Small Ruminant Research 79 (2008) 152–157

Contents lists available at ScienceDirect

Small Ruminant Research

journa l homepage: www.e lsev ier .com/ locate /smal l rumres

Prevalence and distribution of peste des petits ruminants virusinfection in small ruminants

Haider Ali Khana,∗, Muhammad Siddiqueb, Muhammad Abubakarc,Muhammad Javed Arshadc, Manzoor Hussaind

a Department of Microbiology, University of Agriculture, Faisalabad 38040, Pakistanb Faculty of Veterinary Science, University of Agriculture, Faisalabad, Pakistanc National Veterinary Laboratory, Islamabad, Pakistand FAO project (GTFS/INT/907/ITA) for Central Asian Countries, Pakistan

a r t i c l e i n f o

Article history:Received 22 February 2008Received in revised form 30 June 2008Accepted 22 July 2008Available online 7 September 2008

Keywords:Peste des petits ruminantsCompetitive ELISAPrevalenceSmall ruminants

a b s t r a c t

Peste des petits ruminants (PPR) is an acute febrile viral disease of small ruminants char-acterized by mucopurulent nasal and ocular discharges, necrotizing stomatitis, enteritisand pneumonia. The disease is endemic in Pakistan causing heavy economic losses due tohigh rate of mortality and morbidity. The present study was conducted in view of deter-mining the disease situation in different geographical regions, seasons, age, sex groups andspecies of small ruminants. A total of 933 serum samples were collected from the south-ern, northern, western, eastern and central parts of the Punjab province. Samples werecollected from the animals suffering from diarrhoea and showing severe respiratory signs.Serum samples were used for the detection of antibodies against PPR virus (PPRV) by apply-ing competitive enzyme linked immuno-sorbent assay. Based on the screening of the 933sera samples, the antibody prevalence of PPRV in small ruminants in Punjab was 51.34%(P < 0.432). The frequency of antibodies against PPR recorded was 67.65, 71.11 and 60.23%in the months of December, January and February and 50.67 and 53.0% in the months ofSeptember and October, respectively. The higher numbers of positive cases were observed insouthern and western districts of Punjab province, compared to other parts of the province.A greater proportion of the sheep (56.80%) versus the goat (48.24%) population was foundto be infected with PPRV (P < 0.011). The distribution and prevalence of antibodies to PPRV

among various age groups of animals indicated that the higher prevalence (72.86%) occurredat >2 years compared with the other age groups. It was found that PPR has high frequency(59.24%) in females than males (41.18%) of sheep and goat (P < 0.001). These findings maybe correlated with variations in the sheep and goat husbandry practices within different

s, the t.

geographic regionindividual farmers

∗ Corresponding author. Tel.: +92 41 8710624.E-mail addresses: imhkhan2002@gmail.com (H.A. Khan),

profdrmsiddiqueuaf@gmail.com (M. Siddique), Hayee42@yahoo.com(M. Abubakar), manzoorh@isb.paknet.com.pk (M. Hussain).

0921-4488/$ – see front matter © 2008 Elsevier B.V. All rights reserved.doi:10.1016/j.smallrumres.2008.07.021

opography of different states and the socio-economic status of

© 2008 Elsevier B.V. All rights reserved.

1. Introduction

Peste des petits ruminants (PPR) is an acute highly con-tagious febrile viral disease of sheep and goat, which is

characterized by high fever, ocular and nasal discharges,pneumonia, necrosis and ulceration of mucous membraneand inflammation of gastrointestinal tract leading to severediarrhoea. The disease is caused by PPR virus belongingto the genus morbillivirus in the family paramyxoviridae

inant Re

(ovdutu

(nmiaetr2

sAoPiwwgoig2vPtcmc(cf

taIp

TA

A

SNWECG

T

T

C

H.A. Khan et al. / Small Rum

Gibbs et al., 1979). The genus morbillivirus form a groupf antigenically related viruses: measles virus, rinderpestirus, canine distemper virus, phocid distemper virus andolphin distemper virus (Barrett et al., 1993). It causesp to 50–80% mortality and about 90% morbidity amonghe small ruminants. Goats are affected severely but sheepndergo a mild form of disease (Lefevre and Diallo, 1990).

It was first described in West Africa in early 1940sGargadennec and Lalanne, 1942), when it was used to beamed as Kata, pseudo-rinderpest and stomatitis pneu-oentritis syndrome (Braide, 1981). It has been reported

n Sudan (El Hag and Taylor, 1984), Ethiopia (Roeder etl., 1994), Kenya and Uganda (Wamwayi et al., 1995). It isndemic in the Arabian Peninsula, the Middle East and inhe Indian subcontinent (Shaila et al., 1996). PPR has beeneported in various parts of Asia and Africa (Dhar et al.,002).

The existence of PPR has been recognized in Pakistanince 1991 on the basis of clinical signs (Pervez et al., 1993;thar et al., 1995; Amjad et al., 1996; Tahir et al., 1998) andn the basis of cELISA (Khan et al., 2007) in Punjab province.PR is considered to be one of the main constraints inmproving productivity of small ruminants in the regions

here it is endemic. Pakistan is an agricultural countryith a total population of 264 and 537 millions sheep and

oat, respectively. In Punjab province, the total populationf sheep and goat is 63 and 198 millions, respectively. Its almost 24 and 37% of overall population of sheep andoats, respectively in Pakistan (Pakistan Livestock Census,006). The ratio of sheep to goats’ population intensityaries greatly under different agro-climatic conditions. Inakistan, sheep and goats play an important role in sus-ainable agriculture and for poverty alleviation. The diseaseauses heavy economic losses on the basis of mortality,orbidity, losses through body wastage, poor feed effi-

iency, loss of meat, milk and milk products and offspringNawathe, 1984; Durojaiye et al., 1983). Presence of diseasean limit trade and export and there is loss of animal proteinor human consumption.

PPR is endemic in many countries including the Sul-anate of Oman and Saudi Arabia (Taylor et al., 1990; Asmarnd Radwan, 1980) in Jordan (Lefevre et al., 1991) and inndia (Shaila et al., 1989; Singh et al., 2004a). However,attern of PPR infection and its seroprevalence in small

able 1ntibody-based prevalence of peste des petits ruminants virus (PPRV) in sheep an

rea wise distribution Sheep total Sheep positive % G

outhern districts 60 44 73.33 66orthern districts 88 18 20.45 24estern districts 33 26 78.79 31

astern districts 30 14 46.67 11entral districts 55 35 63.64 10overnment farmsKhizrabad government farm 60 49 81.67 8BLPRI Kherimurat 12 6 50 35

otal 72 55 76.39 43

otal 338 192 59Positive % 56.80

.I. for sheep 51.33–62.15; C.I. for goats 44.15–52.33; C.I. for overall population 48

search 79 (2008) 152–157 153

ruminants in Pakistan has not been systematically stud-ied. In the present study, efforts have been made to collectpreliminary information for the prevalence of antibodies inunvaccinated animals, its distribution in different groupsof animals and the host affinity of PPRV in various regionsof Punjab province. All the observations are based on theinvestigations of data generated from the screening of 933sera samples originating from these regions. This informa-tion will be very useful in the development of a PPR controlprogramme using an indigenously developed PPR vaccine.

2. Materials and methods

2.1. Study area

A total of 25 districts of southern, northern, western, eastern and cen-tral parts of Punjab province were selected. In randomly selected villagesof each district, the owners of the animals were interviewed according tothe pre-designed questionnaire. Two government farms: Barani Area Live-stock Production Research Institute (BLPRI), district Attock and KhizrabadLivestock Farms, district Sargodha were selected to determine the preva-lence of disease at these farms (Table 1).

2.2. Clinical samples

A total of 933 serum samples (338 sheep and 595 goats) were collectedfrom the animals with diarrhoea, mouth lesions and severe respiratorysigns. All the sera were stored at −20 ◦C for further use. Postmortem ofthe dead animals was conducted and the findings were recorded.

2.3. Determination of antibodies

A competitive ELISA (cELISA) kit was used for the detection of PPRVantibodies in the collected serum samples (IAH, Pirbright Laboratory, UK).The test is based upon the competition between the anti-H protein mon-oclonal antibody and antibodies in the serum samples for binding to theantigen. The 50% competition cut-off was taken as the positive value as rec-ommended by the manufacturer. The negative and positive cut-off valueswere used from the controls of the test procedure. The ELISA micro-plateswere read with an Immunoskan (Flow Laboratories, UK) reader with aninference filter of 492 nm. The reader was connected to computer loadedwith ELISA Data Interchange (EDI) software (FAO/IAEA, Vienna, Austria),which was used to automate the reading and calculation of percentageinhibition (PI) values. The OD (optical density) values were converted topercentage inhibition by using the following formula:

PI = 100 − OD control/test serumOD monoclonal control

× 100

The data was be analyzed for the species, sex, age, and area wiseprevalence of PPRV in small ruminants.

d goat in various regions of Punjab province

oat total Goat positive % Total Total positive %

46 69.70 126 90 71.433 125 51.44 331 143 43.20

16 51.61 64 42 65.631 23 20.72 141 37 26.241 50 49.50 156 85 54.49

5 62.5 68 54 79.4122 62.86 47 28 59.57

27 62.79 115 82 71.30

5 287 933 479Positive % 48.24 Positive % 51.34

.07–54.59 (P < 0.011) (confidence interval).

inant Research 79 (2008) 152–157

Fig. 3. PI-based frequency distribution of negative population of goats inPunjab.

154 H.A. Khan et al. / Small Rum

3. Results

3.1. Clinical and postmortem findings

The most frequent clinical findings in diseased ani-mals were high temperature (up to 105.6–107 ◦F), markeddepression, severe mucopurulent nasal and ocular dis-charges, necrotic stomatitis, respiratory distress anddiarrhoea was observed in some cases when the tem-perature subsided. The varying degrees of erosion ofmucosa of the whole gut, from the mouth to the rec-tum was observed in the morbid animals. The rumen wasempty and had congested papillae. The colon, rectum,liver, kidneys, pancreas, lungs and brain were congested.The mesenteric lymph nodes were edematous. The tra-chea, nostrils and bronchi were filled with mucopurulentfroth.

3.2. Frequency distribution of antibodies to PPRV insheep and goat

The cELISA was conducted to determine antibodiesagainst PPRV. The sera showing PI value greater than 50%were considered as positive. The competitive ELISA wasused to clearly differentiate the exposed (infected) pop-ulation from the unexposed (not infected) population.Considerable differences were observed between the sheepand goat populations when the results of the competitiveELISA were plotted as a frequency of the percent inhibi-

tion (Figs. 1–4). Among the samples considered negativefor PPRV, (PI < 50%) the maximum number of samples hada percent inhibition of between 5 to 35 and 10 to 20 for goatsand sheep, respectively. Alternatively, among the samplesconsidered positive for PPRV, (PI > 50%) a peak frequency

Fig. 1. PI-based frequency distribution of negative population of sheep inPunjab.

Fig. 2. PI-based frequency distribution of positive population of sheep inPunjab.

Fig. 4. PI-based frequency distribution of positive population of goats inPunjab.

distribution between 90 and 95% was observed for thesheep and goats population.

3.3. Species-wise antibody-based prevalence of PPRV

The antibody-based prevalence against PPRV in sheepand goats was 56.80% (95% C.I.) and 48.24% (95% C.I.),respectively. A significant proportion of sheep versus goatspopulation was infected (P < 0.011). The overall prevalenceof PPRV in small ruminants was 51.34%.

3.4. Sex-wise antibody-based prevalence of PPRV insheep and goats

The prevalence of antibodies to PPRV among male andfemale sheep and goats was studied. The antibody-basedprevalence against PPRV in female of sheep and goats were

65.20 and 54.70%, respectively, compared to 39.64 and41.75% for corresponding males. The females were moreprone to infection of PPRV and showed significantly highernumber of positive cases (P < 0.011) at 95% C.I. (Table 2).

Table 2Sex-wise antibody-based prevalence of peste des petits ruminants virus(PPRV) in sheep and goats

Sheep Goat Overall

Male Female Male Female Male Female

44/111 148/227 124/297 163/298 168/408 311/52539.64% 65.20% 41.75% 54.70% 41.18% 59.24%

95% C.I. for male 39.25–49.48; C.I. for female 48.42–58.13 (P < 0.011).

H.A. Khan et al. / Small Ruminant Research 79 (2008) 152–157 155

Table 3Age-wise antibody-based prevalence of peste des petits ruminants virus (PPRV) in sheep and goats

Sheep +ve Goat +ve

0–12 months 1–2 years >2 years 0–12 months 1–2 years >2 years

67/141 78/132 59/75 101/238 148/292 43/6547.52% 59.09% 78.67% 42.44% 50.68% 66.15%

95% C.I. for 0–10 months 36.12–46.40; C.I. for 1–2 years 47.60–57.39; C.I. for >2 years population 65.56–80.40.

Table 4Antibody-based prevalence of peste des petits ruminants virus (PPRV) in two government livestock farms of sheep and goats

Name of farms Sheep total Sheep +ve % Goat total Goat +ve % Total Total +ve %

Khizrabad government farm 60 49 81.67 8 5 62.5 68 54 79.41B 3

T 4

9 opulatio

3

ahtbtpwp

3y

bSFr(

3l

dfa(

3P

re(tC(

virus for the ovine species versus the caprine species hasbeen observed (Khan et al., 2007). These laboratory find-ings suggested that the same virus capable of inducing highmortality in goats may not produce as severe infection insheep, but the reverse may not be true. Further investiga-

Table 5Month-wise antibody-based prevalence of peste des petits ruminantsvirus (PPRV) in 2005–2006

Months Sheep Goats Total Positive %

December 2005 39 97 136 92 67.65January 2006 38 50 88 53 60.23February 2006 36 54 90 64 71.11

LPRI Kherimurat 12 6 50

otal 72 55 76.39

5% C.I. for sheep 64.91–85.60; C.I. for goats 46.72–77.02; C.I. for overall p

.5. Age-wise antibody-based prevalence of PPRV

The prevalence of antibodies to PPRV among variousge groups of sheep and goats was studied (Table 3). Theighest prevalence of PPRV was observed in animals olderhan 2 years of age. A higher proportion (47.52%) of sheepetween the age group of 0–12 months were found posi-ive for PPRV as compared to goats (42.44%). Similarly theercentage positive of adult animals (1–2 years) for PPRVas greater in the sheep (59.09%) versus the goat (50.68%)opulation.

.6. Month-wise antibody-based prevalence of PPRV inear 2005–2006

The higher frequency of positive cases was foundetween December 2005 to February 2006 and duringeptember 2006 and October 2006 (Table 5). December toebruary appeared to be the period of greatest risk of smalluminants to PPR each year while in April (45%) and June48.28%) the disease was present moderately.

.7. Antibody-based prevalence of PPRV at governmentivestock farms

Peste des petits ruminants antibodies were alsoetected in sheep and goats kept at two government

arms. The prevalence of antibodies to PPRV in the sheepnd goat population was 76.39 and 62.79%, respectivelyTable 4).

.8. Region-wise antibody-based prevalence of PPRV inunjab province

The overall prevalence of antibodies to PPRV in smalluminants was higher in southern (71.43%) and west-rn (65.63%) districts of Punjab as compared to central54.49%), northern (43.20%) and eastern (26.24%) dis-ricts of Punjab. The southern districts and desert ofholistan had a higher proportion of PPR antibodiesTable 1).

5 22 62.86 47 28 59.57

3 27 62.79 115 82 71.30

n 62.12–79.35.

4. Discussion

The majority of PPR outbreaks in the past have beendiagnosed based on clinical signs. An extensive clinical sur-vey of PPRV infection has been difficult up to this pointbecause the diagnostic tests that were available for thedetection of PPRV were not commonly implemented. Thedevelopment of a MAb-based competitive ELISA kit forPPRV antibody detection has greatly facilitated the diag-nosis of PPRV. The competitive ELISA used in the presentinvestigation had high diagnostic specificity (99.8%) andsensitivity (90.5%) for the detection of PPRV antibody inconvalescent sera when compared with the gold stan-dard VNT (Anderson and McKay, 1994; Singh et al., 2004b;Libeau et al., 1992). The implementation of this diagnostictest aided in tracking PPR outbreaks in different geographi-cal regions, measuring economic losses resulting from PPRVinfection and studying the epidemiology of the disease insusceptible populations.

The present investigation revealed differences in theseverity of PPRV infection in goats and sheep. In the presentstudy, as well as in previous studies of PPRV isolates orig-inating from northern districts, a higher affinity of the

March 2006 22 36 58 28 34.88April 2006 8 32 40 18 45.00May 2006 31 33 64 20 31.25June 2006 18 25 43 15 48.28July 2006 16 17 33 14 34.78August 2006 24 15 39 14 35.90September 2006 52 98 150 76 50.67October 2006 32 68 100 53 53.00November 2006 22 70 92 32 42.42

inant R

156 H.A. Khan et al. / Small Rum

tion is required to determine reasons for the difference inthe pathogenicity of PPRV in caprine and ovine species.

The greater severity of the disease in goats may beattributed to a greater susceptibility of the goat populationto infection with PPRV. The recovery rate of goats infectedwith PPRV is considerably less than that of sheep infectedwith the virus (Wosu, 1994; Dhar et al., 2002). In addition,the productivity of goats is higher than that of sheep, sonewborn kids replace a large proportion of the goat popu-lation each year. Newborn animals become susceptible toPPRV infection at 3–4 months of age (Srinivas and Gopal,1996), corresponding with the natural decline in mater-nal antibodies (Saliki et al., 1993), and this large number ofyoung susceptible stock may also account for the severityof PPRV infection in the goat population.

The higher antibody-based prevalence against PPRV inthe sheep versus goat population should not be misinter-preted as an increased susceptibility of sheep to infectionwith PPRV. Rather, this may be attributed to a higher recov-ery rate (lower case fatality rate) and/or a greater longevityof sheep versus goats. In another study a case fatality rate of34.4% versus 46.9% was observed in the sheep versus goatpopulation, respectively (Shankar et al., 1998). The overallantibody response to PPRV was observed 22.4% by Ozkulet al. (2002) which comprises many other PPRVs whoseorigins are in the Middle East, the Arabian Peninsula, andSouthern Asia, were isolated from Turkish sheep.

A significantly higher antibody-based prevalence ofPPRV was observed in females than males. The femalesare maintained for a longer period of time as compared tomales in order to promote production practices, which mayindirectly account for the high prevalence of antibodies toPPRV in female animals.

A large number of animals become infected during theperiod of December to February due to the nomadic graz-ing of the areas. The animals leave the area due to harshweather and move towards the plain areas. These animalsthen help to maintain the circulation of the virus through-out the year by frequent animal-to-animal transmission(Singh et al., 2004a). Climatic factors favourable for the sur-vival and spread of the virus may also contribute to theseasonal distribution of PPR outbreaks. With the start of therainy season between July/August, the migratory activity ofanimals is reduced due to the increased availability of localfodder. The nutritional status of the animals also improves,resulting in an increased resistance to infection. These fac-tors may play a key role in limiting the transmission ofdisease.

Obi (1983) and Durojaiye et al. (1983) reported out-breaks of PPR during the dry and cold months of the year. InOyo state (western Nigeria), Opasina (1983) also reportedfour outbreaks of PPR in the same months of the year.Bourdin (1983) on the other hand stated that in the Sahe-lian climate of Senegal, outbreaks of PPR occurred mostlyduring the rainy season. Reported occurrence of new out-breaks within 48 h of rainfall as in Ondo state in Nigeria

(Ojo, 1983) was not confirmed in this study.

Antibody-based prevalence against PPRV among vari-ous age groups of animals were carried out and findingssuggested that the higher proportion of sheep between theages of 0–12 months were positive for PPRV as compared

esearch 79 (2008) 152–157

to goats because sheep has a longevity life and somewhatresistant to PPR, whereas the goats are much susceptible toPPR. Similarly the percentage positive of adult animals (1–2years) for PPRV was greater in the goats versus the sheeppopulation. The distribution and prevalence of antibodiesto PPRV among various age groups of animals indicatedthat the goats were exposed at an earlier age than sheep,suggesting that goats may be more susceptible to infectionwith PPRV and the animals of >2 years of age may haveexperienced numerous outbreaks during the life span.

A high prevalence of PPRV was observed in southern andwestern regions of Punjab province as compared to north-ern, eastern and central regions. Between 1991 and 1995severe outbreaks of PPRV were reported in the southernand western parts of Punjab (Pervez et al., 1993; Athar etal., 1995; Hussain et al., 1998; Tahir et al., 1998). The greaterlength of time that PPRV has been endemic in the southernand western districts may account for the higher prevalenceof infection observed in these regions.

The northeastern parts of the province have got rel-atively small sheep and goat population, and, althoughprevious outbreaks have been reported in this region fol-lowing the transport of goats from endemic zones of theprovince (Athar et al., 1995) and these factors may respon-sible for the low PPRV antibody prevalence (43.20 and26.24%) reported in this region as compared to the rest ofthe province.

References

Amjad, H., Islam, Q.U., Forsyth, M., Barrett, T., Rossiter, P.B., 1996. Peste despetits ruminants in goat in Pakistan. Vet. Rec. 139, 118–119.

Anderson, J., McKay, J.A., 1994. The detection of antibodies against pestedes petits ruminants virus in cattle, sheep and goats and the possibleimplications to rinderpest control programmes. Epidemiol. Infect. 112(1), 225–231.

Asmar, J.A., Radwan, A.I., 1980. A PPR like disease in central Saudi Arabia:evidence of its immunologic relation to rinderpest; prospects for acontrol method, Proceedings of the 4th Conference Biological Aspectsof Saudi Arabia University of Riyadh, Riyadh 10–13 March 1980, pp325–338.

Athar, H., Islam, Q.U., Azim, F., Shakoor, A., Maqbool, A., Chaudhary, N.I.,1995. An outbreak of peste des petits ruminants-like disease amonggoats in Punjab (Pakistan). Pak. Vet. J. 15, 140–143.

Barrett, T., Visser, I.K.G., Mamaev, L., Goatley, L., Bressem, M.F., VanOsterhaus, A.D.M., 1993. Dolphine and porpoise morbilliviruses aregenetically distinct from phocine distemper virus. Virology 193,1010–1012.

Bourdin, P., 1983. History, epidemiology and economic significance of PPRin West Africa and Nigeria in particular. In: Hill, D.H. (Ed.), Peste despetite ruminants (PPR) in sheep and goats. Proceedings of the Interna-tional Workshop held at IITA. Ibadan, Nigeria, 24–26 September 1980.ILCA (International Livestock Centre for Africa), Addis Ababa, Ethiopia,pp. 10–11.

Braide, V.B., 1981. Peste des petits ruminants. World Anim. Rev. 39, 25–28.Dhar, P., Sreenivasa, B.P., Barrett, T., Corteyn, M., Singh, R.P., Bandyopad-

hyay, S.K., 2002. Recent epidemiology of peste des petits ruminantsvirus (PPRV). Vet. Microbiol. 88 (2), 153–159.

Durojaiye, O.A., Obi, T.U., Ojo, O., 1983. Virological and serological diagnosisof peste des petits ruminants. Trop. Vet. 1, 13–17.

El Hag, B., Taylor, T.W., 1984. Isolation of PPR virus from Sudan. Res. Vet.Sci. 36, 1–4.

Gargadennec, L., Lalanne, A., 1942. La peste des petits ruminants. Bull. Serv.Zoo. A. O. F. 5, 15–21.

Gibbs, E.P., Taylor, W.P., Lawman, M.J.P., Bryant, J., 1979. Classification ofpeste des petits ruminants virus as the fourth member of the genusMorbillivirus. Intervirology 11 (5), 268–274.

Hussain, M., Afzal, M., Muneer, R., Ashfaq, M., Haq, E.U., 1998. An outbreakof peste des petits ruminants in goats in Rawalpindi. Pak. Vet. J. 18,224–225.

inant Re

K

L

L

L

N

O

O

O

O

P

P

H.A. Khan et al. / Small Rum

han, H.A., Siddique, M., Arshad, M.J., Khan, Q.M., Rehman, S.U., 2007. Sero-prevalence of peste des petits ruminants (PPR) virus in sheep and goatsin Punjab province of Pakistan. Pak. Vet. J. 27, 85–87.

efevre, P.C., Diallo, A., 1990. Peste des petits ruminants virus. Rev. Sci.Tech. Off. Int. Epiz. 9 (4), 951–965.

efevre, P.C., Diallo, A., Schenkel, F., Hussein, S., Staak, G., 1991. Serologicalevidence of peste des petits ruminants in Jordan. Vet. Rec. 128 (5), 110.

ibeau, G., Diallo, A., Calvez, D., Lefever, P.C., 1992. A competitive ELISAusing anti-N monoclonal antibodies for specific detection of RP anti-bodies in cattle and small ruminants. Vet. Microbiol. 31, 147–160.

awathe, D.R., 1984. The control of peste des petits ruminants in Nigeria.Prev. Vet. Med. 2, 147–155.

bi, T.U., 1983. Symptomatology. In: Hill, D.H. (Ed.), Peste des petiteruminants (PPR) in sheep and goats. Proceedings of the Interna-tional Workshop held at IITA. Ibadan, Nigeria, 24–26 September 1980.ILCA (International Livestock Centre for Africa), Addis Ababa, Ethiopia,p. 10.

jo, M.O., 1983. Role of other agents and factors responsible for the patho-genesis of PPR. In: Hill, D.H. (Ed.), Peste des petite ruminants (PPR)in sheep and goats. Proceedings of the International Workshop heldat IITA. Ibadan, Nigeria, 24–26 September 1980. ILCA (InternationalLivestock Centre for Africa), Addis Ababa, Ethiopia, p. 54.

pasina, B.A., 1983. Epidemiology of PPR in the humid forest and thederived savanna zones. In: Hill, D.H. (Ed.), Peste des petite ruminants(PPR) in sheep and goats. Proceedings of the International Workshopheld at IITA. Ibadan, Nigeria, 24–26 September 1980. ILCA (Interna-tional Livestock Centre for Africa), Addis Ababa, Ethiopia, pp. 14–21.

zkul, A., Akca, Y., Alkan, F., Barrett, T., Karaoglu, T., Dagalp, S.B., Anderson,J., Yesilbag, K., Cokcaliskan, C., Gencay, A., Burgu, I., 2002. Prevalence,distribution, and host range of peste des petits ruminants virus, TurkeyEmerg. Infect. Dis., 8 (7), 708–712.Rev. Sci. Tech. Off. Int. Epiz., 23 (3)

818.

akistan Livestock Census, 2006, Agricultural Census Organization, Statis-tics Division, Government of Pakistan.

ervez, K., Ashfaq, M., Khan, M.S., Hussain, M.M., Azim, E., 1993. A rinder-pest like disease in goats in Punjab, Pakistan. Pak. J. Livest. Res. 1,1–4.

search 79 (2008) 152–157 157

Roeder, P.L., Abraham, G., Kenfe, G., Barrett, T., 1994. PPR in Ethiopian goats.Trop. Anim. Health Prod. 26, 69–73.

Saliki, J.T., Libeau, G., House, J.A., Mebus, C.A., Dubovi, E.J., 1993. Mon-oclonal antibody based blocking ELISA for specific detection andtitration of peste des petits ruminants antibody in caprine and ovinesera. J. Clin. Microbiol. 31 (5), 1075–1082.

Shaila, M.S., Purushothaman, V., Bhavasar, D., Venugopal, K., Venkatesan,R.A., 1989. Peste des petits ruminants in India. Vet. Rec. 125 (24),602.

Shaila, M.S., Shamaki, D., Forsyth, M.A., Diallo, A., Goatley, L., Kitching, R.P.,Barrett, T., 1996. Geographic distribution of peste des petits ruminantsviruses. Virus Res. 43 (2), 149–153.

Shankar, H., Gupta, V.K., Singh, N., 1998. Occurrence of peste des petitsruminants like disease in small ruminants in Uttar Pradesh. Indian J.Anim. Sci. 68 (1), 38–40.

Singh, R.P., Saravanan, P., Sreenivasa, B.P., Singh, R.K., Bandyopadhyay, S.K.,2004a. Prevalence and distribution of peste des petits ruminants (PPR)virus infection in small ruminants. Rev. Sci. Tech. Off. Int. Epiz. 23 (3),807–819.

Singh, R.P., Sreenivasa, B.P., Dhar, P., Shah, L.C., Bandyopadhyay, S.K., 2004b.Development of monoclonal antibody based competitive ELISA fordetection and titration of antibodies to peste des petits ruminants(PPR) virus. Vet. Microbiol. 98 (1), 3–15.

Srinivas, R.P., Gopal, T., 1996. Peste des petits ruminants (PPR): a newmenace to sheep and goats. Livest. Advis. 21 (1), 22–26.

Tahir, M.T., Ahmad, R., Hussain, I., Hussain, M., 1998. Counter Immuno-electrophoresis—a rapid technique for the diagnosis of PPR. Pak. Vet.J. 18, 55–56.

Taylor, W.P., Al Busaidy, S., Barrett, T., 1990. The epidemiology of pestedes petits ruminants in the Sultanate of Oman. Vet. Microbiol. 22 (4),341–352.

Wamwayi, H.M., Rossiter, P.B., Kariuki, D.P., Wafula, J.S., Barrett, T., Ander-son, J., 1995. Peste des petits ruminants antibodies in East Africa. Vet.Rec. 136, 199–200.

Wosu, L.O., 1994. Current status of peste des petits ruminants (PPR) dis-ease in small ruminants. A review article. Stud. Res. Vet. Med. 2, 83–90.