Introduction

Goats are one of the earliest domesticated ruminants which have served mankind longer than cattle and sheep. It is reared for the production of milk, meat and hair, particularly in arid, semi-tropical or mountainous areas. In temperate, tropical and sub-tropical zones, goats are kept often as supplementary animals by small farmers. Helminthiosis, especially parasitic gastro-enteritis, constitutes to pose a serious health threat and a limitation to the productivity of small ruminants due to the associated morbidity, mortality, cost of treatment and control measures (Nwosu et al. 2007). The climate in a certain locality is one of the factors that determine the type and severity of parasitic infections in goats. In Jammu and Kashmir State, the incidence of parasitic infection in goats from Jammu region has been reported by Khajuria and Kapoor (2003) and by Yadav et al. (2006) and from Kashmir Valley, a single study done so far is on record by Tariq et al. (2010). Therefore, there is a need to carry out further studies on regional basis to determine GastroIntestinal (GI) helminths burden so as to evolve the package of practices for control of these parasites in order to prevent economic losses. So, the present study was undertaken to work out the prevalence of GI helminths of goats of Kashmir Valley.

Materials and methods

Study area: The study was restricted to Govt. Farms of twin districts of Bandipora and Ganderbal and locally reared goats of district Baramulla of the Valley over a period of one year from December 2011 to November 2012. The Farms included Mountain Research Centre for Sheep and Goat, Shuhama, Ganderbal and Govt. Sheep Breeding Farm, Hardshua, Bandipora. Ganderbal is located in north east of Kashmir, lying between latitude 34.7°–34.22°N and longitude 74.4°–74.56°E, at an average altitude of 5100 ft. above sea level. Climatically winters are extremely cold with heavy snowfall while as summers are pleasant. The mean temperature, rainfall and relative humidity ranged from 1 to 30 °C, 39 to 81 mm and 51 to 90%, respectively. Bandipora comprises of three tehsils and is situated at 34.25°N and 74.38°E with an average altitude of 5541 ft above sea level. The climate is of temperate type with cold snowy winters and pleasant weather in summer. Baramulla covers an area of 3353 sq. km and is situated at an average height of 5226 ft. above sea level and at 74.3°E longitude and 34.2°N latitude. Average minimum and maximum temperature varied from −2.08 to 16 °C. The average annual rainfall was 100.89 mm.

Parasitological examination: A total of 1016 samples were collected during all the four seasons of the Valley viz; Winter (December–February), Spring (March–May), Summer (June–August), and Autumn (September–November). The samples were collected directly from rectum and brought to the laboratory in mini polythene bags for examination. The samples were collected from either sex and included both the age groups viz; adult goats (age > 1 year) and young goats (age < 1 year). Samples were first examined grossly for colour, consistency, presence of blood, mucous and dead worms. Then these were examined by standard sedimentation and floatation techniques (Soulsby 1982). Randomly selected positive faecal samples in each season were then examined by quantitative technique (Stoll’s dilution method) to determine the parasitic load i.e. eggs per gram of faeces. Faecal samples positive for strongyle eggs were also subjected to coproculture randomly using jar and petridish methods in each season and the third stage larvae were harvested to find out prevalence of different genera of strongyle worms.

Stastical analysis: The results were subjected to standard statistical analysis as per Snedecor and Cochran (1994). The data on the prevalence between different seasons and groups, which included males and females, adult and young goats was analyzed using ‘Z’ test. Mean EPG between different groups on different dates was compared using ANOVA and LSD.

Results and discussion

The prevalence of GI helminths was studied taking into consideration the overall prevalence, seasonal prevalence, age wise prevalence and sex wise prevalence in goats of Kashmir Valley.

Overall Prevalence: The overall prevalence of GI Helminths was found to be 74.70%. This is in accordance with Khajuria and Kapoor (2003) who recorded the overall prevalence of 78.82% for various parasites found in goats of Kathua region of J&K. Sutar et al. (2010) and Hassan et al. (2011) reported prevalence of 62.75 and 63.00% in the goats of Maharashtra and Chittagong respectively. Pathak and Pal (2008) reported prevalence of 85.22% in goats of Durg district of Chhattisgarh. The variation in the present study might be attributed due to the differences among the geographical locations and climatic conditions of the study areas, method of study, sample size, breed of the animals and managemental practices involved. Prevalence of platyhelminths was found to be 14.76% with trematodes in 8.07% animals. Among trematodes, prevalence of Dicrocoelium spp. (3.44%) was highest followed by paramphistomes (3.05%) and Fasciola spp. (2.75%). Among cestodes the only genus reported was Moniezia spp. with a prevalence rate of 9.44%. Sharma et al. (1989) reported 14.8% prevalence of Fasciola spp. infection in goats of Kashmir Valley while as Khajuria and Kapoor (2003) had recorded the incidence of 5.83% of Fasciola spp. in goats in Kathua region of Jammu. Jithendran (1996) found 4.1% of goats from Kangra valley of Himachal Pradesh positive for Dicrocoeliosis, whereas Khajuria and Kapoor (2003) reported prevalence of Dicrocoelium spp. in goats of Kathua region of Jammu as 2.55%. Khajuria et al. (2013) recorded a prevalence of 5.4% of Paramphistomes in stationary goat flocks of the middle agro-climatic zone of Jammu province. Khajuria and Kapoor (2003) reported Moniezia spp. infections in goats of Kathua district of Jammu. Pathak and Pal (2008) and Nath et al. (2011) reported prevalence of Moniezia spp. to be 17.04 and 11.33% in goats of Durg district of Chattisgarh and in Black Bengal goats in Chittagong, Bangladesh respectively. The reason for low prevalence of platyhelminth infection can be due to the fact that the animals are mostly stall fed. These animals are not allowed to graze in the open, thus exposure of animals to the snails is avoided, and hence low infection was reported in the present study. Nemathelminths were found in 70.07% samples with strongyle worms including Nematodirus spp. (68.30%) being highest followed by Strongyloides spp. (5.90%) and Trichuris spp. (4.29%) (Table 1). Tariq et al. (2010) reported prevalence of gastrointestinal nematodes to be 54.3% while examining goats from Kashmir valley respectively. Prevalence of 77.31% was reported by Pal papri and Bandyopadhyay (2004) and Jithendran (1998) during a study on GI Nematodosis in goats in Sikkim. Predominance of strongyle infection to the tune of 67.46 and 44.62% was reported by Khajuria and Kapoor (2003) and Yadav et al. (2006) respectively in the Jammu region of J&K. Khajuria and Kapoor (2003) recorded the prevalence of Trichuris spp. to be 8.11% in goats of Kathua region of Jammu. Prevalence of 6.45, 3.5 and 3.08% for Trichuris spp. has been reported by Palampalle et al. (2002), Hassan et al. (2011) and Yadav et al. (2006) respectively. The higher prevalence of nemathelminth parasites in the present study can be due to the fact that these animals are kept in close confinement, stall fed, which increases the temperature and moisture of the shed. This makes the conditions favourable for the hatching of the nematode eggs and completions of life cycle in a short period of time. This close confinement also increases the chances of transmission of infection from an infected animal to other healthy animals.

Table 1 Overall prevalence of GI helminths of goats in Kashmir Valley
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Seasonal Prevalence: Highest prevalence of GI helminths was observed in summer (78.03%) followed by spring, winter and autumn (75.39, 74.90 and 70.47% respectively), the difference being non-significant (P > 0.05). This is in accordance with the findings recorded by Makhdoomi et al. (1995) in sheep in Kashmir valley and Khajuria and Kapoor (2003) in goats in Kathua region of J&K. Sutar et al. (2010) reported higher prevalence in monsoon season (77.33%) followed by winter (60.83%) and summer (51.53%) in goats of Ahmednagar district of Maharashtra. Climatic factors influence the rate of larval movement. Hawkins (1945) suggested that heavy rainfall lower the resistance of animals and this is taken as advantage by the infective larvae in establishment of heavy infection. Platyhelminth infection (20.00%) was observed highest in winter followed by 15.07, 12.54 and 11.41% in spring, summer and autumn respectively, the variation being statistically non-significant (P > 0.05). Owing to the prolonged-staged life cycle of the platyhelminths, the animals are exposed to infection during the vulnerable months of summer and autumn and while completing the stages of life cycle, the parasite reaches its sexual maturity during winter months and as harsh conditions of winter lowers the immune resistance of the animal, the platyhelminth infection increases. Trematodes showed non-significantly (P > 0.05) highest prevalence in winter (10.19%) followed by summer, autumn and spring with prevalence rate of 7.84, 7.48 and 6.74% respectively. Among trematodes, Dicrocoelium spp. and Fasciola spp. showed highest prevalence in winter followed by spring, autumn and summer. Dicrocoelium spp. infection being highest in winter is in correspondence with the study of Jithendran (1996) and Godara et al. (2014) who recorded prevalence of Dicrocoelium spp. in goats of Kangra valley of Himachal Pradesh (4.1%) and Jammu (28.9%) respectively. The seasonal trend shown by Fasciola spp. in the present study is in accordance with Khallaayoune and Hari (1991) and Kumar et al. (2007) in goats of Haouz area of Morocco (23.8%) and of Uttaranchal (2.62%). Paramphistomes showed a different seasonal pattern with highest prevalence in summer followed by autumn, spring and winter. Goats being browsers exhibit lesser infection of paramphistomes than other ruminants. Khajuria and Kapoor (2003) could not detect any ova of paramphistomes in goats of Kathua region of Jammu. Summers being the drier months of the year, lead to concentration of snails in an around the areas of natural waters. This coincides with the grazing area of the animal and hence increased influx of infection to the animals. The prevalence of trematodes with respect to their seasons differed non-significantly (P > 0.05). Moniezia spp. showed highest prevalence rate in winter (12.54%) and lowest in autumn (5.90%). 11.11 and 8.23% was its prevalence in spring and summer seasons respectively, the variation being non-significant (P > 0.05). The prevalence of Nemathelminth parasites was recorded highest in summer (75.68%) followed by spring (71.82%), autumn (68.50%) and winter (64.31%), however the variation was non-significant (P > 0.05). The same trend was observed for strongyle worms. The prevalence of Strongyloides spp. and Trichuris spp. was highest in summer followed by autumn, spring and winter. The prevalence of these nematodes differed non-significantly (P > 0.05) with respect to their seasons (Table 2). After a winter period, spring rise is evident which reaches to maximum in summer and again drops to low levels in autumn. The rainy season starting in spring and continuing to early summer makes environmental conditions more favourable for the development and survival of pre-parasitic stages of nematodes and led to an increased availability of infective larvae in the rainy and post rainy seasons. This seasonal variation and trend is in line with the results of Tariq et al. (2010) and Khajuria and Kapoor (2003).

Table 2 Seasonal prevalence of GI helminths of goats in Kashmir Valley
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Agewise Prevalence: Overall prevalence was found more in adults (77.85%) compared to young ones (67.42%). The study revealed significant statistical difference between the two age groups (P < 0.05). Hassan et al. (2011) reported the similar findings while determining prevalence of GI helminths in Black Bengal goats of Chittagong, Bangladesh. Shahnawaz et al. (2011) and Wani et al. (2011) also reported the high prevalence of GI platyhelminths and nemathelminths, respectively in adult sheep than in young in Kashmir valley. The prevalence of platyhelminths was found non-significantly (P > 0.05) higher in adults (15.51%) compared to the young (13.02%). Higher trematode infection was found in adults (9.59%) as compared to young (4.56%), the difference being significant (P < 0.05). Dicrocoelium spp., Fasciola spp. and paramphistomes were also found higher in adults compared to young, the variation being statistically significant (P < 0.05). The higher infection in adults may be attributed to the cause that adults graze in the low land area where by increasing the possibility of incurring more infection. Moniezia spp. showed different trend with higher prevalence in young goats (13.02%) compared to adults (7.89%), the variation being statistically significant (P < 0.05). Previous infection and age of the host afford some protection against reinfection and hence disease is usually seen in young animals (Soulsby 1982). Nemathelminths were found higher in adults (72.63%) than young (64.19%), the variation being significant (P < 0.05). Among nemathelminth parasites, strongyle worms were also found significantly higher (P < 0.05) in adults than young goats. Strongyloides and Trichuris spp. also followed the same trend with higher prevalence rate in adults compared to young, the variation being non-significant (P > 0.05) (Table 1). Decreased young one infection may also be associated with the intake of immunoglobin rich colostrum which increases the immunity of the young animals.

Sexwise Prevalence: 66.12 and 75.89% males and females were found positive for GI helminths respectively, the variation being non-significant (P > 0.05). The prevalence of platyhelminths was found non-significantly (P > 0.05) higher in females (15.24%) compared to males (11.29%). Trematodes were found higher in females (8.29%) as compared to males (6.45%), the variation being non-significant (P > 0.05). Dicrocoelium spp., paramphistomes and Fasciola spp. were found higher in females than males, the variation being non-significant (P > 0.05). Moniezia spp. followed similar trend with higher prevalence in females (9.97%) than males (5.64%), the variation being non-significant (P > 0.05). Nemathelminths were found non-significantly (P > 0.05) higher in females (70.85%) compared to males (64.51%). Strongyle worms followed a similar pattern with non-significantly (P > 0.05) higher prevalence in females compared to males. However, Strongyloides and Trichuris spp. followed a different trend with higher prevalence rate in males than females, the variation being non-significant (P > 0.05) (Table 3). Patel et al. (2001) and Shahiduzzaman et al. (2003) observed the similar trend of higher infection in female goats than males. However Gorsky et al. (2004) reported that males were more infected with nematode species than females. Moreover Tariq et al. (2010) did not find any difference in the susceptibility to the nematode infection between sexes in Valley. The reason for higher EPG in females is because females experience periparturient rise in faecal egg counts due to pregnancy and lactation stress. In lactating animals there is also marked increase in susceptibility to newly acquired infection in the periparturient period (Shubber et al. 1981).

Table 3 Sex-wise prevalence of GI helminths of goats in Kashmir Valley
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Intensity of Infection: EPG ranged from 0 to 1500 with an average EPG count of 312.7 ± 17.76 (Table 4). EPG was found highest in summer followed by spring, autumn and winter. The study revealed a statistical difference of summer with all the other seasons (P < 0.05). Spring season was found to have a statistical difference with summer and winter (P < 0.05). Autumn season was found to show statistical difference with summer (P < 0.05). The winter season was found to show statistical difference with summer and spring seasons (P < 0.05) (Table 5). The similar seasonal trend of mean EPG was observed by Tariq et al. (2010) with the mean EPG of 2552.3 ± 85.7 in summer and 134.1 ± 9.1 in winter. Palpari and Bandyopadhyay (2004) however reported higher mean EPG of 3500 in autumn and least mean EPG of 150 in winter. The findings of high EPG in summer correlates with the agro-climatic conditions of the Valley. The Valley being temperate in climate with a marked difference in the four seasons influence the occurrence of infection in the goats. Valley observes maximum rainfall in late spring which increases the chances of hatching and dissemination of larvae. Similarly in winters the inhibitory signals in the form of high precipitation and hypobiosis leads to decreased availability of the infective larvae and eggs to the animals. Moreover less contact of animals with grassland during autumn and winter reduces the chance of infection. EPG ranged from 0 to 1500 in both the age groups but the average EPG was 274.57 ± 32.0 and 332.7 ± 21.0 in young and adult goats, respectively. The figures indicate higher average EPG in adult goats than young ones, the variation being statistically non-significant (P > 0.05) (Table 4). In females and males EPG ranged from 0 to 1500 and 0 to 1400, respectively with an average of 316.8 ± 21.4 and 302.1 ± 39.7, respectively. Average EPG was found higher in females than males, but the variation was non-significant (P > 0.05) (Table 6).

Table 4 Overall parasitic load of GI helminths of goats in Kashmir Valley
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Table 5 Seasonal comparison of parasitic load of GI helminths of goats in Kashmir Valley
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Table 6 Sex-wise parasitic load of GI helminths of goats in Kashmir Valley
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Coproculture Examination: On coprocultural examination, Haemonchus spp. (71.05%) was found to be the predominant strongyle worm followed by Trichostrongylus spp. (12.86%), Chabertia spp. (8.47%) and Ostertagia spp. (7.62%). This predominance of Haemonchus spp. over the other strongyle worms has also been reported by Tariq et al. (2010) and Wani et al. (2011) in goats and sheep of Kashmir valley respectively. This is because of the fact that the females of Haemonchus spp. are prolific egg layers (Urquhart et al. 1996) and infective stages of Haemonchus spp. survive for prolonged periods on pastures (Soulsby 1982). However, Saiful-Islam and Taimur (2008) has reported predominance of Trichostrongylus spp. over other strongyle worms in goats in Bangladesh.