Occurrence of GI parasites in ruminants of Kashmir and Ladakh

Abstract

The study was conducted in Kashmir and Ladakh Divisions of the erstwhile state of Jammu and Kashmir to work out the occurrence of gastrointestinal parasites in ruminants. The qualitative faecal examination of 476 samples revealed an overall prevalence of GI parasites to the tune of 80.04% comprising of 80.61% in cattle, 96.70% in sheep and 66.27% in goats. In Kashmir overall prevalence of GI parasites was 88.33% comprising of 80.61% in cattle, 98.41% in sheep and 100% in goats. Highest prevalence was observed for strongyles (84.00%) followed by Eimeria spp. (31.67%), Moniezia spp. (20.00%), Ascaris spp. (5.33%) and Strongyloides spp. (1.67%). Mixed infection was observed in 37.67% samples. In cattle, the parasites observed were strongyles (68.37%) and Eimeria spp. (13.27%) with mixed infection in 1.02% samples. In sheep highest prevalence was observed for strongylid eggs (97.88%) followed by Eimeria spp. (43.38%), Moniezia spp. (31.74%), Ascaris spp. (8.47%) and Strongyloides spp. (2.64%) with mixed infection in 59.26% samples. Amongst goats, only strongylid eggs (100%) were observed. In Ladakh region overall prevalence of GI parasites was 65.91% with 82.61% in sheep and 63.40% in pashmina goats. Highest prevalence was observed for Eimeria spp. (63.64%) followed by strongyles (9.09%) Moniezia spp. (5.11%) and Thysanosoma spp. (1.14%). Mixed infection was observed in 13.07% samples. In sheep, highest prevalence was observed for Eimeria spp. (73.91%) followed by strongyles (17.39%) and Thysanosoma spp. (8.70%) with mixed infection in 17.39% samples. In pashmina goats, the prevalence of Eimeria spp. (62.09%) was observed highest followed by strongylid eggs (7.84%) and Moniezia spp. (5.88%) with mixed infection in 12.42% samples.

Introduction

Gastrointestinal (GI) helminths, a serious constraint to the productivity of ruminants induce losses in terms of morbidity, mortality, costs incurred on their treatment and control (Lashari and Tasawar 2011). It is well established fact that controlling parasitic infections in animals can substantially increase their body weight and productivity (Fitzpatrick 2013). In order to develop suitable control measures for parasitic diseases there is a need to map out the parasitic fauna from every geographic zone of the world as local climatic conditions of an area and the prevailing managemental practices mainly affect the prevalence of parasites. From Kashmir valley, several workers have reported the incidence of parasitic infection in ruminants (Wani et al. 2011; Shahnawaz et al. 2011; Bushra et al. 2013; Tramboo et al. 2015; Aiman et al. 2017; Bihaqi et al. 2017; Allaie et al. 2018; Maqbool et al. 2018; Shah et al. 2019a, b), while due to the inclement weather, no transport facility, and very remoteness of the Ladakh region from Srinagar city, only few studies by Kuchai et al. (2011, 2012) and Maqbool et al. (2016) are on record till date. Keeping this background information in mind, the present study was conducted to work out the prevalence of GI parasites of ruminants in Kashmir and Ladakh Divisions of the erstwhile state of Jammu and Kashmir.

Materials and methods

Study area

The study on prevalence of GI parasites of ruminants was carried out in Kashmir province that constituted Kashmir and Ladakh regions in the erstwhile state of J&K. Kashmir valley located in the lap of Pir Panjal and the Zanskar range has latitude and longitude of 33.27 and 76.2519, respectively, and is spread for about 15,220 sq. km with average height of 1850 m above the sea level. Temperate cum Mediterranean type of climate is observed in the valley, but in the higher reaches, the temperature remains cold throughout the year. Ladakh being one of the highest places on earth with average altitude of about 12,000 feet constitutes the easternmost part of the erstwhile state of Jammu and Kashmir and covers about 117,000 sq. km area. Climate of Ladakh is characterized by extremely cold winters followed by heavy snowfall, but it hardly rains there owing to the presence of the lofty surrounding mountainous ranges. The average temperature during summers and winters in Ladakh ranges approximately from − 3 to 30 °C and − 20 to 15 °C, respectively. This area remains cut off from J&K during most parts of the year due to blockage of roads by snow and avalanches.

Parasitological examination

For working out the prevalence of GI parasites, samples were collected randomly. A total of 476 faecal samples (300 from Kashmir & 176 from Ladakh) were collected directly from the rectum in mini polythene bags, which were then brought to the Divisional Helminthology laboratory, SKUAST-K, for examination. Gross examination of samples was first carried out followed by standard sedimentation and floatation techniques (Soulsby 1982).

Results and discussion

An overall prevalence of GI parasites in ruminants was observed to be 80.04% comprising of 80.61% in cattle, 96.70% in sheep and 66.27% in goats (Table 1). The present study revealed presence of strongyles, Eimeria spp., Moniezia spp., Ascaris spp., Strongyloides spp. & Thysanosoma spp. in ruminants  (Fig. 1).

Table 1.

Prevalence of GI parasites in ruminants of Kashmir & Ladakh

Region	Parasites	Hosts (n = animals examined)
		Cattle	Sheep	Goats	Overall
Kashmir		(n = 98)	(n = 189)	(n = 13)	(n = 300)
	Moniezia spp.	0	60 (31.74)	0	60 (20.00)
	Ascaris spp.	0	16 (8.47)	0	16 (5.33)
	Strongyles	67 (68.37)	185 (97.88)	13 (100.00)	252 (84.00)
	Strongyloides spp.	0	5 (2.64)	0	5 (1.67)
	Eimeria spp.	13 (13.27)	82 (43.38)	0	95 (31.67)
	Mixed	1 (1.02)	112 (59.26)	0	113 (37.67)
	Overall (A)	79 (80.61)	186 (98.41)	13 (100.00)	265 (88.33)
Ladakh		(n = 0)	(n = 23)	(n = 153)	(n = 176)
	Moniezia spp.		0	9 (5.88)	9 (5.11)
	Thysanosoma spp.		2 (8.70)	0	2 (1.14)
	Strongyles		4 (17.39)	12 (7.84)	16 (9.09)
	Eimeria spp.		17 (73.91)	95 (62.09)	112 (63.64)
	Mixed		4 (17.39)	19 (12.42)	23 (13.07)
	Overall (B)		19 (82.61)	97 (63.40)	116 (65.91)
Overall (A + B)		79 (80.61)	205 (96.70)	110 (66.27)	381 (80.04)

Figures in the parenthesis indicate per cent prevalence

Fig. 1.

Different types of parasitic eggs/oocysts in ruminants of Kashmir & Ladakh

In Kashmir 88.33% prevalence of GI parasites was recorded which comprised of 80.61% in cattle, 98.41% in sheep and 100% in goats (Table 1). Highest prevalence was observed for strongyles (84.00%) followed by Eimeria spp. (31.67%), Moniezia spp. (20.00%), Ascaris spp. (5.33%) and Strongyloides spp. (1.67%). Mixed infection was observed in 37.67% samples (Table 1). In cattle, highest prevalence was observed for strongyles followed by Eimeria spp. Mixed infection was found in 1.02% samples (Table 1). The observed prevalence of strongyles in the present study is almost similar to Bushra et al. (2013) and Maqbool et al. (2018), who observed strongylid eggs to the tune of 73.85% and 62.85% in cattle of central and southern Kashmir, respectively. Aiman et al. (2017) and Shah et al. (2019a) reported lower prevalence of strongylid eggs (49.91 and 31.19%) among cattle of northern zone and marshy areas of Kashmir valley, respectively, compared to the present study. Prevalence of strongylid eggs in the present study is higher because of the fact that strongyle worms are prolific egg layers and take lesser time for completion of life cycle and thus grazing areas become heavily infected with the larvae of strongyle worms within fortnight period. In the present study, the prevalence of Eimeria spp. differ from Pandit et al. (2004) (73.20%) in cattle of Kashmir valley. In sheep highest prevalence was observed for strongylid eggs followed by Eimeria spp., Moniezia spp., Ascaris spp. and Strongyloides spp. Mixed infection was found in 59.26% samples (Table 1). Prevalence of strongyles recorded in this study is higher than observed by Bhat et al. (2012), Tramboo et al. (2015) and Allaie et al. (2018), who reported 24.61, 57.75 and 72.85% prevalence of strongylid eggs in the ovine population of Kashmir valley, Budgam district and among small ruminants of Kashmir valley, respectively. The observed prevalence of Eimeria spp. also differed from those of Rehman et al. (2011), Reshi and Tak (2014), who observed higher prevalence of Eimeria spp. (55.99 and 54.68%, respectively), in goats of Pakistan and sheep of Kashmir, respectively. However, Bhat et al. (2012) and Maqbool et al. (2016) reported prevalence of Eimeria spp. (9.8 & 28.33%, respectively) in ovine of Kashmir and Pashmina goats of Ladakh, respectively, which is lower as compared to the present study. The observed Moniezia spp. prevalence is in contradiction to that of Pandit et al. (2003), Shahnawaz et al. (2011) and Tramboo et al. (2015), who recorded Moniezia spp. prevalence to the tune of 9.03, 11.83 and 7.92%, respectively in ovine population from different regions of Kashmir valley. In the present study, occurrence of Ascaris spp. in sheep correlates well with the fact that Ascaris worms occur occasionally in the small intestines of sheep and lambs in Europe and America, and they have been considered by some to belong to a distinct species, namely Ascaris ovis Rudolphi, and by others to be identical with Ascaris lumbricoides Linnaeus (Goodey 1926). Majority of the helminthologists attribute it to A. lumbricoides (Ransom 1911; Ransom and Foster 1920), but others hold a different view, in fact Neuveu-Lemaire (1923) reported a single specimen of Ascaris from a goat as Ascaris ovis. Goodey (1926) collected adult Ascarids from sheep at an abattoir in London and identified them as A. lumbricoides. Goodey (1926) further concluded that there is no distinct species A. ovis and that the worms occurring occasionally in sheep are morphologically identical with A. lumbricoides, which can attain sexual maturity in the sheep as a host and that the eggs can become fertilised and can carry on the race. Infact Schwartz (1925) records the occurrence of A. lumbricoides in the small intestines of a calf slaughtered at Illinois, USA, thereby confirming it to be the first authentic report of the species from a bovine host. The list of hosts for A. lumbricoides published by Goodey (1926) is man, chimpanzee, orang-outang, pig, sheep, cattle, and squirrels. The prevalence of Ascaris spp. reported in the present study is in line with Owhoeli et al. (2014), who reported almost similar incidence of 8.3% among indigenous goats slaughtered in selected Abattoirs in Nigeria. However, results differed from those of Ibukun and Oludunsin (2015) and Owhoeli et al. (2014), who recorded prevalence of 1.8% and 2.6% in sheep and slaughtered exotic goats in North central and south Nigeria, respectively. Prevalence of Strongyloides spp. is in close approximation with Yadav et al. (2006) in Jammu region (1.15%), but differ from Pandit et al. (2003), Sharma et al. (2007) and Bihaqi et al. (2017), who observed Strongyloides spp. prevalence as 22.9, 16.66 and 5.90% in sheep of Kashmir, Palam valley of northwestern Himalayan region and among goats of Kashmir, respectively. In goats the only observed eggs were of strongyle type with 100% prevalence (Table 1), which differed from that of Bihaqi et al. (2017), who reported prevalence of strongylid eggs to the tune of 68.03% in caprines of Kashmir.

In Ladakh region overall prevalence of GI parasites was 65.91% with 82.61% in sheep and 63.40% in pashmina goats (Table 1). Highest prevalence was observed for Eimeria spp. (63.64%) followed by strongyles (9.09%) Moniezia spp. (5.11%) and Thysanosoma spp. (1.14%). Mixed infection was observed in 13.07% samples (Table 1). An overall prevalence of 68.54% of GI parasites in sheep of Jammu region has also been reported by Khajuria et al. (2013). However, results showed variation from Tramboo et al. (2015) and Shah et al. (2019b), who have recorded prevalence of GI parasites as 77.00 and 41.90% in ovine population of district Budgam and small ruminants of marshy areas of Kashmir valley, respectively. The prevalence of GI parasites in pashmina goats showed variation from Kuchai et al. (2012), Maqbool et al. (2016) and Bihaqi et al. (2017), who observed prevalence of GI parasites to the tune of 31.42, 56.66 and 74.70% in pashmina goats of Ladakh and among goats of Kashmir valley, respectively. Amongst sheep highest prevalence was observed for Eimeria spp. followed by strongyles and Thysanosoma spp. Mixed infection was found in 17.39% samples (Table 1). The observed prevalence of Eimeria spp. is in line with that of Verma et al. (2017), who recorded 73.85% overall prevalence of Eimeria spp. in goats of west Uttar Pradesh. However, results differed from those of Rehman et al. (2011), Reshi and Tak (2014) and Maqbool et al. (2016), who observed prevalence of Eimeria spp. as 55.99, 54.68 and 28.33% in goats of Pakistan, sheep of Kashmir and pashmina goats of Ladakh, respectively. A lower prevalence of strongylid eggs has been recorded as compared to the findings of Bihaqi et al. (2017) and Allaie et al. (2018), who have reported prevalence of strongylid eggs to the tune of 68.30 and 72.85% in goats and small ruminants of Kashmir, respectively. Among pashmina goats highest prevalence was observed for Eimeria spp. followed by strongyles and Moniezia spp. Mixed infection was found in 12.42% samples (Table 1). The results showed variation from Maqbool et al. (2016), who reported prevalence of Eimeria spp. to the tune of 28.33%, 26.66% strongylid eggs and 15.00% Moniezia spp. among pashmina goats of Ladakh region. The observed prevalence of strongyles also differs from that of Bihaqi et al. (2017) and Allaie et al. (2018), who observed prevalence of strongyles as 68.30 and 72.85%, respectively in Kashmir.

Conclusion

The present study revealed prevalence of GI parasites in ruminants of Kashmir (Moniezia spp., Ascaris spp., strongyles, Strongyloides spp. & Eimeria spp.) and Ladakh (Moniezia spp., Thysanosoma spp., Strongyles and Eimeria spp.) regions of erstwhile state of Jammu and Kashmir. Hence it is concluded that appropriate managemental practices be adopted including use of those anthelmintics/anticoccidials which are effective against GI helminths/coccidia therapeutically as well as prophylactically to prevent production losses.

Authors’ contributions

Authorship order among AA & SRT was determined alphabetically as they contributed equally in this work by processing and examining the samples; IMA collected some samples; compiled the data & prepared the manuscript; KHB & RAS assisted in identification of parasitic stages; ZAW & IM assisted in preparation of the manuscript and FDS collected some samples from Ladakh.

Declarations

Conflict of interest

The authors declare that there is no conflicts of interest.

Ethical standards

The authors declare that the study was conducted on naturally infected animals in the field. As no experimental infection was established during this research work, so there was no need to take the approval for execution of the work from animal ethics committee. The animals belonged to the local farmers, and they had given full consent for this research work.