Prevalence and Intensity of Ovine Gastrointestinal Nematodes in Balochistan, Pakistan.
An epidemiological study was conducted to evaluate the prevalence and intensity of gastrointestinal nematodes of sheep in slaughter house at Quetta, Balochistan, from April 2011 to March 2012. A total of 960 gastro- intestinal tract samples (80 per month) of sheep were examined during the study period. The overall prevalence of gastrointestinal nematode was 49.47% with the intensity of 516.63 in sheep. The higher monthly prevalence of gastrointestinal nematodes was observed during April (65%) followed by November (62.5%) and October (57.5%). Statistically there was significant differences (P Less than 0.05) amongst months. The genus-wise intensity among gastrointestinal nematodes was presented higher by Haemonchus (213.05), followed by Trichostrongylus (137.05), Trichuris (90.1), Ostertagia (44.21) and Nematodirus (32.21). Breed-wise prevalence of gastrointestinal nematodes was higher in Balochi (50.20%) than the Harnai breed (48.75%).
While, sex-wise prevalence of gastrointestinal nematodes was higher in female (56.87%) as compared to the male (42.08%). Age-wise prevalence of gastrointestinal nematodes in sheep was higher in the age group of Less than 1 year (60.83%) followed Greater than 2 years (43.33%) and 1-2 years (41.25%). Statistically there was no significant difference P Greater than 0.05 between breeds, sex and age groups. Five genera of gastrointestinal nematode parasites were recovered during study period. Among these Haemonchus was the highest (71.36%) prevalent followed by Trichostrongylus (58.49%), Trichuris (28.84%), Ostertagia (17.26%) and Nematodirus (9.47%).
Keywords: Prevalence, gastrointestinal nematodes, sheep, Haemonchus, Trichostrongylus, Trichuris, Ostertagia.
Parasitic diseases remain a main constraint to animal production systems across all agro ecological zones throughout the world. The productive and reproductive potential of domesticated livestock is adversely impaired by clinical and sub-clinical helminthes diseases. Among helminthes, gastrointestinal nematodes significantly affect the production of sheep due to reduction in appetite, loss of body condition, anemia, hypoproteinaemia, impaired digestive absorptive efficiency, other pathogenic complications and even death of animals (FAO, 1974; Barger, 1982; Steel and Symons, 1982; Holmes, 1986). Khan et al. (1988a) reported 100% sheep in upland Balochistan infected with internal parasites. Ahmed et al. (2005) recorded overall helminthiasis of 23.75% in slaughtered sheep at Quetta. Razzaq et al. (2002) recorded 93% gastrointestinal nematodes of sheep in Asghara valley district Ziarat. Several epidemiological factors influence the parasitic diseases in small ruminants.
These include weather conditions, husbandry practices and the physiological status of the animals and for sustainable and normal control of gastrointestinal nematodes of sheep a comprehensive knowledge of epidemiology is a prerequisite (Pal and Qayyum, 1992; Wall et al., 2004; Keyyu et al., 2005). Therefore, the present study has been designed to assess the epidemiological factors contributing gastrointestinal nematodosis in sheep production system of Balochistan.
MATERIALS AND METHODS
The present study was conducted from April 2011 to March 2012, during which a total of 960 gastrointestinal tracts (40/fortnightly) samples of sheep (Balochi and Harnai breed) from Quetta district abattoir was collected randomly and transferred to the Disease Investigation Laboratory of Livestock Department, Quetta for isolation and identification of gastrointestinal nematodes. A complete record of the animal i.e., age, sex and breed were maintained at the time of sampling. Age of sheep was determined by the presence of incisors teeth in the lower jaw (Khan, 1969). Sampled animals were segregated into three age groups i.e., Less than year, 1-2 year and Greater than 2 year of age. Sheep breeds were identified based on their phenotypic characteristics (Hasnain, 1985).
Nematodes from the abomasums, small and large intestine were isolated within four hours after the slaughtering of animals. Abomasums, small and large intestine were ligated at omasal-abomasal, abomasal-duodenal and ileo-caecal junctions to prevent worms spilling from one location to another. The abomasum was cut opened longitudinally, the contents of abomasum was poured in a 10 L bucket. Abomasal wall was washed thoroughly under a stream of water from a tap and mucous membrane rubbed with thumb finger to remove any adhering worms to it in the same bucket. The contents of bucket were sieved through a wire mesh screen with an aperture of 0.15 mm, and then washed with a stream of water. The screen having food materials and worms was inverted into another bucket and then washed with stream of water. More water was added to make up total volume of 4L which was then agitated vigorously and sample was taken by wide mouthed pipette. The sample was transferred to a measuring cylinder until a total volume of 40 ml.
Small quantity of this 40 ml were placed in a Petri dish having parallel line and examined under stereomicroscope for worms count. The large and small intestine were processed same as abomasam. Worms from abomasam, large and small intestine were collected and counted (Charles and Baker, 1988). The collected nematodes were washed in physiological saline (0.89 gm/100 ml distilled water) and were fixed in 70% alcohol for 24 hours. The nematodes were then transferred to a vial containing a hot mixture of 70% ethyl alcohol (Merck) and glycerol (Merck) equal parts. The worms were kept in this vial partly covered until all ethyl alcohol was evaporated and worms were left in pure glycerol. The worms were cleared in lacto phenol and then placed on microscopic slide and mounted in pure glycerol. Excess of glycerol was removed with the help of filter paper and the edges of the cover slip were sealed with slide sealer.
The gastrointestinal nematodes were examined under 4x and 10x magnification of compound microscope and identified using standard keys and morphological characteristics described by (Yamaguti, 1961; Maff,1979; Soulsby, 1982; Urquhart et al., 1996).
The mean intensity was calculated (total number of worms recovered/ number of infected sheep) and the prevalence of infection (number of infected host/number of surveyed sheep). The intensity for each genus (number of worms/infected sheep) and the frequency (number of worms of one particular genus/total number of worms recovered) were calculated. The data collected from this study were analyzed by using Graph Pad Prism-5 computer statistical package. The prevalence of different nematodes in different age, breeds and sex- wise were analyzed through one way analysis of variance at (P Less than 0.05). Metrological data were calculated on simple mean and percentage basis.
The overall prevalence of gastrointestinal nematodes was 49.47% with intensity of 516.63 in sheep at Slaughter-house Quetta, Balochistan. The higher monthly prevalence of gastrointestinal nematodes was observed during April (65%) followed by November (62.5%) and October (57.5%). Similarly, higher monthly mean intensity was recorded during October (65.68) followed by November (54.94). Statistically there was significant difference P Less than 0.05 among months (Table I).
Table I.- Month, age, breed and sex-wise gastro-intestinal nematodes prevalence, intensity and frequency in slaughtered sheep at Quetta.
Age###Under 12 months###60.83
###Greater than 2 Year###43.33
Meteorological record of district Quetta
The meteorological data of district Quetta from April 2011 to March 2012 were obtained from Land and Water Resources Research Program, Arid Zone Research Centre (PARC), Quetta. The rainfall was very low (less than 20 mm) through out the study period, however higher rainfall recorded during April 2011 and January to March 2012. The temperature was higher (above 30degC) during June to August 2011, while lower during the rest of study period. Similarly, humidity was also lower (30%) round the year except January to March 2012 (Fig.1).
Genus-wise intensity and frequency of nematodes In the present study, GIT samples (n=960) assessments showed intensity of five nematodes genera in sheep at Quetta slaughter-house. Among these higher intensity of Haemonchus (213.05) was recorded followed by Trichostrongylus (137.05), Trichuris (90.1), Ostertagia (44.21), Nematodirus (32.21) during the one year study. Similarly, the higher frequency was also presented by Haemonchus (0.41) followed by Trichostrongylus (0.26), Trichuris (0.17), Ostertagia (0.08) and Nematodirus (0.06) in sheep (Table I).
Breed-wise prevalence of nematodes
In present study, GIT samples of two sheep breeds i.e., Balochi and Harnai (n=480 from each breed) were analyzed for presence of nematodes. The results showed that overall prevalence of gastrointestinal nematodes was 49.47% (475/960). The Balochi breed showed higher (50.20%)
Fig. 1. Meteorological record of district Quetta during April 2011 to March 2012.
prevalence of gastrointestinal nematodes than Harnai breed (48.75%) (Table I). Statistically there was no significant difference P Greater than 0.05 between breeds.
Sex-wise prevalence of nematodes
The prevalence of gastrointestinal nematodes was higher in female (56.87%) as compared to male (42.08%), while the overall prevalence was 49.47% (Table I). Statistically there was no significant difference P Greater than 0.05 between either sex of sheep.
Age-wise prevalence of nematode
The present study results showed that the sheep under Less than 1 year age showed higher prevalence (60.83%) of gastrointestinal nematodes followed by Greater than 2 years (43.33%) and 1-2 years (41.25%) age groups (Table I). Statistically there was no significant difference among age-wise at P Greater than 0.05.
Genus-wise prevalence of nematode
In present study, five genera of gastrointestinal nematode parasites were recovered in slaughtered sheep. Among these Haemonchus was found highest (71.36%) prevalent followed by Trichostrongylus (58.49%), Trichuris (28.84%), Ostertagia (17.26%) and Nematodirus (9.47%) (Table I).
The overall prevalence of gastrointestinal nematodes as 49.47% with intensity of 516.63. These findings are in agreement with Shimelis et al. (2011) who observed the overall prevalence of gastrointestinal nematodes as 47.67% in North Gondar zone of Northwest Ethiopia. Khan et al. (2010) reported nematodes prevalence (44.17%) which is almost close to the present study. However, Lateef et al. (2005) reported higher prevalence (65%) of gastrointestinal nematode than the present study. Abunna et al. (2009) reported 83.6% and even higher (91.7%) by Sing et al. (1997) at India and 91.32% by Tefera et al. (2011) in South- Western Ethiopia, respectively. The reasons might be due to variation in environmental conditions such as the related results of present study with Ethiopia due to similar dry environment, while higher prevalence in different areas like Punjab, India due to hot and humid environment.
The month-wise higher prevalence of gastrointestinal nematodes was observed during April, November and October in the present study which was in agreement with Nginyi et al. (2001). They recorded higher monthly prevalence of gastrointestinal nematodes during the months of April and October which might be due to the similarities in the climatic conditions. Githigia et al. (2001) also reported two peaks of nematodes prevalence. The first peak was during August/September which may be due to uptake of larvae during June/July and the second peak was during November/December (due to uptake of larvae during the short rainy season). Similarly in the present study two peaks were recorded during April and November which might be due to favorable environmental conditions as described by Rafique et al. (1997) that parasitic burden of range- animals in an area might be associated with different climatic conditions, husbandry practices and other managemental factors.
Qamar (2009) described the role of meteorological data like humidity, rainfall and temperature which was correlated with the occurrence of the disease. Difference in the incidence of different gastrointestinal nematode parasites in the present study may be due to differences in arid environment and nematodes susceptibility as mention by Durrani et al. (1981) that incidence of few species of gastrointestinal nematode parasites was relatively higher and some other species had relatively lower incidence under arid conditions of upland Baluchistan as compared to semi-humid, subtropical Punjab province.
In present study the prevalence of gastrointestinal nematodes in Balochi breed was higher (50.20%) than Harnai breed (48.75%). These findings were in agreement with Mushtaq and Tasawar (2011) who observed higher infection of gastrointestinal nematodes in Kacchi breed than Lohi breed. Tasawar et al. (2011) also observed higher infection of gastrointestinal nematode parasites in Lohi breed (87.09%) than Awassi (76.9%) and Hisardale breed (74.2%). Chaudhry et al. (2009) also pointed out that the H. contortus was the most ubiquitous and predominated gastrointestinal parasite in Bulkhi ewes followed by Trichostrongylus spp. and Oesophagostomum columbianum. AL-Shaibani et al. (2008) recorded Kooka breed slightly more susceptible as compared to Kacchi and Dumbi breeds. In contrast to the current results, Chaudry et al. (2007) recorded significant variation in larval counts among sheep breeds from different ecologies, while no difference was recorded among different breeds at same ecology.
Similarly, Abunna et al. (2009) observed significant difference between host risk factors in prevalence of different nematode species. Urquhart et al. (1996) stated that the susceptibility by various breeds of animal to parasites varies and is genetically determined.
In present study the prevalence of gastrointestinal nematodes was higher in female (56.87%) as compared to male (42.08%). These findings were also in agreement with some researchers (Maqsood et al., 1996; Lateef et al.,2005; Al-Shaibani et al., 2008; Shimelis et al.,2011; Khan et al., 2010) who observed relatively higher prevalence of gastrointestinal nematode in female animals as compared to male. This may be due to the gestation stress, pre- parturient parasitic rise as the pre-disposing factors for higher prevalence in female stock. In contrast to present study Mushtaq and Tasawar (2011) observed the prevalence of gastrointestinal nematode parasites was higher in male sheep (81.4%) as compared to female sheep (73.1%). Barger (1993), Bilbo and Nelson (2001) reported that such differential prevalence of gastrointestinal nematodes in sheep may be due to stimulatory effects of estrogens and inhibitory effect of androgens on immune responses.
While, Qamar (2009) was of view, that the animals of either sex were equally affected by the helminths. Similarly, Urquhart et al. (1996) correlated the hormonal difference in either sex with parasitic susceptibility and found that males are more susceptible than female due to androgen hormones. The females are more resistant to infection might be due to the stimulatory effects of estrogen on immune response, whereas the androgen have an opposite effect in males. In contrast, Raza et al. (2009) clarified that the higher prevalence in females might be due to lower resistance on the part of their reproductive events and insufficient/ unbalanced feed against higher need. The female animals generally harbored a significantly higher worm burden than male animals due to the enhanced grazing of females during lactation and their low resistance during pregnancy and parturition.
Silva et al. (2011) also supported the rearing systems and observed that the goats in the organic system had higher fecal egg counts (P Less than 0.05) than the goats in the conventional system.
Age-wise results in the present study presented higher prevalence of gastrointestinal nematode parasites in sheep of less than one year age (60.83%) followed by Greater than 2 years (43.33%) and 1- 2 years (41.25%) age groups. These findings were also in line with other researchers (Lateef et al.,2005; Qamar, 2009; AL-Shaibani et al., 2008; Khan et al., 2010; Shimelis et al., 2011) who recorded higher prevalence of gastrointestinal nematodes in sheep of less than one year Less than 1 (69.2%), followed by 1-2 years (50.8%) and Greater than 2 years (37%) old animals.
In contrast to the present study, Tasawar (2011) reported higher prevalence of gastrointestinal nematodes in older age animals than younger. This might be due to low immunity in younger than the older ones. Urquhart et al. (1996) also stated that a significant immunity develops with age against a few parasites in adult stock. Radostits et al. (1994) pointed out that two age groups of sheep most commonly affected are weaned lambs and yearlings. They added that the sheep over 18 month of age are less commonly affected because of immunity, resulting from previous infection. The low nematode prevalence in younger sheep at might be due to grazing on (nearby home) low contaminated pastures and supplemental feeding (barley grain, green wheat, barseem etc.). While higher nematode prevalence in adult sheep might be due to grazing on larger area of pastures being contaminated with various flocks and different stress conditions like climate, long daily traveling and gestation etc.
In contrast, Abunna et al. (2009) stated that there was no significant difference of sheep nematodes prevalence between age and month. Young animals also get infected with internal parasitic ova from the contaminated pastures being spread for the female animals during gestation period because of higher parasitic load at this stage.
Five genera of gastrointestinal nematode parasites were recovered from gastrointestinal tract during study period. Among these Haemonchus was highest (71.36%) in prevalence followed by Trichostrongylus (58.49%), Trichuris (28.84%), Ostertagia (17.26%) and Nematodirus (9.47%), respectively. These findings are in agreement with Lateef et al. (2005) who recorded the highest prevalence of H. contortus (61.5%) followed by Trichostrongylus spp. (46.1%) and Ostertagia spp (33.0%). Similarly, Asif et al. (2008) reported that Haemonchus was higher in prevalence (80.64%) followed by Trichuris (32.25%) and Nematodirus (29.03%), respectively. Gadahi et al. (2009) recorded the prevalence of Haemonchus (28.88%), Trichuris (40%) and Nematodirus (11.11%) in sheep. Nginyi et al. (2001) recorded the genera of nematodes Haemonchus and Trichostrongylus as 33% and 29%, respectively. Abunna et al. (2009) observed the prevalence of Haemonchus (78.1%) and Trichostrongylus spp. (90.4%) in sheep.
Zeryehun (2012) recorded genera-wise prevalence in sheep for strongly type eggs, Strongyloides sp., Trichuris sp., as 39.84%, 17.45% and 7.81%, respectively. Kantzoura et al. (2012) reported prevalence in sheep for Nematodirus spp. as 1.1% and for Trichuris spp. as 2.9%. Mushtaq and Tasawar (2011) recorded prevalence of Haemonchus contortus and Trichuris, 6.50% and 5.73%, respectively. While Al- Shaibani et al. (2008) recorded higher prevalence of H. contortus (24.6%) which was found to be predominant of gastrointestinal nematode parasites while Trichostrongylus spp. (18.0%) was the next most prevalent specie. while Khan et al. (1988b) reported the same parasites in upland districts of Baluchistan. Difference in the occurrence of different gastrointestinal nematode parasites in the present and other studies carried out in different locations might be due to different ecologies, temperature and pastures.
Durrani et al. (1981) reported that occurrence of gastrointestinal nematodes was higher and lower in arid conditions of upland Baluchistan as compared to semi-humid, subtropical climate of Punjab province. Radostits et al. (1994) pointed out that warm, wet weather provides favorable conditions for the translation of eggs to larvae in the majority of helminthes. The areas having severe summer and dry winter reduced the parasitic burden on the local livestock. It was observed in present study that most of the flocks were sedentary and they were under strict confinement which leads to high risk of helminthes infection (Anene et al.,1994).
In present study among five genera of gastrointestinal nematode Haemonchus was most prevalent nematode. It might be due to its biotic potential which justified the percentage of infection (Nginyi et al., 2001). The H. contortus larval development occurs when there is high temperature, rainfall and high humidity favorable microclimate of herbage and faeces (Urquhart et al., 1996). Trichostrongylus was next most prevalent nematode parasite in the present study. These findings are in contrast to those of Suarez and Busetti (1995) mentioned that Trichostrongylus populations were high in autumn and reached their peaks in June to July, while the highest larval availability was in developed and survive at lower temperature (Mallet and Kerboeuf, 1986). Furthermore, Trichostrongylus is the dominant parasite in temperate areas with the cooler environment creating optimum condition for larval development (O'Connor et al., 2006) the overall prevalence of Ostertagia spp. was 17.26% in the present study.
Some researchers (Tasawar et al., 2011; Umur and Yukari, 2005; Craig et al., 2006) recorded higher prevalence of Ostertagia spp. that were 77%, 64.6%, 73.58%, 94.8%, 80%, 75%, respectively and Sajid et al. (1999) recorded lower (16.2%). These differences in the percentage reported by different researchers could be due to different managemental practices (Lindquist et al., 2001), natural resistance based on genetic background and anthelmintic treatment (Soulsby, 2005) and geo-climatic factors of the regions (Pal and Qayyum, 1993). In present study the prevalence of Trichuris was 28.84%. These findings are near to Asif et al. (2008) who recorded 32.25% prevalence of Trichuris. Gadahi et al. (2008) recorded higher than these (40%) while others (Reda et al., 2011; Zeryehun, 2012; Mushtaq and Tasawar, 2011) reported the lower prevalence i.e. 5.8%, 2.9% and 5.73%, respectively.
These differences in the percentage reported by different researchers might be due to differential management practices and geo- climatic factors of the regions (Pal and Qayyum, 1993). The prevalence of Nematodirus was 9.47% in present study. These findings are close to the findings of Asif et al. (2008) who reported prevalence in sheep for Nematodirus spp. as 11.11% and Kantzoura et al. (2012) reported lower prevalence 1.1%. Some particular parasites, Nematodirus, have no obvious seasonal pattern of occurrence and chill temperature requirement for larval development are important factors for their prevalence during different period of year. Similarly, some climatic factors like warmness and moisture favor development and allow the accumulation of large numbers of infective stages on the rangelands (Urquhart et al., 1996).
ABUNNA, F., TSEDEKE, E., KUMSA, B., MEGERSA, B., Nematodes: Prevalence in Small Ruminants Slaughtered at Bishooftu Town, Ethiopia. Int. J. Vet. Med., 7 Number 1, ISSN: 1937-8165. (www.ispub.com).
AHMED, S., NAWAZ, M., GUL, R., ZAKIR, M. AND RAZZAQ, A., 2005. Diversity and prevalence of trematodes in livers of sheep and goats in Quetta, Pakistan. Pakistan J. Zool., 37: 205-210.
AL-SHAIBANI, I.R.M., PHULAN, M.S., ARIJO, A. AND QURESHI, T.A., 2008. Epidemiology of ovine gastrointestinal nematodes in Hyderabad District, Pakistan. Pak. Vet. J., 28: 125-130.
ANENE, B.M., ONYEKWODIRI, E.O., CHIME, A.B. AND ANIKA, S.M., 1994. Gastrointestinal parasites in sheep and goats of Southern Nigeria. Small Rum. Res., 13:187-192.
ASIF, A., AZEEM, S., ASIF, S. AND NAZIR, S., 2008. Prevalence of Gastrointestinal Parasites of Sheep and Goats in and around Rawalpindi and Islamabad, Pakistan. J. Vet. Anim. Sci., 1: 14-17.
BARGER, I.A., 1982. Helminth parasites and animal production. In: Biology and control of endoparasites, (eds. L.E.A. Symons, A.D. Donald and J.K. Dineen), Academic Press, Sydney, pp. 133-155.
BARGER, I.A., 1993. Influence of sex and reproductive status on susceptibility of ruminants to nematode parasitism. Int. J. Parasitol., 23: 463-469.
BILBO, S.D. AND NELSON, R.J., 2001. Sex steroids hormones enhance immune functions in male and female hamsters. Am. J. Physiol. Regul. Integr. Comp. Physiol., 280: 207-213.
CHARLES, T.P. AND BAKER, N.F., 1988. Seasonal prevalence of gastrointestinal nematodes of beef calves grazed on irrigated pasture in the lower Sacramento valley of California. Am. J. Vet. Res., 49:566-571.
CHAUDARY, F.R., KHAN, M.F.U. AND QAYYUM, M.,2007. Prevalence of Haemonchus contortus in naturally infected small ruminants grazing in the Potohar area of Pakistan. Pak. Vet. J., 27: 73-79.
CHAUDHRY, F.R., QAYYUM, M., KHAN, M.F., AHMAD, T., KHANUM, A., SHAKIR, M.R., JAMES, D.H. AND MILLER, E., 2009. Peri-parturient rise in faecal nematode egg counts with reference to Haemonchus contortus in bulkhi ewes in Northern Punjab, Pakistan.Pakistan J. Zool., 41: 437-443.
CRAIG, B.H., PILKINGTON, J.G. AND PEMBERTON, JM., 2006. Gastrointestinal nematodes species burdens and host mortality in a feral sheep population. Parasitology, 133: 45-96.
DURRANI, M.S., CHAUDHRY, N.I. AND ANWAR, AH., 1981. The incidence of gastro-intestinal parasites in sheep and goats of Jhelum Valley (Azad Jammu Kashmir). Pak. Vet. J., 1: 164-165.
FAO, 1974. Pakistan Livestock Sector Survey Report No. 32/74/Pak/7. F.A.O./World Bank Cooperative Programme. pp. 11
GADAHI, J.A., ARSHED, M.J., ALI, Q., JAVAID, S.B. AND SHAH, S.I., 2009. Prevalence of Gastrointestinal Parasites of sheep and goat in and around Rawalpindi and Islamabad. Pak. Vet. World., 2: 51-53.
GITHIGIA, S.M., THAMSBORG, M.S., MUNYUA, W.K. AND MAINGI, N., 2001. Impact of gastro-intestinal helminthes on production in goats in Kenya. Small Rum. Res., 42: 21-29.
HASNAIN, H.U., 1985. Sheep and goats in Pakistan. Anim. Hlith. Prod., 6: 55-135.
HOLMES PH, 1986. Pathogenesis of trichostrogylosis. Vet. Parasitol., 18: 89-101.
KANTZOURA, V., KOUAM, M.K., THEODOROPOULOU, H., FEIDAS, H. AND THEODOROPOULOS, G., 2012. Prevalence and risk factors of gastrointestinal parasitic infections in small ruminants in the Greek temperate mediterranean environment. Open J. Vet. Med., 2: 25-33.
KEYYU, D., KYVSAARD, N.C., MONRAD, J. AND KASSUKU, AA., 2005. Epidemiology of gastrointestinal nematodes in cattle on traditional, small-scale dairy and large-scale dairy farms in Iringa district, Tanzania. Vet. Parasitol., 127: 285-294.
KHAN, A.W., 1969. Animal production. Ilmi Book Depot, Canal Park Road, Lahore (1st Ed.). pp. 779-814.
KHAN, K.N., REHMAN, M.A. AND CHAUDHRY, M.B.A.,1988a. Incidence of internal and external parasites in sheep in Kovak Valley upland Balochistan. Research report No.13, The MART/AZR Projects ICARDA- PARC AZRI, Quetta, Balochistan.
KHAN, K.N.M., REHMAN, A., MUNIR, M. AND KHAN, BR., 1988b. Incidence of internal parasites of sheep in upland districts of Baluchistan. Research Report No.18, The MART/AZR Projects ICARDA-PARC, AZRI Quetta, Baluchistan.
KHAN, M.N., SAJID, M.S., KHAN, M.K., IQBAL, Z. AND HUSSAIN, A., 2010. Gastrointestinal helminthiasis: prevalence and associated determinants in domestic ruminants of district Toba Tek Singh, Punjab, Pak. Parasitol. Res., 107: 787-794.
LATEEF, M., IQBAL, Z., JABBAR, A., KHAN, M.N. AND AKHTAR, M.S., 2005. Epidemiology of trichostrongylid nematode infections in sheep under traditional husbandry system in Pakistan. Int. J. Agric. Biol., 7: 596-600.
LINDQUIST, A., LJUNGSTROM, B.L., NILSSON, O. AND WALLER, P.J., 2001. The dynamics, prevalence and impact of nematode infections in organically raised sheep in Sweden. Acta Vet. Scand., 42: 377-389.
MAFF. 1979. Ministry of Agriculture Fisheries and food Manual of veterinary parasitologcal laboratory techniques. Tech. Bull. No. 18., H.M.S.O., London, pp.131.
MALLET, S. AND KERBOEUF, D., 1986. Winter survival of third stage Trichostrongylus colubriformis larvae: effects on infectivity and fecundity of adult worms. Res. Vet. Sci. 41: 265-267.
MAQSOOD, M., IQBAL, Z. AND CHAUDHRY, A.H., 1996. Prevalence and intensity of haemonchosis with reference to breed, sex and age of sheep and goats. Pak. Vet. J., 16: 41-3.
MUSHTAQ, H.L. AND TASAWAR, Z., 2011. Prevalence of some gastrointestinal parasites in sheep in Southern Punjab, Pakistan. Pak. Vet. J., 31: 295-298.
NGINYI, J.M., DUNCAN, J.L., MELLOR, D.J., STEAR, M.J., WANYANGU, S.W., BAIN, R.K. AND GATONGI, PM., 2001. Epidemiology of parasitic gastrointestinal nematode infections of ruminants on smallholder farms in central Kenya. Res. Vet. Sci., 70: 33-39.
O'CONNOR, L.J., WALKDEN-BROWN, S.W. AND KAHN, L.P., 2006. Ecology of the free-living stages of major trichostrongylid parasites of sheep. Vet. Parasitol., 142:1-15.
PAL, RL. AND QAYYUM, M., 1993. Prevalence of gastrointestinal nematodes of sheep and goats in upper Punjab, Pakistan. Pak. Vet. J., 13: 138-141.
QAMAR MF., 2009. Epidemiology, sero-diagnosis, economic losses and control of haemonchosis in sheep and goats. Ph.D. thesis, Dept. of Parasitology, Univ. of Vet. and Animal Sc., Lahore, Pakistan. p. 63-113.
QAMAR, M.F., MAQBOOL, A., KHAN, M.S., AHMAD, N.AND MUNEER, M.A., 2009. Epidemiology of Haemonchosis in sheep and goats under different managemental conditions. Vet. World, 2: 413-417.
RADOSTITS, O.M., BLOOD, D.C. AND GAY, C.C., 1994. Veterinary medicine. A textbook of diseases of cattle, sheep, pig, goat and horses. 7th Ed. Bath Press Avon,Great Britain. 38-106, 1311-1367.
RAFIQUE, S., QUDOOS, A., ALVI, A.S. AND HAYAT, C.S.,1997. Parasitic infection of sheep and goats in Quetta and Kalat areas of Baluchistan. Pak. Vet. J., 17: 94-97.
RAZA, MA., MURTAZA, S., BACHAYA, HA., DASTAGER, G. AND HUSSAIN, A., 2009. Point prevalence of haemonchosis in sheep and goats slaughtered at Multan abattoir. J. Anim. Pl. Sci., 19: 158-159.
RAZZAQ, A., RAFIQUE, S. AND TAREEN, S., 2002. Incidence of internal parasites in sheep and goat at Asghara valley district Ziarat. Baluchistan J. agric. Sci.,3: 43-50.
SAJID, M.S., ANWA, A.H., IQBAL, Z., KHAN, M.N. AND QUDOOS, A., 1999. Some epidemiological aspects of gastrointestinal nematodes of sheep. Int. J. Agric. Biol.,1: 306-308.
SHIMELIS, D., ASMARE, A. AND WUDU, T., 2011.Epidemiology of gastrointestinal helminthiasis of small ruminants in selected sites of North Gondar zone, Northwest Ethiopia. Ethiop.Vet. J., 15: 57-68.
SILVA, J.B., FAGUNDES, G.M. AND FONSECA, A.H.,2011. Dynamics of gastrointestinal parasitoses in goats kept in organic and conventional production systems in Brazil. Small Rum. Res., 98: 35-38.
SINGH, D.C., SWAMKAR, P., KHAN, FA., SRIVASTAVA, C.P. AND BHAGWAN, PSK., 1997. Epidemiology of ovine gastrointestinal nematodes at an organized farm in Rajasthan, India. Small. Rum. Res., 26: 3 l-37.
SOULSBY, E.J.L., 1965. Textbook of veterinary clinical parasitology. Vol. 1. Helminths. Blackwell, Oxford, pp.1120.
SOULSBY, E.J.L., 1982. Helmenths, Arthropods and protozoa of domesticated Animals. 7th edition. The English Liguar Book Society and Bailliere Tindal, London, pp.765-766.
SOULSBY, E.J.L., 2005. Helminths, arthropods and protozoa of domesticated animals. 7th ed. Bailliere Tindall.Delhi, pp. 232-233.
STEEL, J.W. AND SYMONS, L.E.A., 1982. Nitrogen metabolism in nematodiasis of sheep in relation to productivity. In: Biology and control of endoparasites (eds. L.E.A. Symons, A.D. Donald and J.K. Dineen). Academic Press, Sydney, pp. 235 -256.
SUAREZ, V.H. AND BUSETTI, M.R., 1995. The Epidemiology of helminth infections of growing sheep in Argentina's Western Pampas. Int. J. Parastol., 25:489-494.
TASAWAR, Z., NAZ, F., LASHARI, M.H. AND HAYAT, CS., 2011. Prevalence of ostertagia spp., in a sheep herd. Sarhad J. Agric., 27: 275-278.
TEFERA M, G BATU, M. AND BITEW, 2011. Prevalence of gastrointestinal parasites of sheep and goats in and around Bedelle, South-Western Ethiopia. Int. J. Vet. Med., 8: 60-65.
UMUR, S. AND YUKARI, BA., 2005. An abattoir survey of gastrointestinal nematodes in sheep in the Burder region, Turkey. Turk J. Vet. Anim. Sci., 29: 1195-1201.
URQUHART, GM., ARMOUR, J., DUNCAN, J.L. AND JENNINGS, F.W., 1996. Veterinary parasitology. 2nd Ed. The Faculty of Veterinary Medicine, University of Glasgow, Scotland. pp. 19-34,131, 133 and 225.VLASSOFF A, BISSIET, S.A. AND MCMURTRY, L.M.,1999. Faecal egg counts in Angora goats following natural or experimental challenge with nematode parasites; within-flock variability and repeatability. Vet. Parasitol., 84: 113-123.
VLASSOFF A, LEATHWICK DM. AND HEALTH, ACG., 2001. The epidemiology of nematode infection in sheep. N. Z. Vet. J., 49: 213-222.
WALL, PJ., MARTIN, LR., LJUNGSTRONM, BL., RYDZIK, A., 2004. Epidemiology of abomasal nematodes of sheep in Sweden with particular reference to over- winter survival strategies. Vet. Para., 122: 207-220.
YAMAGUTI, S., 1961. Systema Helminthum. Vol. III. The nematodes of vertebrates (Part I, II). Inter Science Publisher Inc., New York, 1261.
ZERYEHUN, T., 2012. Helminthosis of sheep and goats in and around Haramaya, Southeastern Ethiopia. J. Vet. Med. Anim. Hlth., 4: 48-55.
1Livestock and Dairy Development Department, Spiny Road, Quetta, Balochistan
2Department of Parasitology, University of Veterinary and Animal Sciences, Outfall Road, Lahore, Punjab
3Centre for Advanced Studies in Vaccinology and Biotechnology, University of Balochistan, Brewery Road, Quetta
4Arid Zone Research Centre, Pakistan Agriculture Research Council, Western Bypass, Quetta, Balochistan
5Department of Parasitology, University of Balochistan, Seryab Road, Quetta, Pakistan
Corresponding author: email@example.com 0030-9923/2013/0006-1669 $ 8.00/0 Copyright 2013 Zoological Society of Pakistan
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|Author:||Kakar, Hamdullah; Lateef, Mohammad; Maqbool, Azhar; Jabbar, Makhdoom Abdul; Abbas, Farhat; Jan, Saad|
|Publication:||Pakistan Journal of Zoology|
|Date:||Dec 31, 2013|
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