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Small Ruminant Research 110 (2013) 57– 61

Contents lists available at SciVerse ScienceDirect

Small Ruminant Research

jou rn al h om epa ge: www. elsev ier .com/ locate /smal l rumres

revalence of lung affections in sheep in northern temperate regions ofndia: A postmortem study

atief Mohammad Dara,∗, Mohammad Maqbool Darzib, Masood Saleem Mirb,hayuaib Ahmad Kamilb, Adil Rashida, Swaid Abdullahc

Department of Veterinary Pathology, Khalsa College of Veterinary & Animal Sciences, Amritsar 143002, Punjab, IndiaShere-e-Kashmir University of Agriculture Sciences and Technology, Kashmir 191121, J&K, IndiaDepartment of Veterinary Parasitology, Khalsa College of Veterinary and Animal Sciences, Amritsar 143002, Punjab, India

r t i c l e i n f o

rticle history:eceived 26 December 2011eceived in revised form 9 August 2012ccepted 13 August 2012vailable online 7 September 2012

eywords:ung affectionsheeprevalence

a b s t r a c t

A total of 1385 sheep slaughtered in different abattoirs were screened. The overall preva-lence of lung affections was found to be 24.18%. Age was taken as a risk factor for theoccurrence of infection. The prevalence was significantly (P ≤ 0.01) higher in sheep lessthan 2 years of age (25.40%) as compared to the sheep greater than 2 years of age (19.01%).Assessment of different lung affections in association with body condition of the animalsrevealed that lung affections were more frequent and severe in animals whose generalbody condition was weak. Patho-morphological characterization of the lung affectionsincluded acute bronchopneumonia, fibrinous bronchopneumonia, chronic bronchopneu-monia, suppurative pneumonia, interstitial pneumonia, verminous pneumonia, bronchitis

neumoniaashmir

and bronchiolitis, haemorrhage, congestion and emphysema/atelectasis. It was concludedthat lung affections were highly prevalent in the sheep destined for slaughter in Kashmirvalley owing to multiple factors, viz., adverse climatic conditions during winters, poor man-agement and lack of proper feeding regimen leading to substantial economic losses due to

th and

reduced lamb grow

. Introduction

In a developing agriculture based country like India,he importance of animal husbandry in the economicrogress of people cannot be underestimated. Among live-tock sector, sheep husbandry plays a multifaceted rolen socio-economic development of the rural householdsy providing mutton, wool, manure and hides. Economic

osses associated with various diseases in sheep andther domestic animals are often the result of a complex

nteraction between infection, poor management and envi-onmental conditions. Among the various health relatedroblems, respiratory ailments are the major cause of

∗ Corresponding author. Tel.: +91 8146161619.E-mail addresses: shaheenlatief@gmail.com (L.M. Dar),

waidabdullah@gmail.com (S. Abdullah).

921-4488/$ – see front matter © 2012 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.smallrumres.2012.08.006

decreased carcass value.© 2012 Elsevier B.V. All rights reserved.

deaths in the lambs and decreased productivity in theolder animals. The respiratory system constitutes the mostextensive surface that is exposed directly to the ambientenvironment. Although, it possesses a local innate defensesystem, yet it is highly vulnerable to the various environ-mental insults. Lung affections, particularly, pneumoniacan have considerable consequences. It is estimated thatpneumonia alone causes at least 10% mortality in the sheeppopulation in India (Maru et al., 1990). However, most ofthe pneumonic cases being insidious are usually detectedeither at necropsy or after slaughter. Inability to detectand characterize the disease in the live animal warrants anunderstanding of the epidemiology of pneumonia in sheepin order to facilitate proper disease management.

Kashmir valley is located in the northern Himalayas atan altitude of 1730 m above the sea level and falls between32◦17′ to 36◦58′ North latitude and 73◦26′ to 80◦30′ Eastlongitude. Average temperature ranges between −4 ◦C and

58 L.M. Dar et al. / Small Ruminant Research 110 (2013) 57– 61

Table 1Prevalence of various lung affections in sheep destined for slaughter indifferent regions of Kashmir valley.

Geographical region NSS NAS PP

North Kashmir 391 89 22.76Central Kashmir 589 151 25.63South Kashmir 405 95 23.45

Table 3Percentage prevalence of ovine lung affections based on different agegroups.

Age group >1 year <1 year

Numbers of sheep screened 1122 263

Total 1385 335 24.18

NSS, number of screened sheep; NAS, number of affected sheep; PP, per-centage prevalence.

32 ◦C during various months of the year and average annualprecipitation is around 70 mm. Spring is the wettest sea-son while autumn is the driest. Sheep rearing is practicedextensively in Kashmir and contributes to 60% of the totalmeat consumption in the region (Dar et al., 2012). To theauthors’ knowledge, the base line epidemiological datadescribing the prevalence and pathology of various ovinelung affections in the region have not been published inthe peer-reviewed journals until now; however, a few casereports have been reported (Maqbool et al., 1990; Bhatet al., 1996; Shahardar et al., 2001; Darzi et al., 2007). Hence,the present study was undertaken to investigate the preva-lence of lung affections in the sheep destined for slaughterin Kashmir valley.

2. Materials and methods

2.1. Study material

The study was conducted on the sheep destined for slaughter fromlocal farms in different regions of Kashmir valley, India. The study area ofthe northern temperate region was divided in to three zones: NorthernKashmir (Baramullah, Bandipora and Kupwara), Central Kashmir (Srina-gar, Ganderbal and Budgam), and South Kashmir (Anantnag, Pulwamaand Shopian). A total of 1385 slaughter sheep including 391, 589 and 405from areas of Northern, Central and South Kashmir, respectively, werescreened.

2.2. Screening and sampling

During examination each study animal was given an identificationnumber and its age, sex, breed and origin was recorded. The age was deter-mined by dentition and owner’s information and animals (depending onthe age of slaughter) were grouped into two age groups >1 years of ageand <1 year of age. Thorough examination of the carcass was done andgeneral body condition score (BCS) noted. The body condition was classi-fied into five categories as emaciated (BCS 1), thin (BCS 2), average (BCS3), fat (BCS 4) and obese (BCS 5) in accordance with the score card givenby Thompson and Meyer (1994).

Following slaughter and evisceration, lungs were first examined insitu and any lesions observed were noted. Then whole lungs from all theanimals were collected and thoroughly screened by visual examination,palpation and dissection of the bronchial tree. Following observationswere recorded:

Table 2Prevalence of lung affections in sheep with respect to body condition score (BCS)

BCS Numbers of sheepscreened

Emaciated (BCS 1) 410

Thin (BCS 2) 358

Average (BCS 3) 306

Fat (BCS 4) 208

Obese (BCS 5) 103

Total 1385

Numbers of sheep with lung affections 285 50Percentage prevalence 25.40 19.01*

* Significant at P ≤ 0.05.

• Type and nature of the lesions, viz., congestion, haemorrhage, abscess,adhesions, colour and consistency.

• Distribution of various lesions in different lung lobes.• Type of bronchial exudates.• Presence of parasites.

The parasites recovered were washed in phosphate buffered solu-tion (PBS), immediately fixed in warm 70% alcohol and then processedfor identification on morphological basis (Soulsby, 1982). Representativetissue specimens from grossly affected lungs were collected in 10% neutralbuffered formalin for routine histopathological examination.

2.3. Statistical analysis

The association if any between the factors and the lung was measuredthrough chi-square test (Thursfield, 1995).

3. Results and discussion

In general, a total of 335 sheep revealed at least onetype of gross pathological lesion in the lungs giving anoverall prevalence of 24.18% (335/1385) (Table 1). Over-all prevalence of lung affections in sheep in North, Centraland South zones was observed to be 20.71% (89/391),24.11% (151/589), 20.49% (95/405). This difference inzone-wise prevalence was statistically non-significant (Pvalue < 0.05). However, lower prevalence rates of ovinelung affections have been reported from various subtrop-ical regions of northern India. Kamil (1989) and Kumar(2005) reported prevalence rates of 8.62% and 17.65% inUttar Pradesh, respectively. In the present study, the higherprevalence in locally reared sheep might be attributed tothe unfavourable and frequently fluctuating environmen-tal conditions in the Kashmir valley to which they mightget exposed over a period of time. Also, sheep for mostpart of the year except summer season are maintainedunder intensive rearing system with minimal ventilationfavouring transmission of respiratory infections besidesdepressing the defense system of the respiratory tract

(Brogden et al., 1998). Further, physical and psychologicalstresses have also been incriminated for altering immunefunction in animals (Kelley, 1980, 1982, 1984; Albani-Vangili, 1985; Kelley, 1985; Siegel, 1985; Blecha, 1988).

.

Numbers of sheep withlung affections

Percentage of lungaffections

138 33.6588 24.5866 21.5624 11.5419 18.44

335 24.18

L.M. Dar et al. / Small Ruminant Research 110 (2013) 57– 61 59

Fig. 1. (a) Red hepatization on the anteroventral areas of sheep lung. (b)Acute bronchopneumonia: section of lung revealing presence of inflam-matory exudates in the bronchiolar lumen and infiltration of neutrophilsiev

aaititT3ta

Fig. 2. (a) Fibrinous bronchopneumonia: lung showing bilateral consoli-

TT

A

n and around the bronchiole. H&E, 400×. (For interpretation of the ref-rences to colour in this figure legend, the reader is referred to the webersion of this article.)

Out of a total of 1385 sheep screened, 410 were scoreds emaciated, 358 as thin, 306 as average, 208 as fat and 103s obese (Table 2). Assessment of different lung affectionsn association with body condition of the animals revealedhat lung affections were more frequent and more severen animals whose general body condition was weak andhe difference was statistically significant (P value < 0.001).

he occurrence of grossly visible abnormities of lungs was3.65% (138/410) in emaciated sheep, 24.58% (88/358) inhin, 21.56% (66/306) in average, 11.54% (24/208) in fatnd 18.44% (19/103) in obese sheep. Respiratory conditions

able 4ype and distribution of various lung lesions observed in sheep.

Gross pathological lesion AL CL IL

Congestion 9 5 3

Red hepatization 42 33 19

Grey hepatization 19 10 7

Lung abscess 6 5 1

Parasitic lesions 1 3 –

Pock lesions 4 2 2

Froth/exudate – – –

Emphysema and atelectasis 3 2 2

Haemorrhage 2 3 –

Total 86 63 34

L, apical lobe; CL, cranial lobe; IL, intermediate lobe; DL, diaphragmatic lobe; ML

dation and deposition of fibrin over the consolidated areas. (b) Fibrinousbronchopneumonia: section of lung showing fibrinocellular exudates inthe alveoli. H&E, 400×.

have been associated with severe health impairment andeven mortality among sheep (Orr and Black, 1996; Orret al., 1998; Clark et al., 2001; Goodwin et al., 2005). Poorhealth condition may either predispose the animals to lungdisease or the lung affections themselves might be reduc-ing the health status of the animals. The latter might beattributed to the fact that lungs constitute a central organand any lung affection has wider impact on general health.Pneumonia or any other affections of lung render the ani-

mal to stress resulting into derangement of the normalbody metabolism leading to the loss of appetite and rapidcatabolism of the body reserves resulting into the weightloss (Jones et al., 1982; Goodwin et al., 2004).

DL ML T B Total (%)

4 3 3 – 27 (8.05)22 17 – – 133 (39.70)

9 24 – – 69 (20.59)6 9 – – 27 (8.05)5 2 1 2 14 (4.17)5 3 2 – 18 (5.37)– – 10 7 17 (5.07)7 5 – – 19 (5.67)3 – 1 2 11 (3.28)

61 63 17 11 335

, more than one lobe; T, trachea; B, bronchi.

60 L.M. Dar et al. / Small Ruminant Research 110 (2013) 57– 61

Fig. 3. (a) Cut section of lung showing dirty grey to greenish cheesy pusin the abscesses. (b) Suppurative pneumonia: section of lung revealingcentral caseo-necrotic core surrounded by pyogenic membrane with infil-

Fig. 4. (a) Intersitial pneumonia: cut section of lung showing cir-cumscribed consolidated area in the lung parenchyma. (b) Interstitial

tration of polymorphonuclear cells. H&E, 400×. (For interpretation of thereferences to colour in this figure legend, the reader is referred to the webversion of this article.)

Age-wise distribution of lung lesions (Table 3) revealedhigher prevalence 25.40% (285/1122) in less than 1 yearof age group as compared to 19.01% (50/263) in greaterthan 1 year of age group (significant, P < 0.05). The find-ings recorded in the present study were in accordance withobservations made by earlier workers (Hartley and Boyes,1955; Orr, 1995; Smits et al., 1998; Clark et al., 2001; Fairleyet al., 2002; Alley, 2002) who reported higher prevalenceof pneumonic lesions in lambs (due to progressive wan-ing of passive immunity increasing their susceptibility tomicrobial infection) compared to the adult sheep.

The type and distribution of lung lesions observed havebeen tabulated (Table 4). The gross lesions observed in theaffected lungs included red hepatization 39.70% (133/335),grey hepatization 20.59% (69/335), lung abscesses 8.05%(27/335), congestion 8.05% (27/335), frothy lungs 5.07%(17/335), pock lesions 5.37% (18/335), emphysema andatelectasis 5.67% (19/335), and pulmonary haemorrhage3.28% (11/335), in that order. Parasitic lesions due tolungworms were present in 4.17% (14/335). In thepresent study, the predominant gross lesions were redhepatization (37.31%) and grey hepatization (23.88%)

which was in agreement with the observations made byRaji et al. (2000).

Lesions were observed either in a single lung lobe orinvolved multiple lobes (Table 4). Out of the total of 335

pneumonia: section of lung revealing interstitial pneumonia with thick-ening of interalveolar septae along with infiltration of lymphocytes,neutrophils and macrophages. H&E, 400×.

grossly affected lungs, 86 (25.67%) were having lesionsonly in apical lobes, 63 (18.80%) in cardiac lobes only,34 (10.15%) in intermediate lobe only, and 61 (18.21%)in diaphragmatic lobes only, whereas, 63 (18.80%) lungshad lesions distributed in more than one lobe. Also, 17(5.07%) and 11 (3.28%) lungs were having lesions con-fined only to trachea and bronchi, respectively. Duringthe present study, it was noticed that lung lobes on theright side were affected more frequently than on the leftside. The spatial distribution of lesions observed in presentstudy was in accordance with reports of earlier workers(Suryanarayanmurthy et al., 1977; Rahman and Iyer, 1979;Jubb et al., 1985; Lal Krsihna Gupta, 1989; Kamil, 1989;Kumar, 2005). The predominance of the lesions in cranio-ventral portions of lung has been attributed to shortnessand abrupt branching of air ways, greater deposition ofinfectious organisms, inadequate defense mechanisms,reduced vascular perfusion, gravitational sedimentation ofexudates and regional differences in ventilation (Lopez,2001).

All the 335 affected lungs were screened histopatho-logically. The lesions were classified on the basis ofthe predominant pathological changes observed. Further,

prevalence of individual lesions was also estimated aspercentage of the affected lungs screened. The histopatho-logical lesions observed included acute bronchopneumonia(Fig. 1a and b) 36.11% (121/335), fibrinous pneumonia

L.M. Dar et al. / Small Ruminant Re

Fig. 5. (a) Verminous pneumonia: lung showing copious foamy froth intmi

(maaa((

idvelaasa

R

AA

B

B

pneumonia in Madras. J. Vet. Sci. Anim. Husb. 6, 48–52.

rachea-bronchial tree with slender thread-like worms (arrow). (b) Ver-inous pneumonia: section of lung showing cross section of lungworm

n the lumen of bronchus. H&E, 400×.

Fig. 2a and b) 9.55% (32/335), chronic bronchopneu-onia 15.22% (51/335), suppurative pneumonia (Fig. 3a

nd b) 10.74% (36/335), interstitial pneumonia (Fig. 4and b) 5.67% (19/335), verminous pneumonia (Fig. 5and b) 2.98% (10/335), bronchitis and bronchiolitis 4.47%15/335), haemorrhage 3.28% (11/335), congestion 6.56%22/335), and emphysema/atelectasis 5.37% (18/335).

In summary, the present survey constituted a start-ng point towards a better knowledge of ovine respiratoryiseases in Kashmir valley. Slaughter sheep served as aaluable study material for screening and monitoring thevolution of ovine lung affections in our region. High preva-ence of ovine lung affections owed to multiple factors suchs adverse climatic conditions during winters, poor man-gement and lack of proper feeding regimen leading toubstantial economic losses due to reduced lamb growthnd decreased carcass value.

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