Transboundary and Emerging Diseases

ORIGINAL ARTICLE

Peste des Petits Ruminants Virus: An Emerging Threat to Goat Farming in Pakistan M. Abubakar1 and M. Munir2 1 2

National Veterinary Laboratory, Islamabad, Pakistan The Pirbright Institute, Newbury, Berkshire, UK

Keywords: goat farming; PPR virus; outbreaks; Pakistan; economic losses Correspondence: M. Abubakar. National Veterinary Laboratory, Park Road, Islamabad, Pakistan. Tel.: +92519255104; Fax: +92519255105; E-mail: [email protected] Received for publication August 30, 2013 doi:10.1111/tbed.12192

Summary Pakistan at present is having more than 60 million head of goats, which consist of about 37 well-recognized breeds found in different regions of the country. Although the goat farming on commercial level is escalating in Pakistan, there are threats, which result this initiative into a loss. Among these threats, Peste des Petits Ruminants (PPR) outbreaks are causing huge economic damages. In this study, three outbreaks of PPR were confirmed at three different commercial farms in various regions of Punjab province and their economic impact on small ruminants farming was calculated. The disease started after 1–2 months of the establishment of these farms as the animals were purchased from different livestock markets. Disease started with sudden onset of respiratory and enteric clinical signs and spreads quickly. Disease caused mortality and morbidity of 10–15% and 20–40%, respectively, within a time period of 01–03 weeks. At these three farms, 116 of 365 animals exhibited the clinical disease, with an overall morbidity rate of 31.78%. A total of 43 animals died with mortality rate of 11.78% (43/365) causing a direct financial loss of $4300 (Pakistan Rupees 430 000/-), while the indirect cost due to treatment, loss of animal body condition, reduction in market value, increase veterinary services and labour was $7911 (Pak Rs. 791 100/-). Taken together, the results demonstrate that there is an urgent need to assess the economic impact of the disease throughout the country and to give proper emphasis for controlling PPR in sensitive regions where it is discouraging the investment in goat farming.

Introduction Livestock are natural factories to convert roughage (grasses, shrubs, etc.) into quality food that is, milk and meat. Goats are well-admired and well-documented worldwide for providing food in terms of milk and meat. They are playing a key role in supporting millions of people who are poor, landless and living in the rural areas, especially in developing countries. Peste des Petits Ruminants (PPRV) has caused significant economic losses in many parts of Africa and Asia that contain high densities of small ruminant population. According to a 2009 United Nations Food and Agricultural Organisation (FAO) report, the proportion of the global small ruminant population that is at risk of PPR can be as high as 62.5% (OIE, 2009). Peste des Petits Ruminants is

considered to be a major limiting factor in the development of the small ruminant industry in disease epidemic areas (Munir et al., 2013a). It is especially prevalent in developing countries of Africa and Asia, where small ruminants play a vital role in sustainable agriculture employment (Singh et al., 2004). Pakistan, being an agricultural country, has a huge livestock population including sheep and goats. Goats play a significant role in the country’s economy by producing approximately 366 thousand tons of mutton (Economic Survey, 2012–13). The main stock occurs in the form of nomadic and transhumant production system, but the goat farming at commercial level for meat production is also emerging as a successful business. Although the goat farming on commercial level is increasing in the country, there are threats, which result this initiative into a loss.

© 2014 Blackwell Verlag GmbH • Transboundary and Emerging Diseases. 61 (Suppl. 1) (2014) 1–4

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PPR and Goat Farming in Pakistan

M. Abubakar and M. Munir

Among these threats, PPR outbreaks are causing huge economics damages. Every year, thousands of small ruminants die with this disease and therefore substantially affecting production of small ruminants and economy of the country. Goat farming is a profitable business only if protected from infectious diseases. In country like Pakistan, where husbandry conditions are poor, all possible procedures should be followed to prevent this disease (Munir et al., 2013b). This report is designed to highlight the economic importance of PPRV in three outbreaks only, which indicate the impact of the disease on the production of small ruminants during onset of PPR. Materials and Methods Outbreaks description and study plan Outbreaks were investigated at three commercial farms (Farms A, B & C) of sheep and goats in various regions of Punjab province (Taxila, Attock and Rawalpindi), Pakistan (Fig. 1). One farm (Farm A) also had the population of sheep that were also affected (Table 1). The disease started after 1–2 months of the establishment of these farms. The animals (6–10 months of age) were purchased from different livestock markets with no history of PPRV vaccination. So animals from different sources were purchased and combined at a single farm. The average cost of each animal was around $100 (Pak Rs.10 000/animal). The other costs including treatment cost (both for medicine and disinfectants), loss of animal body condition, reduction in market

Taxilla Jammu & Kashmir (disputed territory)

Attock Rawalpindi

Pakistan

Areas of commercial farms with PPR outbreaks

Fig. 1. Map of the country indicating sampling sites.

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value, veterinary services and labour costs were also calculated. These were estimated based on the duration of disease, number of clinically affected animals and course of treatment. Collection of samples and laboratory confirmation Nasal and ocular swabs were taken from sick animals, while tissues from lungs, liver, spleen, intestines and lymph nodes were collected from dead animals. Blood serum was also collected from sick animals. Twenty swabs and twenty serum samples, collected from clinically suspected animals, were tested for PPRV with immunocapture enzyme-linked immunosorbant assay (IcELISA) and competitive ELISA (cELISA), respectively. Representative samples of dead animals from each infected herds (05 from each herd) were also taken and tested through IcELISA and RT-PCR. The details of these samples are given in the Table 2. Tests used for the confirmation of outbreaks IcELISA The kit used to analyse these samples was imported from World Reference Laboratory for PPR antigen detection (Pirbright, UK). Ortho-phenylenediamine (OPD) was used as chromogen, and the absorbance was measured at a wavelength of 492 nm. The reader was connected to computer loaded with ELISA Data Interchange (EDI) software (FAO/ IAEA, Vienna, Austria), which was used to automate the reading and calculation of percentage positivity (PP) values. The optical density (OD) values were converted to PP, and the samples with PP >18% were considered as positive (Libeau et al., 1994). cELISA Competitive ELISA was carried out to detect the presence of antibodies against PPRV. The PPR cELISA kit collectively produced by Biological Diagnostic Supplies Ltd, Flow Laboratories and The Pirbright Institute (formerly Institute for Animal Health), Pirbright, Surrey, UK, was used for testing and analysis of samples. The test depends on the competition between monoclonal antibodies against nucleoprotein (N) of PPRV and the specific anti-N antibodies in the test serum samples binding the PPR antigen (Libeau et al., 1995). The OD values were converted to percentage inhibition (PI), and the samples with PI >50% were considered as positive. RT-PCR From tissue samples, total cellular RNA was extracted to assess the presence of viral nucleic acid using the RNAeasy kit (Qiagen, Valencia, CA, USA) as per the manufacturer’s

© 2014 Blackwell Verlag GmbH • Transboundary and Emerging Diseases. 61 (Suppl. 1) (2014) 1–4

M. Abubakar and M. Munir

PPR and Goat Farming in Pakistan

Table 1. Areawise distribution of Peste des Petits Ruminants with species and mortality rate Area

Animal species

Total animal kept

Diseased

Mortality

Morbidity rate (%)

Mortality rate (%)

Taxila

Goat Sheep Goat Goat

110 35 150 70 365

35 13 45 23 116

15 3 18 07 43

31.82 37.14 30 32.86 31.78

13.64 8.57 12 10 11.78

Attock (Fateh Jang) Rawalpindi Total

Table 2. Summary of samples tested with different tests Type of samples

No. of samples

Swab

20

Serum Tissue

Test applied cELISA

IcELISA

RT-PCR

Results



15

17

20

20





15



13

15

Positive for PPR antigen + F-gene detection Positive for PPR antibodies Positive for PPR antigen + F-gene detection

PPR, Peste des Petits Ruminants.

instructions. Reverse transcription polymerase chain reaction (RT-PCR) was performed for the F-gene of PPRV using one-step RT-PCR kit (Invitrogen) as per the manufacturer’s instructions. PCR was carried out using PCR primers and conditions as described previously (Forsyth and Barrett, 1995). Results Disease started with sudden onset of fever, respiratory and enteric clinical signs and spreads quickly. At all the three farms, overall 365 animals were present, among them 116 depicted disease, giving morbidity rate of 31.78%. Disease caused mortality of 10–15% and morbidity of 20–40% within a time period of 1–3 weeks. There were 43 animals died, giving an overall mortality rate of 11.78% (43/365). The case fatality rate was about 37% (43/116) (Table 1). Among the samples tested, swab and tissue samples were positive with both IcELISA and RT-PCR, while all the serum samples were found positive for PPR antibodies (Table 2). All positive samples on IcELISA gave high PP values depicting the acute phase of outbreak situation. In terms of economics, there was a direct loss of $4300 (Pak Rs. 430 000/- taking 1$ = Pak Rs.100) due to the high case fatality rate. Keeping in view, the average treatment duration was 7 days (Pak Rs. 300/animal/day), while other costs were about Pak Rs. 100/animal/day. Additionally, indirect losses including the cost for the treatment of sick animals were $2436 (Pak Rs. 243 600/-), while the other

costs due to loss of animal body condition, reduction in market value, increased labour and veterinary services were $5475 (Pak Rs. 547 500/-). So the overall indirect losses due to PPR for these three outbreaks were $7911 (Pak Rs.791 100/-). Discussion The study presents an important scenario for the goat farming industry in Pakistan. As the efforts are going on to enhance this industry to meet the food demands, also to improve the quality of meat. The emergence of diseases like PPR has a huge impact on this industry. Due to lack of awareness and unavailability of quality PPR vaccine, the disease has become endemic in Pakistan (Abubakar et al., 2009, 2011; Zahur et al., 2011; Munir et al., 2013a). The other reason for endemicity is that there is no national control programme for PPR in the country. One of the finding of the study is that although different levels of mortality rate occurred at the affective farms, there were also the financial implications like the treatment cost and decline in farm productivity. There was a direct loss of $4300 (Pak Rs. 430 000/-), and indirect losses including the cost for the treatment of sick animals, loss of animal body condition, reduction in market value, increased labour and veterinary services were $7911 (Pak Rs.791 100/-). In a similar study in neighbouring country, India, Thombare and Sinha (2009) presented the data from PPR affected villages pertaining to disease incidence, production losses, costs incurred and impact on farm productivity collected though personal interview method (Thombare and Sinha, 2009). Reduction in the market value of animals has been recorded as the major loss component as appearance of the animal changes drastically after the illness. It is followed by losses in production yield. Expenditure on medicine and infertility has been found to cause more than 80% of the total cost, followed by veterinary and labour services. They suggested that timely vaccination could be the best and low-cost preventive measure to control this disease. In this study, it was found that outbreaks occurred 1–2 months after setting up the farm. One possible explanation for this could be the excretion of PPR virus in body secretion from the infected animals and subsequent

© 2014 Blackwell Verlag GmbH • Transboundary and Emerging Diseases. 61 (Suppl. 1) (2014) 1–4

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PPR and Goat Farming in Pakistan

M. Abubakar and M. Munir

transmission to uninfected one. Similarly, we have previously demonstrated that the secretion of PPRV antigen in faecal material in which they described a possible mechanism of virus transmission following natural infection and this approach may demonstrate a potential method by which PPRV outbreaks occur spontaneously in areas not previously known to have circulating virus (Abubakar et al., 2012). Shedding of PPRV antigen in the faecal material of the recovered goats following a disease incursion put forward the possibility that goats may be shedding the PPR virus in their faeces. These findings are also in agreement with Ezeibe et al. (2008) and may reinforce the idea that virus can subclinically infect animals and excrete and/or transmit virus to na€ıve ‘in contact’ animals. Nevertheless, the main reason for these outbreaks is the endemic nature of PPR in Pakistan. Findings in this study clearly indicate that PPR is one of the major barriers in the commercialization of small ruminant farming in Pakistan. Such high economic losses are unbearable for the small farmer, leading to termination of this business. This situation is further aggravated by the unavailability of the quality PPR vaccine for routine use in goats, especially in the endemic regions. Therefore, it is recommended, for the sake of food security issues, to assess the economic impact of the disease throughout the country and to give proper emphasis for controlling PPR in sensitive regions where it is discouraging the investment in goat farming. Acknowledgements The support of field veterinary staff is appreciated in reporting the outbreaks. Financial support of FAO Regional Project (GTFS/INT/907/ITA) is acknowledged. Conflicts of Interest The authors have no potential conflicts of interest. References Abubakar, M., S. M. Jamal, M. J. Arshed, M. Hussain, and Q. Ali, 2009: Peste des petits ruminants virus (PPRV) infection: its association with species, seasonal variations and geography. Trop. Anim. Health Prod. 41, 1197–1202. Abubakar, M., M. J. Arshed, M. Hussain, and Q. Ali, 2011: Evidence of Peste des petits ruminants in serology of sheep and goats from Sindh, Pakistan. Transbound. Emerg. Dis. 58, 152–156.

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Abubakar, M., M. J. Arshed, A. B. Zahur, Q. Ali, and A. C. Banyard, 2012: Natural infection with Peste des petits ruminants virus: a pre and post vaccinal assessment following an outbreak scenario. Virus Res. 167, 43–47. Economic Survey. 2012–13. Economic Adviser’s Wing, Finance Division, Government of Pakistan, Islamabad. Ezeibe, M. C. O., O. N. Okoroafor, A. A. Ngene, J. I. Eze, I. C. Eze, and J. A. C. Ugonabo, 2008: Persistent detection of peste de petits ruminants antigen in the faeces of recovered goats. Trop. Anim. Health Prod. 40, 517–519. Forsyth, M. A., and T. Barrett, 1995: Evaluation of polymerase chain reaction for the detection and characterisation of rinderpest and peste des petits ruminants viruses for epidemiological studies. Virus Res. 39, 151–163. Libeau, G., A. Diallo, and L. Colas Fand Guerre, 1994: Rapid differential diagnosis of rinderpest and peste des petits ruminants using an immunocapture ELISA. Vet. Rec. 134, 300–304. Libeau, G., C. Prehaud, R. Lancelot, F. Colas, L. Guerre, D. H. L. Bishop, and A. Diallo, 1995: Development of a competitive ELISA for detecting antibodies to the peste des petits ruminants virus using a recombinant nucleoprotein. Res. Vet. Sci. 58, 50–55. Munir, M., S. Zohari, and M. Berg, 2013a: Current advances in molecular diagnosis and vaccines for peste des petits ruminants. In: Munir, M., S. Zohari and M. Berg (eds), Molecular Biology and Pathogenesis of Peste des Petits Ruminants Virus, pp. 105–133. Springer, Berlin, Germany. Munir, M., A. Saeed, M. Abubakar, S. Kanwal, and M. Berg, 2013b: Molecular characterization of Peste des Petits Ruminants viruses from outbreaks caused by unrestricted movements of small ruminants in Pakistan. Transbound. Emerg. Dis. doi: 10.1111/tbed.12089. Singh, R. P., P. Saravanan, B. P. Sreenivasa, R. K. Singh, and S. K. Bandyopadhyay, 2004: Prevalence and distribution of peste des petits ruminants virus infection in small ruminants in India. Rev. Sci. Tech. 23, 807–819. Thombare, N. N., and M. K. Sinha, 2009: Economic implications of Peste des petits ruminants (PPR) disease in sheep and goats: a sample analysis of district Pune, Maharashtra. Agric. Econ. Res. Rev. 22, 319–322. World Organisation for Animal Health (OIE), 2009.Technical Disease Cards: Peste des Petits Ruminants. Availale at http:// www.oie.int/eng/maladies/Technical%20disease%20cards/PESTE%20DES%20PETITS%20RUMINANTS_FINAL.pdf (accessed February 19, 2013). Zahur, A. B., A. Ullah, M. Hussain, H. Irshad, A. Hameed, M. Jahangir, and S. M. Farooq, 2011: Sero-epidemiology of peste des petits ruminants (PPR) in Pakistan. Prev. Vet. Med. 102, 87–92.

© 2014 Blackwell Verlag GmbH • Transboundary and Emerging Diseases. 61 (Suppl. 1) (2014) 1–4

Peste des Petits Ruminants virus: an emerging threat to goat farming in Pakistan.

Pakistan at present is having more than 60 million head of goats, which consist of about 37 well-recognized breeds found in different regions of the c...
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