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Small Ruminant Research 104 (2012) 195– 200

Contents lists available at SciVerse ScienceDirect

Small Ruminant Research

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

hort communication

isk of seroconversion to peste des petits ruminants (PPR) and itsssociation with species, sex, age and migration

umit Mahajana,∗, Rajesh Agrawala, Mahesh Kumarb, Anand Mohanb, Nishi Pandec

Division of Veterinary Epidemiology and Preventive Medicine, F.V.Sc & AH, SKUAST-Jammu, J&K, IndiaDepartment of Epidemiology and Preventive Medicine, C.V.A.Sc., GBPUA&T, Pantnagar, Uttrakhand, IndiaDivision of Animal Reproduction Gynecology and Obstetrics, F.V.Sc & AH, SKUAST-Jammu, J&K, India

r t i c l e i n f o

rticle history:eceived 1 June 2011eceived in revised form 16 October 2011ccepted 18 October 2011vailable online 15 November 2011

eywords:iskssociationeste des petits ruminants (PPR)heepoat

a b s t r a c t

The present investigation included a detailed description of risk of PPR in small ruminantsand its association with various host and environmental factors. A total of 432 serumsamples comprising of 216 samples (108 sheep and 108 goats) from migratory and 216samples (108 sheep and108 goats) from non-migratory flocks of sheep and goat werescreened for PPR antibodies using competitive-ELISA. The overall seroprevalence of PPR inmigratory flocks (33.79%) was significantly (p < 0.05) higher as compared to non-migratoryflocks (24.07%). The seroprevalence of PPR in sheep (29.16%) was higher than that of goat(28.70%) but the difference was non-significant, age wise seroprevalence was significantly(p < 0.05) higher in >12 months age group (39.58%) followed by 8–12 months (26.38%) and4–8 months (20.83%) age group. On risk factor analysis, it was observed that at 95% confi-dence interval, odd ratio was higher in migratory (1.610) than non-migratory (0.612) flocks,in sheep (1.023) than goats (0.978), the value of odd ratio was higher in >12 months agegroup (2.490 and 1.828) as compared to 4–8 months and 8–12 months, respectively. The

overall sex wise seroprevalence in males (33.33%) was significantly (p < 0.05) higher thanin females (24.53%) and also risk factor analysis revealed a higher odd ratio in males (1.538,overall; 1.581, migratory and 1.503, non-migratory) than in females (0.650, overall; 0.633,migratory and 0.655 non-migratory). The present study relates the variation of PPR risk inassociation with species, age, sex, sheep and goat husbandry practices.

. Introduction

Peste des petits ruminants (PPR), which literally meansPlague of small ruminants”, is an acute viral disease ofmall ruminants caused by a Morbillivirus belonging tohe family Paramyxoviridae (Gibbs et al., 1979) and iselated to Canine distemper, Rinderpest and Measles virusVan mol et al., 1995), The natural disease affects mainly

oats and sheep, but it is usually more severe in goatshere, it causes severe morbidity and mortality and is only

ccasionally severe in sheep (Raghavendra et al., 2000).

∗ Corresponding author. Tel.: +91 01923 250242.E-mail address: sumit22 mahajan@rediffmail.com (S. Mahajan).

921-4488/$ – see front matter © 2011 Elsevier B.V. All rights reserved.oi:10.1016/j.smallrumres.2011.10.009

© 2011 Elsevier B.V. All rights reserved.

The course of disease is about 2 weeks and generallydeath occurs within 10–12 days after infection (Lefevreand Diallo, 1990). Disease is characterized by high riseof temperature, oral and oculo-nasal discharges, necroticstomatitis, severe pneumonia, dyspnoea, coughing, enteri-tis and severe diarrhoea followed by death (Roeder and Obi,1999; Pawaiya et al., 2004). The disease is endemic in Indiaand is a major threat to about 200 million small ruminantpopulation of the country (Dhar et al., 2002), causing aneconomic loss of about 1800 million Indian rupees annually(Bhadyopadhyay, 2002). Close contact is the most impor-

tant way of transmitting the disease. It is suspected thatthe infectious materials can also contaminate water, feedtroughs and bedding, turning them into additional sourcesof the infection. These are however short term sources,

inant Re

196 S. Mahajan et al. / Small Rum

since the PPRV, like its close relative the Rinderpest virus,would not be expected to survive for a long time outsidethe host (Diallo, 2003). In addition to these sources of infec-tion movement of animals across the boundaries of statescommonly acts as source of PPR epidemics. There is noknown carrier state in PPR and the infected animal maytransmit the disease itself during the stage of incubationperiod. However, the PPR infected animal’s sero-convertand become immune to PPR and RP viruses (Sudarshanet al., 1995). Singh et al. (2004a) discussed the relation ofmigration of animals with that of maintenance and trans-mission of PPRV in nature. The close relations betweenPPR outbreaks and transportation of sheep and goats flockshave been reported (Boniwell, 1980; Dhand et al., 2002;Kataria et al., 2007; Shankar et al., 1998). Migration mayalso spread infection to cattle (Shaila et al., 1989). In India,animal rearing is practiced in two major ways: one is unor-ganized back yard rearing (where 5–10 sheep or goats arereared in backyards and fed up on the agriculture byprod-uct) and the other is the traditional rearing of sheep andgoats by nomadic communities (where the animals are fedon pasture lands and uncultivated or barren fields dur-ing the course of migration). Most of the earlier studiesfrom India were conducted on sheep and goats of non-migratory flock (Singh et al., 1996, 2004a; Kataria et al.,2007; Bhanuprakash et al., 2008) but the present study cov-ered animals of both migratory and non-migratory flocks.The study was conducted with the prime aim to assess therisk of PPR in unvaccinated animals in relation to the vari-ous host factors and migration. This may prove to be helpfulin rational decision making for formulating preventive andcontrol strategies against PPR.

2. Materials and methods

2.1. Study area

The present study was conducted during the year 2009–2010 in stateof Jammu and Kashmir (J&K) India. A total of 6 major migratory routes usedby nomadic community were selected for migratory flocks of sheep andgoats. For studying non-migratory flocks, villages from 6 districts of J&Kwere selected randomly. A pre-designed questionnaire was used to inter-view the owners of the flocks. Data related to species, age, sex and routeof migration was gathered to ascertain the difference in seroprevalenceand risk in migratory versus non-migratory flocks along with species, ageand sex predisposition to PPR in sheep and goats.

2.2. Sample collection

A total of 432 serum samples comprising of 216 samples (108 sheepand 108 goats) of migratory and 216 samples (108 sheep and 108 goats) ofnon-migratory flocks were collected from animals unvaccinated againstPPR. Of the 108 samples 56 each from males and females of sheep andgoats of migratory and non-migratory flocks. The animals of three agegroups viz., 4–8 months, 8–12 months and >12 months were includedin the study. Blood was collected from animals by jugular-vein punctureusing vacuette tubes (Greiner Laboratortechnik, Germany) and left to clotat 4 ◦C until transported to laboratory. The serum was collected after cen-trifugation, transferred to 2 ml centrifuge tube and stored at −20 ◦C untilused for detection of PPR antibodies.

2.3. Determination of antibodies

The PPR specific antibodies were detected using competitive ELISA(cELISA) kit for PPR, developed by National Rinderpest Laboratory, Divi-sion of Virology, IVRI, Mukteswar, India. As per the protocol the ELISAplates showing proper colour development in control wells were read at

search 104 (2012) 195– 200

492 nm in ELISA plate reader (Multiskan plus, LabSystem). To interpret theresults of the c-ELISA, EDI (ELISA Data Interchange) software developedby the FAO/IAEA (Jeggo and Anderson, 1992) was used.

2.4. Interpretation of test results

The test sera samples showing per cent inhibition (PI) value of 50%or above of mean OD values of Cm (monoclonal antibody control) weretaken as positive and less than 50% were considered as negative for PPRantibodies. The results were expressed in terms of PI by converting theoptical density (OD) to PI according to the following formula:

PI = 100 −[(

OD of the test wellsOD of the Cm wells

)× 100

]

2.5. Statistical analysis of risk factor

The statistical association of PPR disease with regard to species (sheepand goats), age, sex, migration and non-migration was analyzed throughindependent Chi-square test and the odd ratio was determined at 95% CIusing online program (http://statpages.org/ctab2x2.html).

3. Results

3.1. Flock wise seroprevalence and risk of PPR

The seroprevalence of PPR in migratory flocks were sig-nificantly (p < 0.05) higher (33.79%) than in non-migratory(24.07%) flocks of different districts (Table 1).

3.2. Species wise seroprevalence and risk of PPR

The seroprevalence of PPR in sheep (29.16%) was higherthan that of goat (28.70%) but the differences were non-significant in both migratory and non-migratory flocks.Similarly the odd ratio was higher in sheep (1.023) as com-pared to goats (0.978). Further detailed statistical analysishas been shown in Table 2.

3.3. Age wise seroprevalence and risk of PPR

Age wise analysis of data revealed significantly (p < 0.05)higher seroprevalence of PPR in >12 months age group(39.58%) followed by 8–12 months (26.38%) and 4–8months (20.83%) age group. On risk factor analysis, it wasobserved that at 95% confidence interval, the value of oddratio was higher in >12 months age group (2.490 and 1.828)as compared to 4–8 months and 8–12 months, respectively.

In migratory animals of >12 months age group, theodd ratio was 3.500 and 2.429 when compared with 4–8months and 8–12 months, respectively. A similar trendbut with lower odd ratio values was recorded in the non-migratory flock. The detailed age wise analysis of riskfactor between different age groups of migratory and non-migratory flocks of sheep and goats has been shown inTables 3–5.

3.4. Sex wise seroprevalence and risk of PPR

The overall seroprevalence in males (33.33%) was non-

significantly (p < 0.05) higher than in females (24.53%).In sheep, the overall seroprevalence was significantly(p < 0.05) higher in males (38.88%) than in females (19.44%)(Table 6).

S. Mahajan et al. / Small Ruminant Research 104 (2012) 195– 200 197

Table 1Antibody based seroprevalence and risk of PPR in migratory and non-migratory flocks of sheep and goat.

Species Risk factor Odd ratio 95% CI Percentpositive (%)

SheepMigration 1.802 0.996–3.261 35.18Non-migration 0.555 0.307–1.004 23.15

GoatMigration 1.438 0.797–2.594 32.40Non-migration 0.695 0.358–1.254 25.00

OverallMigration 1.610 1.059–2.448 33.79Non-migration 0.612 0.408–0.945 24.07

CI, confidence interval.

Table 2Antibody based species wise seroprevalence and risk of PPR in migratory and non-migratory sheep and goat.

Type of flock Risk factor Odd ratio 95% CI Percentpositive (%)

MigratorySheep 1.132 0.646–1.986 35.18Goat 0.883 0.504–1.549 32.40

Non-migratorySheep 0.904 0.486–1.679 23.15Goat 1.107 0.596–2.056 25.00

Migratory + non-migratorySheep 1.023 0.676–1.548 29.16Goat 0.978 0.732–1.322 28.70

CI, confidence interval.

Table 3Antibody based risk of PPR between different age groups of migratory sheep and goats.

Risk factor 4–8 M 8–12 M >12 M

Migratory flocks

4–8 M

– 1.000 (0.388–2.956) (sheep) 0.550 (0.212–1.431) (sheep)0.419 (0.133–0.337) (goat) 0.129 (0.042–0.398) (goat)0.694 (0.329–1.462) (overall) 0.286 (0.140–0.585) (overall)

8–12 M

1.000 (0.388–2.956) (sheep) – 0.550 (0.212–1.431) (sheep)2.000 (0.794–5.249) (goat) 0.308 (0.117–0.813) (goat)1.441(0.754–2.306) (overall) 0.412 (0.208–0.815) (overall)

1.455 (0.799–2.689) (sheep) 1.818 (0.699–4.725) (sheep) –3.2502.429

F

4

mdP

TA

F

>12 M 7.750 (2.511–23.667) (goat)

3.500 (1.708–7.166) (overall)

igures in parenthesis indicate 95% confidence interval.

. Discussion

The primary base of any disease control program is itsonitoring and diagnosis. Three methods may be used to

iagnose and monitor the distribution and prevalence ofPR: case recording of PPR outbreaks, serological detection

able 4ntibody based risk of PPR between different age groups of non-migratory sheep

Risk factor 4–8 M 8–12

Non-migratory flocks

4–8 M

– 1.0000.6000.781

8–12 M

1.000 (0.338–2.956) (sheep) –

1.667 (0.541–5.113) (goat)

1.281 (0.583–2.813) (overall)

>12 M

1.125 (0.387–3.268) (sheep) 1.1252.500 (0.838–7.406) (goat) 1.5001.706 (0.793–3.664) (overall) 1.332

igures in parenthesis indicate 95% confidence interval.

(1.230–8.575) (goat) (1.227–4.807) (overall)

of PPR specific antibodies and detection of the virus.Although, case recording of PPR outbreaks could give some

clues in the areas where the disease is endemic, laboratorydiagnosis is essential for confirmation. The development ofMAb-based competitive ELISA kit for PPRV antibody detec-tion has greatly facilitated the diagnosis of PPRV in India.

and goats.

M >12 M

(0.338–2.956) (sheep) 0.857 (0.296–2.487) (sheep) (0.196–1.850) (goat) 0.400 (0.135–1.193) (goat)

(0.335–1.717) (overall) 0.586 (0.273–1.260) (overall)

0.857 (0.296–2.487) (sheep)0.667 (0.244–1.827) (goat)0.751 (0.359–1.596) (overall)

(0.387–3.268) (sheep) – (0.547–4.102) (goat)

(0.637–2.783) (overall)

198 S. Mahajan et al. / Small Ruminant Research 104 (2012) 195– 200

Table 5Antibody based risk of PPR between different age groups of migratory and non-migratory sheep and goats.

Risk factor 4–8 M 8–12 M >12 M

Migratory flocks + non-migratory

4–8 M

– 1.000 (0.480–2.084) (sheep) 0.674 (0.332–1.369) (sheep)0.503 (0.223–1.139) (goat) 0.255 (0.103–0.494) (goat)0.734 (0.426–1.246) (overall) 0.402 (0.239–0.676) (overall)

8–12 M

1.000 (0.480–2.084) (sheep) – 0.674 (0.332–1.369) (sheep)1.988 (0.878–4.492) (goat) 0.448 (0.224–0.899) (goat)1.362 (0.791–2.346) (overall) 0.547 (0.333–0.900) (overall)

1.484 (0.730–3.013) (sheep) 1.484 (0.730–3.013) (sheep) –2.2321.828

>12 M 4.436 (2.026–9.692) (goat)

2.490 (1.479–4.189) (overall)

Figures in parenthesis indicate 95% confidence interval.

Singh et al. (2004b) developed this MAb-based c-ELISA fordetection of antibodies to PPRV using a virus neutralis-ing Mab directed against the epitope of haemagglutininprotein specific to PPRV. The competitive ELISA used inthe present investigation has high diagnostic specificity(99.8%) and sensitivity (90.5%) for the detection of PPRVantibody in convalescent sera when compared with thegold standard VNT (Anderson and McKay, 1994; Libeauet al., 1992; Singh et al., 2004b). The implementation of c-ELISA test in tracking PPR in different geographical regionsof India and abroad may help in assessing economic lossesresulting from PPRV infection as it is a faster means ofstudying the epidemiology of the disease in susceptiblepopulations.

In the present, study the risk of PPR was 1.610 timeshigher in migratory flocks than in non-migratory flocks.The animals of these migratory flocks were brought fromhilly areas through different routes after the completionof their seasonal migration to escape severe winters. Thisseasonal movement of animals may increase the chanceof transmission among the migratory flocks. Moreover, inmigratory flocks, there is transportation stress, underfeed-ing and underlying parasitic infection which may decreasethe immunity, thereby increasing the susceptibility of ani-mals to disease. This may be supported by the findings ofother workers who reported out breaks of PPR in migratoryherds in Himachal Pradesh (Joshi et al., 1996) and Rajasthan

(Singh et al., 1996). Similarly Khan et al. (2007) reportedhigher seroprevalence of PPR in southern and western partsof Punjab of Pakistan where nomadic rearing of sheep andgoats was common.

Table 6Antibody based sex wise prevalence and risk of PPR in migratory and non-migrat

Species Riskfactor

Migratory Non-migrato

Oddratio

95% CI Percentpositive (%)

Oddratio

9

SheepMale 2.719 1.204–6.130 46.29 2.642 1Female 0.368 0.163–0.830 24.07 0.379 0

GoatMale 0.919 0.413–2.043 31.48 0.906 0Female 1.088 0.490–2.419 33.33 1.104 0

OverallMale 1.581 0.897–2.784 38.88 1.503 0Female 0.633 0.359–1.115 28.70 0.665 0

CI, confidence interval.

(1.113–4.474) (goat) (1.112–3.004) (overall)

The seroprevalence of PPR and odd ratio was higherin sheep (28.16%; 1.023) as compared to goats (28.70%;0.978). The higher seroprevalence in sheep can be due tothe fact that the disease is more severe in goats as com-pared to sheep (Radostits et al., 2000). Hence, more numberof infected animals survive the infection in sheep therebyincreasing the seroprevalence. The results follow the sim-ilar pattern as observed by Bhaskar et al. (2009), Krishnaet al. (2001), Singh et al. (2004a) from India and Goossenset al. (1998), Khan et al. (2007, 2008) and Ozkul et al. (2002)from other countries. The higher risk of PPR in sheep ascompared to goats revealed by the odd ratio should notbe misinterpreted for increased susceptibility of sheep toinfection with PPRV. This higher seroprevalence may beattributed to fact that the disease is less severe in sheepleading to higher recovery rate in infected sheep than goats.Shankar et al. (1998) reported high survival and lower casefatality rate in sheep (34.4%) than goats (46.9%). Similarly,Sharma et al. (2007) observed significantly higher (p < 0.05)morbidity and mortality in case of goats as compared tosheep.

Age wise analysis of data revealed a higher seropreva-lence in >12 months (39.58%) than 8–12 months (26.38%)and lowest in 4–8 months (20.83%) age group. The lowerprevalence of PPR in young stock may be due to the passiveimmunity provided to them by colostral antibodies up to 4months of age in the young ones of exposed (or vaccinated)

females. Susceptibility to PPRV infection in kids increasesthereafter corresponding with the natural decline in mater-nal antibodies. Ata and Al-Sumry (1988) reported a lowerprevalence of PPR in kids of dam with previous history of

ory sheep and goat.

ry Migratory + non-migratory

5% CI Percentpositive (%)

Oddratio

95% CI Percentpositive (%)

.044–6.661 31.48 2.636 1.433–4.849 38.88

.150–0.958 14.81 0.379 0.206–0.698 19.44

.384–2.140 24.07 0.913 0.508–1.642 27.78

.467–2.607 25.92 1.095 0.609–1.968 29.62

.803–2.808 27.78 1.538 1.012–2.337 33.33

.356–1.243 20.38 0.650 0.428–0.988 24.53

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S. Mahajan et al. / Small Rum

PR up to 3–5 months of age. The findings are also in agree-ent with Abubakar et al. (2009), Agrawal et al. (2006), Obi

t al. (1983), Shukla et al. (2008) and Tahir et al. (2000),ho observed an increase in seropostivity of PPR with an

dvancement of age. However, in sheep a higher seropreva-ence of 26.38% was noted in 4–8 months age group thann goats (15.27%) of similar age group. This may be due tohe higher survival rate in young stock of sheep. In addi-ion to this, the fecundity of goats is higher than that ofheep, so new born kids replace a large proportion of stockach year and these new born animals become suscepti-le to PPRV infection at 3–4 months of age (Singh et al.,004a). Odd ratio values in present investigation, indicatehat the risk of PPR was higher in >12 and 8–12 monthsge group than in 4–8 months age group of animals. Buthis should not be misinterpreted, that the severity of dis-ase increases with age, rather this higher odd ratio maye due to higher survival rate of adults in which severityf disease is less as compared to young ones. Sharma et al.2007) observed significantly higher morbidity, mortalitynd case fatality rate in kids and lambs than the adults.hmad et al. (2005) also reported higher mortality rate inucklers (1–3 months) than in young ones (4–12 months)nd adults (>1 years).

Sex wise seroprevalence of PPR in sheep was signif-cantly (p < 0.05) higher in males than females and thendings are in alignment with Rahman et al. (2004). Onhe other hand seroprevalence of PPR was higher in femaleoat than its male counterpart but the difference wason-significant. Swai et al. (2009) observed similar resultsith non-significant values whereas Khan et al. (2008)

nd Munir et al. (2008) observed significantly higher sero-revalence in female goats. The possible reason of highereroprevalence in male sheep than male goats is that theale goats are sold at an earlier age (1–2 years) in localarkets for meat purpose whereas the males of sheep are

etained for longer period for wool production. Furthernalysis of odd ratio between male and female revealedhat males of sheep and goats are 1.538 times more proneo PPR than females. The higher seroprevalence and oddatio in males in both the species may be attributed to sex-al behavior of the males during breeding season, as malesf both the species come in contact with females of dif-erent flocks frequently during mating, thus increasing therobability of getting infected.

. Conclusion

In nutshell it can be concluded that PPR is widely preva-ent in sheep and goats of J&K state of India. The studyhows the evidences of natural transmission of PPR inheep and goats of J&K with considerable variation in riskf PPR between species whereas within species the riskf PPR varies considerably with age and sex and type ofock viz., migratory or non-migratory. It is important thathe increase in seroprevalence or seroconversion should

ot be misinterpreted for the increased susceptibility toPRV infection. The results of the present study are alsomportant to direct further studies like virus isolation andharacterization of isolates to explore the epidemiological

search 104 (2012) 195– 200 199

pattern of PPR in sheep and goats which are much neededto formulate a control and eradication programme for PPR.

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