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Point prevalence of bovine fascioliasis and the influence of chemotherapy on the milk yield in a lactating bovine population from the district of Toba Tek Singh, Pakistan

Published online by Cambridge University Press:  10 November 2010

M.K. Khan,
M.S. Sajid,
M.N. Khan,
Z. Iqbal,
M. Arshad and
A. Hussain
M.K. Khan*
Affiliation:
Department of Parasitology , University of Agriculture, Faisalabad, Pakistan
M.S. Sajid
Affiliation:
Department of Parasitology , University of Agriculture, Faisalabad, Pakistan
M.N. Khan
Affiliation:
Department of Parasitology , University of Agriculture, Faisalabad, Pakistan
Z. Iqbal
Affiliation:
Department of Parasitology , University of Agriculture, Faisalabad, Pakistan
M. Arshad
Affiliation:
Department of Microbiology, University of Agriculture, Faisalabad, Pakistan
A. Hussain
Affiliation:
Veterinary Officer (Health), District Sheikhupura, Livestock and Dairy Development Department, Punjab, Pakistan
*
*E-mail: kasibdadra@hotmail.com
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Abstract

This paper provides an estimation of the point prevalence of fascioliasis and its economic impact in terms of increased milk yield after chemotherapy of a bovine population from the district of Toba Tek Singh, Punjab, Pakistan. A total of 2400 cattle and buffaloes were examined quantitatively using the McMaster egg-counting technique. Infected cattle and buffaloes (50 of each) were randomly selected and each divided into two groups of 25 animals. Groups A (buffaloes) and C (cattle) were treated with oxyclozanide (orally, 16.6 mg kg− 1 body weight). Groups B and D served as negative controls for buffaloes and cattle, respectively. Pre- and post-treatment milk yield was recorded to determine if there were any changes in milk yield after treatment. Of 2400 faecal samples analysed, 654 (27.25%) were positive for Fasciola spp. with a mean number of eggs per gram (EPG) of 503.2. The point prevalence and worm burden of fascioliasis was significantly higher (OR = 2.13; P < 0.05) in buffaloes (34.58%; 415/1200; mean EPG maximum likelihood = 521.4) as compared to that of cattle (19.92%; 239/1200; mean EPG maximum likelihood = 415.8). Among the parasite species, F. gigantica (19.88%; 477/2400) was predominant (OR = 3.12; P < 0.05) as compared to F. hepatica (7.38%; 177/2400). An average daily increase of 0.67 and 0.87 litres of milk, with 0.41% and 0.37% more fat per animal, was observed in oxyclozanide-treated buffaloes and cattle, respectively. The economic value of reduced production of infected animals was estimated as US$0.33 and 0.32 per animal per day for cattle and buffaloes, respectively.

Information

Type
Research Papers
Information
Journal of Helminthology , Volume 85 , Issue 3 , September 2011, pp. 334 - 338
Copyright
Copyright © Cambridge University Press 2010

Introduction

Fascioliasis, commonly called liver fluke disease, is an economically important parasitic disease of livestock which infects more than 300 million cattle and buffaloes worldwide (Boray, Reference Boray, Gaafar, Howard and Marsh1985). This is primarily caused by two species of Fasciola (Trematoda: Fascioliidae): Fasciola hepatica and F. gigantica. Asexual development of the trematode requires an aquatic snail (Andrews, Reference Andrews and Dalton1999; Spithill et al., Reference Spithill, Smooker, Copeman and Dalton1999), increasing the prevalence of infection up to 80% in animals with a closed interaction with ponds (Khan et al., Reference Khan, Sajid, Khan, Iqbal and Iqbal2009). Both the species can give rise to acute and chronic infection in livestock (Sampaio-Silva et al., Reference Sampaio-Silva, Da Costa, Da Costa, Pires, Lopes, Castro and Monjour1996), with an estimated blood loss of 0.2–0.5 ml per worm per animal per day (Dawes & Hughes, Reference Dawes and Hughes1970). However, severe infection by this parasite may lead to anaemia (Dawes & Hughes, Reference Dawes and Hughes1970), hypoalbuminaemia and often depresses total protein levels in the animal (Soulsby, Reference Soulsby1987). Chronic fascioliasis reduces growth rate, feed conversion ratio (Oakley et al., Reference Oakley, Owen and Knapp1979), and wool and milk production (Hawkins & Morris, Reference Hawkins and Morris1978). The worldwide annual economic losses due to fascioliasis were estimated to be over US$3 billion (Boray, Reference Boray, Gaafar, Howard and Marsh1985; FAO, 1994). Recently, in Ethiopia, fascioliasis has been reported to cause losses of US$0.27 million per annum (Berhe et al., Reference Berhe, Berhane and Tadesse2009).

Bovine fascioliasis has been found to be endemic in various districts of the Punjab province of Pakistan, with an estimated prevalence ranging from 10.48 to 40.31% (Chaudhry & Niaz, Reference Chaudhry and Niaz1984; Masud & Majid, Reference Masud and Majid1984; Sahar, Reference Sahar1996; Maqbool et al., Reference Maqbool, Hayat, Akhtar and Hashmi2002; Khan et al., Reference Khan, Sajid, Khan, Iqbal and Iqbal2009). This paper is the first report of the prevalence of bovine fascioliasis and the estimation of economic losses in terms of lowered productivity of infected animals from the district of Toba Tek Singh (T.T. Singh), Punjab, Pakistan. Hence, our findings may have implicit significance for determining the benefits of control measures against bovine fascioliasis in this district.

Materials and methods

Study area

The district of T.T. Singh lies between 30°33′–31°2′N and 72°08′–72°48′E and comprises lowlands that are flooded frequently by the Ravi River. The district is divided into three administrative divisions (tehsils), namely Gojra, Kamalia and T.T. Singh. Important, distinct geographical aspects of the district are wetlands, swamps, flood plains and emergent vegetation. Climatically, it is a muggy domain with an average maximum humidity of 63%. The average annual rainfall varies from 254 to 381 mm. Average minimum and maximum temperatures each year are 6°C (December, January) and 39°C (June, July), respectively (Population Census Organization, 2008).

Surveillance

A survey of the bovine population was conducted from August 2008 to March 2009. The numbers of primary units (farms) and secondary units (animals) were determined through two-stage cluster random sampling (Thrusfield, Reference Thrusfield2008). Selected animals were screened fortnightly using the McMaster egg-counting technique (MECT) for the quantitative examination of infection (Iqbal et al., Reference Iqbal, Sajid, Jabbar, Abbas and Khan2006). Briefly, 5 g of faeces were mixed with 5 ml of distilled water followed by the straining of faecal samples through a sieve into a dish containing 39% ZnSO4 (55 ml; specific gravity = 1.18). The mixture was placed in both chambers of a McMaster slide with a pipette. Eggs (N) in both chambers were counted. Eggs per gram of faeces (EPG) were calculated according to the following equation (Iqbal et al., Reference Iqbal, Sajid, Jabbar, Abbas and Khan2006):

\begin{eqnarray} EPG = \frac { N }{Number\,of\,chambers}\times \frac {60\hairsp ml/5\hairsp g}{0.15\hairsp ml} \end{eqnarray}

Eggs of Fasciola spp. were identified using standard keys (Soulsby, Reference Soulsby1987). The copro-parasitoscopic analysis was repeated three times and averaged in order to raise the sensitivity of the test, as recommended by Rapsch et al. (Reference Rapsch, Schweizer, Grimm, Kohler, Bauer, Deplazes, Braun and Torgerson2006).

Chemotherapeutic efficacy of oxyclozanide

Fifty cattle and buffaloes each, found to be naturally infected with Fasciola spp., were selected for the determination of the effect of chemotherapeutic treatment on their milk production. The criteria of selection of animals included: (a) similar nutritional and lactational status; (b) no history of deworming; (c) heavy burden of infection but statistically insignificant between all groups. Selected animals were divided into four groups (A through D) using a randomized complete block design, having 25 animals in each group. Buffaloes were in groups A and B; while, cattle were distributed in C and D. Groups A and C were administered oxyclozanide (Oxanid, Glaxowellcome Limited, Lahore, Pakistan), orally, at the recommended dose rate of 16.6 mg kg− 1 body weight, while groups B and D received normal saline as controls. The pre- (PR) and post-treatment (PT) values of mean EPG were calculated using the MECT (Iqbal et al., Reference Iqbal, Sajid, Jabbar, Abbas and Khan2006).

The efficacy (E) of a drug was calculated using the formula for faecal egg count reduction (FECR; %) (Coles et al., Reference Coles, Bauer, Borgsteede, Geerts, Klei, Taylor and Waller1992) according to the recommendations of World Association for Advancement of Veterinary Parasitology (WAAVP) guidelines (Wood et al., Reference Wood, Amaral, Bairden, Duncan, Kassai, Malone, Pankavic, Reinecke, Slocombe, Taylor and Vercruysse1995). The drug was considered effective if FECR was more than 95% and the lower limit of the 95% confidence interval was more than 90%.

Effect of chemotherapy on the milk yield and fat

PR and PT milk production (litres) and fat (%) records were maintained for 14 days in order to calculate per animal per day increase in the quantity and quality of milk yield (if any). These data were used to estimate the economic value of daily milk loss of infected bovines.

Data analyses

Parasitic abundance followed an aggregated distribution in naturally infected animals, as evident by the greater value of the variance of the mean than of the arithmetic mean (see table 1). Thus, the frequency distribution of faecal egg count (FEC) was modelled as a negative binomial distribution (Torgerson et al., Reference Torgerson, Schnyder and Hertzberg2005). The data obtained for determinants were analysed through multiple logistic regression (Thrusfield, Reference Thrusfield2008). The odds ratio (OR) was used for the pairwise comparison of different risk factors influencing the prevalence of fascioliasis by considering the tehsils of Kamalia and Gojra, F. gigantica and buffaloes as group 1 and the tehsil of T.T. Singh, F. hepatica and cattle as group 2. The differentiation between PR and PT milk yield was made through a paired t-test. The EPG and drug efficacy between buffaloes and cattle were compared through analysis of variance. All the analyses were carried out using the SAS (1998) software package at 95% confidence level.

Table 1

Mean faecal egg counts (EPG) of Fasciola spp. in oxyclozanide-treated buffaloes (A) and cattle (C) and controls (B, buffaloes; and D, cattle) from the district of Toba Tek Singh, Punjab, Pakistan.

CI, confidence interval.

Results

Prevalence

The overall prevalence of fascioliasis in the lactating bovine population was 27.25% (654/2400) with a mean EPG of 503.22 (95% CI maximum likelihood = 60–1061). The distribution of fascioliasis was higher (OR = 2.13; P < 0.05) in buffaloes (34.58%; 415/1200) than in cattle (19.92%; 239/1200). The prevalence of F. gigantica (19.88%; 477/2400) was significantly higher (OR = 3.12; P < 0.05) than that of F. hepatica (7.38%; 177/2400). The species-wise distribution of F. gigantica was also significantly higher (OR = 2.68; P < 0.05) in buffaloes (27.42%; 329/1200) than in cattle (12.33%; 148/1200). However, the prevalence of F. hepatica was insignificantly different (P>0.05) between cattle (7.58%; 91/1200) and buffaloes (7.17%; 86/1200). Quantitative analysis revealed a significantly higher (P < 0.05) mean EPG in buffaloes (mean EPG maximum likelihood = 521.4) than in cattle (mean EPG maximum likelihood = 415.8). Insignificant differences (P>0.05) were found in the distribution of fascioliasis among three tehsils of district T.T. Singh.

Effect of chemotherapy on the milk yield and fat

A significant (P < 0.05) decrease in FEC of Fasciola spp. was documented on day 14 in both buffaloes (E = 95.6%) and cattle groups (E = 96.7%) (table 1). Relative to this effect, differences between PR and PT milk yields of oxyclozanide-treated buffaloes (0.67 litres) and cattle (0.87 litre) were positive, indicating an increase in the milk yield of fasciolicide-treated bovines. Statistically, PT milk yield increased significantly (P < 0.05) in oxyclozanide-treated buffaloes (t value = 2.15) and cattle (t value = 5.55) as compared to those of control groups. Differences between PT and PR fat (%) of oxyclozanide-treated buffaloes (0.41%; t value = 4.78) and cattle (0.37%; t value = 2.70) were also statistically significant (P < 0.05) as compared to those of control groups (table 2).

Table 2

Mean milk yield and the proportion of fat (%) in oxyclozanide-treated buffaloes (A) and cattle (C) infected with Fasciola spp. compared with controls (B, buffaloes; and D, cattle).

PR, pre-treatment; PT, post-treatment.

Estimation of economic value

The local unit price of cattle's and buffaloes' milk was recorded as US$0.38 and 0.47, respectively. It was observed that fascioliasis caused US$0.33 and 0.32 losses per animal per day in cattle and buffaloes, respectively, because of decreased milk yield from their productive potential.

Discussion

In the present study, the estimated prevalence of bovine fascioliasis (27.25%) in the district of T.T. Singh is higher than noticed previously in other regions of Punjab, as for example 10.48% in Lahore (Sahar, Reference Sahar1996), 17.68% in Bahawalpur (Chaudhry & Niaz, Reference Chaudhry and Niaz1984), 23.97% in Multan (Masud & Majid, Reference Masud and Majid1984) and 40.31% in Sargodha, 34.27% in Jhang, 20.83% in Muzaffargarh, 20.10% in Lodhran and 11.77% in Layyah districts (Khan et al., Reference Khan, Sajid, Khan, Iqbal and Iqbal2009). The probable reasons for sustained endemics of fascioliasis over the past many decades may include: (1) lack of treatment for the disease due to the poor socio-economic status of the local farming community (Jabbar et al., Reference Jabbar, Iqbal, Kerboeuf, Muhammad, Khan and Affaq2006); (2) frequent use of the same fasciolicide (triclabendazole) at an inappropriate dose for a longer time in the study area (Khan, personal observation) causing an increased population of drug-resistant disease-causing agents (Boray, Reference Boray, Boray, Martin and Roush1990; Fairweather & Boray, Reference Fairweather, Boray and Dalton1999); (3) lack of periodic evaluation of over-the-counter anthelmintic drugs for their efficacy or the use of non-specific drugs against any parasitic disease (Jabbar et al., Reference Jabbar, Iqbal, Kerboeuf, Muhammad, Khan and Affaq2006). In addition, the topsoil of most domains of district T.T. Singh is enclosed with alluvial deposits (Population Census Organization, 2008), resulting in stagnation of water, creating suitable habitats for the development of snails (Kendall, Reference Kendall1953; Rondelaud et al., Reference Rondelaud, Vignoles, Abrous and Dreyfuss2001). This can directly increase the likelihood of transmission of Fasciola spp. to the final host.

The foremost reason for high vulnerability of buffaloes towards fascioliasis, as reported in this survey, may be their usual practice of living in boggy, muddy and marshy areas (Banerjee, Reference Banerjee1991). Marshy areas favour the propagation of snails (intermediate hosts) of F. gigantica, as their habitat is more aquatic than that of F. hepatica (Spithill et al., Reference Spithill, Smooker, Copeman and Dalton1999). So, the facts that, by nature, the host is attracted towards marshy areas and the higher probability of intermediate hosts in that habitat, make buffaloes more prone to fascioliasis than cattle.

In this study, random assignment of different categories of animals (i.e. old, young, male, female) to treatments made them fall into different groups based on EPG values (moderate or high). However, the large size of groups increased the probability of drug efficacy, as indicated by Torgorson et al. (Reference Torgerson, Schnyder and Hertzberg2005). After assigning the cattle and buffaloes into different experimental groups, treatments were given blindly without knowing which groups the animal belonged to. In addition, a negative binomial model was used to minimize the random variation in highly aggregated EPGs in different experimental groups (Torgorson et al., Reference Torgerson, Schnyder and Hertzberg2005).

PT average daily milk production was increased by 0.67 litres and 0.87 litres per animal, with 0.41% and 0.37% more fat in buffaloes and cattle, respectively. This might indicate a lower production of animals infected with Fasciola spp. than their potential under the same husbandry conditions (Hawkins & Morris, Reference Hawkins and Morris1978; Randell & Bradley, Reference Randell and Bradley1980; Kumar & Pachauri, Reference Kumar and Pachauri1989). In addition, this infection can reduce milk yield by 14%, although 8% is recoverable by treatment (Ross, Reference Ross1970). However, some reports show no or a minimal effect of fascioliasis on the productivity of bovines (Whitehead, Reference Whitehead1976; Castagnetti et al., Reference Castagnetti, Losi, Morini and Padovani1982; Hope, Reference Hope1984; Dargie, Reference Dargie, Leaning and Guerrero1987). The possible causes of decreased production of infected animals may include: (1) lowered feed conversion ratio (FCR) and (2) decreased absorption of energy molecules from the intestine of the host due to sharing of feed intake with the flukes (Oakley et al., Reference Oakley, Owen and Knapp1979). Although statistically insignificant, the higher drug efficacy (%) and PT increase in the production of cattle than of buffaloes may be associated with heavy burdens of helminths in the latter.

Fascioliasis has been reported to cause an annual loss of over US$3 billion to the livestock industry around the globe (FAO, 1994). Fascioliasis has been reported to cause economic loss of €52 million in Switzerland (Schweizer et al., Reference Schweizer, Braun, Deplazes and Torgerson2005), KES3.5 million in Kenya (Mungube et al., Reference Mungube, Bauni, Tenhagen, Wamae, Nginyi and Mugambi2006), and US$0.27 million in Ethiopia (Berhe et al., Reference Berhe, Berhane and Tadesse2009), based on the economic value of condemned livers of infected animals. However, Schweizer et al. (Reference Schweizer, Braun, Deplazes and Torgerson2005) also included the effect of lower production of infected animals on the economics of livestock.

Based on our findings, it can be concluded that fascioliasis is one of the important sub-clinical diseases of livestock in Pakistan, suggesting a widescale study of small and large ruminant populations, including those of slaughter houses, to determine the effect of fascioliasis on blood and milk composition, liver damage and productivity in terms of milk, meat, draught power and reproduction. Periodic fasciolicidal FECR trials may help suggest the most effective drug to the farming community.

Acknowledgements

The cooperation of local farmers, veterinary surgeons and assistants is appreciated for making this survey possible. This project was funded by the Endowment Fund Secretariat, University of Agriculture, Faisalabad, Pakistan. The authors would like to thank Dr Thomas Nolan, Laboratory of Parasitology, University of Pennsylvania, Philadelphia, USA for reviewing the manuscript.

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Figure 0

Table 1Mean faecal egg counts (EPG) of Fasciola spp. in oxyclozanide-treated buffaloes (A) and cattle (C) and controls (B, buffaloes; and D, cattle) from the district of Toba Tek Singh, Punjab, Pakistan.

Figure 1

Table 2Mean milk yield and the proportion of fat (%) in oxyclozanide-treated buffaloes (A) and cattle (C) infected with Fasciola spp. compared with controls (B, buffaloes; and D, cattle).