Prevalence of fasciolosis and dicrocoeliosis in slaughtered sheep and goats in Amol Abattoir, Mazandaran, northern Iran

Abstract

Objective

The liver flukes, Fasciola spp. and Dicrocoelium dendriticum, infect ruminants and other mammalian extensively and cause major diseases of livestock that produce considerable economic losses.

Methods

A survey of 2391 sheep and goats slaughtered at an abattoir in Amol region, northern Iran was used to determine the prevalence of the liver flukes infection based on season, sex and specie of the animals.

Results

The results revealed that the prevalence rate of Fasciola spp. and Dicrocoelium dendriticum was 6.6% and 4.3% respectively. Dicrocoeliosis was more dominant in female animals (7.1%) whereas there was no sex-related difference in the prevalence of Fasciola spp. in male and female animals. Furthermore, Fasciolosis was significantly more prevalent than dicrocoeliosis in both sheep and goats. The Seasonal prevalence of Fasciola spp. was highest (P<0.005) during spring (8.3%) followed in order by autumn (8.1%), winter (5.9%) and summer (4.0%) but Dicrocoeliosis did not follow any seasonal pattern.

Conclusions

According to this study, it can be concluded that Amol is regarded as an endemic region for Fasciola spp and D. dandriticum infection. Moreover, Fasciola spp. is the most widespread liver fluke found in sheep and goats which is more dominant in sheep than goats.

1. Introduction

The liver flukes are recognized as one of the most important ruminants helminthic parasites which are found in many parts of the world[1],[2]. Fasciola spp. and Dicrocoelium dendriticum(D. dendriticum) are the common liver flukes in Iran. The principal definitive hosts of these parasites are cattle, sheep and goat. However, certain other mammals, including humans, may be infected as an accidental host[3],[4]. Due to the increasing number of human cases, the liver flukes should be considered as an emerging public health concern[5]. On the other hand, they cause major diseases of livestock that produce important economic losses due to mortality, liver condemnation, reduced production of meat, milk, and wool, and expenditures of anthelmintics[6].

Fasciola spp. has an indirect life cycle involving domestic and wild herbivorous mammals and humans as definitive hosts, and freshwater gastropods of the family Lymnaeidae as intermediate hosts[7]. Fasciola hepatica (F. hepatica) occurs in temperate areas, while Fasciola gigantica mainly occurs in tropical zones, but both species overlap in subtropical areas[8]. Temperature, rainfall and soil moisture influence the activity and abundance of the intermediate hosts of F. hepatica and Fasciola gigantica. Consequently, current climatic conditions can be influential in the development of Fasciolosis[9].

In Iran, fasciolosis is present in many provinces including Kurdistan, Zanjan, Kermanshah, Mazandaran, Tehran, Azerbaijan, Gilan, Fars and Khuzestan[10]. Although the prevalence of fasciolosis among domestic animals is higher in the southern part of the country, the number of reported human disease cases is significantly higher in the Northern provinces situated along the shore of the Caspian Sea[11]. Both Fasciola hepatica and Fasciola gigantica are endemic in the Northern regions of Iran[10],[11],[12].

Dicrocoeliasis, a disease of grazing ruminants, is less severe than fasciolosis. While the economic losses, mainly as a result of affected liver condemnation, are considerable[13]. Two intermediate hosts are necessary to complete parasite development: a land snail (Zebrina sp., Helicella sp., Cionella sp.) and an ant (Formica sp., Lasius sp.). The Final host infection occurs by ingesting the infected ants[14]. Unlike Fasciola spp., the intermediate hosts of D. dendriticum do not require a moist environment and are widely present in pastures [15].

This study was conducted to estimate the prevalence of the liver flukes infection in sheep and goats slaughtered in Amol abattoir, Mazandaran, Iran, based on season, sex and specie of the animals.

2. Materials and methods

This survey was conducted from September 23, 2010 to September 23, 2011 at an abattoir in Amol region, Mazandaran province, Iran. Amol is located in the middle of the Mazandaran province which is in the north of Iran and has a borderline humid subtropical/Mediterranean climate.

A total number of 2 391 sheep and goats, presented to be slaughtered at the abattoir, were randomly sampled during 4 seasons. Specie and sex information were documented before inspection, on the basis of physical appearance of each sample, then the livers were inspected according to the method described by Ogambo-Ongoma (1972) to recognize fasciolosis and dicrocoeliosis[16]. The parasites were identified by their morphological characteristics.

The recorded data, acquired by visualization, palpation and incision of livers, was used to extract the prevalence rate of these parasites. The prevalence rate was sorted seasonally to determine the association of infection rate and seasons. Analysis of data was done, using SPSS software (Version 6.0). Seasonal pattern was investigated with Chi-square (χ²) test and P-value less than 0.05 considered statistically significant.

3. Results

According to the results, among 2 391 sheep and goats sampled during the study, 157 (6.6%) and 104 (4.3%) were infected by Fasciola spp. and D. dendriticum respectively. Dicrocoeliasis was recognized in 7.1% of female animals, whereas only 2% of male animals were infected by D. dendriticum. The difference of D. dendriticum prevalence in relation to the animals sex was statistically significant (P<0.005). However, there was no sex-related difference in the prevalence of Fasciola spp. in male and female animals (P>0.1). More details are shown in Table 1.

Table 1. Sex-wise prevalence of Fasciola spp. and Dicrocoelium dendriticum in sheep and goats slaughtered in Amol region abattoir.

Liver fluke	Male animals		Female animals				χ2	P
	Slaughtered	Infected	Infected	Slaughtered	Infected	Infected
	No.	No.	%	No.	No.	%
Fasciola spp.	1 287	13	1.0%	1104	144	13.0%	1.403	0.2362
D. dendriticum	1 287	26	2.0%	1104	78	7.1%	36.354	0.000

The results revealed that 7.7% and 5.4% of the sheep and goats were infected by Fasciola spp. respectively. On the other hand, dicrocoeliasis was recognized in 5.7% of the sheep and 3.0% of the goats. Thus, fasciolosis was significantly more prevalent than dicrocoeliasis in both sheep and goats (Table 2).

Table 2. Prevalence of Fasciola spp. and Dicrocoelium dendriticum in sheep and goats slaughtered in Amol region abattoir.

Liver fluke	Sheep	Goats					χ2	P
	Slaughtered	Infected	Infected	Slaughtered	Infected	Infected
	No.	No.	%	No.	No.	%
Fasciola spp.	1 215	93	7.7%	1176	64	5.4%	4.767	0.0290
D. dendriticum	1 215	69	5.7%	1176	35	3.0%	10.493	0.0011

Furthermore, the prevalence of fasciolosis and dicrocoeliasis was evaluated during four seasons of the year and as it is shown in Table 3, the Fasciola spp. seasonal prevalence was highest during spring (8.3%) followed in order by autumn (8.1%), winter (5.9%) and summer (4.0%) (P=0.0071). Dicrocoeliasis prevalence did not follow any seasonal pattern, and seasonal differences were not statistically significant (P=0.6607).

Table 3. seasonal prevalences of Fasciola spp. and Dicrocoelium dendriticum in sheep and goats slaughtered in Amol region abattoir.

Season	Slaughtered No.	Fasciola spp. Infected No.	Fasciola spp. Infected %	D. dendriticum Infected No.	D. dendriticum Infected %
Spring	601	50	8.3%	30	5.0%
Summer	599	24	4.0%	27	4.5%
Autumn	595	48	8.1%	21	3.5%
Winter	596	35	5.9%	26	4.4%
Total	2 391	157	6.6%	104	4.3%

4. Discussion

This study was carried out during a one-year period at an abattoir in Amol region, Mazandaran province in the North of Iran. Previous studies in Asia have shown that the liver flukes occur in various countries including Iraq, Pakistan, Turkey, Saudi Arabia, Tunisia, Bangladesh, India, China, Japan and Korea[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28]. Moreover, there are numerous reports of fasciolosis and dicrocoeliasis from different parts of Iran including Fars, Mazandaran, Azarbaijan, Tehran, Khorasan and Gilan provinces[11],[12],[29],[30],[31],[32],[33].

In the current study, the prevalence of Fasciola spp. in sheep and goats was 7.7% and 5.4% respectively. In a study in 2004 at Amol city abattoir, Fasciolosis rate was 5.8% for sheep and 0.5% for goats[12]. On the other hand, Oryan et al. in 2011 reported that The infection rate due to Fasciola spp. was 0.35% in the sheep and 0.2% in the goats in Northeastern Iran[32]. As with the development of the intermediate host, temperature (>9.5 °C), rainfall and soil moisture are important factors influencing the development of the parasite from egg to miracidium. Thus, regional and annual variations in the prevalence of F. hepatica are associated with prevailing weather conditions[9]. In regard to host species, Facsiolosis was significantly more prevalent in sheep than goats. Both sheep and goats are very susceptible to F. hepatica, have no resistance to reinfection[7]. Higher prevalence in sheep may be due to the grazing habits of the animal species; goats graze on leaves and branches on bushes and trees but sheep graze on plants on the ground where metacercaria are mostly found. So, the possibility of infection with metacercaria is higher in sheep than goats[34].

According to the results, the occurrence rate of D. dendriticum was 5.7% in sheep and 3.0% in goats. Dicrocoeliasis prevalence has been reported 4.53% and 1.4% in northeast of Iran[32]and 2.4% and 1.85% in Mazandaran province[35]in sheep and goats respectively. The infection has been described in either lowlands or mountain pastures at high altitudes and it appears that chalk or alkaline soils favour the development of the snail intermediate hosts and ants[36]. In addition, Cringoli et al. showed that large pastures and the presence of streams/brooks in pasture may be risk factors for D. dendriticum infection [37]. Sheep seem to be more susceptible to D. dendriticum than goats[38], which is in agreement with the results of the present study. Our results could not support any association between fasciolosis rate and sex of the animals which is observed by other investigators[39]. However, D. dendriticum was significantly more prevalent in female animals. Females show a higher dicrocoeliasis prevalence than males, probably as a result of different grazing habits[38]. On the other hand, it is assumed that sex is a determinant influencing prevalence of parasitism and females are more prone to parasitism during pregnancy and peri-parturient period due to stress and decreased immune status[18].

The prevalence of Fasciola spp. showed significant seasonal differences in this study. The hatching of fluke eggs and the multiplication of the snail intermediate host require high rainfall and temperatures (>10 °C)[40]. These conditions generally occur in the spring and autumn, when many fluke eggs hatch, snails multiply and then cercariae develop and are released on wet pastures before encysting onto herbage. The seasonality pattern in fasciolosis prevalence has been also observed by other investigators[41],[42].

There are two important features that differentiate the epidemiology of D. dendriticum from that of Fasciola spp. Firstly, unlike Fasciola spp., the intermediate hosts of Dicrocoelium do not require a moist environment and are widely present in pastures and secondly, the fluke eggs can survive for months on these pastures[40]. Seasonality of this infection is favored by movement of the animals from lowland to mountain pastures where they become infected by the ants and then bring the infection back to the valley during the winter [38]. However, no significant correlation between D. dendriticum prevalence and seasons was detected in this study.

This abattoir survey generally reflected the disease situation in the Amol region. According to this study, it can be concluded that Amol is regarded as an endemic region for Fasciola spp and D. dandriticum infection. Moreover, Fasciola spp. is the most widespread liver fluke found in sheep and goats which is more dominant in sheep than goats. More surveys are suggested to be carried out to collect more data about the liver flukes infection prevalence and risk factors for developing a prediction model in small ruminants in northern Iran. The identified risk factors and the prediction model can be useful to formulate appropriate control strategies and decrease the economic loss due to condemnation of infected livers.

Comments

Background

Fasciolosis and dicrocoeliosis are common parasitic diseases of ruminants in Iran, making significant economic losses due to weight loss, reduction of milk production and condemned livers. Both parasites have indirect life cycle, thus various factors such as pasture habits, climate conditions may affect the prevalence.

Research frontiers

This study reports the prevalence of common liver flukes (dicrocoeliosis and fasciolosis) in a northern province of Iran located next to the Caspian sea in relation to season, sex and species of 2 391 sheep and goats presented to the slaughter throughout one year.

Related reports

In the regions with similar climate condition to Iran, Fasciolosis is more prevalent than dicrocoeliosis. According to the intermediate host which needs moist to complete the life cycle, Fasciolosis prevalence shows more seasonal pattern than dicrocoeliosis. Sex related differences are less reported.

Innovations and breakthroughs

Collecting data about the liver fluke occurrence in sheep and goats in a region simultaneously may help to highlight the specie regarded differences. Also little data is reported about liver fluke prevalence in goats and seasonal pattern differences in Iran.

Applications

New prevalence data from the different regions may help to understand the factors affecting the occurrence of the disease and improve control strategies.

Peer review

This manuscript contains useful information with regard to an important parasitic disease which is responsible for considerable economic losses in developing countries. In my point of view, Authors have been successful to demonstrate the relationship between the prevalence of the liver fluke and the sex/ season/ specie factor.