminuta infection in humans is uncommon (Levi et al., 1987; Hamrick et al., 1990; Varghese, 1998); with few hundred cases have been reported (Tesjaroen et al., 1987; Lo et al., 1989). H. nana is more commonly detected as a cause of human infection since its transmission does not require intermediate host, so it can be directly spread from infected person to another.

Paragonimiasis is a cosmopolitan in many parts of Africa, Asia and South America (Gary, 2009). In humans, infection occurs by ingestion of raw or undercooked freshwater crabs or crayfishes (Singh    et al., 2005). Capillaria hepatica, the causative agent of hepatic capillariasis, mainly affects rats and is rarely seen in man. Pinworms spread through human-to-human transmission, by fecal-oral route (Burkhart and Burkhart 2005). 

Household pets often carry eggs in their fur, while infection by this route is not recorded yet (Wolfe 1978).

Rats act as reservoir host for many zoonotic pathogens including parasites that pose a health risk to humans (Paramasvaran et al., 2009). Several helminthes parasites are common in both man and rodents. Some are accidentally infect and have a little public health importance, while others naturally occur in rodents and play a significant role in the prevalence of some of human parasites (Flynn, 1973).

The current work aimed to detect the prevalence of different zoonotic parasites infecting humans and rats in different localities of Beni-Suef province, Egypt with determination of the role of rats in transmission of such zoonotic parasites among human beings.

MATERIALS and METHODS

2.1. Rat fecal samples:

A total of 95 fecal samples were collected from rats from different areas in Beni-Suef province (coordinates:  29°04′N 31°05′E), Egypt. Each sample was put into individual plastic container and was transferred to the Laboratory of Parasitology, Faculty of Veterinary Medicine, Beni-Suef University and stored at 4°C for parasitological examination.

2.2 Human stool samples:

Human stool samples were collected from nearby hospitals from Beni-Suef province and from outpatients admitted to clinics. Accordingly, a total of 536 samples were collected. Data of patients were recorded for each sample (residence, age, sex, consistency of the stool,... etc). According to age grouping, patients were classified into 5 groups, each of 10 years interval and beginning from the old of one year. Samples were collected in accordance with WHO guidelines of collection of fecal samples (WHO 1991). Each sample was labelled and sent to the laboratory for further parasitological examination.

3. Laboratory procedures 

3.1. Macroscopic examination:

All fecal samples were visually examined by naked eyes to detect adult nematodes and proglottides of tapeworm.

3.2. Floatation and sedimentation techniques:

Each sample was subjected to fecal floatation technique using different solutions (saturated salt solution, zinc sulphate solution and Sheather's solution) according to Zajac and Conboy (2006). Furthermore, formol ether sedimentation technique was applied for each sample (Lee et al., 2010). Lugol's iodine solution was used to facilitate identification of protozoal cysts and trophozoites. Parasite eggs/oocysts were identified based on color, shape and contents according to the key given by Soulsby (1982) and examined by light microscopy using different magnifications. 

RESULTS

Table 1: Distribution patterns of enteroparasitic stages recovered from patients in different localities in Beni-Suef province, Egypt.

*Mixed infection with Hymenolepis nana & Entamoeba histolytica found in 7 (1.3%), Hymenolepis nana, Enterobius & Entamoeba histolytica in 1(0.18%) and Enterobius and Entamoeba histolytica in 1 (0.18%).

Table 2: incidence of enteric parasite in examined rats.

DISCUSSION

Light microscopic examination of randomly selected fecal samples obtained from patients revealed the presence of multiple parasitic infections including species belonging to trematoda, cestoda, nematode and protozoa. Among trematodes, Paragonimus-like digenean was found only in four (0.7%) patients. This finding is consistent with that obtained by Nworie    et al. (2013) who found a prevalence rate of 0.78% (7 out of 900 stool samples) in Ebonyi, Nigeria. They attributed the low prevalence to the fact that paragonimiasis is a lung infection and eggs are expected to be highly found in sputum not in stool samples. Meanwhile, in few cases, swallowing of sputum may probably give rise to the occurrence of few eggs could be observed in stool samples. The present study revealed that there were no significant differences of infections rates between males and females. Previous literature reported that there were no sex- related differences in prevalence rates (Uchiyama et al., 1999; Ashitani et al., 2000). On the other hand, Nworie et al. (2013) found that infection rate in males was significantly higher (11.11%) than females (5.19%) (P≤0.05). Likewise with data obtained by Singh et al. (1986); Udonsi (1987); Uttah et al. (2013) who found that males are more infected than females. This opinion opposed the results of Ibenga et al. (1997); Asor et al. (2003); Uttah et al. (2013) who determined that infection rates were significantly higher in females than males. It is worthy to mention that, although both sexes can acquire the infection through food, males encounter crabs more than females.

The current work revealed that Hymenolepis nana was found in 67 (12.5%) examined human stool samples. H. nana, the dwarf tapeworm infecting humans, was the second most prevalent cestodal worm detected in this study. Most infected patients were children aged one to 10 years. Mild infections usually passed asymptomatic. In severe infection patients suffered from headache, dizziness, purities, diarrhea, restlessness or even convulsion (Sun, 1988). Lower infection rate by H. nana was recorded in Baghdad by Alia and Afkar (2009) (1.8%). Khalaf    et al. (1979) in Egypt found that out of 471 stools samples obtained from patients suffering from gastrointestinal disease, 62.6% had ova of H. nana in their stools. Moreover, Jassim et al. (1986) estimated infection rate of 8% in Kirkuk city. In the authors’ opinion, the considerably higher infection rate in the present investigation might be related to the habits of wandering outdoors with neglected personal hygiene as well consuming foods from outdoor vendors whom may be carrier of some parasites with high possibilities to human transmission. The present findings revealed one (0.18%) positive sample for Hymenolepis diminuta in accordance with Daniel (1998) who found one case of H. diminuta infection in a child from Guadalajara, Spainand Massimo et al. (2003) in Italy who reported a case of H.diminuta infection in an Italian child. Other studies recorded infection rate ranging between 5.5 and 0.001 Panpiglione et al. (1987) and Mercado and Arias (1995), respectively. Human infection with H. diminuta is rather uncommon due to the accidental mode of transmission by swallowing of rat fleas which contains the infective cysticercoids. Our study exhibited investigation rate of 7.1% for pinworms. This prevalence is lower than the results obtained by Rafique et al. (2009) who found Enterobius spp. in 76% of human stool samples. On the other hand, lower infection ratewas obtained by Khalaf et al. (1979) as Enterobius was detected in 5.8% ofexaminedstool samples. Pinworms infection are often less dangerous but remain one of the most common parasitic nematodes seen by the family physician, particularly prevalent in the pediatric age group, but less in adults. In both groups, the most common symptoms wereanal purities. These helminths were also found in GIT contents of commensal rats and mice (Flynn 1973 and Ceruti     et al., 2001).

Microscopic examination showed infection rate of 11 % for Giardia spp. Higher infection rates (44%) were recorded in Egypt by Zaki et al. (1986) and 44.1%in the aborigine community in Pahang, Malaysia by Noor et al. (2007). Yakubu and Sathiakumar (1985) in Nigeria donated that Giardia lamblia represented 41% of the enteropathogenic agents identified in patients stool samples. In Amman, Jordan Shakkoury and Wandy (2005) recorded infection rate of 78% among the examined children. Even lower prevalence has been reported by other authors in different areasas in Kumasi, Ghana (11.0%) by Addy and Aikins (1986) and in Gaza, Palestine (10.3%) by Al-Hindi and El-Kichaoi (2008). Results exhibited that the age groups 1-10 and 11-20 years showed higher incidence rates. Wongjindanon et al. (2005); Ayeh et al. (2009); Nyarango et al. (2008) explained that the nature of everyday activities exposing people, particularly children, to be contact with natural sources of contamination such as soil and water, with consequent increase of their risk to infection with parasites.

The present study revealed infection rate for             E. histolytica/dispar 16% in the age group 1-10 years and the incidence was higher in males than females. Lower percentages have been reported by Inabo et al. (2000) in Northern Nigeria, conducting that the prevalence of E. histolytica in primary school pupils in five villages in Kaduna and Zaria districts were 8.55%. Regarding to age, it has beennoted that 5-9 years age group was prone to the infection than the 10-15 years group. Moreover, in Makkah, Saudi Arabia, a prevalence rate of 2.6% was reported by Saeed and Manal (2007). Higher incidence was recorded by Yakubu and Sathiakumar (1985) in Nigeria. Theyobserved that enteropathogenic agents were identified in stools of 26(23%) patients representing E. histolytica. Aza et al. (2003) in Malaysia reported that the prevalence of E. histolytica was 21%.Meanwhile, Obadiah (2012) found that 72 (37.9%) were positive for E. histolytica in stool samples. The age groups mostly infected were 0–9 years, and most cases were significantly associated with diarrhea. Zoonotic transmission of E. histolytica has been suggested by Jackson et al. (1984). Experimental infections with E. histolytica have been done in dogs, cats, rats, monkeys and other laboratory animals. Previous literature determined the presence of E. histolytica in wild rats. Among those, Fagir and El-Rayah (2009) in Sudan; Tung et al. (2009) in Taiwan, and Paramasvaran et al. (2009) in Malaysia. Krishnasamy et al. (1980) in Malaysia reported the protozoan in the wood rat. These animals might acquire human strains as a result of the close contact with humans. Amoebiasis is an invasive protozoal infection caused by Entamoeba histolytica (WHO, 1997), and considered the most aggressive protozoal disease that affects the human bowel and incriminatedin some deaths. Among the parasitic diseases, Amoebiasisare worldwide, with approximately 50 million people infected annually, causing close to 100,000 deaths (WHO, 1997 and Gatti et al., 2002). It is said to be more common in areas of poor sanitation and nutrition, particularly in the tropics (Gatti et al., 2002).

Rats are highly adaptable to many environments throughout the world. Unfortunately they act as reservoir host for many zoonotic pathogens including parasites that pose a health risk to humans (Paramasvaran et al., 2009). Several species of helminthes parasites are common to both man and rodents. From which some are accidentally infect humans and are of minor public health importance; while the others play a significant role in human diseases (Flynn, 1973).

Our examination of fecal samples obtained from rats as shown in table (2) revealed the presence of multiple parasitic stages belonging to cestoda and nematode. The results exhibited infection rate of 12.6%, 20%, and 1.05%, for Hymenolepis nana, Hymenolepis diminuta and Capillaria hepatica respectively with overall prevalence of 33.7%. This result is lower than that obtained by Tung et al. (2009) who found that the overall prevalence of parasitesin rodents from different localities in Taichung, Taiwan was 93.7%.

From the result it was obvious that H. nana and H. diminuta were the common parasites in examined rodents with H. diminuta is the most prevalent one. The results are nearly in agreement with Webster and MacDonald (1995) who found that 22% H. diminuta eggs in 225 examined rats in one farm in UK. Furthermore Easterbrook et al. (2008) recorded that Hymenolepis diminuta represent (34.4%) in 162 examined rats in Baltimore, Maryland, USA. Moreover Mohd Zain (2008) stated that H. diminuta represented (35%) in two urban rat populations in Kuala Lumpur, Malaysia.

Lower percentage of H. nana (11%) recovery recorded by Webster and MacDonald (1995) in the rats they examined. In contrast higher percentage (48%) was detected by Rafeique et al. (2009) in wild rodents in Pakistan. Moreover Gilioli et al. (2000) and Mohd Zain (2008) stated that H. nana represented 40% and 28.4% in rats they examined.

Hymenolepis species are tapeworms occurring throughout the world. Over 400 species are found in higher vertebrates, while the definitive hosts are rodents (Little and Ambrose, 2000 and Bahadir, 2002). It is the most notorious for causing pathologic effect of public health importance (Ceruti et al., 2001). H. nana and H. diminuta are the two most problematic for humans. Although H. nana is mainly a parasite of humans, but it is found more commonly in rats and mice, and has been widely used as a model system for the study of cestode tape worm biology (Ito and Itagaki, 2003) H. nana is a zoonotic parasite and is common in children and institutionalized groups (Rauch, 1993 and Alvez et al., 2003). H. diminuta has also been reported among rats in Belgrade (Kataranovski et al., 2011), Sudan (Fagir and El-Rayah, 2009), Baltimore, USA (Easterbrook  et al., 2008), in the city of Doha, Qatar (Abu-Madi   et al., 2001), Nigeria (Mafiana et al., 1997), Kuala Lumpur, Malaysia (Leong et al.,1979) and peninsula Malaysia (Krishnasamy et al., 1980). Man acquires the infection via ingestion of infected intermediate host. Its infection may cause diarrhea or occasionally cachexia in man (Sun, 1988).

Capillaria hepatica, reported in this study was also reported among rats in Belgrade (Kataranovski et al., 2011), Taiwan, (Tung et al., 2009), and Malaysia (Paramasvaran et al., 2009). Moreover Elshazly et al. (2008) studied the prevalence of helminths in rodents in Egypt. The overall prevalence of helminths was 52.8%. The commonest cestode detected was H. diminuta and the commonest nematode detected was Capillaria hepatica. Siti et al. (2012) found that out of 137 samples among wild rats in urban area of Kuala Lumpur, Malaysia, 81.8% samples were positive with intestinal parasites .Six different parasites were detected. The most common intestinal helminth parasite detected was Hymenolepis nana (23.4%), Capillaria hepatica (13.9%) and Hymenolepis diminuta (2.9%).

Capillaria hepatica is a very rare zoonotic infection which primarily infects rodents and is rarely found in humans. Infection manifested by fever of unknown origin and hepatomegaly peripheral eosinophilia.

From the results it is clear the high prevalence of parasitic infection in rats exhibiting no signs in rats except in heavy infection (Tanaka et al.,1974; Baker, 1998). The study throw light on the role of rodents in the spread of enteric parasite in environment and the need for application of appropriate control measures to prevent the human disease transmission.

CONCLUSION

Rats being closely associated with humans and may harbors many different kinds of intestinalparasites serving as great potential for zoonotic infections to man. These rodentscan serve as a source of human infection especially with poor environmental/hygienic conditionsso control of rats is of prime importance in the prevention and control of zoonotic infections in man. The continuous increasing in the amount of garbage collected contributes high rat prevalence. Close proximity of man with rats as well contributing significantly in the increase of zoonotic disease spread.

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