J Parasit Dis

https://doi.org/10.1007/s12639-021-01437-3

ORIGINAL ARTICLE

Occurrence of GI parasites in ruminants of Kashmir and Ladakh

A. Ashraf1 • S. R. Tramboo1 • I. Maqbool2 • I. M. Allaie1 • K. H. Bulbul1 •

R. A. Shahardar1 • Z. A. Wani1 • F. D. Sheikh3

Received: 14 September 2020 / Accepted: 7 August 2021

Ó Indian Society for Parasitology 2021

Abstract The study was conducted in Kashmir and Highest prevalence was observed for strongyles (84.00%)
Ladakh Divisions of the erstwhile state of Jammu and followed by Eimeria spp. (31.67%), Moniezia spp.
Kashmir to work out the occurrence of gastrointestinal (20.00%), Ascaris spp. (5.33%) and Strongyloides spp.
parasites in ruminants. The qualitative faecal examination (1.67%). Mixed infection was observed in 37.67% samples.
of 476 samples revealed an overall prevalence of GI par- In cattle, the parasites observed were strongyles (68.37%)
asites to the tune of 80.04% comprising of 80.61% in and Eimeria spp. (13.27%) with mixed infection in 1.02%
cattle, 96.70% in sheep and 66.27% in goats. In Kashmir samples. In sheep highest prevalence was observed for
overall prevalence of GI parasites was 88.33% comprising strongylid eggs (97.88%) followed by Eimeria spp.
of 80.61% in cattle, 98.41% in sheep and 100% in goats. (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
& I. M. Allaie (100%) were observed. In Ladakh region overall preva-
idreesmehraj@skuastkashmir.ac.in lence of GI parasites was 65.91% with 82.61% in sheep
A. Ashraf and 63.40% in pashmina goats. Highest prevalence was
aimanashrafmir@gmail.com observed for Eimeria spp. (63.64%) followed by strongyles
S. R. Tramboo (9.09%) Moniezia spp. (5.11%) and Thysanosoma spp.
shahanatramboo@gmail.com (1.14%). Mixed infection was observed in 13.07% samples.
I. Maqbool In sheep, highest prevalence was observed for Eimeria spp.
naikirshad919@gmail.com (73.91%) followed by strongyles (17.39%) and Thysano-
K. H. Bulbul soma spp. (8.70%) with mixed infection in 17.39% sam-
drkhbulbul@gmail.com ples. In pashmina goats, the prevalence of Eimeria spp.
R. A. Shahardar (62.09%) was observed highest followed by strongylid
rafiqshahardar@gmail.com eggs (7.84%) and Moniezia spp. (5.88%) with mixed
Z. A. Wani infection in 12.42% samples.
drzahoorwani@skuastkashmir.ac.in
F. D. Sheikh Keywords Ascaris
GI parasites
Kashmir
Ladakh

aizar22@gmail.com Prevalence
Ruminants
Thysanosoma
1
Division of Veterinary Parasitology, Faculty of Veterinary
Sciences and Animal Husbandry, Sher-e-Kashmir University
of Agricultural Sciences and Technology of Kashmir, Introduction
Shuhama Campus, Alusteng, Srinagar, Kashmir 190006,
India Gastrointestinal (GI) helminths, a serious constraint to the
2
Present Address: Sheep Husbandry Department, Srinagar, productivity of ruminants induce losses in terms of mor-
Kashmir, India bidity, mortality, costs incurred on their treatment and
3
Present Address: KVK, Leh, Ladakh, India control (Lashari and Tasawar 2011). It is well established

123

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 pre-
vailing managemental practices mainly affect the preva-
lence of parasites. From Kashmir valley, several workers
have reported the incidence of parasitic infection in rumi-
nants (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, respec-
tively, 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 pla-
ces 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
123
J Parasit Dis
directly from the rectum in mini polythene bags, which
were then brought to the Divisional Helminthology labo-
ratory, SKUAST-K, for examination. Gross examination of
samples was first carried out followed by standard sedi-
mentation 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 pre-
sent study revealed presence of strongyles, Eimeria spp.,
Moniezia spp., Ascaris spp., Strongyloides spp. & Thysa-
nosoma spp. in ruminants (Fig. 1).
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, com-
pared 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). Preva-
lence 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 rumi-
nants 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,
J Parasit Dis

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

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. preva-
lence 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 Strongy-
loides 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%)

123

Strongyle in cattle (10x)
Eimeria in sheep (10x)
Ascaris in sheep (40x)
Fig. 1 Different types of parasitic eggs/oocysts in ruminants of Kashmir & Ladakh
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 pash-
mina 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%
123
J Parasit Dis
Eimeria in cattle (40x)
Strongyle and Ascaris in sheep (10x)
Moniezia in sheep (10x)
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
J Parasit Dis
prevalence of Eimeria spp. to the tune of 28.33%, 26.66%
strongylid eggs and 15.00% Moniezia spp. among pash-
mina 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., stron-
gyles, 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 prophylacti-
cally to prevent production losses.
Acknowledgements The help rendered by the officials of the Divi-
sion of Veterinary Parasitology and Sheep Husbandry Department,
Kashmir is greatfully acknowledged.
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 prepara-
tion 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 infec-
tion 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.
References
Aiman A, Shahardar RA, Wani ZA, Allaie IM (2017) Prevalence of
gastrointestinal helminth in cattle of north Kashmir. Indian J
Anim Sci 87:147–152
Allaie IM, Shahardar RA, Tramboo SR, Bulbul KH, Wani ZA, Khan
AA (2018) Prevalence of gastrointestinal nematodes in small
ruminants of Kashmir valley. J Entom Zoo Stud 6:2554–2559
Bhat SA, Mir MR, Qadir S, Allaie IM, Khan HM, Husain I (2012)
Prevalence of gastrointestinal parasitic infections in sheep of
Kashmir valley of India. Vet World 5:667–671
Bihaqi SJ, Allaie IM, Banday MAA, Wani ZA, Shahardar RA (2017)
Prevalence of caprine GI helminths in temperate areas of Jammu
and Kashmir. J Parasit Dis 41:843–849
Bushra M, Shahardar RA, Maria A (2013) Prevalence of gastroin-
testinal helminth parasites of cattle in central zone of Kashmir
valley. J Vet Parasitol 27:33–36
Fitzpatrick JL (2013) Global food security: the impact of veterinary
parasites and parasitologists. Vet Parasitol 195:233–248
Goodey T (1926) On the Ascaris from sheep. J Helminthol 1:1–6
Ibukun AV, Oludunsin F (2015) Prevalence of intestinal helminths
and protozoa parasites of ruminants in Minna, north central,
Nigeria. J Agric Vet Sci 8:62–67
Khajuria JK, Katoch R, Yadav A, Godara R, Gupta SK, Singh A
(2013) Seasonal prevalence of gastrointestinal helminths in
sheep and goats of middle agro-climatic zone of Jammu
province. J Parasitic Dis 37:21–25
Kuchai JA, Chishti MZ, Bhat AA, Tak H (2011) A survey on caprine
nematodiasis in Ladakh. Worlds Vet J 1:1–4
Kuchai JA, Chishti MZ, Tak H, Lone BA (2012) Faecal examinations
of pashmina goats (C. siberica) of Ladakh for nematode
infections. G J Sci Front Res Biol Sci 12:37–40
Lashari MH, Tasawar Z (2011) Prevalence of some gastrointestinal
parasites in sheep in southern Punjab, Pakistan. Pak Vet J
31:295–298
Maqbool I, Wani ZA, Allaie IM, Shahardar RA, Baba FA, Ashraf A
(2016) Parasitic fauna infections in pashmina goats of cold arid
region of Ladakh, India. Indian J Anim Sci 86:42–44
Maqbool I, Shahardar RA, Wani ZA, Allaie IM, Shah MM (2018)
Prevalence of gastrointestinal helminths of cattle in south
Kashmir. Indian J Anim Sci 88:910–914
Neveu-Lemaire M (1923) Presence d’Ascaris ovis chez le Chevreuil
(Capreolus capreolus). Ann Parasitol 1:265–268
Owhoeli O, Elele K, Gboeloh LB (2014) Prevalence of GI helminths
in exotic and indigenous goats slaughtered in selected abattoirs
in south, Nigeria. Chin J Biol 6:30–38
Pandit BA, Shahardar RA, Bhat AS, Darzi MM (2003) Prevalence of
gastrointestinal parasitic infection in sheep of Kashmir valley
under different management practices. Biol Res 5:1–5
Pandit BA, Shahardar RA, Banday MMA, Darzi MM, Matoo FA
(2004) Gastrointestinal helminth parasites of cattle in Kashmir
valley. J Vet Parasitol 18:63–65
Ransom BH, Foster WD (1920) Observations on the life history of
Ascaris lumbricoides. U.S Dept Agric Bull 817:29–30
Ransom BH (1911) The nematodes parasitic in the alimentary tract of
cattle, sheep and other ruminants. Bur Anim Ind Bull 127:24–25
Rehman TU, Khan MN, Khan IA, Ahmad M (2011) Epidemiology
and economic benefits of treating goat coccidiosis. Pak Vet J
31:227–230
Reshi AA, Tak H (2014) The study of some potential risk factors
associated with coccidiosis (Eimeria) in sheep in Kashmir
valley. J Agric Vet Sci 7:11–13
Schwartz B (1925) Occurrence of Ascaris in cattle in the United
States. N Am Vet 11:24–30
Shah MM, Shahardar RA, Maqbool I, Allaie IM, Wani ZA (2019a)
Prevalence of GI helminths of cattle in low lying and marshy
areas of Kashmir valley. Indian J Anim Sci 89:359–364
Shah MM, Shahardar RA, Maqbool I, Wani ZA, Allaie IM (2019b)
Prevalence of GI helminths in small ruminants of low lying and
marshy areas of Kashmir valley. Indian Vet J 96:30–33
Shahnawaz M, Shahardar RA, Wani ZA (2011) Seasonal prevalence
of platyhelminthosis of sheep in Gandarbal area of Kashmir
valley. J Vet Parasitol 25:59–62
Sharma D, Katoch R, Agnihotri RK (2007) Gastrointestinal helminths
in Gaddi sheep. J Vet Parasitol 21:141–143
Soulsby EJL (1982) Helminths, arthropods and protozoa of domes-
ticated animals, 7th edn. ELBS and Baillere Tindal, London,
p 156
123
 J Parasit Dis

Tramboo SR, Shahardar RA, Allaie IM, Wani ZA, Bushra MS (2015) Yadav A, Khajuria JK, Raina AK (2006) Seasonal prevalence of
Prevalence of gastrointestinal helminth infections in ovine gastrointestinal parasites in sheep and goats of Jammu. J Vet
population of Kashmir valley. Vet World 8:1199–1204 Parasitol 20:65–68
Verma R, Sharma DK, Gururaja K, Paula S, Banerjee PS, Tiwaria J
(2017) Molecular epidemiology and point mutations in ITS1 and Publisher’s Note Springer Nature remains neutral with regard to
18S rDNA genes of Eimeria ninakohlyakimovae and E. chris- jurisdictional claims in published maps and institutional affiliations.
tenseni isolated from Indian goats. Vet Parasitol 9:51–62
Wani ZA, Shahardar RA, Shahnawaz M (2011) Prevalence of
nemathelminth parasites in sheep of Ganderbal district of
Kashmir valley. J Vet Parasitol 25:26–29

123