Point prevalence of gastrointestinal helminthiasis in ruminants in southern Punjab, Pakistan

Journal of Helminthology (2007) 81, 323 328 doi: 10.1017/S0022149X07818554 Point prevalence of gastrointestinal helminthiasis in ruminants in southern Punjab, Pakistan Muhammad Asif Raza 1, Zafar Iqbal 1, Abdul Jabbar 1 * and Muhammad Yaseen 2 Departments of 1 Veterinary Parasitology and 2 Mathematics and Statistics, University of Agriculture, Faisalabad-38040, Pakistan Abstract The present study was carried out to determine the prevalence of gastrointestinal helminthiasis in ruminants in an irrigated area of lower Punjab (Pakistan). For this purpose, 100 faecal samples were collected from sheep, goats, cattle and buffaloes. Parasitological procedures including direct and indirect methods (sedimentation and floatation) and coproculture were used for the identification of helminths. The overall prevalence of helminthiasis was 51% in cattle, 47% in buffaloes, 62% in sheep and 52% in goats, with nematodes being the most common helminths. The prevalence of helminths was higher in young animals compared with adults in cattle (P, 0.0001), buffaloes (P, 0.0001), sheep (P, 0.059) and goats (P ¼ 0.010). The prevalence of different species of helminths also varied in different age groups, with Toxocara vitulorum being higher in calves than adults both in cattle (P ¼ 0.017) and buffaloes (P, 0.0001). Sex-wise prevalence of helminths was higher in males than females for buffaloes (P, 0.0001) and sheep (P ¼ 0.014) in contrast to cattle and goats. Introduction The prevalence of helminths in tropical and subtropical areas has reduced production potential of livestock development programmes by causing countless deaths and economic losses (Al-Quaisy et al., 1987). Helminthiasis adversely affects ruminants, e.g. haematological and biochemical disturbances (Iqbal et al., 1998; Hayat et al., 1999), anorexia, weight loss (Khan et al., 1988), hypoproteinaemia, loss of meat (27%) and wool (40%) (Hussain & Akram, 1967), impaired digestive efficiency, poor reproductive performance (Terblanches, 1979) and even death of lambs (FAO, 1974; Barger, 1982). In Pakistan, parasitism is one of the major menaces for livestock, causing obstacles to the development of a profitable livestock industry, as in sheep (Khan et al., 1989; Iqbal et al., 1993; Sajid et al., 1999), goats (Iqbal et al., 1993), cattle and buffaloes (Hayat et al., 1990). Geoclimatic conditions and a poor awareness of livestock farmers *E-mail: jabbaruaf@yahoo.co.uk contribute towards a conducive environment for the development and growth of parasites. Critical analyses (Iqbal et al., 2005; Lateef et al., 2005) have revealed that most surveys carried out on the prevalence of parasites in Pakistan were based on convenience of access in the vicinity of veterinary institutions. Therefore, there are numerous geographical regions in which the livestock population needs to be examined for the presence of gastrointestinal helminths. This paper describes the prevalence of helminths in some domesticated ruminants in Tehsil Jatoi (District Muzaffar Garh), a riverine belt, which has remained unexplored as far as the parasite fauna is concerned. Materials and methods Study area and sample collection District Muzaffar Garh, sprawling over an area of 8249 km 2, lies in the form of strip between the rivers Chenab and Indus, which pass along the eastern and

324 M.A. Raza et al. western boundaries, respectively, of the district and form a triangle at Alipur tehsil of the district. This riverine belt is rich in livestock, due to its geographical location and availability of lush green pastures. The district is located between latitude 28857 0 to 30846 0 N and longitude 70830 0 to 71847 0 E. The climate alternates between extremely hot and cold throughout its area. A large area of the district consists of sand dunes and barren land. Almost all the area of Tehsil Alipur and some parts of Muzaffar Garh tehsil are flooded each year. The people of Muzaffar Garh are an agricultural community who practise subsistence crop agriculture as their main livelihood. Livestock husbandry is very important in the community, and traditionally wealth has been assessed based on the number of livestock, especially buffalo and cattle, owned by an individual (Anonymous, 2000). One hundred livestock, comprising cattle, buffaloes, sheep and goats which had not been dewormed for at least 12 weeks, in three villages representing three union councils (Tehsil Jatoi), were sampled to determine the prevalence of gastrointestinal helminths during March and April 2005. Faecal samples were collected randomly in sterile polythene bags directly from the rectum of each animal and brought to the District Diagnostic Laboratory, Muzaffar Garh for identification of eggs/larvae of helminths or adult worms. Parasitological procedures Faecal samples were examined for helminth eggs/larvae using direct and sedimentation/floatation techniques (Soulsby, 1982). Coproculture was performed to obtain larval stages for genus/species identification of nematodes (MAFF, 1979). Identification of eggs and larvae was made according to the description given by MAFF (1979) and Soulsby (1982). Statistical analyses Data were analysed by analysis of variance and tests for two proportions using MINITAB software (MINITAB, 2000). Results The overall prevalence of helminths was the highest (P ¼ 0.060) in sheep (62%) followed by goats (52%), cattle (51%) and buffaloes (47%). The distribution of different classes of helminths included nematodes, followed by trematodes and cestodes in all host species. The most prevalent helminth species included: Toxocara vitulorum; Fasciola hepatica; Moniezia expansa in cattle, T. vitulorum; Paramphistomum cervi; M. expansa in buffaloes, Haemonchus contortus, P. cervi, M. expansa in sheep and H. contortus, P. cervi, M. expansa in goats (table 1). All host species showed varying degrees of mixed infections comprising differences in the number and species of helminths, i.e. cattle (10%), buffaloes (8%), sheep (11%) and goats (12%). Table 1. Overall prevalences (%) of helminths in ruminants. Species of helminth Cattle Buffalo Sheep Goat Toxocara vitulorum 15 14 Fasciola hepatica 9 4 2 3 Paramphistomum cervi 7 11 7 5 Oesophagostomum radiatum 3 2 Haemonchus contortus 28 20 Teladorsagia circumcincta 3 2 Host-age prevalences The overall prevalence of helminthiasis was higher in young animals compared with adults in all host species, i.e. cattle (P, 0.0001), buffaloes (P, 0.0001), sheep (P ¼ 0.059) and goats (P ¼ 0.010) (table 2). These differences were, however, only attributed to T. vitulorum in cattle and buffaloes (P ¼ 0.017) and H. contortus and Teladorsagia circumcincta in sheep (P ¼ 0.045) and goats (P ¼ 0.062), respectively, as none of the other helminth species differed in prevalence between young and adult animals. Host-sex prevalences The results revealed higher (P, 0.0001) prevalences of helminths in male buffaloes (91%) compared with females (35%). Similar trends were also recorded in male (77%; P ¼ 0.014) and female (52%) sheep (table 3). However, there were no sex-related differences in helminth prevalences in cattle and goats, except for P. cervi in cattle (P ¼ 0.006) and H. contortus in goats (P ¼ 0.020). Discussion The present study showed that the highest prevalence of helminths was recorded in sheep followed by goats, cattle and buffaloes. The higher prevalence of helminths in sheep and goats correlates well with a higher proportion of time spent on grazing compared with cattle and buffaloes, which are grazed proportionately less and kept mainly in stalls for feeding. The helminths recorded in the study area have also been reported previously in other areas of Pakistan (Shah et al., 1980; Siddiqi & Ashraf, 1980; Mohiuddin et al., 1984; Khan et al., 1989) and elsewhere in the world (Specht, 1982; Vercruysse, 1983; Hunter & Heath, 1984; Gupta et al., 1987; Charles, 1989; Van Aken et al., 1990; Pandey et al., 1994; Dorny et al., 1995; Jacquiet et al., 1995). However, these workers have also recorded the occurrence of other helminths and this regional variation may be attributed to different geographical distributions, host factors and climatic conditions required for the development of free-living stages of the nematodes. In the present study, the highest prevalence of helminths was recorded in sheep. The rate of helminth infection in sheep varies from one part of the world to another. A variety of factors such as host age, sex and breeding status, grazing habits, the level of education and economic capacity of farmers, the standard of management and anthelmintic used can influence the prevalence of helminths (Asanji & Williams, 1987; Gulland & Fox, 1992;

Gastrointestinal helminthiasis in ruminants 325 Table 2. The prevalence (%) of helminths in ruminants relative to host age. Cattle Buffalo Sheep Goat Calf Adult Calf Adult Lamb Adult Kid Adult Toxocara vitulorum 25.64 8.19 35.48 4.34 Fasciola hepatica 12.82 6.55 12.9 10.14 2.63 1.61 2.7 3.17 Paramphistomum cervi 10.25 4.91 3.22 4.34 7.89 6.45 8.1 3.17 Oesophagostomum radiatum 2.56 3.27 0.00 2.48 Haemonchus contortus 39.47 20.96 24.32 17.46 Teladorsagia circumcincta 2.63 3.22 5.40 0.00 Mixed infections 18.0 7.00 23.0 9.00 16.0 16.0 30.0 11.0 Overall (%) 77.0 34.0 74.0 35.0 74.0 55.0 73.0 40.0 Pal & Qayyum, 1992; Maqsood et al., 1996; Jorgensen et al., 1998; Komoin et al., 1999; Valcárcel & García Romero, 1999; Ouattara & Dorchies, 2001). The most prevalent nematode recovered in this study was T. vitulorum in cattle and buffaloes and H. contortus in sheep and goats. Previous studies have also shown T. vitulorum to be the most frequently occurring nematode in cattle and buffaloes (El- Moukdad, 1979; Iqbal et al., 1984; Mourad et al., 1985; Pal & Balakrishnan, 1987; Anwar et al., 1996) and H. contortus in sheep and goats (Bali & Singh, 1977; Grant, 1981; Ahmed & Ansari, 1987; Gupta et al., 1987). The high prevalence of H. contortus is likely to be related to a relatively short generation interval and an ability to maximize favourable environmental conditions (Grant, 1981). A mean monthly maximum temperature of 18 8C or above and total monthly rainfall of 50 mm are conducive for the transmission of H. contortus (Gordon, 1953), especially propagation of H. contortus larvae. Climatic conditions in the study area, which vary from tropical to subtropical, are conducive for the development of larval forms or the intermediate hosts of helminths with indirect life cycles. A warm and moist summer is well suited to the development and survival of free-living stages of nematodes (Grant, 1981). Moreover, the availability of green pastures in irrigated or waterlogged areas also assist in the perpetuation of helminth life cycles. Pasture larval counts and helminth fecundity also play a role in the epidemiology of helminths. Pasture contamination is therefore likely to have a direct influence on the population dynamics of nematodes such as Trichostrongylus colubriformis (Barnes & Dobson, 1990). This is also true for nematodes, such as H. contortus, which is highly prolific, laying up to 10,000 eggs/day for several months. Thus under optimum climatic conditions, gross contamination of pasture can occur in a very short time (Radostits et al., 1994). It is evident from table 1 that T. vitulorum in cattle and buffaloes and H. contortus and T. circumcincta in sheep and goats are responsible for the overall higher prevalence in young animals compared with adults. Toxocara vitulorum is a parasite of the small intestine of ruminants, particularly in calves of 15 90 days of age, with a peak egg output occurring 31 45 days post-infection (Gupta et al., 1976; Starke et al., 1983; Roberts, 1990). It is responsible for high morbidity and mortality rates in ruminants (Das & Singh, 1955; Patnaik & Pande, 1963) resulting in serious economic losses (Enyenihi, 1969). The high prevalence of T. vitulorum in young animals indicates a high degree of susceptibility, unlike the adults which acquire immunity to T. vitulorum. Rajapakse et al. (1994) reported high titres of anti-larval ES antibodies in buffalo cow colostrum and in the serum of their suckling calves. This correlated with low T. vitulorum faecal egg counts in calves, suggesting that antibodies have a protective role against activated or migrating larvae. Likewise, H. contortus and T. circumcincta are highly immunogenic, as older ruminants develop a resistance against these parasites: two types of antigens have been recognized in H. contortus. The first type includes natural Table 3. The prevalence (%) of helminths in ruminants relative to host sex. Cattle Buffalo Sheep Goat Male Female Male Female Male Female Male Female Toxocara vitulorum 19.35 13.04 22.72 11.53 Fasciola hepatica 12.9 7.24 27.27 6.41 0.00 3.27 4.65 1.75 Paramphistomum cervi 9.67 5.79 4.54 3.84 10.25 4.91 6.97 3.50 Oesophagostomum radiatum 3.22 2.89 0.00 2.56 Haemonchus contortus 41.02 19.67 20.93 19.29 Teladorsagia circumcincta 2.56 3.27 0.00 3.50 Mixed infections 16.0 9.00 36.0 6.00 18.0 15.0 19.0 18.0 Overall (%) 65.0 45.0 91.0 35.0 77.0 52.0 56.0 49.0

326 M.A. Raza et al. antigens that are recognized by the host during the course of infection, generating an immune response; whereas the second type of antigen is hidden. Although hidden antigens are not exposed to the host s immune system during natural infections, some of these have shown promising results in protection trials (Knox, 2000). It is interesting to note that the prevalence of helminths was higher in males compared with females in buffaloes and sheep, as opposed to cattle and goats. Normally, females are assumed to be more heavily infected due to stress during pregnancy and parturition. The present results may be due to the practice of stall feeding females during pregnancy, therefore lessening the degree of exposure to pasture contamination. Most researchers have observed higher rates of nematode infections/worm burdens in female hosts compared with males (Asanji & Williams, 1987; Pal & Qayyum, 1992; Iqbal et al., 1993; Maqsood et al., 1996; Komoin et al., 1999; Valcárcel & García Romero, 1999). In contrast, Gulland & Fox (1992) reported that the prevalence and intensity of infection (faecal egg counts) were higher in males than females, except during the lambing periods, and decreased with host age in both sexes. Therefore, there is no possible explanation for host-sex differences among different ruminants except for variation in the stages of pregnancy. The present study was based on random sampling for about 2 months during March and April; therefore, any seasonal effect on helminth prevalences could not be ascertained. Some species, such as T. circumcincta thrive better in cool, moist conditions (Kates, 1950; Gordon, 1953). 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