Research Article

 

Coexistence of Anti-NP-PPRV, VP7-BTV, and NS-FMDV Antibodies among Non-Vaccinated Domestic Ruminants in Hail Saudi Arabia

 

Ahmed Zein Elabdeen Mahmoud1, Muaz Magzob Abdellatif2,3*, Yahia Hassan Ali2,4

1Hail Veterinary Laboratory, Ministry of Agriculture. Saudi Arabia; 2Department of Biology (Microbiology), Northern Border University, Saudi Arabia; 3Department of Microbiology, Faculty of Vet Science, University of Nyala, Sudan; 4Department of Virology, Central Veterinary Research Laboratory, Khartoum, Sudan.

 

Received | August 22, 2020; Accepted | December 03, 2020; Published | January 01, 2021

*Correspondence | Muaz Magzob Abdellatif, Department of Biology (Microbiology), Northern Border University, Saudi Arabia; Email: [email protected]

Citation | Mahmoud AZE, Abdellatif MM, Ali YH (2021). Coexistence of anti-NP-PPRV, VP7-BTV, and NS-FMDV antibodies among non-vaccinated domestic ruminants in Hail Saudi Arabia. Adv. Anim. Vet. Sci. 9(2): 289-294.

DOI | http://dx.doi.org/10.17582/journal.aavs/2021/9.2.289.294

ISSN (Online) | 2307-8316; ISSN (Print) | 2309-3331

Copyright © 2021 Mahmoud et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

 

INTRODUCTION

 

Peste des Petits Ruminants (PPR), Blue tongue (BT) and Foot and mouth disease (FMD) are among the most important viruses in ruminants. PPRV infects domestic and wild ruminants causing significant economic losses in Africa, Middle East, Asia, and new regions (Banyard et al., 2010, 2014). The virus belongs to morbillivirus genus of the Paramyxoviridae (Zahur et al., 2009), it was reported in Saudi Arabia for the first time in 1990 (EME et al., 1990), later it spread to eastern, central, and northern regions (Adel et al., 2004; Boshra et al., 2015; Mahmoud et al., 2016, 2017). BTV is an arbovirus that is transmitted by certain species of Culicoides biting midges, affecting domestic and wild ruminants, it is one of the 22 serogroups in the Orbivirus genus of the Reoviridae (Mertens et al., 2005). It is characterized by high morbidity and mortality in sheep, while the infection is sub-clinical in some domestic and wild ruminants (Ratinier et al., 2011), it was described in different parts of the country (Hafez et al., 1984; Abu Elzein et al., 1998; Housawi et al., 2004a; Yousef et al., 2012b). FMDV is a member of the Apthovirus of the Picornaviridae, it causes direct production losses and indirect losses due to the implementation of control measures (Knight-Jones and Rushton, 2013). Introduction of subclinical animals acts as a source of new serotypes (Hafez et al., 1994; El-Rahim et al., 2016; Mahmoud and Galbat, 2017).

 

Co-infection may change the clinical picture, epidemiology and hamper diagnosis and preventive measures against these devastating viruses. The present survey was undertaken to highlight evidence of the coexistence of PPRV, BTV, and FMDV antibodies among domestic ruminants in Hail. Saudi Arabia.

 

MATERIALS AND METHODS

 

Sampling

Sera (n=841) were collected randomly from non-vaccinated clinically healthy sheep (n=270), goats (n=270), camels (n=270) and cattle (n=31) of different ages and sexes across 9 villages in Hail, Saudi Arabia during 2018 (Table 1), samples were stored at –20ºC until tested.

 

Serological examination

Samples were tested at once for anti-NP-PPRV, BTV-VP7, and NS-FMDV antibodies using competitive ELISA as follows:

 

NP-PPR ELISA

The NP-epitopes based competitive ELISA kit (310rue Louis Pasteur, 34790 Grabels, FRANCE) was used for the detection of PPRV-antibodies according to the manufacturer’s protocol (Libeau et al., 1995). Results were presented as sample-to-negative control ratio (S/N%), S/N=50% were read as positive, >50=60% were doubtful and >60% were negative.

 

VP7- BTV ELISA

Competitive enzyme immunoassay for the detection of antibodies against BT-VP7 protein was used (IDEXX Blue tongue Competition Ab test, 34090 Montpellier, France) according to the recommended procedure. Samples with S/N ≥80% were considered negative, >70% and ˂ 80% were doubtful and ≤70% were positive.

 

3ABC-FMD ELISA

The 3ABC-FMD ELISA (IDEXX FMD 3ABC Ab test. IDEXX Laboratories, Inc. Westbrook, Maine 04092, USA) was used for the detection of non-structural Polyprotein (NSP), it was performed according to the manufacturer’s instructions. Samples with percentage values >30% were considered positive, >20% were negative and samples between 20 and 30% were suspicious.

 

Statistical analysis

Spearman correlation was adopted to estimate the significant correlation of PPRV, FMDV, BTV antibodies and animal species if any (r = 0.7, P-value = 0.01). The analysis was performed using SPSS-22 (Statistical Package for Social Sciences 22).

 

Table 1: Descriptive analysis of the study area.

 

		Location									Total
Herd NO		Alagfar	Alshamly	Jaba	Hail	Baggaa	Samera	Alhaet	Alshenan	Algazala
1	Count	18	18	18	23	24	18	18	24	18	179
	% within Herd NO	10.1%	10.1%	10.1%	12.8%	13.4%	10.1%	10.1%	13.4%	10.1%	100.0%
	% within Location	20.0%	20.0%	20.0%	24.2%	23.1%	20.0%	20.0%	23.5%	20.0%	21.3%
	% of Total	2.1%	2.1%	2.1%	2.7%	2.9%	2.1%	2.1%	2.9%	2.1%	21.3%
2	Count	18	18	18	18	23	18	18	24	18	173
	% within Herd NO	10.4%	10.4%	10.4%	10.4%	13.3%	10.4%	10.4%	13.9%	10.4%	100.0%
	% within Location	20.0%	20.0%	20.0%	18.9%	22.1%	20.0%	20.0%	23.5%	20.0%	20.6%
	% of Total	2.1%	2.1%	2.1%	2.1%	2.7%	2.1%	2.1%	2.9%	2.1%	20.6%
3	Count	18	18	18	18	21	18	18	18	18	165
	% within Herd NO	10.9%	10.9%	10.9%	10.9%	12.7%	10.9%	10.9%	10.9%	10.9%	100.0%
	% within Location	20.0%	20.0%	20.0%	18.9%	20.2%	20.0%	20.0%	17.6%	20.0%	19.6%
	% of Total	2.1%	2.1%	2.1%	2.1%	2.5%	2.1%	2.1%	2.1%	2.1%	19.6%
4	Count	18	18	18	18	18	18	18	18	18	162
	% within Herd NO	11.1%	11.1%	11.1%	11.1%	11.1%	11.1%	11.1%	11.1%	11.1%	100.0%
	% within Location	20.0%	20.0%	20.0%	18.9%	17.3%	20.0%	20.0%	17.6%	20.0%	19.3%
	% of Total	2.1%	2.1%	2.1%	2.1%	2.1%	2.1%	2.1%	2.1%	2.1%	19.3%
5	Count	18	18	18	18	18	18	18	18	18	162
	% within Herd NO	11.1%	11.1%	11.1%	11.1%	11.1%	11.1%	11.1%	11.1%	11.1%	100.0%
	% within Location	20.0%	20.0%	20.0%	18.9%	17.3%	20.0%	20.0%	17.6%	20.0%	19.3%
	% of Total	2.1%	2.1%	2.1%	2.1%	2.1%	2.1%	2.1%	2.1%	2.1%	19.3%
Total	Count	90.0	90.0	90.0	95.0	104.0	90.0	90.0	102.0	90.0	841.0
	% within Herd NO	10.7%	10.7%	10.7%	11.3%	12.4%	10.7%	10.7%	12.1%	10.7%	100.0%
	% within Location	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%
	% of Total	10.7%	10.7%	10.7%	11.3%	12.4%	10.7%	10.7%	12.1%	10.7%	100.0%

RESULTS AND DISCUSSION

 

This work aimed to investigate the coexistence of PPRV, BTV, and FMDV antibodies among domestic ruminants in Hail, Saudi Arabia. The prevalence of NP-PPRV-antibodies was 51.8%, sheep exhibited the highest percentage (79.3%) (Figure 1). The incidence of PPRV antibodies was significantly higher in sheep and goats compared to cattle and camels, as a matter of fact, goats and sheep are the natural hosts of the virus (Lefèvre and Diallo, 1990; Abubakar et al., 2008; Salih et al., 2014). The prevalence of PPRV was higher than the reports from Tchad (34%) (Bidjeh et al., 1995), Sudan (51%) (Osman et al., 2009), Algeria (33%) (De Nardi et al., 2012), Tunisia (8%) (Ayari-Fakhfakh et al., 2011) and Saudi Arabia (38.2%) (Mahmoud et al., 2016). In contrast, it was lower than the data from Egypt (63%) (El-Rahim et al., 2010), Libya (59.2%) (Almeshay et al., 2017), Hail (59.9%) (Mahmoud et al., 2017) and Riyadh (64%) (Mahmoud and Galbat, 2017). Discrepancy may be attributed to sample size, diagnostic tests, levels of immunity, and management (Waret-Szkuta et al., 2008). Diverse occurrence of PPRV antibodies in cattle have been published in Kazakhstan (9%) (Lundervold et al., 2004), Pakistan (41.86%) (Khan et al., 2008), India (4.58%) (Balamurugan et al., 2014) and Sudan (25.8%) (Intisar et al., 2017), a higher prevalence may be due to the virulence of the strains involved (Khan et al., 2008; Balamurugan et al., 2012). Natural transmission of PPRV from sheep and goats to cattle has been confirmed without any clinical signs but cattle were seroconverted (Sen et al., 2014). Literature reported the absence of PPRV antibodies in dromedary camels in the Canary Islands and the KSA (Mahmoud et al., 2016, 2017). However, exposure of 2.97% dromedary camels from eastern and south regions of the country to PPR was published by Hemida and Al-Ghadeer (2019). Low percentage may be due to the fatal picture of PPR or to the nature of camel sera (Intisar et al., 2017; Omani et al., 2019), Since, unique classes and antibody binding of camel immunoglobulins was described by Li et al. (2012). Daley et al. (2010) reported divergences in the regulation and function among camelid heavy-chain isotypes on testing immunized alpacas for West Nile virus antibodies. Furthermore, inconsistency of the results obtained by ELISA and virus neutralization in testing camel sera for camel pox virus antibodies was described by Mentaberre et al. (2013), may indicate the need of standardization of ELISA when screening camel sera.

 

The incidence of VP-BTV-antibodies was 48.9%, a higher rate (74.1%) was found in sheep (Figure 1). The prevalence of BTV antibodies was comparable to the data reported by Sharma et al. (2016). In contrast, it was higher than results found in Ethiopia (46.67%) (Woldemeskel et al., 2000), India (2.63, 29.5 to 45.7%) (Lundervold et al., 2004; Sreenivasulu et al., 2004; Ravishankar et al., 2005), Turkey among small ruminants (29.5%), cattle (18.9%), Albania among small ruminants (4.4%) (Di Ventura et al., 2004), Ethiopia among sheep (29.5-34.93%) (Darsema, 2009; Di Ventura et al., 2004), Iraq (39.47%) (Shlash et al., 2012), Kazakhstan among small ruminants (28.6%) (Bitew et al., 2013), Iran (34.9%) (Khezri and Azimi, 2013) and in Algerian goats (13.7%) and sheep (5.70%) (Kardjadj et al., 2016). In KSA BTV was detected in sheep (54.1%), goats (53.3%), cattle (44.8%) (Yousef et al., 2012b) and camels (1.5-25.7%) (Al-Afaleq et al., 2007; Yousef et al., 2012b).

 

 

The prevalence of NS-FMDV-antibodies was 17.5%, sheep presented the highest positivity (23.3%), compared to goats (19.6%), cattle (22.6%), and camels (8.89%) (Figure 1). Infections among sheep are mild or inapparent and often have been considered as disseminators of the virus (Barnett and Cox, 1999; Mohanty et al., 2015). Frequency of 20.1 to 51.5% among cattle (El-Rahim et al., 2016; Lyons et al., 2017), 28.3% in sheep (El-Rahim et al., 2016) was documented in Saudi Arabia during importation. Introduction of animals from enzootic countries might act as a potential source of new serotypes, asymptomatic animals may actively excrete the virus (Hafez et al., 1994). Variation in the prevalence may be due to the virus strains, ecological and geographical factors, serological technique, and the control measures adopted.

 

Coexistence of PPRV/BTV and FMDV antibodies was confirmed in sheep (6.5%), goats (4.4%) and camels (0.2%), anti-PPRV and BTV antibodies was confirmed in sheep (17.4%), goats (15.5%) and camels (0.1%), antibodies against PPRV and FMDV was detected in goats (0.7%) and cattle (0.2%) and co-occurrence of FMDV and BTV antibodies was proved in goats (0.5%) and camels (0.1%) (Figure 2). A significant correlation between the prevalence of the antibodies and animal species, while a strong positive correlation between PPRV and BTV antibodies was estimated (0.716), a weak correlation between PPRV and FMDV (0.178), BTV and FMDV (0.179) antibodies was observed (Table 2). Data on PPR-FMD infection among small ruminants in Hail and Riyadh, Saudi Arabia were reported (Mahmoud et al., 2017; Mahmoud and Galbat, 2017). Simultaneous infection of PPRV and BTV was described in goats (Malik et al., 2011; Mondal et al., 2009; Saeed et al., 2015). Concurrent infection may be a consequence of immunosuppression induced by PPR as demonstrated by leukopenia, lymphopenia, and reduced immune response (Jagtap et al., 2012).

 

 

Table 2: Correlation between the species and prevalence of PPRV, FMDV and BTV antibodies.

 

		Spp	PPRV	FMDV	BTV
Spp	Correlation Coefficient	1.000	-.618**	-.153**	-.591**
	Sig. (2-tailed)	.000	.000	.000	.000
PPRV	Correlation Coefficient	-.618**	1.000	.178**	.716**
	Sig. (2-tailed)	.000	.	.000	.000
FMDV	Correlation Coefficient	-.153**	.178**	1.000	.179**
	Sig. (2-tailed)	.000	.000	.	.000
BTV	Correlation Coefficient	-.591**	.716**	.179**	1.000
	Sig. (2-tailed)	.000	.000	.000	.

**: Correlation is significant at the 0.01 level (2-tailed).

 

CONCLUSION

 

The results provided evidence of concurrent PPRV, BTV, and FMDV infections among farm animals in Hail, Saudi Arabia. Attention should be paid to explore the effects of virus interaction on the pathogenesis, clinical and/or epidemiological features that may hinder the diagnosis and execution of prevention and control policies. Development of rapid, sensitive, and specific multiplex immunoassays is necessary to improve the management against these infectious viruses.

 

Author’s Contribution

 

Mahmoud AZE participated in the design of the study, collect samples and perform ELISA tests. Abdellatif MM design the study, participated in the lab work, analysed the results and wrote the manuscript. Ali YH participated in the design of the study, participated in the lab work and revised the manuscript.

 

CONFLICTS OF INTEREST

 

The authors have declared no conflict of interest.

 

REFERENCES

 

• Abu Elzein E, Aitchison H, Al-Afaleq A, Al-Bashir A, Ibrahim A, Housawi F (1998). A study on bluetongue virus infection in Saudi Arabia using sentinel ruminants. Onderstepoort J. vet. Res., 65(4): 243-251. https://doi.org/10.1016/S0021-9975(98)80041-8

• Abubakar M, Ali Q, Khan HA (2008). Prevalence and mortality rate of peste des petitis ruminant (PPR): possible association with abortion in goat. Trop. Anim. Health Prod., 40: 317-321. https://doi.org/10.1007/s11250-007-9105-2

• Adel AA, Abu-Elzein E, Al-Naeem AM, Amin M (2004). Serosurveillance for peste des petits ruminants (PPR) and rinderpest antibodies in naturally exposed Saudi sheep and goats. Vet. Arh., 74: 459-465.

• Al-Afaleq A, Abu-Elzein E, Hegazy A, Al-Naeem A (2007). Surveillance of camels (Camelus dromedarius) to detect antibodies against viral diseases in Saudi Arabia. J. Camel Pract. Res., 14: 91-96.

• Almeshay MD, Gusbi A. Eldaghayes I, Mansouri R, Bengoumi M, Dayhum AS (2017). Peste des petits ruminants in Tripoli Region, Lybia. Vet. Ital., 53: 235-242.

• Ayari-Fakhfakh E, Ghram A, Bouattour A, Larbi I, Gribâa-Dridi L, Kwiatek O, Bouloy M, Libeau G, Albina E, Cêtre-Sossah C (2011). First serological investigation of peste-des-petits-ruminants and Rift Valley fever in Tunisia. Vet. J., 187: 402-404. https://doi.org/10.1016/j.tvjl.2010.01.007

• Balamurugan V, Krishnamoorthy P, Raju D, Rajak K, Bhanuprakash V, Pandey A, Gajendragad M, Prabhudas K, Rahman H (2014). Prevalence of Peste-des-petits-ruminant virus antibodies in cattle, buffaloes, sheep and goats in India. Virusdisease, 25: 85-90. https://doi.org/10.1007/s13337-013-0177-5

• Balamurugan V, Krishnamoorthy P, Veeregowda BM, Sen A, Rajak KK, Bhanuprakash V, Gajendragad MR, Prabhudas K (2012). Seroprevalence of Peste des petits ruminants in cattle and buffaloes from Southern Peninsular India. Trop. Anim. Health Prod., 44: 301-306. https://doi.org/10.1007/s11250-011-0020-1

• Banyard A C, Parida S, Batten C, Oura C, Kwiatek O, Libeau G (2010). Global distribution of peste des petits ruminants virus and prospects for improved diagnosis and control. J. Gen. Virol., 91: 2885-2897. https://doi.org/10.1099/vir.0.025841-0

• Banyard AC, Wang Z, Parida S (2014). Peste des petits ruminants virus, eastern Asia. Emerg. Infect. Dis., 20: 2176. https://doi.org/10.3201/eid2012.140907

• Barnett P, Cox S (1999). The role of small ruminants in the epidemiology and transmission of foot-and-mouth disease. Vet. J., 158: 6-13. https://doi.org/10.1053/tvjl.1998.0338

• Bidjeh K, Bornarel P, Imadine M, Lancelot R (1995). First-time isolation of the peste des petits ruminants (PPR) virus in Chad and experimental induction of the disease. Rev. Elev. Med. Vet. Pays Trop., 48: 295-300.

• Bitew M, Sukdeb N, Ravishankar C (2013). Bluetongue: Virus proteins and recent diagnostic approaches. Afr. J. Microbiol. Res., 7: 5771-5780. https://doi.org/10.5897/AJMR2013.6305

• Boshra H, Truong T, Babiuk S, Hemida MG (2015). Seroprevalence of sheep and goat pox, peste des petits ruminants and Rift Valley fever in Saudi Arabia. PLoS One, 10: e0140328. https://doi.org/10.1371/journal.pone.0140328

• Daley LP, Kutzler MA, Bennett BW, Smith MC, Glaser AL, Appleton JA (2010). Effector functions of camelid heavy-chain antibodies in immunity to West Nile virus. Clin. Vaccine Immunol. Clin. Vaccine Immunol., 17: 239-246. https://doi.org/10.1128/CVI.00421-09

• Darsema G (2009). Seroepidemiological study of bluetongue in indigenous sheep in selected districts of Amhara National Regional State, north western Ethiopia. Ethiop. Vet. J., 13: 1-15.

• De Nardi M, Lamin Saleh S, Batten C, Oura C, Di Nardo A, Rossi D (2012). First evidence of peste des petits ruminants (PPR) virus circulation in Algeria (Sahrawi territories): Outbreak investigation and virus lineage identification. Transbound. Emerg. Dis., 59: 214-222. https://doi.org/10.1111/j.1865-1682.2011.01260.x

• Di Ventura M, Tittarelli M, Semproni G, Bonfini B, Savini G, Conte A, Lika A (2004). Serological surveillance of bluetongue virus in cattle, sheep and goats in Albania. Vet. Ital., 40: 101-104.

• El-Rahim I, Asghar A, Mohamed A, Fat’hi S (2016). The impact of importation of live ruminants on the epizootiology of Foot-and-mouth disease in Saudi Arabia. Rev. Sci. Tech. Off. Int. Épizoot., 35: 769-778. https://doi.org/10.20506/rst.35.3.2567

• El-Rahim I, Sharawi S, Barakat M, El-Nahas E (2010). An outbreak of peste des petits ruminants in migratory flocks of sheep and goats in Egypt in 2006. Rev. Sci. Tech., 29: 655-662. https://doi.org/10.20506/rst.29.3.2004

• EME AE, Hassanien M, Alafaleq A, Abdelhadi M, Housawi, F (1990). Isolation of PPR virus from goats in Saudi Arabia. Vet. Rec., 127: 309-310.

• Hafez S, Farag M, Mazloum K, Al-Bokmy A (1994). Serological survey of foot and mouth disease in Saudi Arabia. Rev. Sci. Tech. Off. Int. Epiz., 13: 711-711. https://doi.org/10.20506/rst.13.3.791

• Hafez S, Radwan A, Bekairi S, Al-Mukayel A (1984). Serological evidence for the occurrence and prevalence of bluetongue among ruminants in Saudi Arabia. Arab Gulf J. Sci. Res., 2(1): 289-290.

• Hemida MG, Al-Ghadeer HM (2019). Evidence of Peste des petits Ruminants’ Virus in Dromedary Camels in the Kingdom of Saudi Arabia between 2014 and 2016. Vet. Med. Int., 2019: 1-4. https://doi.org/10.1155/2019/4756404

• Housawi F, Abu Elzein E, Ramadan R, Gameel A, Al-Afaleq A, Al-Mousa J (2004a). Abortions, stillbirths and deformities in sheep at Al-Ahsa oasis in eastern Saudi Arabia: Isolation of a bluetongue serogroup virus from the affected lambs. Rev. Sci. Tech. Off. Int. Épizoot., 23: 913-920. https://doi.org/10.20506/rst.23.3.1540

• Intisar K, Ali, YH, Haj M, Sahar M, Shaza M, Baraa A, Ishag O, Nouri Y, Taha KM, Nada E (2017). Peste des petits ruminants infection in domestic ruminants in Sudan. Trop. Anim. Health Prod., 49: 747-754. https://doi.org/10.1007/s11250-017-1254-3

• Jagtap SP, Rajak KK, Garg UK, Sen A, Bhanuprakash V, Sudhakar SB, Balamurugan V, Patel A, Ahuja A, Singh RK (2012). Effect of immunosuppression on pathogenesis of peste des petits ruminants (PPR) virus infection in goats. Microb. Pathog., 52: 217-226. https://doi.org/10.1016/j.micpath.2012.01.003

• Kardjadj M, Luka PD, Benmadhi MH (2016). Sero-epidemiology of bluetongue in Algerian ruminants. Afr. J. Biotechnol., 15: 868-871. https://doi.org/10.5897/AJB2016.15343

• Khan HA, Siddique M, Abubakar M, Ashraf M (2008). The detection of antibody against peste des petits ruminants virus in sheep, goats, cattle and buffaloes. Trop. Anim. Health Prod., 40: 521-527. https://doi.org/10.1007/s11250-008-9129-2

• Khezri M, Azimi SM (2013). Seroprevalence of bluetongue disease in sheep in west and northwest provinces of Iran. In: Veterinary research forum. Fac. Vet. Med. Urmia Univ. Urmia, Iran, 4: 195.

• Knight-Jones T, Rushton J (2013). The economic impacts of foot and mouth disease, what are they, how big are they and where do they occur? Prev. Vet. Med., 112: 161-173. https://doi.org/10.1016/j.prevetmed.2013.07.013

• Lefèvre PC, Diallo A (1990). Peste des petits ruminants. Rev. Sci. Tech., 9: 935-981. https://doi.org/10.20506/rst.9.4.532

• Li J, Xia L, Su Y, Liu H, Xia X, Lu Q, Yang C, Reheman K (2012). Molecular imprint of enzyme active site by camel nanobodies. J. Biol. Chem., 287: 3713-13721. https://doi.org/10.1074/jbc.M111.336370

• Libeau G, Prehaud C, Lancelot R, Colas F, Guerre L, Bishop D, Diallo A (1995). Development of a competitive ELISA for detecting antibodies to the peste des petits ruminants virus using a recombinant nucleobrotein. Res. Vet. Sci., 58: 50-55. https://doi.org/10.1016/0034-5288(95)90088-8

• Lundervold M, Milner-Gulland E, O’callaghan C, Hamblin C, Corteyn A, Macmillan A (2004). A serological survey of ruminant livestock in Kazakhstan during post-Soviet transitions in farming and disease control. Acta Vet. Scand., 45: 211. https://doi.org/10.1186/1751-0147-45-211

• Lyons NA, Ludi AB, Wilsden G, Hamblin P, Qasim IA, Gubbins S, King DP (2017). Evaluation of a polyvalent foot-and-mouth disease virus vaccine containing A Saudi-95 against field challenge on large-scale dairy farms in Saudi Arabia with the emerging A/ASIA/G-VII viral lineage. Vaccine, 35: 6850-6857. https://doi.org/10.1016/j.vaccine.2017.10.029

• Mahmoud A, Abdellatif M, Abdalla A (2017). High seroprevalence of PPRV-antibodies among sheep and goats in Hail, Saudi Arabia. Vet. Sci. Res. Rev., 3: 1-5. https://doi.org/10.17582/journal.vsrr/2017.3.1.1.5

• Mahmoud AZ, Abdellatif M, Shazali L (2016). Prevalence of PPR-virus antibodies in sheep, goats and camels in Hail, Saudi Arabia. Br. J. Virol., 3: 86. https://doi.org/10.17582/journal.bjv/2016.3.3s.86.89

• Mahmoud M, Galbat S (2017). Outbreak of foot and mouth disease and peste des petits ruminants in sheep flock imported for immediate slaughter in Riyadh. Vet. World, 10: 238. https://doi.org/10.14202/vetworld.2017.238-243

• Malik Y, Singh D, Chandrashekar K, Shukla S, Sharma K, Vaid N, Chakravarti S (2011). Occurrence of dual infection of peste‐des‐petits ruminants and goatpox in indigenous goats of central India. Transbound Emerg. Dis., 58: 268-273. https://doi.org/10.1111/j.1865-1682.2011.01201.x

• Mentaberre G, Gutiérrez C, Rodríguez NF, Joseph S, González-Barrio D, Cabezón O, De la Fuente J, Gortazar C, Boadella M (2013). A transversal study on antibodies against selected pathogens in dromedary camels in the Canary Islands, Spain. Vet. Microbiol., 167: 468-473. https://doi.org/10.1016/j.vetmic.2013.07.029

• Mertens P, Maan S, Samuel A, Attoui H (2005). Orbiviruses, reoviridae. In: Fauquet CM, Mayo MA, Maniloff J., Desselberger U. and Ball LA, editor. Virus taxonomy eighth report of the international committee on taxonomy of viruses. London: Elsevier/Academic Press.

• Mohanty NN, Subramaniam S, Rout M, Sarangi LN, Bisht P, Pandey LK, Mohapatra JK, Panda HK (2015). Serosurveillance of foot-and-mouth disease in ruminant population of Coastal Odisha, India. Beni-Suef Univ. J. Basic Appl. Sci., 4: 279-283. https://doi.org/10.1016/j.bjbas.2015.11.002

• Mondal B, Sen A, Chand K, Biswas S, De A, Rajak K, Chakravarti S (2009). Evidence of mixed infection of peste des petits ruminants virus and bluetongue virus in a flock of goats as confirmed by detection of antigen, antibody and nucleic acid of both the viruses. Trop. Anim. Health Prod., 41: 1661. https://doi.org/10.1007/s11250-009-9362-3

• Omani R, Gitao G, Gachohi J, Gathumbi P, Bwihangane B, Abbey K, Chemweno V (2019). Peste des petits ruminants (PPR) in dromedary camels and small ruminants in Mandera and Wajir Counties of Kenya. Adv. Virol., 2019: 4028720. https://doi.org/10.1155/2019/4028720

• Osman N A, Ali A, Fadol M (2009). Antibody seroprevalences against Peste des Petits Ruminants (PPR) virus in sheep and goats in Sudan. Trop. Anim. Health Prod., 41: 1449. https://doi.org/10.1007/s11250-009-9333-8

• Ratinier M, Caporale M, Golder M, Franzoni G, Allan K, Nunes SF, Armezzani A, Bayoumy A, Rixon F, Shaw A (2011). Identification and characterization of a novel non-structural protein of bluetongue virus. PLoS Pathog., 7: e1002477. https://doi.org/10.1371/journal.ppat.1002477

• Ravishankar C, Nair G K, Mini M, Jayaprakasan V (2005). Seroprevalence of bluetongue virus antibodies in sheep and goats in Kerala State, India. Rev. Sci. Tech., 24: 953. https://doi.org/10.20506/rst.24.3.1626

• Saeed IK, Ali YH, AbdulRahman MB, Mohammed ZA, Osman HM, Taha KM, Musa MZ, Khalafalla AI (2015). Mixed infection of peste des petits ruminants virus (PPRV) and other respiratory viruses in dromedary camels in Sudan, an abattoir study. Trop. Anim. Health Prod., 47: 995-998. https://doi.org/10.1007/s11250-015-0798-3

• Salih, HAM, Elfadil AAM, Saeed IK, Ali YH (2014). Seroprevalence and risk factors of Peste des Petits Ruminants in sheep and goats in Sudan. J. Adv. Vet. Anim. Res., 1: 42-49. https://doi.org/10.5455/javar.2014.a12

• Sharma RN, Beckford S, Tiwari K, Vinet E, Thomas D, de Allie C, Chikweto A (2016). Seroprevalence of bluetongue virus antibody in ruminants from Grenada. Open J. Vet. Med., 6: 99. https://doi.org/10.4236/ojvm.2016.66013

• Shlash KH, Abdul-Rasoul LM, Naji MM, Hussain MH (2012). A serologicalsurveillance of bluetongue disease in sheep and goats in Iraq by using acompetitive ELISA Technique. Iraqi J.Vet. Sci., 36: 89-94.

• Sreenivasulu D, Subba RM, Reddy Y, Gard G (2004). Overview of bluetongue disease, viruses, vectors, surveillance and unique features: The Indian sub-continent and adjacent regions. Vet. Ital., 40: 73-77.

• Waret-Szkuta A, Roger F, Chavernac D, Yigezu L, Libeau G, Pfeiffer DU, Guitián J (2008). Peste des Petits Ruminants (PPR) in Ethiopia: Analysis of a national serological survey. BMC Vet. Res., 4: 34. https://doi.org/10.1186/1746-6148-4-34

• Woldemeskel M, Tilahun G, Tibbo M, Potgieter L (2000). Prevalence of bluetongue virus antibodies in sheep in central Ethiopia. DTW. Dtsch Tierarztl Wochenschr, 107: 408-410.

• Yousef MR, Al-Eesa AA, Al-Blowi MH (2012b). High seroprevalence of bluetongue virus antibodies in Sheep, Goats, Cattle and Camel in different districts of Saudi Arabia. Vet. World, 5(7): 389-393. https://doi.org/10.5455/vetworld.2012.389-393

• Zahur A, Ullah A, Irshad H, Farooq M, Hussain M, Jahangir M (2009). Epidemiological investigations of a peste des petits ruminants (PPR) outbreak in Afghan sheep in Pakistan. Pak. Vet. J., 29: 174-178.