Serological evidence of camel exposure to peste des petits ruminants virus (PPRV) in Nigeria

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Trop Anim Health Prod (2015) 47:603–606 DOI 10.1007/s11250-014-0747-6

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Serological evidence of camel exposure to peste des petits ruminants virus (PPRV) in Nigeria Timothy Yusufu Woma & Demo Joab Usman Kalla & Pius Stephen Ekong & Hussaini Gulak Ularamu & Solomon Chuwang Chollom & Iliya Iliyasu Lamurde & Dogonyaro Benjamin Bajehson & Nenfa Danjuma Tom & Gideon Bature Aaron & David Shamaki & Dalan Bailey & Adama Diallo & Melvyn Quan

Received: 17 April 2014 / Accepted: 11 December 2014 / Published online: 30 December 2014 # Springer Science+Business Media Dordrecht 2014

Abstract Peste des petits ruminants (PPR), a viral disease of sheep and goats, is endemic in Nigeria. There are reports indicating the involvement of peste des petits ruminants virus (PPRV), the causative agent of PPR, in a camel respiratory syndrome in Africa. Considering that camels share the same grazing land and drinking points with other ruminants, this study was undertaken to determine the seroprevalence and extent of PPRV antibodies in Nigerian camels. A total of 1517 camel sera samples were collected from four states (Borno, Kano, Kastina and Sokoto). The seroprevalence was determined by the H-protein-based competitive ELISA. The overall prevalence was 3.36 % (51/1517, 95 % confidence interval of 2.51–4.39 %). There was no significant differences in prevalence between states (p=0.8921) and between male and female camels (p=0.7424). The prevalence differed

significantly (p5 years (p=0.0042). These results show occasional transient PPRV infection of camels in Nigeria, and there is the need to include camels among species to be studied in elucidating the epidemiology of the disease in sheep and goats. Keywords PPRV . Seroprevalence . Camel . c-ELISA . Nigeria

Introduction T. Y. Woma (*) : M. Quan Department of Veterinary Tropical Diseases, University of Pretoria, Private Bag X04 0110, Onderstepoort, South Africa e-mail: [email protected] T. Y. Woma : A. Diallo Animal Production and Health Laboratory, International Atomic Energy Agency, Wagramer Strasse 5, P.O.Box 100, 1400 Vienna, Austria T. Y. Woma : P. S. Ekong : H. G. Ularamu : S. C. Chollom : I. I. Lamurde : D. B. Bajehson : N. D. Tom : G. B. Aaron : D. Shamaki Morbilliviruses Research Laboratory, National Veterinary Research Institute, P.M.B 01, Vom 930001, Nigeria D. J. U. Kalla Animal Production Programme, Abubakar Tafawa Balewa University, P.M.B 0248, Bauchi 740001, Nigeria D. Bailey School of Immunity and Infection, University of Birmingham, B15 2 TT, Birmingham, UK

Peste des petits ruminants (PPR), caused by peste des petits ruminants virus (PPRV), belongs to the genus Morbillivirus, family Paramyxoviridae, which includes a small group of other antigenically related viruses such as canine distemper virus of dogs, measles virus of man, rinderpest virus of cattle, feline morbillivrus of cats, and phocine, dolphin and porpoise morbilliviruses of sea living mammals (Woo et al 2012). In Nigeria, the camel population estimated at about 20,000 heads (FAO 2012) is located in the Northern States, and camels represent an important economic resource for the pastoral population in these states. Evidence of camels infection by PPRV has been recorded in many reports (Shamaki 2002; Haroun et al. 2002; Abraham et al. 2005; Khan et al. 2008; Chauhan et al. 2009; Albayrak and Gür 2010; Khalafalla et al. 2010; Kinne et al. 2010; Balamurugan et al. 2012). The aim of this study was to determine the seroprevalence and extent of PPRV antibodies in camels in Nigeria. The results of this study will enhance the knowledge of the

604

epidemiology of PPR in the country as camels share grazing land and drinking points with sheep, goats and cattle.

Materials and methods Abattoirs in Maiduguri (Borno State), Kano (Kano State), Katsina (Katsina State) and Sokoto (Sokoto State), northern Nigeria were selected as sites for sample collection. The majority of the camels in Nigeria (an estimated 80 %) occur in these four states and they cover a combined area of about 70,714 km2 and are the desert gateways with important camel trade (Fig. 1). Our aim was to collect a maximum of 384 samples per state based on calculations using a prevalence of 50 %, a confidence of 95 % and a margin of error of 5 % (Dohoo et al. 2009). Convenience sampling was used: samples were collected from every fifth slaughtered camel every other day

Trop Anim Health Prod (2015) 47:603–606

(excluding Sundays) between July 2011 and April 2013. Approximately 10 ml of blood was collected from the jugular vein of each slaughtered animal in a serum vacutainer tube (Becton Dickson, UK). Each sample was labelled using codes to describe the state, sex, age and body condition score of the camel. The serum was obtained after allowing the blood to clot overnight and centrifugation at 2500g for 15 min. Samples were transported to the laboratory on ice and stored at −20 °C until analysed. A PPRV H-protein-based monoclonal antibody (Mab) competitive enzyme-linked immunosorbent assay (c-ELISA) kit (BDSL, UK) was used for the detection of antibodies to PPRV according to the manufacturer’s instruction (Anderson et al. 1991). The overall and group apparent prevalence (total positive/total sample analysed) and the exact binomial 95 % confidence intervals were computed. Pearson’s chi-squared test was used to test if there were significant differences in the number of positive and negative tests results within each

Fig. 1 Map of Nigeria showing the states where camels are predominantly found and where samples were collected

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variable. A p5 years) Young (≤5 years)

one species to another. This situation highlights the importance of including camels among the group of animals to be monitored for PPRV infection and to define their role in the epidemiology of the disease in Nigeria and elsewhere. In this study, the overall apparent prevalence for all states studied was 3.36 %. The PPRV antibodies that were detected result from natural infection of the camels, as there is no documented evidence that camels are vaccinated against PPRV in and around Nigeria. This agrees with earlier reports of 4 % (out of 250 samples) from camels in Sokoto (Daneji et al. 1997), Kano and Maiduguri (Ibu et al. 2008). The seroprevalence rate detected in this survey is also comparable to studies done in other African countries. PPRV seroprevalence rate in camels has been reported to be 3 % in Ethiopia (Abraham et al. 2005), 2.6 % in Tanzania (Swai et al. 2011), 4.2 % (using the serum neutralization test) and 14 % a decade later in Egypt (Ismael et al. 1992; Haroun et al. 2002). A lower seroprevalence rate of 0.3 % was recorded in camels in Sudan (Saeed et al. 2010) even though there was an outbreak of PPR in camels in the country with devastating clinical signs (Khalafalla et al. 2010). The variation in seroprevalence of PPRV in camels observed in different countries might be attributed partly to differences in diagnostic techniques, sample size and method, seasons of the year, management system, health care practices and presence of other concurrent disease infections (Bekele 1999; Roger et al. 2001; Khalafalla et al. 2010). Although the detection of PPR antibodies in camels in this study may not indicate clinical disease, it remains to be investigated whether the existence of the virus in camels has any epidemiological significance of virus persistence and transmission to other animal species.

No. of samples analysed

No. of positive

Percentage positive

χ2

p value

433 517 296 271

13 17 12 9

3.00 3.29 4.05 3.32

0.6189

0.8921

984 532

32 19

3.25 3.57

0.1084

0.7424

42 846 628

7 29 15

16.67 3.43 2.39

24.7109

1241 275

34 17

2.74 6.18

8.2043

0.000004

0.0042

606

The higher seroprevalence of PPRV among camels with poor body condition score (16.67 %, p5 years) camels in this study may be due to the ability of PPRV, like all other morbilliviruses to cause severe immunosuppression in its host. In conclusion, the findings of this study show that there may be occasional transient infection of Nigerian camels by PPRV probably from nearby infected sheep and goats. There is a need for further investigations into the genome characterization and epidemiology of PPRV to determine if camels play any role in the endemicity of PPRV in the Nigerian sheep and goat populations. Acknowledgments This work was supported by a grant (RFA 2 No.48) from the Agricultural Research Council of Nigeria through the Competitive Agricultural Research Grant Scheme (CARGS). We sincerely thank the staff of the Morbillivirus laboratory, NVRI Vom and all the field staff that helped during the sample collection and other logistics. D.Shamaki is a recipient of an IAEA project on PPR. T.Y. Woma is a recipient of an IAEA intern fellowship. Ethical standards This manuscript does not contain clinical studies or patient data. Conflict of interest The authors declare that they have no conflict of interest.

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