Coprological prevalence of bovine fascioliasis, its epidemiology and economic significance in Chittagong district, Bangladesh

P Chakraborty and M A M Prodhan

Department of Medicine and Surgery, Chittagong Veterinary and Animal Sciences University, PO Box 4225, Chittagong, Bangladesh
pcb23m@yahoo.com

Abstract

The study was aimed to determine the prevalence of fascioliasis, its associated risk factors and economic significance in cattle in Chittagong district, Bangladesh. Faecal samples from 283 cattle were examined microscopically using direct smear and sedimentation methods and epidemiological and production data were collected using a pre-set questionnaire.

 The overall coprological prevalence of fascioliasis in Chittagong was 14.8%. The prevalence of fascioliasis was found to be significantly associated with age, sex and breed as revealed by the multivariate analysis of risk factors. The infection rate was higher in males than in females. Adult cattle seemed to be more infected than their younger counterparts and within breed, local zebu type Red Chittagong cattle showed more resistance to Fasciola infection than the crossbred cattle. There was also 17.0% reduction in milk production in Fasciola positive lactating cows reared in household based semi-intensive farming condition. The result from this study denotes that further surveys should be carried out to strengthen the result and also for a better understanding on the epidemiology of bovine fascioliasis in the study area.

Key words: cattle, faecal examination, liver fluke infection, milk production, risk factors

Introduction

Livestock plays a key role in the agro based economy of Bangladesh by contributing a significant proportion to GDP (Gross domestic production). However, parasitism is one of the most vulnerable causes of livestock diseases which claim to be the main obstacle in livestock rearing in Bangladesh. Parasitic diseases are the major obstacle in the growth and development of animal health (Mahfooz et al 2008; Raza et al 2010). Helminthiasis has long been recognized and still are problems resulting in losses in ruminant production in almost all regions of the world including Bangladesh (Alawa et al 2010). Among the parasitic diseases, fascioliasis is most important in Bangladesh. Fascioliasis is a parasitic disease of herbivorous mammals caused by trematodes of the genus Fasciola that migrate in the hepatic parenchyma and establish in the bile ducts (Troncy 1989). Fascioliasis is recognized as one of the most important helminth diseases of the domesticated ruminants (Lessa et al 2000). It is an emerging parasitic infection, having significant impacts on both veterinary and human health throughout the world (Lazara et al 2010). Infection to host animals usually takes place with Fasciola metacercariae by ingesting contaminated vegetation near to or within wet grazing land. Due to the tropical climate, the causal agent Fasciola gigantica is prevalent in this part of the world (Amin and Samad 1988; Islam and Samad 1989). In the tropical plain dry lands, the infection is seasonal and is primarily governed by climatic factors and is endemic in high rainfall and waterlogged areas (Muraleedharan 2005). The clinical signs of this disease in cattle are characterized by weight loss, anemia and development of bottle jaw due to hypoproteinemia. The prevalence of fascioliasis may differ in cattle. Earlier reports suggest around 19-53% prevalence of fascioliasis in cattle in various districts of Bangladesh (Rahman and Mondal 1983; Chowdhury et al 1994; Affroze et al 2013).

The prevalence of Fasciola infection depends on several risk factors related to the biology of the host, biology of the parasite and the management of flocks and herds. It also relates with the availability of intermediate host snail (Lymnea auricularia), temperature, moisture, season, health status of animal, availability of flooded area or irrigated land which is used as grazing field for animals (Anne and Gary 2006).

Fascioliasis is an economically important parasitic disease as it causes huge economic losses in terms of reduction of milk and meat and high morbidity in all ages of animals (Saleha 1991). The estimated worldwide economic losses due to fascioliasis in domestic animals were US$ 200 million per year for rural agricultural communities and the commercial sector (Boray 1985). In the years 1975 to 1997, it has been estimated that economic losses in tropical countries reached more than US$ 3200 million (Spithill et al 1999). In Bangladesh, until now there is no available report about the economic losses due to fascioliasis in cattle. However, the economic losses have been estimated in goats. Hossain et al (2011) reported that the economic loss caused by Fasciola infection in goats in terms of liver damage was US$ 115.44 per thousand livers of slaughtered goats. Apart from the reductions in milk and meat yield, it also involved in losses due to decreased fertility (Abunna et al 2010; Sariözkan and Yalcin 2011). Though the direct economic impact of fascioliasis is increased condemnation of liver meat, the far more harmful effects are reduced animal productivity, low calf birth weight, and decreased growth in infected animals (Usip et al 2014). Berando et al (2011) also reported that the parasite may cause loss of production in milking cows. Though fascioliasis was supposed to cause loss of milk production, until now there is no available report regarding the estimation of reduction of milk production due to fascioliasis in ruminants.

To our knowledge, there has also been no detailed study on the prevalence of fascioliasis in cattle in Chittagong district based on faecal or abattoir survey. Therefore, this study was undertaken to estimate prevalence of fascioliasis using coprological procedure as a survey tool, its associated risk factors and economic significance in terms of milk production in cattle in Chittagong district, Bangladesh.

Materials and methods

Area of study, cattle and management conditions

This cross-sectional study was conducted from January to June 2011 in Chittagong district, located around 300 km south-east from the capital city Dhaka in Bangladesh (Wikipedia, 2015). The area has a latitude and longitude of 22°22′0″N 91°48′0″E.

Faecal samples were collected from crossbred and Red Chittagong (RC) cattle from Chittagong Metropolitan area and also from Patia Upazilla, Chittagong. Crossbred cattle were defined as cattle which were mainly bred by crossing local cattle with Holstein Friesian or Jersey cattle. The ‘Zebu’ type RC cattle are indigenous in Bangladesh developed and distributed mainly in the Chittagong district. Pure RC cattle were identified by observing the characteristic features of these cattle such as red hoof, red switch on tail and red eyelashes.

A total of 283 cattle were selected from the study areas using following criteria by simple random sampling method. As there was no previous research work on fascioliasis in the area, to determine the sample size, an expected prevalence of 20% was taken into consideration based on the prevalence of fascioliasis (19.7%) in Savar, Bangladesh (Chowdhury et al 1994), because fascioliasis is more prevalent in lowland areas (Muraleedharan 2005) and compared to Savar, Chittagong is a highland area. The desired sample size for the study was calculated using the formula given by Thursfield (2005) with 95% confidence interval and 5% absolute precision:

n = 1.96²PE (1-PE)/d²

Where PE= expected prevalence; d= absolute precision; n= sample size.

The required sample size was 246 cattle.

A total of 143 cattle faecal samples were tested from Chittagong Metropolitan area. On the other hand, 140 faecal samples were collected and tested from Patia Upazilla. Cattle in Metropolitan area were reared in intensive farming systems whereas in Patia Upazilla, cattle were managed at household based semi-intensive farming conditions.

Faeces collection and examination of eggs

Fresh faecal samples were collected from rectum of individual animals in a dry, clean polythene bags and were brought to the laboratory after proper labeling. A total of 283 faecal samples were collected and processed in the laboratory by standard direct smear and sedimentation techniques as described previously (Soulsby 1983) for the detection of Fasciola eggs. Faecal samples with even one Fasciola egg were considered as positive forFasciola infestation. The eggs of Fasciola were identified according to the key described by Soulsby (1983) and Thienpont et al (1986).Fasciola eggs were confirmed by the detection of large number of characteristics operculated eggs in the faeces under the microscope.Fasciola eggs are thin walled and stained yellow-brown by biliary pigments. Operculated fluke eggs are also characteristics of Paramphistomum but somewhat larger and do not stain yellow, have a transparent shell, a much more distinct operculum and well defined embryonic shell.

Data collection

During sample collection, all related epidemiological data were recorded in a pre-set questionnaire. Data on animal ID, age, sex, breed, body weight, health status, parity and milk production were recorded. Age of the cattle was determined on the basis of owner’s information and also by dentition (Delahunt and Habel 1986; Pace and Wakeman 2003). Animals were categorized into two age groups as young (<3 years) and adult (> 3 years). Health status of cattle was measured by BCS (body condition score) by observing the condition of tail head and loin areas and was categorized as good (3-4), medium (2-3) and poor (1-2) (Nicholson and Butterworth 1986).

Effect of Fasciola infection on milk production

To estimate the effect of fascioliasis on milk production, daily milk production (liter/day) of each of all lactating cows were recorded retrospectively for last one month from the date of sample collection. The animals and their milk production values were then analyzed on the basis of two groups positive and negative to Fasciola infestation. Out of 154 female cattle, 4 were in dry period. Cows were divided into two groups during analysis based on their management as semi-intensive and intensive rearing conditions. The statistical difference of milk production between Fasciola positive and negative animals was measured by T-test with significance at p<0.05. The percentage of reduction of milk production was calculated using the formula: difference of milk production between Fasciola positive and negative cow’s × 100/ Average milk production of Fasciola negative cows.

Statistical analysis

Data generated from the study was entered and managed in MS Excel spreadsheet and analyzed using computerized software package Minitab version 16. General linear models were used to assess the association between the different risk factors (age, sex, health and breed of animals) and the prevalence of bovine fascioliasis. A 95% confidence interval was used to determine whether there is significant difference between measured parameters as described by Thrusfield (2005). A statistically significant association between variables was considered to exist if the calculated p value is less than 0.05.

Results

An overall prevalence of Fasciola eggs were found in 6.99% cattle in Chittagong Metropolitan area and 22.8% in Patia Upazilla which constituted a total 14.8% (42 positive out of 283) prevalence of fascioliasis in Chittagong district (Table 1).

Out of 143 cattle examined in Chittagong Metropolitan area, 09 (6.29%) and 11 (5.9%) faecal samples were found positive by direct smear and sedimentation methods, respectively (Table 2). In Patia Upazilla, the values were 30 (21.4%) and 34 (24.2%) by the two methods out of 140 cattle (Table 2).

Table 3 represents the results of univariate logistic regression of risk factors. There was no association between prevalence of fascioliasis and health status of cattle as revealed by univariate analysis. Among all the variables, only sex was associated with prevalence of fascioliasis (Table 3). As described in Madsen et al (2013), variables with p value ≤0.25 in the univariate analysis were carried out for multivariate analysis (Table 4). Hence, other than sex, age and breed were also included in multivariate analysis. Results from multivariate analysis indicated that the risk factors (age, sex and breed), which were considered into this study, associated with the infection of fascioliasis (Table 4).

Fascioliasis and milk production

The comparison of the average milk production records of lactating cows between the positive and negative to fascioliasis in two farming conditions are presented in Tables 5 and 6. It revealed that there was no difference between milk productions of cows positive and negative to fascioliasis maintained in intensive farming condition (Table 5). On the other hand, a difference was observed between Fasciola positive and negative cows reared in household based semi-intensive farming condition which also resulted in 17% reduction of milk production in Fasciola infected cows (Table 6).

Discussion

In this study, coprological prevalence of fascioliasis, its epidemiology and economic significance were measured in cattle in the two selected areas of Chittagong district, Bangladesh. Faecal examination revealed that the overall prevalence of fascioliasis in Chittagong was 14.8% (Table 1). The prevalence found in this study is much lower than the earlier findings of Rahman and Mondal (1983) who reported a 53% prevalence of bovine fascioliasis in Bangladesh. The rate of infection of Fasciola may vary in different agro-climatic conditions as observed in Pakistan by Bhutto et al (2012). Similarly, the prevalence of fascioliasis varied among various districts of Bangladesh. For example, Chowdhury et al (1994) examined faecal samples of cattle from Savar, Dhaka, Bangladesh and found 19.7% samples positive for fascioliasis. Affroze et al (2013) recorded a 31.1% coprological prevalence of fascioliasis in Netrokona district, Bangladesh. The climatic condition and geographic position of locality influence the type and severity of parasitic infestation in grazing animals (Arambulo and Moran 1981). Fascioliasis is more prevalent in lowland tropical areas as Lymnea auricularia (the intermediate host snail of Fasciola) breeds throughout the year in these favorable habitats (Chartier et al 1990). The lower infection rate in Chittagong in this study may be due to the geographical position of Chittagong district which is located in comparatively higher altitude than Dhaka and Netrokona districts.

Compared to present study, a lower prevalence (6.8%) fascioliasis based on faecal examination was reported by Upadyay and Pachauri (2001) in Tarai region of Kumaon, India. On the other hand, the coprological prevalence of bovine fascioliasis was 41.4% in and around Woreta, Northwestern Ethiopia (Tsegaye et al 2012).

The coprological prevalence of fascioliasis was measured in another bovine species (buffalo) in Bangladesh and there was no sheer variability in those reports. For example, Saha et al (2013) found 26.17% prevalence of fascioliasis in buffaloes in Barisal district of Bangladesh. Mamun et al (2011) reported 22.46% prevalence of Fasciola gigantica in water buffaloes in Kurigram district of Bangladesh and Islam et al (1992) reported an 18.9% prevalence of Fasciola gigantica in water buffalos in Bangladesh.

There was noteworthy difference in the rate of Fasciola infection between male and female cattle. In the male cattle, the infection rate was recorded higher with (19.3%) than the female cattle in which the infection rate was 11.0% (Tables 3 and 4). This variation could be due to the intrinsic factors (genetics, physiology, and immunology) and extrinsic factors (environment and management practices) exist between male and female cattle. The findings in this study are in contrast to the findings of Affroze et al (2013) who recorded a higher prevalence in females (41.3%) than males (13.8%). However, Ibrahim (2004) recorded no significant difference in Fasciola infection rate between male (6.66%) and female (7.14%) cattle in the Beni-Suef Governorate. Similar result was also observed by Tsegaye et al (2012) in Northwestern Ethiopia.

Among the age group, considerably high rate of infection was found in adult cattle (>3 years) (Table 4). Affroze et al (2013) also reported that cattle over 4 years of age had the highest (33.3%) prevalence of fascioliasis in Netrokona district in Bangladesh. Likewise, Tasawar et al (2007) observed high infection in older animals in Pakistan. In contrast, it was previously reported that high Fasciola infection was found in cattle of 2-3 years of age in Bangladesh (Rahman and Mondal 1983). High prevalence in the adult in this study could be due to the intake of parasites for longer period and their grazing habit close to water-logged areas. Keyyu et al (2005) also reported that the high infection rates in older animals might be associated with age and consequently longer exposure time.

The infection rate of bovine fascioliasis on the basis of breed showed difference between RC and crossbred cattle (Table 4). In this study, infection rate in RC cattle (9.52%) was lower than crossbred cattle (20.3%). As mentioned before, RC cattle are local zebu type cattle. Chowdhury et al (1993) recorded a low prevalence (3.7%) of fascioliasis in zebu cattle at Savar, Dhaka, Bangladesh by coprological examination. Low prevalence of fascioliasis could be due to the inherent genetic resistance to various diseases exist in local cattle. However, Tsegaye et al (2012) found higher prevalence of fascioliasis in local breeds (44%) than in crossbred cattle (14.7%).

It was revealed that fascioliasis might cause 3.28% (Table 5) and 17.0% (Table 6) reductions of milk production in cattle reared in intensive and semi-intensive farming conditions, respectively. The economic importance of fascioliasis has so far been reported by estimating the loss due to condemnation of liver in affected cattle (Mebrahtu and Beka 2013; Magaji et al 2014). However, in this study, loss of milk production due to fascioliasis has been estimated as a way to evaluate the economic significance of this disease. It should be noted that realistic economic loss assessment due to fascioliasis is difficult as other vital parameters such as mortality rates due to disease, chronic ill effects (weight gain, feed conversion efficiency, malnutrition and decreased fertility), anthelmintic treatment costs should be included during evaluation (Khoramian et al 2014). Therefore, our estimated data and procedure used in this study should be interpreted with caution.

In conclusion, the results of the current study suggests that bovine fascioliasis is an alarming parasitic disease in Chittagong district, Bangladesh and proper measures such as use of anthelmintic, control of intermediate host should be implemented to eradicate this disease.

Acknowledgements

The authors are grateful to all the farmers who participated in the survey and provided samples for the research work.

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Received 14 September 2015; Accepted 11 October 2015; Published 1 November 2015

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