Outbreaks of PPR-FMD among Sheep and Goats in Hail, Saudi Arabia
Ahmed Zein Elabdeen Mahmoud1, Muaz Magzob Abdellatif2* and Mohamed Abdelsalam Abdalla3
1Veterinary Laboratories, Ministry of Environment, Water and Agriculture, Saudi Arabia; 2Department of Biology (Microbiology), Faculty of Arts and Science, Northern Borders University, Saudi Arabia; 3Sudan University of Sciences and Technology, Veterinary Medicine and Surgery, Sudan.
Abstract | Peste des petits ruminants (PPR) is a viral disease which primarily affects small ruminants, causing significant economic losses for the livestock industry. Clinical investigation was carried out during the suspected outbreaks of PPR/FMD in sheep and goats in Hail. Saudi Arabia. During the outbreaks 271 (20.6%) died out of 648 (49.3%) of affected animals, the overall morbidity in goats (33.3%) was higher as compared to sheep (12.3%), with a case fatality rate in goats reached 74.69% in the 2nd outbreak. Affected animals exhibited fever, stomatitis, mucopurulent to bloody nasal/ocular discharges, watery to bloody diarrhea and lameness. The major gross lesions were erosive stomatitis, hemorrhages in lung, liver, abomasum, small and large intestine. PPRV NP was detected in sheep (n=20) and goats (n=18), anti-PPRV NP was also detected among sheep and goats (n=162) by ELISA, 3ABC-FMD enzyme immunoassay were positive (n=6) when ovine sera were tested. The study revealed that PPR-FMD viruses were circulating in the region and warrants proper control measures.
Editor | Muhammad Abubakar, National Veterinary Laboratories, Park Road, Islamabad, Pakistan.
Received | April 17, 2017; Accepted | June 19, 2017; Published | June 25, 2017
*Correspondence | Muaz Magzob Abdellatif, Department of Biology (Microbiology), Faculty of Arts and Science, Northern Borders University, Saudi Arabia; Email: muazm20@gmail.com
Citation | Mahmoud, A.Z.E., M.M. Abdellatif and M.A. Abdalla. 2017. Outbreaks of PPR-FMD among sheep and goats in Hail, Saudi Arabia. Veterinary Sciences: Research and Reviews, 3(2): 38-44.
DOI | http://dx.doi.org/10.17582/journal.vsrr/2017/3.2.38.44
Key words: Outbreaks, PPR, FMD, ELISA, Hail, Saudi Arabia
Introduction
Peste des petits ruminants (PPR) is a highly contagious often fatal viral disease of domestic and wild ruminants caused by PPR virus (PPRV) of the family Paramyxoviridae (Venkataramanan et al., 2005; Diallo et al., 2007; Banyard et al., 2010). PPR is transmitted by direct contact with infectious animals shedding the virus in both ocular-nasal discharges and in fecal matter (Munir et al., 2013). Fomite contamination with the virus from infected animals such as feed troughs and bedding is an additional source of infection (Lefèvre et al., 1990). The disease is characterized by pyrexia, purulent mucous nasal/ocular discharges, necrotizing and erosive stomatitis, gastroenteritis, diarrhea and bronchopneumonia (Balamurugan et al., 2014). Geographically, PPR has been reported in the Middle East, South Asia, China and sub-Saharan Africa (Shaila et al., 1996), serological evidence has been documented in Uganda, Sudan, Tanzania and Ethiopia (Waret-Szkuta et al., 2008; Luka et al., 2011). In Saudi Arabia, it was first reported in 1990 (Abu Elzein et al., 1990), the disease has since spread to different parts of the country (Housawi et al., 2004; Al-Afaleq et al., 2004; Boshra et al., 2015; Mahmoud et al., 2016, 2017).
Foot and mouth disease (FMD) is one of the most serious transboundary animal diseases. It is a highly contagious viral disease, and may have rapid and unanticipated national and international spread and is characterized by fever and vesicular eruption in the mouth and on the feet and teats (Radostits et al., 2000; Alexandersen, 2005; Wernery and Kinne, 2012). The virus was classified under the genus aphthovirus of the family Picornaviridae (Radostits et al., 2000). Mild or unapparent infections in sheep and goats may hinder control programs (Kitching and Hughes, 2002). Outbreaks of FMD was repeatedly documented among sheep and goats in various regions of Saudi Arabia (Hafez et al., 1993a; Hafez et al., 1993b; Hamada et al., 2008; Alsayeqh and Fathi, 2012).
The current investigation was aimed at describing the pathology and epidemiology of PPR-FMD infections in four mixed flocks (sheep, goats and camels) in Hail district. Saudi Arabia.
Materials and Methods
Epidemiological investigation
Outbreaks occurred among four mixed farms (sheep, goats and camels) in Hail district. Saudi Arabia were investigated during February to May 2016 (Table 1).
Sample collection
Nasopharyngeal, ocular and rectal swabs (n=46) were collected from affected goats (n=18), sheep (n=20) and clinically healthy camels (n=8). Sera were collected from goats (n=38), sheep (n=124) and camels (n=8), samples were preserved at 4ºC until tested.
P.M Examination
Autopsy were performed on recently dead sheep (n=26) and goats (n=20), gross pathology was recorded.
PPR-NP ELISA
Immune capture ELISA kits for detection of PPR-NP antigen was used (ID Screen®PPR Antigen Capture- CIRAD, Montpellier, France) according to the manufacturer’s protocol. The absorbance was read at 450nm with an ELISA reader (BioTek ELX800). The results were calculated as sample positivity (S/P%) and the level of PPRV was expressed as percentage of the positive control. If S/P ˃20% it was considered negative, S/P ≥20% it was considered positive.
Anti-NP ELISA
The NP-epitopes based competitive ELISA kits (ID screen®PPR competition, ID vet, Grabels, FRANCE) was used for screening of anti-PPRV nucleoprotein antibodies in serum according to the manufacturer’s protocol. The absorbance was read at 450nm with an ELISA reader (BioTek ELX800). Samples were presented as S/N%, S/N ≤ 50% - positive, >50 - ≥60%- doubtful and >60% were considered negative.
Table 1: Epidemiological data of outbreaks in Hail, Saudi Arabia
Outbreak (Date) | Species | Vaccination | No. affected (%) | No. dead (%) | Case fatality rate (%) | Total |
1st Outbreak
(February 2016) |
Goats | X | 130 (65) | 57 (29) | 43.8 | 200 |
Sheep | X | 150 (50) | 37 (12) | 24.7 | 300 | |
Camels | X | 0 | 0 | 0 | 0 | |
Total | 280 | 94 | 33.6 | 500 | ||
2nd Outbreak
(April 2016) |
Goats | X |
83 (63.8) |
62 (47.7) | 74.69 | 130 |
Sheep | √ | 0 | 0 | 0 | 70 | |
Camels | X | 0 | 0 | 0 | 9 | |
Total | 83 | 62 | 24.53 | 209 | ||
3rd Outbreak
(April 2016) |
Goats | X | 35 (70) | 7 (14) | 20 | 50 |
Sheep | X | 150 (50) | 47 (16) | 31.3 | 300 | |
Camels | X | 0 | 0 | 0 | 4 | |
Total | 185 | 54 | 29.19 | 354 | ||
4th Outbreak
(May 2016) |
Goats | X | 0 | 0 | 0 | 0 |
Sheep | X | 100 (40) | 61 (24.4) | 61 | 250 | |
Camels | X | 0 | 0 | 0 | 0 | |
Total | 100 | 61 | 61 |
250 |
Table 2: Morbidity& mortality rates according to age
Age group | No. affected (%) | No. dead (%) | Case fatality rate (%) | Total | |
1st Outbreak |
Young | 150 (73.5) | 54 (26.5) | 36 | 204 |
Adult | 130 (76.5) | 40 (23.5) | 30.8 | 170 | |
Total | 280 (74.9) | 94 (25.1) | 33.8 | 374 | |
2nd Outbreak |
Young | 44 (52.4) | 40 (47.6) | 90.9 | 84 |
Adult | 39 (63.9) | 22 (36.1) | 56.4 | 61 | |
Total | 83 (57.2) | 62 (42.8) | 74.7 | 145 | |
3rd Outbreak |
Young | 75 (80.6) | 18 (19.4) | 24 | 93 |
Adult | 110 (75.3) | 36 (24.7) | 32.7 | 146 | |
Total | 185 (77.4) | 54 (22.6) | 29.2 | 239 | |
4th Outbreak |
Young | 100 (62.1) | 61 (37.9) | 61 | 161 |
Adult | 0 | 0 | 0 | 0 | |
Total | 100 (62.1) | 61 (37.9) | 61 |
161 |
Table 3: Morbidity& mortality rates according to sex
Male | Female | |||||
No. affected (%) | No. dead (%) | No. affected (%) | No. dead (%) | Total | ||
1st Outbreak |
Goats | 37 (19.8) | 13 (6.9) | 93 (49.7) | 44 (23.5) | 187 |
Sheep | 23 (12.3) | 7 (3.7) |
127 (67.9) |
30 (16) | 187 | |
Camels | 0 | 0 | 0 | 0 | 0 | |
Total | 60 (16) | 20 (5.3) | 220 (58.8) | 74 (19.9) | 374 | |
2nd Outbreak |
Goats | 35 (24.1) | 24 (16.6) | 48 (33.1) | 38 (26.2) | 145 |
Sheep | 0 | 0 | 0 | 0 | 0 | |
Camels | 0 | 0 | 0 | 0 | 0 | |
Total | 35 (24.1) | 24 (16.6) | 48 (33.1) | 38 (26.2) | 145 | |
3rd Outbreak |
Goats | 3 (7.1) | 0 | 32 (76.2) | 7 (16.7) | 42 |
Sheep | 23 (11.7) | 4 (2) | 127 (64.5) | 43 (21.8) | 197 | |
Camels | 0 | 0 | 0 | 0 | 0 | |
Total | 26 (10.9) | 4 (1.7) | 159 (66.5) | 50 (20.9) | 239 | |
4th Outbreak |
Goats | 0 | 0 | 0 | 0 | 0 |
Sheep | 100 (62.1) | 61 (37.9) | 0 | 0 | 161 | |
Camels | 0 | 0 | 0 | 0 | 0 | |
Total | 100 (62.1) | 61 (37.9) | 0 | 0 |
161 |
3ABC-FMD ELISA
Enzyme immunoassay kits (IDEXX FMD 3ABC Ab test. IDEXX Laboratories, Inc.Westbrook, Maine 04092.USA) was used for detection of nonstructural polyprotein (NSP) 3ABC of FMD antigen, it was performed in accordance to the manufacturers’ instructions. Samples with percentage values >30% - positive, >20% -negative and samples between 20 and 30% were considered suspicious.
Results
Epidemiological investigation
During the four outbreaks 271 (20.6%) died out of 648 (49.3%) of affected animals, with a case fatality reached 41.8%, no record of vaccination, the overall morbidity in goats (33.3%) was higher as compared to sheep (12.3%) (Figure 1 and Table 1). The disease affected all age groups (Table 2), morbidity and mortality rates were high among female animals (Table 3).
Clinical signs
Affected animals exhibited fever (up to 41˚C), loss of appetite, stomatitis, hyper salivation, respiratory distress, mucopurulent to bloody nasal/ocular discharges, watery to bloody diarrheaand lameness (Figure 2).
Necropsy findings
Dissection of animals revealed erosions on the soft and hard palates, hemorrhages in lung (evidence of pneumonia), iver, abomasum, small and large intestine (Figure 3).
Sandwich ELISA
The presence of PPRV-antigen was detected in 38 swabs (82.6%) from sheep (n=20) and goats (n=18). Camel swabs were non-reactive.
c-ELISA
Screened sheep and goat sera were positive, camels were seronegative for anti-PPRV nucleoprotein antibodies.
FMD ELISA
Six ovine sera (30%) were positive for anti-NP antibodies while goats were negative.
PPRV is one of the most prevalent infectious diseases among sheep and goats and is considered an emerging economically important disease in Saudi Arabia (Abu-Elzein et al., 1990; Al-Dubaib., 2009; Banyard et al., 2010; Mahmoud et al., 2016, 2017). In the present study, outbreaks occurred in four mixed farms were investigated, PPRV-NP, anti-PPRV-NP were detected from sheep and goats and FMD-NSP were positive from sheep sera. During the outbreaks 271 (20.6%) died out of 648 (49.3%), the overall morbidity in goats (33.3%) was higher as compared to sheep (12.3%), a case fatality rate was high in goats (74.69%), other authors found a mortality of 23 – 100% (Abu Elzein et al., 1990; Taylor et al., 1990; Chowdhury et al., 2014). Mahmoud and Galbat (2017) reported high susceptibility of sheep flocks to the infection with FMD and PPR viruses, with positivity rates of 76% for FMD and 64% for PPR antigen, the susceptibility of sheep and goats can vary with the breed of animal and strain of virus (Kitching and Hughes, 2002). Previous studies indicated that more severe disease results from mixed infection of bacteria and viruses (Osman et al., 2009). We did not take any attempt to isolate bacteria from these cases.
Young animals (6–12 months) were more susceptible than the aged, which are inconsistent with the findings of Taylor et al. (1990). This may be due to maternally derived PPR antibody that persists up to 4 months (Libeau et al., 1992). It is likely that antibody derived from sub-clinical infection in aged goats protected themselves as well as their young progenies. This observation was in accordance with reports of Taylor et al. (1979).
Foot and mouth disease (FMD) is considered one of the enzootic diseases in Saudi Arabia (Al-Mezaini et al., 1985; Aidros, 2002; Yousef et al., 2012). Sheep infections are frequently mild or in apparent (Geering, 1967; Donaldson and Sellers, 2000), often been implicated as disseminators of the virus (Krystynak, 1987; Barnett and Cox, 1999). Saudi Arabia imports annually millions of live ruminants for slaughter. The majority of these animals are imported from countries where FMD is enzootic, importing either carrier animals which might act as potential source of infection or subclinical infected animals which might actively excrete FMD virus (Hafez et al. 1994).
The present investigation detected mixed PPR-FMD infections among small ruminants in Hail. Saudi Arabia, large-scale sero-prevalence and molecular identification of the circulating strains will help in implementing proper control measures.
Authors’ Contribution
Mahmoud, A.Z., M. Abdellatif investigate the clinical picture of the outbreaks, test samples and wrote the manuscript. M. Abdalla supervised the study and revised the manuscript, all read and approved it for submission.
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