Seasonal Prevalence of Gastro-Intestinal Helminths of Sheep

(Ovis Aries) and Goat (Capra Hircus) with Respect to Age and

Gender of Gurez Valley, Kashmir

Sheikh B. A., Ahmad F. and Sofi T. A.

J Anim Sci Adv 2016, 6(3): 1609-1625

DOI: 10.5455/jasa.20160409122017

Journal of Animal Science Advances

Online version is available on: www.grjournals.com

SHEIKH ET AL.

1609 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

Seasonal Prevalence of Gastro-Intestinal

Helminths of Sheep (Ovis Aries) and Goat (Capra

Hircus) with Respect to Age and Gender of Gurez

Valley, Kashmir

Sheikh B. A., Ahmad F. and Sofi T. A.

* Parasitology Research Laboratory, Department of Zoology, University of Kashmir, Srinagar- 190 006, India.

Abstract

The present study was carried out with an objective to assess the seasonal dynamics of intestinal helminth

parasites in association with age and gender of sheep (Ovis aries) and goat (Capra hircus) in Gurez valley. Out

of the total of 123 sheep and 96 goats examined through gut examination during May 2013 - May 2015,

25.20%, 17.07%, 27.64% in sheep and 22.91%, 15.62%, 26.04% in goats was the prevalence of trematodes,

cestodes and nematodes respectively. Comparatively goats harbored low infection level as compared to sheep.

There was no significant difference (P>0.05) in gastrointestinal parasite infection in Ovis aries and Capra

hircus examined. Data showed that infection was moderately positive all year round but highest infection was

found in the autumn season. A significant relationship was found between seasons and prevalence of infection

(P<0.05). Generally lower age groups and nomad breed reported high infection. In conclusion, the present study

states that seasons affected the prevalence of intestinal cestodes significantly while as gender and age of host

were not significant factors in the onset of infection under temperate climatic conditions of Gurez valley. These

findings may contribute to the existing epidemiological knowledge of the intestinal cestodes of Sheep and will

also improve the control strategies of intestinal helminthiasis.

Keywords: Age, gender, sheep, goat, intestinal cestodes, prevalence, season.

Corresponding author: Parasitology Research Laboratory, Department of Zoology, University of Kashmir, Srinagar- 190 006, India.

Received on: 02 Jan 2016 Revised on: 12 Jan 2016

Accepted on: 09 Mar 2016

Online Published on: 30 Mar 2016

Original Article

ISSN: 2251-7219

SEASONAL PREVALENCE OF GASTRO-INTESTINAL HELMINTHS OF …

1610 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

Introduction

The temperate agro-climatic conditions,

traditional animal husbandry practices and poor

veterinary infrastructure, abundance of alpine and

sub alpine pastures are natural determining factors

of incidence and severity of various parasitic

diseases of livestock in Kashmir valley (Tariq,

2007). Gastrointestinal parasitism is the major cause

of damage and decreased productivity in the goat

industry particularly in developing countries.

Soulsby (1982) mentioned that tape worms are

relatively less pathogenic, but in heavy infections

may cause reduced weight gain, diarrhoea and

intestinal obstruction. Numerous epidemiological

studies have been conducted throughout the world

to arrive at the detailed information on the

gastrointestinal parasites of livestock but scanty

references are available on epidemiology and

prevalence of intestinal helminths of sheep and

goats. According to Odoi et al., (2007), the major

risk factors of helminthiasis are broadly classified

as parasite factors (including epidemiology of the

different species), host factors (genetic resistance,

age and physiological status of the animal) and

environmental factors (climate, nutrition, stocking

density and management). No epidemiological

information was available on intestinal helminth of

sheep and goat in Gurez valley. The present study

was carried out with an objective to assess the

seasonal epidemiological prevalence of intestinal

helminths in association with age and sex of sheep

and goat in Gurez valley, India.

Materials and Methods

During this study a total of 123 sheeps and 96

goats were examined over two consecutive years

from May 2013 to May 2015. All intestinal tracts

belonged to sheeps of Bhakarwal (nomad) and

Gurez (local) breed. The animals were of both

genders and age ranged from less than one year to

more than four years. The samples were collected

on monthly basis and later expressed seasonally in

order to analyze the seasonal prevalence. The

collected samples were carefully labelled with

animal identification, sex, dental age and month of

collection.

Gastrointestinal Tract of Animals

The gastrointestinal tracts of freshly

slaughtered animals in various abattoirs of the

valley were collected, tied off at both ends and

brought to the laboratory and immediately

processed to analyze the parasite species present.

The abomasum and the small and large intestines

were thoroughly opened and examined separately

for the presence of tapeworms using standard

procedures and worms were identified using the

descriptions of Soulsby (1982). The faecal samples

were obtained directly from the rectum of the

animals in suitable air tight containers properly

labelled and brought to the laboratory in 4%

formalin and kept at 4oC until processing. The

laboratory procedure was as per the methods of

Soulsby (1982).

Statistical Analysis

Percentages to measure prevalence and chi-

square test to measure association between the

prevalence of infection and the age, gender and

breed were the statistical methods applied. The

association between seasons and prevalence of

infection was analyzed by Pearson’s coefficient of

correlation ‘r’. Means and standard error of means

with their respective 95% confidence intervals were

also calculated for each parameter tested in this

study. The level of significance was statistically

accepted at the 5% level (P≤0.05). The data was

analyzed using Statistical packages MINITAB

software version 13.2 for Windows.

Results and Discussion

Understanding the biology and epidemiology of

gastro-intestinal parasites of sheep and goat, it is

essential to improve the control measures and

decrease in production losses (Pal and Qayyum,

1992). The epidemiology of gastrointestinal helminth

parasites is governed by host-parasite relationship and

reaction with environmental conditions. Tembely et

al., (1997) and Vlassoff et al., (2001) demonstrated

that the effect of helminth infection on production

of particular livestock species depend mostly up on

the age of the animals, the breed, the parasite species

involved and the intensity of the worm populations

within the host. The prevalence and distribution of

SHEIKH ET AL.

1611 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

parasitic nematodes are largely governed by a

combination of their ecological requirements for

development and survival outside the host and farm

management practice. The epidemiology of GIT

parasites of sheep and goat in Gurez has been

studied taking into consideration the overall

prevalence (overall, seasonal, age-wise, sex wise)

and the associated risk factors with GIT parasites.

Overall Prevalence

Out of the total of 123 sheep and 96 goats

examined through gut examination during the study

period, 25.20%, 17.07%, 27.64% in sheep and

22.91%, 15.62%, 26.04% in goats was the

prevalence of trematodes, cestodes and nematodes

respectively (Table 1, 2, 3 & Fig. 1, 2, 3).

Comparatively goats harbored low infection level as

compared to sheep. There was no significant

difference (P>0.05) in gastrointestinal parasite

infection in Ovis aries and Capra hircus examined.

Table 1: Distribution of Helminths in Ovis aries and Capra hircus.

Host Examined Uninfected Infected %age P-Value

Ovis aries 123 89 34 27.64 P-Value =

0.071 Capra hircus 96 71 25 26.04

Total 219 160 59 26.94

Fig. 1: Graph showing the overall prevalence of sheep and Goat.

Table 2: Distribution of trematodes, cestodes and nematodes in Ovis aries and Capra hircus.

Host Examined Uninfected Infected Parasites collected

Trematodes Cestodes Nematodes P-Value

Ovis aries 123 89 34 31 (25.20) 21 (17.07) 34 (27.64) P-Value = 0.002

Capra hircus 96 71 25 22 (22.91) 15 (15.62) 25 (26.04) P-Value = 0.002

Total 219 160 59 53 (24.20) 36 (16.43) 59 (26.94) (Figures in parentheses indicate percentage)

Fig. 2: Prevalence of recovered Helminth parasites.

Sheep Goat

No. Examined

No. Infected

Sheep Goat

No. Examined

No. Infected

Trematode

Cestode

Nematode

SEASONAL PREVALENCE OF GASTRO-INTESTINAL HELMINTHS OF …

1612 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

In case of small ruminants, 89 out of 123

(27.64%) sheep and 71 out of 96 (26.04%) goat

were infected with helminth parasites. A mean

intensity & relative abundance of 81.64, 59.07 &

52.78, 39.04 in sheep and goat respectively was

observed. The observed parasites were Haemonchus

contortus, Ostertagia, Chabertia ovina, Fasciola

hepatica, Dicrocoelium dendriticum & Moneizia

expansa in both sheep & goat, and showed mean

intensity & relative abundance of 88.23, 24.39;

32.93, 8.30; 26.79, 5.22; 5.00, 1.05; 82.86, 19.53 &

4.31, 0.56 in sheep and 74.4, 19.37; 23.81, 5.45;

16.82, 2.97; 3.90, 0.85; 43.72, 10.02 & 3.4, 0.35 in

goat respectively.

Table 3: Mean intensity and Relative abundance of Helminths in Ovis aries and Capra hircus.

Host No.

Examined

No.

Infected

% age No. of

parasites

Mean

Intensity

Relative

Abundance

Sheep 123 89 27.64 7266 81.64 59.07

Goats 96 71 26.04 3748 52.78 39.04

Fig. 3: Graph showing the mean intensity and relative abundance of Helminths in sheep and goat.

Table 4: Mean intensity and Relative abundance of different Helminths in Ovis aries.

Parasite No.

Examined

No.

Infected

% age No. of

parasites

Mean

Intensity

Relative

Abundance

Haemonchus

contortus

123

34 27.64 3000 88.23 24.39

Ostertagia 31 25.20 1021 32.93 8.30

Chabertia ovina 24 19.51 643 26.79 5.22

Fasciola hepatica 26 21.13 130 5.00 1.05

Dicrocoelium

dendriticum

29 23.57 2403 82.86 19.53

Moneizia expansa 16 13.00 69 4.31 0.56

Sheep

Goats

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1613 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

Fig. 4: Graph showing the mean intensity and relative abundance of different Helminths in sheep.

Table 5: Mean intensity and Relative abundance of different Helminths in Capra hircus.

Parasite No.

Examined

No.

Infected

%

age

No. of

parasites

Mean

Intensity

Relative

Abundance

Haemonchus

contortus

96

25 26.04 1860 74.4 19.37

Ostertagia 22 22.91 524 23.81 5.45

Chabertia ovina 17 17.70 286 16.82 2.97

Fasciola hepatica 21 21.87 82 3.90 0.85

Dicrocoelium

dendriticum

22 22.91 962 43.72 10.02

Moneizia expansa 10 10.41 34 3.40 0.35

Fig. 4: Graphg showing the mean intensity and relative abundance of different Helminths in goat.

Based on post mortem examination of sheep

and goats obtained from different areas of Gurez the

present endeavour revealed the presence of variety

of gastrointestinal helminth parasitic fauna in them

(Table 6). The parasites encountered during the

present investigation in sheep were: Haemonchus

contortus (27.64%), Ostertagia ostertagia

(25.20%), Chabertia ovina (19.51%), Fasciola

heptica (21.13%), Dicrocoelium dendriticum

(23.57%), Moneizia expansa (13.008%). In goats

the prevalence was Haemonchus contortus

(26.04%), Ostertagia Ostertagia (22.91%),

No. Examined

No. Infected

No. of parasites

Mean Intensity

Relative Abundance

No. Examined

No. Infected

No. of parasites

Mean Intensity

Relative Abundance

SEASONAL PREVALENCE OF GASTRO-INTESTINAL HELMINTHS OF …

1614 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

Chabertia ovina (17.70%), Fasciola hepatica;

(21.87%), Dicrocoelium dendriticum (22.91%),

Moneizia expansa (10.41%).

Table 6: Overall prevalence of gastrointestinal helminth parasites in Ovis aries and Capra hircus.

Parasite Ovis aries (123 examined) Capra hircus (96 examined) P-Value

Number infected %age Number infected %age

Haemonchus contortus 34 27.64% 25 26.04% P-Value = 0.071

Ostertagia ostertagia 31 25.20% 22 22.91% P-Value = 0.069

Chabertia ovina 24 19.51% 17 17.70% P-Value = 0.071

Fasciola hepatica 26 21.13% 21 21.87% P-Value = 0.071

Dicrocoelium

dendriticum 29 23.57% 22 22.91%

P-Value = 0.071

Moneizia expansa 16 13.00% 10 10.41% P-Value = 0.071

The epidemiological study of GIH infection

revealed that sheep and goats harbour a spectrum of

GIH fauna in Gurez valley. Sheep and Goats

exhibited similar type of helminth fauna; this can be

attributed to the co-rearing and mixed grazing in

pastures and in other grazing areas. The proportions

of the genera of gastrointestinal parasites identified

in the present study in which Haemonchus was the

most prevalent (27.64% sheep & 26.04% goats) and

Monezia (13.00% sheep & 10.41% goats) the least,

is in conformity with the findings of other studies

carried out in many other climatic areas of India and

other parts of world.

Trematodes

The prevalence rate of trematodes in the

present study was 25.20% in sheep and 22.91% in

goats, among trematodes Dicrocoelium spp.

(23.57% in sheep and 22.91% in goats) was found

most prevalent followed by Faciola spp. (21.13% in

sheep and 21.87% in goats) as shown in Table 4.35.

The prevalence of Dicrocoelium spp. (Sheep: 23.57%;

Goats: 22.91%) which is in conformity with the

observations of other authors who also reported quite

similar prevalences of Dicrocoelium spp. Garg et al.,

(2009) reported the overall abbatoir prevalence of

fasciolosis was 16.54%. The prevalence of infection

was almost similar in sheep (4.78%) and goats

(4.68%).

Cestodes

The prevalence rate of cestodes in the present

study was 17.07% in sheep and 15.62% in goats,

among cestodes Monezia expansa (13.008% in

sheep and 10.41% in goats) was the only cestode

found in sheep and goat during the present study as

shown in Table 4.35. Similar results also have been

reported in other parts of the world although

prevalence varies. Sultan et al., (2010) reported

Monezia expensa was the most prevalent parasite

(19.04%) among cestodes followed by Avitellina

centripuctata (1.6%) in Sheep of Gharbia

Governorate, Egypt. Bashtar et al., (2010) also

reported Moniezia expensa was the highest

prevalent cestode parasite in sheep. Aydenizoz and

Yildiz (2003) observed highest infection of

Anoplocephalidae (M. expansa, Avitellina

centripunctata, Thysaneizia ovilla) infections in sheep

from Kirikkale (Turkey) in July (9.89%) and the

lowest in September (1.32%) in sheep. Muraleedharan

(2005) reported the prevalence of Moneizia spp. in

sheep and goats as 1.65% and 0.94% respectively.

Munib et al., (2004) reported the overall prevalence

rate of 28% of M. expansa, M. benedeni and A.

centripunctata. Kiran et al., (2005) found M. expansa

as the most prevalent helminth in sheep and goats in

Dehradun. Abebe and Esayas (2001) reported 26.75%

prevalence of Moneizia spp.; 33.77% of Avitellina

spp., 31.65% of Stilesia spp. in sheep and 24.20%,

35.13%, and 28.80% in goats. Thangathurai et al.,

(2003) recorded the prevalence of Stilesia as 5% and

2.8% in sheep and goats respectively. Zgardan

(2002) from sheep in Moldova recovered M.

expansa, M. benedeni, T. giardi and A. centripunctata.

Naem et al., (2011) recorded most prevalent cestode

in sheep of Fereidoonkenar city, Iran was Moniezia

expansa (10%). From the necroscopy and

coproscopy observations it is possible to deduct that

there is a continuous but moderate cestode

infestation in sheep and goats. The moderate

SHEIKH ET AL.

1615 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

prevalence of cestode parasites in sheep and goat

was perhaps due to adequate nonavailability of

oribated mites (intermediate host of cestodes)

(Soulsby, 1986) in the study area. This was found to

be in close agreement with the climatic conditions

of the Gurez Valley as has been observed by other

authours from Kashmir valley and other similar

areas as discussed above. It is pertinent to mention

here that Gurez valley has short growth periods

which hinders the life history of intermediate hosts

directly and consequently the helminth infestations

indirectly. The helminth infections (although low)

in sheep and goat of Gurez in such non supportive

environmental conditions can be attributed to the

fact that during short summers these ruminants

share the high altitude pastures with non-local

ruminants from Kashmir and Poonch areas where

the transmissions might be occuring.

Nematodes

In present study prevalence of nematodes was

27.64% in sheep and 26.04% in goats which is

lower than 81.17% as reported by Pandit et al.,

(2003). He also reported that Haemonchus and

Bunostomum the predominant among all genera.

However, the present study recorded the highest

prevalence of Haemonchus (27.64%) and

Ostertagia (25.20%) in sheep and Haemonchus

(26.04%) and Ostertagia (23.85%) in goats

respectively. Lone et al., (2011) reported the highest

prevalent nematode Haemonchus (60%) followed

by Trichuris (51%) in goats of Barramulla District

of Jammu and Kashmir. Dhar et al., (1982) also

reported H. contortus most prevalent parasite

among nematodes in sheep of Kashmir. Although,

Haemonchus contortus is particularly adapted to

warm climates of tropics, subtropics and temperate

Kashmir valley, it was very much prevalent in

sheep and goats in the cold and dry climate of

Gurez Valley as well. The increase in

temperature due to climatic alterations and global

warming can be one of the possible factors behind its

occurrence and also the transport of small ruminants

from tropical and sub-tropical parts to the Gurez

valley for meat and for other purposes is also

responsible for its predominance in Gurez valley.

Besides the mixed grazing of sheep and goats of

Gurez with those of Kashmir valley, Poonch and other

areas during summers while sharing the same pastures

for grazing may be the other reason for its occurrence

as well. As reported by Kapahi et al., (1993) the

diversity and abundance of medicinal plants of Gurez,

like Artimesia martima (Noorie) found abundantly on

high altitude pastures (2425 meters asl) acts as

anthelmintic agent for the grazing sheep and goat as

well. Other researchers of Kashmir also recorded

Haemonchus as most dominant parasite in small

ruminants (Sheep and Goat) of Kashmir. Nasreen et

al., (2005) recorded the prevalence of Haemonchus

contortus as 20.73% in sheep of Kashmir. Tariq et

al., (2008) observed the prevalence of Haemonchus

contortus (59.6%); Ostertagia circumcincta (38.0%);

Bunostomum trigonocephalum (37.7%); Chabertia

ovina (37.7%); Trichostrongylus spp. (33.9%);

Nematodirus spathiger (29.4%); Oesophagostomum

columbianum (28.4%); Trichuris ovis (23.5%) and

Marshallagia marshalli (22.1%) in sheep managed

under traditional husbandry system in Kashmir

valley. Outside India similar results have been

observed by other researchers. Kumsa and Wossene

(2006) recorded 91.2% and 82.9% prevalence rate

of Haemonchus in sheep and goats. Likewise, an

overall prevalence of 37.7% and 40.2%

Trichostrongylus axei was recorded in sheep and

goats, respectively in Ogada. Okaiyeto et al., (2008)

recorded prevalence of Haemonchus (49.9%);

Cooperia curtecie (39.6%); Oesophagostomum spp.

(14.9%) and Trichostrongylus spp. (1.9%) in

Nomadic Sheep of Northern Nigeria. Mondal et al.,

(2000) in Bangladesh revealed the presence of H.

contortus, T. axei, Mecistocirrus digitatus,

Oesophagostomum spp., Trichuris spp. and

Bunostomum. Jacquiet et al., (1995) reported H.

contortus, O. columbianum, Trichostrongylus spp and

S. globipunctata as the most prevalent species in

sheep and goats. Morales et al., (2001) reported H.

contortus, T. axei, T. colubriformis,

Cooperiafuelleborni, C. pectina, C. curticei, C.

punctata, T. ovis, O. columbianum, Skrjabinema

ovis, and B. trigonocephalum in ewes from

Venezuela. Alani and Yahya (1991) in Iraq

reported Trichostrongylus spp., Nematodirus spp.,

B. trigonocephalum, Strongyloides papillosus,

Cooperia spp., M. mtarshalli, Camelostrongylus spp.,

T. ovis, T. skrjabini, T. discolor, T. globulosa,

Chabertia ovina, O. venulosum and O. columbianum

SEASONAL PREVALENCE OF GASTRO-INTESTINAL HELMINTHS OF …

1616 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

in sheep. Suarez and Busetti (1995) in Argentina's

Western Pampas reported Haemonchus,

Nematodirus and Trichostrongylus. Borgsteede and

Dercksen (1996) in the Netherlands recovered

Ostertagia, Trichostrongylus, Strongyloides

papillosus, H. contortus and Trichuris from goats.

Nwosu et al., (1996) reported that Haemonchus was

the most common nematode recorded during their

study. Comparing the observations of present study

with those of earlier workers in other parts of the

world it is obvious that differences in prevalence of

nematode parasites is dependent on local

geographical, climatic factors, management and

husbandry strategies.

Age Wise Prevalence

After pooling all the data, age wise

epidemiological observations were made which

revealed highest prevalence rate in lower age

groups in both sheep and goats (Table 7). With the

increase in age, the infection level decreased.

Generally, the <1-year age group was more

infected. The results were significant (P < 0.05) for

all parasites viz; trematodes, Cestodes and

nematodes.

Table 7: Age wise prevalence of GIPs in Ovis aries and Capra hircus.

Host Age group

(in Years)

No.

Examined

Infected P-Value

Trematode Cestode Nematode

Ovis aries

<1 28 9 (32.14) 6 (21.42) 9 (32.14) P-Value =

0.002

1-3 56 15 (26.78) 10 (17.85) 15 (26.78) P-Value =

0.002

>3 39 7 (17.94) 5 (12.82) 10 (25.64) P-Value =

0.002

Total 123 31 (25.20) 21 (17.07) 34 (27.64)

Capra hircus

<1 25 7 (28.00) 4 (16.00) 7 (28.00) P-Value =

0.003

1-3 44 10 (22.72) 8 (18.18) 12 (27.27) P-Value =

0.001

>3 27 5 (18.51) 3 (11.11) 6 (22.22) P-Value =

0.002

Total 96 22 (22.91) 15 (15.62) 25 (26.04)

(Figures in parenthesis indicate percentage).

Fig. 6: Graph showing age wise prevalence of Sheep and Goat.

<1 Year 1-3 Years >3 Years

No. Examined

Trematode (Sheep)

Cestode (Sheep)

Nematode (Sheep)

No. Examined

Trematode (Goat)

Cestode (Goat)

Nematode (Goat)

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1617 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

The lower age groups of animals found to be

infected more with GIHPs in both sheep and goats

is because of the high susceptibility and low

resistance in young animals. Thus age was an

important factor in the onset of infection because

immunity played a great role in the establishment of

parasites in the host body. The more infection

observed in <1 year animals is attributed to the

delay in the development of significant immunity,

which is initially low but increases with intensity

and duration of exposure of infection. When the

animals cross 1 year of age the major part of their

infection is eliminated because of development of

self-cure phenomenon and tend to remain relatively

resistant to reinfection; however, constant exposure

of some level of infection is required to maintain

their resistant status (Vlasoff et al., 2001). Lone et

al., (2011) reported the highest prevalence of

helminth parasites were <1-year age group (58%) as

compared to >1-year age group (34%) in goats of

Barramulla District of Jammu and Kashmir. The

present study revealed that prevalence was higher

(32.14% in sheep and 28.00% in goats) in animals

below 1 year of age than the above 1 year. These

results are closely related to the findings of Pal &

Qayyum, (1992); Maqsood et al., (1996); Vlasoff

et al., (2001); Magona and Musisi, (2002);

Vanimisetti et al., (2004); Lateef et al., (2005).

Maqsood et al., (1996) reported that the prevalence of

haemonchosis was higher in both sheep and goats

less than two years of age (67.1%; 47.8%) compared

with those of above two years (40.4%; 33.3%). Rauf

et al., (2005) in different age groups of sheep in

Government and private farms in Pakistan reported

young animals more prone to infection with tape

worms than adult animals. Lone et al., (2012)

reported that lambs become infected with

nematodes and cestodes very early in life and pass

eggs and ripe proglottids as was witnessed in a

number of clinical cases from Jammu and Kashmir.

According to Soulsby (1986) previous infection and

age of the host afford some protection against

reinfection and hence acute disease is usually seen

in young animals. The high rate of infection with

GINs in young lambs has been observed by Vlasoff

et al., (2001). Young goats were two times more at

risk of infections than adult goats (Magona et al.,

2002). Adult animals harboured low number of

worms, mainly O. ostertagi despite continuous

grazing (Borgsteede and Dercksen 1996). It was

recognized that sheep below 1 year of age are more

susceptible to parasite infection than above 1 year of

age, Wildeus and Zajac, (1992); Watson et al.,

(1991); Colditz et al., (1996). Lateef et al., (2005)

reported higher infection of GIH parasites in young

sheep reared under traditional husbandry system in

Pakistan. Qamar et al., (2011) recorded the

occurrence of haemonchosis was more frequently in

younger (below 9 months) sheep and goats

(39.91%) than in older (above 9 months) animals

(33.23%). Age wise prevalence may be due to the fact

that with the advancement of age, vigor of the animal

becomes better and they develop resistance against

the parasitic diseases. Immune response may not be

fully developed in sheep before 6-10 months (Vlasoff

et al., 2001). The results of the present study are in

proximity with the above-mentioned workers.

Gender Wise Prevalence

After arranging all the data, sex wise

observations were made which revealed that

females were slightly more infected with GIHPs

than males in both sheep and goats (Table 8).

Table 8: Gender wise prevalence in Ovis aries and Capra hircus.

Host Sex No.

Examained

Infected P-Value

Trematodes Cestodes Nematodes

Ovis

aries

Male 56 13 (23.21%) 9 (16.00%) 14 (25.00%) P-Value =

0.001

Female 67 18 (26.86%) 12 (17.91%) 20 (29.85%) P-Value =

0.002

Total 123

31 (25.20%) 21 (17.07%) 34 (27.64%)

P-Value =

0.041

P-Value =

0.050

P-Value =

0.036

Capra Male 50 11 (22.00%) 7 (14.00%) 13 (26.00%) P-Value =

SEASONAL PREVALENCE OF GASTRO-INTESTINAL HELMINTHS OF …

1618 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

hircus 0.002

Female 46 11 (23.91%) 8 (17.39%) 12 (26.08%) P-Value =

0.001

Total 96

22 (22.91%) 15 (15.62%) 25 (26.04%)

P-Value =

0.034

P-Value =

0.039

P-Value =

0.027

Fig. 7: Gender wise prevalence of Helminths.

Over all females found to be more infected with

GIHPs than males in both sheep and goats are

comparable with the observations of many other

workers. However, Gulland and Fox (1992) reported

that the intensity and prevalence of GIHPs infection

were higher in male sheep and goats than females,

except during lambing season, and it decreased as age

progresses in both sexes of sheep and goats. Patel et

al., (2001) observed higher infection of GIF in

female goats than males. Females were also

found to be more infected with helminthes than

males (Valcared et al., 1999). Lateef et al., (2005) in

sheep under traditional husbandry system in Pakistan

also reported highest prevalence in females.

Differences in susceptibility to infection between

sexes have been observed by various workers. The

observed disparity may not solely be due to

differences in susceptibility but may also depend on

a sex-related variation in behaviour that results in

differences in exposure (Barger, 1993). The

influence of sex on the susceptibility of animals to

infections could be attributed due to the

physiological peculiarities of the female animals,

which usually constitute stress factors thus,

reducing their immunity to infections, and for being

lactating mothers, females happen to be

weak/malnourished, as a result of which they are

more susceptible to the infections besides some

other reasons (Blood and Radostists, 2000). Qamar

et al., (2011) reported analysis of the GIH disease

pattern in male and female sheep and goats revealed

no significant difference. Thus, while considering

the present observations and the work of other

researchers it seems that although sex plays a

significant role in the preponderance of helminth

infection but environmental, management and

climatic conditions have a greater role to play in

the onset of GIP in sheep and goats despite the

gender differences reported in this study and by

several authors in other parts of the world.

Seasonal Prevalence

The data pooled for seasonal estimation of

helminth infection revealed definite seasonal

prevalence of infection in both sheep and goats with

highest infection in summer and lowest in winter

(Table 9).

Sheep: Out of 123 sheep examined, 31

(25.20%), 21 (17.07%), and 34 (27.64%) were

infected with trematodes, cestodes and nematodes

respectively. For trematodes the highest infection

(28.57%) was in summer and lowest (19.23%) in

Male Female

No. Examined (Sheep)

Trematode (Sheep)

Cestode (Sheep)

Nematode (Sheep)

No. Examined (Goat)

Trematode (Goat)

Cestode (Goat)

Nematode (Goat)

SHEIKH ET AL.

1619 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

winter (P < 0.05). The maximum cestode infection

(20.00%) was reported in summer and lowest

(11.53%) in winter and also the maximum

nematode infection (31.42%) was observed in

summer and lowest (19.23%) in winter (P < 0.05).

Goats: The number of goats examined was 96.

Out of these 22 (22.91%), 15 (15.62%), and 25

(26.04%) were positive for trematodes, cestodes and

nematodes respectively. The maximum infection of

25.92% (trematode), 18.51% (cestode) and 29.62%

(nematode) was observed in summer and the lowest

15.78% (trematode), 10.52% (cestode) and 21.05%

(nematode) was observed in winter (P < 0.05).

Thus, the gut examination of both sheep and

goats revealed higher infection with helminths

(trematodes, cestodes and nematodes) in summer,

whereas winter revealed low infection of all the three

groups during both the years of study, showing

consistent results.

Table 9: Seasonal prevalence of GIPs according to gut examination.

Season Host No.

Examamined

No. Infected P-Value

Trematodes Cestodes Nematodes

Spring Sheep 25 6 (24.00%) 4 (16.00%) 7 (28.00%) P-Value = 0.002

Goat 21 5 (23.00%) 3 (14.28%) 5 (23.80%) P-Value = 0.002

Summer Sheep 35 10 (28.57%) 7 (20.00%) 11 (31.42%) P-Value = 0.002

Goat 27 7 (25.92%) 5 (18.51%) 8 (27.58%) P-Value = 0.002

Autumn Sheep 37 10 (27.02%) 7 (18.91%) 11 (29.72%) P-Value = 0.002

Goat 29 7 (24.13%) 5 (17.24%) 8 (27.58%) P-Value = 0.002

Winter Sheep 26 5 (19.23%) 3 (11.53%) 5 (19.23%) P-Value = 0.001

Goat 19 3 (15.78%) 2 (10.52%) 4 (21.05%) P-Value = 0.001

Total Sheep 123 31 (25.20%) 21 (17.07%) 34 (27.64%)

Goat 96 22 (22.91%) 15 (15.62%) 25 (26.04%)

Fig. 8: Graph showing seasonal prevalence of recovered helminths.

The present study reported highest GIH

infection in both sheep and goats in the summer

season (P < 0.05). The highest summer infection

could be due to the presence of adequate

temperature and moisture conditions as summer in

Valley is followed in and/by rainfall. Translation of

the infective stages was slow on pastures earlier on,

but as rainfall, temperature and vegetative ground

cover increased towards mid-summer (June-July),

transmission of the infective stages occurred with

increasing frequency. Parasite burdens reached

maximum levels in the late summer and early

autumn. In mid-autumn and onwards the infection

level decreased in both sheep and goats because

there was no or little rain during this period and

faecal pellets rapidly dried out and there were least

chances for the infection. In line with this seasonal

trend are the observations of various authors (Dhar

Sheep Goat

No. Examined (Spring)Trematodes (Spring)Cestodes (Spring)Nematode (Spring)No. Examined (Summer)Trematode (Summer)Cestode (Summer)Nematode (Summer)No. Examined (Autumn)Trematode (Autumn)Cestode (Autumn)Nematode (Autumn)No. Examined (Winter)Trematode (Winter)Cestode (Winter)Nematode (Winter)

SEASONAL PREVALENCE OF GASTRO-INTESTINAL HELMINTHS OF …

1620 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

et al., 1982; Pandit and Mir, 1988; Makhdoomi et

at., 1995; Vlassoff et al., 2001; Magona et al.,

2002; Khajuria and Kapoor, 2003; Kaplan et al.,

2004; Nasreen et al., 2005; Kuchai et al., 2011;

Lone et al., 2011).

The low infection reported during the winter

season in the present study could be attributed to

low temperature which helps in AD (hypobiosis) in

host (Ogunsuri and Eysker, 1979; Gibbs, 1986;

Tariq et al., 2008). Moreover, in winter the area

remains mostly snow covered as such there is no

grazing which hinders in loss of contact between

host and parasites. El-azazy (1995) in Saudi

Arabia also reported the overall worm counts and

infection rates lowest in the winter season in goats.

Valcared and Garcia (1999) observed lowest level

of infection in the winter and rose progressively

till the autumn. Shahadat et al., (2003)

recorded lowest prevalence in the month of

January of H. contortus in Bengal goats. The initial

exposure of native animals to infective larvae on

pasture in spring generates egg production

approximately 3-4 weeks after turnout.

There is peak biotic potential of Haemonchus

contortus which results in rapidly assuming

dominance at times when environmental conditions

on pasture are favourable for the development and

survival of the free-living stages. Nwosu et al., (1996)

reported that Haemonchus was the most common

nematode recorded during their study. They also

reported that Haemonchus eggs and adults were high

in prevalence and seasonal fluctuation was common

in the study area. They further reported the high

prevalence during hot humid season. These seasonal

variations in the nematode worm burdens were

similar to studies in other tropical countries with

distinct rainy and dry seasons (Fritsche et al., 1993;

Magona & Musisi, 2002; Nwosu et al., 1996). In

general, moist and warm environmental conditions

are favourable for the development, survival and

transmission of the pre-parasitic stages of parasitic

nematodes (Hansen & Perry, 1994; Urquhart et al.,

1987). Nasreen et al., (2005) also observed highest

infection (33.18 %) in summer and lowest in winter

(15.25%). Makhdoomi et al., (1995) also observed

highest infection in the summer season. Thus our

findings of higher infection in summer are in

agreement with them although the percent prevalence

in different seasons differs which may be due to the

topographic and climatic factors unique to the study

area.

The 1st peak level of infection as recorded from

April onwards is derived from over wintered larvae of

Haemonchus originating from the eggs deposited.

This contributes to what is known as the spring rise

phenomenon. High rainfall in spring also helps in

providing suitable molarity of salt present in soil

which is an important factor for ecdysis (Soulsby,

1986). It also helps in larval dispersion on herbage

which increases the chance of contact between host

and larvae (Nginyi et al., 2001).

The 2nd peak level of infection from June

onwards till autumn is derived from eggs

deposited in the first grazing cycle (Soulsby,

1986). Ingestion of sufficient numbers of larvae

results in type 1 disease in lambs during their first

summer at pasture. In this study, the presence of

sufficient moisture and optimum temperature

conditions during the rainy season favored the

survival of infective larvae in the pasture and higher

probability of uptake of the infective larvae leading

to higher prevalence rate. The rainy season which

started in the spring and early summer made the

environmental conditions more favourable for

the development and survival of preparasitic

stages and led to increased availability of infective

larvae in the rainy and post rainy season. Climatic

conditions influenced the build-up of pasture

larval contamination and elevated levels were

present in late July-August. This is in contrast to the

situation in other parts of world- the tropical

countries where disease primarily is caused due to

infection with L3 derived from early season

contamination (Vercruysse and Claerebout, 2003),

thus climate plays significant role in epidemiology

of GIH parasites.

It is well documented that GIP in grazing

animals is directly related to the availability of

larvae on pasture and seasonal pasture

contamination (Soulsby, 1986). Kates (1950)

demonstrated that hot and humid weather provides

favourable conditions, for the development and

survival of exogenous stages of H. contortus.

Gordon (1953) stated that total monthly rainfall of

more than 50 mm and a mean monthly maximum

temperature of over 18.3 C provide optimum

SHEIKH ET AL.

1621 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

conditions for the development and survival of

exogenous stages of H. contortus. Therefore, it is

expected that higher incidence of H. contortus and

other nematodes would be restricted to months with

adequate rainfall. H. contortus eggs can withstand

extreme climatic conditions and also survive longer

period during winter season (Blood and Radostits,

1989) resulting in mass hatching of ova and high

summer infection of pasture. Sissay et al., (2007) in

Ethiopia showed distinct seasonal patterns with

high levels of infection during the short and

long rainy seasons with peaks occurring in May

and September of each year.

There are several studies which have reported

highest GIN infection in rainy seasons (Charles,

1989; Ahmad Abdalla et al., 1997; Katoch et al.,

2000; Laha et al., 2001; Fakae, 1990;

Shahiduzzaman et al., 2003; Yadav Khajuria,

2006). Agyei (1997) in coastal Savanna regions of

Ghana observed that the number of infective larvae

of strongylate nematode on pasture was directly

related to the pattern of rainfall. Qamar et al.,

(2011) the overall highest incidence of the year in

sheep and goats was recorded during summer

(43.69%), followed by autumn (38.46%) then

spring (37.12%), while the lowest (28.79%)

prevalence was recorded during winter. Singh et al.,

(2004) at an organized farm in Rajasthan reported

H. contortus as the most predominant parasite and

concluded that the period from July to October

(rainy season) was more favourable for H.

contortus. Tembely et al., (1997) in the highlands

of Ethiopia indicated that rainfall and humidity

seemed to be the most important factors for the

development of eggs and free living stages of

gastrointestinal nematode infections in sheep.

Martinez-Gonzalez et al., (1998) concluded that

environmental factors affected the prevalence and

intensity of GIH infection under semi-intensive

management conditions in dairy sheep flocks in

Leon, Spain. Thamsborg et al., (1998) in Joannina

(Greece) suggested that the factors affecting the

epidemiology of GI nematodes of naturally

infected sheep during grazing include

anthelmintic treatment, host genotype and season.

Rizvi et al., (1999) reported highest Haemonchus

infection in spring season in goats in Pakistan.

Najeeb-ur-Rehman and Akhtar Ali (2001)

observed the highest GIH infection in sheep and

goats in Pakistan in the months of June, July and

August.

Magona and Musisi (2002) indicated that age,

grazing system, season and agro-climatic zone have

significant influence on the level of risk of GIN

infections in Ugandan goats and on the worm egg

output under field conditions. Soundarajan and lyue

(2003) attributed the increasing infection trends of

helminth infection of sheep in Nilgiris hills to

varying climatic factors. Maturation of inhibited

larvae of H. contortus in sheep and the resultant

spring rise in FEC has been related to a loss of

immunity due to the limited exposure to infection in

winter, to stress, to immuno suppression associated

with the late stages of pregnancy and lactation and

to the frequent occurrence of poor nutrition at the

end of winter (Uriarte et al., 2003).

Nganga et al., (2004) indicated that rainfall

distribution was the major factor governing the

development and survival of the pre-parasitic

stages on pastures. Umur and Yukuri (2005)

showed that the parasite counts increased slightly

in spring and summer, and then reached maximum

in autumn. Sreedevi and Murthy (2005) reported the

overall prevalence of GIH in sheep higher in

summer. However, Garg et al., (2009) recorded the

highest incidence of GIN in winter in goats. Thus

seasons have an important role in the prevalence of

helminth parasites of sheep and goats.

From the above discussion it is now clear that

season and the other associated environmental

conditions including temperature and moisture

have a greater role to play in the onset of G1H

infection in sheep and goats. There are several

factors that contribute the disease onset like warm,

humid and wet grazing season, the more time

animals spend on pasture, inefficient selection of

de-wormers, poor husbandry practices and or the

development of anthelmentic resistance. The low

prevalence rate observed in sheep and goats of

Gurez valley could be due to difference in

management system of the animals and more

importantly the environmental conditions prevalent

in the area. However, our results are in close

conformity with Tariq et al., (2006) who reported

that higher parasite prevalence is more common in

sheep than in goats due to the grazing habit of

SEASONAL PREVALENCE OF GASTRO-INTESTINAL HELMINTHS OF …

1622 J. Anim. Sci. Adv., 2016, 6(3): 1609-1625

sheep. The result in this study could be because

most of the goats in this study were from mid and

high altitude areas, which are thought to be suitable

for survival of the larval stage of the parasites.

Likewise, in the highland areas of the Kashmir

where goats are mostly reared, there is poor

veterinary infrastructure and medication to goats.

More importantly, the condition could be due to less

or slow development of immunity in goats to

gastrointestinal parasites compared with the

situation in sheep and cattle (Regassa et al., 2006).

The degree of infection in most of the study animals

was low, agreeing with various works Kuchai et al.,

2011, and 2012 indicating the sub-clinical cases of

gastrointestinal parasites with subsequent subsistent

low degree of pasture contamination. But it is

inconsistent with reports from Kashmir (Dhar et al.,

1988) that could be explained by the difference in

management and breed of the respective animals.

This study revealed that the helminth infection

in ruminants occurs throughout the Gurez valley. It

also disclosed that regardless of the environmental

conditions, the animals are infected with variety of

helminth parasites. The various parasites recovered

during the present study have also been reported

from other two parts of the Jammu and Kashmir

state, as well as from different parts of the world

having almost same geographical locations and

environment (Bali, 1976, Raina et al., 1987,

Troncy, 1989, Nasreen et al., 2005, Fatima et al.,

2012).

However, the various intraspecific

morphological variations observed during the

present study could be due to the variation in age of

parasite, host species, intensity of infection (higher

intensity, smaller parasites), methodology

(fixation), environmental factors of the study area,

body conditions of the host, etc.

The significantly higher prevalence in autumn

than spring is in consent with many reports around

the world, Tembely et al., 1997, 1998; Moyo et al.,

1996; Fritche et al., 1993; Mbae et al., 2004. This

could be due to the existence of a direct relationship

between prevalence with the rainfall, humidity and

temperature. In this study, the presence of sufficient

rainfall and moisture during the autumn season

favored the survival of infective larvae in the

pasture and higher probability of uptake of the

infective larvae leading to higher prevalence rate.

Similarly, a higher prevalence recorded in

younger animals as compared to the adult ones is in

agreement with most literatures Dunn, 1978; Shah-

Fischer and Say, 1989; Keyyu, 2003; Nwosu et al.,

1996; Nganga et al., 2004, from different corner of

the world. This could be due to the fact that younger

animals are more susceptible to infections than

adults. Adult animals may acquire immunity to the

parasites through frequent challenge and expel the

ingested parasite before they establish infection,

(Dunn, 1978; Shah-Fischer and Say, 1989). But the

findings of this study are inconsistent with reports

from Gambia where adults and older animals bear

high worm burden.

Acknowledgments

The authors are greatly thankful to the

Department of Zoology, University of Kashmir for

the facilities they provided. Bashir A. Sheikh is also

thankful to those people of Gurez valley, India who

make them host material available for research

purpose.

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