Sero-Epidemiology and Associated Risk Factors of Foot-and-Mouth Disease (FMD) in the Northern Border Regions of Pakistan
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Research Area
2.2. Study Animals
2.3. Study Design and Sampling Strategy
2.4. Sample Collection Procedures
2.5. FMDV 3ABC-ELISA
2.6. Data Collection
2.7. Data Management and Analysis
3. Results
3.1. Apparent Seroprevalence of FMD in the Northern Border Regions of Pakistan
3.2. Risk Factors Associated with FMD Seropositivity
3.3. Hotspots of the Spatial Distribution of FMD
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Arzt, J.; Baxt, B.; Grubman, M.J.; Jackson, T.; Juleff, N.; Rhyan, J.; Rieder, E.; Waters, R.; Rodriguez, L.L. The Pathogenesis of Foot-and-Mouth Disease II: Viral Pathways in Swine, Small Ruminants, and Wildlife; Myotropism, Chronic Syndromes, and Molecular Virus-Host Interactions. Transbound. Emerg. Dis. 2011, 58, 305–326. [Google Scholar] [CrossRef] [PubMed]
- OIE. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 8th Edition. 2018. Available online: https://www.oie.int/standard-setting/terrestrial-manual/ (accessed on 1 December 2022).
- Carrillo, C.; Tulman, E.R.; Delhon, G.; Lu, Z.; Carreno, A.; Vagnozzi, A.; Kutish, G.F.; Rock, D.L. Comparative Genomics of Foot-and-Mouth Disease Virus. J. Virol. 2005, 79, 6487–6504. [Google Scholar] [CrossRef] [PubMed]
- Domingo, E.; Pariente, N.; Airaksinen, A.; Gonzaĺez-Lopez, C.; Sierra, S.; Herrera, M.; Grande-Pérez, A.; Lowenstein, P.R.; Manrubia, S.C.; Lázaro, E.; et al. Foot-and-mouth disease virus evolution: Exploring pathways towards virus extinction. Curr. Top. Microbiol. Immunol. 2005, 288, 149–173. [Google Scholar] [PubMed]
- Mason, P.W.; Grubman, M.J.; Baxt, B. Molecular basis of pathogenesis of FMDV. Virus Res. 2003, 91, 9–32. [Google Scholar] [CrossRef]
- Radostits, O.M.; Gay, C.C.; Hinchcliff, K.W.; Constable, P.D. A textbook of the diseases of cattle, horses, sheep, pigs and goats. Vet. Med. 2007, 10, 2045–2050. [Google Scholar]
- Mahmoud, M.A.E.-F.; Ghazy, A.A.; Shaapan, R.M. Diagnosis and Control of Foot and Mouth Disease (FMD) in Dairy Small Ruminants; Sheep and Goats. Int. J. Dairy Sci. 2018, 14, 45–52. [Google Scholar] [CrossRef]
- Stenfeldt, C.; Pacheco, J.; Rodriguez, L.L.; Arzt, J. Early Events in the Pathogenesis of Foot-and-Mouth Disease in Pigs; Identification of Oropharyngeal Tonsils as Sites of Primary and Sustained Viral Replication. PLOS ONE 2014, 9, e106859. [Google Scholar] [CrossRef]
- Barnett, P.; Cox, S. The Role of Small Ruminants in the Epidemiology and Transmission of Foot-and-Mouth Disease. Vet. J. 1999, 158, 6–13. [Google Scholar] [CrossRef]
- Donaldson, A.I.; Sellers, R.F.; Martin, W.B.; Aitken, I.D. (Eds.) Foot-and-Mouth Disease. Diseases of Sheep; Blackwell Science: Oxford, UK, 2000; pp. 254–258. [Google Scholar]
- Parida, S.; Fleming, L.; Gibson, D.; Hamblin, P.A.; Grazioli, S.; Brocchi, E.; Paton, D.J. Bovine Serum Panel for Evaluating Foot-and-Mouth Disease Virus Nonstructural Protein Antibody Tests. J. Vet. Diagn. Investig. 2007, 19, 539–544. [Google Scholar] [CrossRef]
- Parida, S. Vaccination against foot-and-mouth disease virus: Strategies and effectiveness. Expert Rev. Vaccines 2009, 8, 347–365. [Google Scholar] [CrossRef]
- Office International des ÉPizooties (OIÉ). World Animal Health Information Database (WAHID) Interface. Available online: http://www.oie.int/wahid-prod/public.php?page=home (accessed on 10 July 2017).
- EUFMD—The European Commission for the Control of Foot and Mouth Disease Reports Executive Committee. 2005. Available online: http://www.fao.org/ag/againfo/commissions/en/eufmd/72report_txt.html (accessed on 12 May 2007).
- Zahur, A.B.; Irshad, H.; Hussain, M.; Anjum, R.; Khan, M.Q. Transboundary animal diseases in Pakistan. J. Vet. Med. B Infect. Dis. Vet. Public Health 2006, 53 (Suppl. S1), 19–22. [Google Scholar] [CrossRef]
- Tosh, C.; Hemadri, D.; Sanyal, A. Evidence of recombination in the capsid-coding region of type A foot-and-mouth disease virus. J. Gen. Virol. 2002, 83 Pt 10, 2455–2460. [Google Scholar] [CrossRef] [PubMed]
- Kesy, A. Global situation of foot-and-mouth disease (FMD)—A short review. Pol. J. Vet. Sci. 2002, 5, 283–287. [Google Scholar] [PubMed]
- Jamal, S.; Ferrari, M.; Ahmed, G.; Normann, S.; Curry, P.S.; Belsham, G.J. Evolutionary analysis of serotype A foot-and-mouth disease viruses circulating in Pakistan and Afghanistan during 2002–2009. J. Gen. Virol. 2011, 92, 2849–2864. [Google Scholar] [CrossRef] [PubMed]
- Osmani, A.; Robertson, I.; Habib, D.I.; Aslami, A.A. History and epidemiology of foot-and-mouth disease in Afghanistan: A retrospective study. BMC Vet. Res. 2019, 15, 340. [Google Scholar] [CrossRef] [PubMed]
- Schumann, K.R.; Knowles, N.J.; Davies, P.R.; Midgley, R.J.; Valarcher, J.F.; Raoufi, A.Q.; McKenna, T.S.; Hurtle, W.; Burans, J.P.; Martin, B.M.; et al. Genetic characterization and molecular epidemiology of foot-and-mouth disease viruses isolated from Afghanistan in 2003–2005. Virus Genes 2008, 36, 401–413. [Google Scholar] [CrossRef] [PubMed]
- Ali, I.; Rehman, A.; Mushtaq, M.H.; Ijaz, M.; Khaliq, M.S.; Khan, M.S.U.; Khalid, S.; Masud, A.; Abbas, A.; Parveen, S.; et al. Outbreak investigation and identification of risk factors associated with the occurrence of foot and mouth disease in Punjab, Pakistan. Prev. Vet. Med. 2022, 202, 105613. [Google Scholar] [CrossRef]
- Megersa, M.; Feyissa, A.; Wondimu, A.; Jibat, T. Herd composition and characteristics of dairy production in Bishoftu Town, Ethiopia. J. Agric. Extention Rural Dev. 2011, 3, 113–117. [Google Scholar]
- Iriarte, M.V.; Gonzáles, J.L.; Costa, E.D.F.; Gil, A.D.; de Jong, M.C.M. Main factors associated with foot-and-mouth disease virus infection during the 2001 FMD epidemic in Uruguay. Front. Vet. Sci. 2023, 10, 1070188. [Google Scholar] [CrossRef]
- Thrusfield, M. Veterinary Epidemiology, 3rd ed.; Black Well Science Ltd.: London, UK, 2007; pp. 178–236. [Google Scholar]
- Fu, Y.; Lu, Z.; Li, P.; Cao, Y.; Sun, P.; Tian, M.; Wang, N.; Bao, H.; Bai, X.; Li, N.; et al. Development of a Blocking ELISA Based on a Monoclonal Antibody against a Predominant Epitope in Non-Structural Protein 3B2 of Foot-and-Mouth Disease Virus for Differentiating Infected from Vaccinated Animals. PLoS ONE 2014, 9, e111737. [Google Scholar] [CrossRef]
- Ur-Rehman, S.; Arshad, M.; Hussain, I.; Iqbal, Z. Detection and sero-prevalence of foot and mouth disease in sheep and goats in Punjab, Pakistan. Transbound. Emerg. Dis. 2014, 61 (Suppl. S1), 25–30. [Google Scholar] [CrossRef] [PubMed]
- Farooq, U.; Irshad, H.; Ullah, A.; Latif, A.; Zahur, A.B.; Naeem, K.; Ahmed, Z.; Rodriguez, L. Sero-prevalence of foot-and-mouth disease in small ruminants of Pakistan. J. Anim. Plant Sci. 2017, 27, 1197–1201. [Google Scholar]
- Anjum, R.; Hussain, M.A.; Zahoor, B.; Irshad, H.; Farooq, U. Epidemiological analyses of foot and mouth disease in Pakistan. Int. J. Agric. Biol. 2006, 5, 648–651. [Google Scholar]
- Nawaz, Z.; Arshad, M.; Rahman, S.U.; Iqbal, Z. Epidemiological investigation of foot and mouth disease in bovines of Faisalabad. J. Agric. Res. 2015, 53, 1. [Google Scholar]
- Mesfine, M.; Nigatu, S.; Belayneh, N.; Wudu TJemberu, W.T. Sero-epidemiology of foot and mouth disease in domestic ruminants in Amhara Region, Ethiopia. Front. Vet. Sci. 2019, 6, 130. [Google Scholar] [CrossRef] [PubMed]
- Abdela, N. Sero-prevalence, risk factors and distribution of foot and mouth disease in Ethiopia. Acta Trop. 2017, 169, 125–132. [Google Scholar] [CrossRef]
- Raouf, Y.A.; Hanan, Y.; Almutlab, A.A.; Hassen, A.A.; Ahmed Al-Majali, A.; Tibbo, M. Role of small ruminants in the epidemiology of foot-and-mouth disease in Sudan. Bull. Anim. Health Prod. Afr. 2017, 65, 145–156. [Google Scholar]
- Phyoe, H.M.M.; Khaing, A.T.; Abba, Y.; Aung, Y.H.; Htun, L.L.; Htin, N.N.; Abdullah, J.F.F.; Lila, M.A.M. Sero-prevalence of Foot and Mouth Disease Virus (FMDV) and associated risk factors in unvaccinated sheep and goats in Pyawbwe and Meikhtila townships of Myanmar. J. Adv. Vet. Anim. Res. 2017, 4, 161–167. [Google Scholar] [CrossRef]
- Asresie, A.; Zemedu, L. Contribution of livestock sector in Ethiopian economy: A review. Adv. Life Sci. Technol. 2015, 29, 79–90. [Google Scholar]
- Bayissa, B.; Ayelet, G.; Kyule, M.; Jibril, Y.; Gelaye, E. Study on seroprevalence, risk factors, and economic impact of foot and mouth disease in Borana pastoral and agro pastoral system, southern Ethiopia. Trop. Anim. Health Prod. 2011, 43, 759–766. [Google Scholar] [CrossRef]
- Gelaye, E.; Ayelet, G.; Abera, T.; Asmare, K. Seroprevalence of foot and mouth disease in Bench Maji zone, Southwestern Ethiopia. J. Vet. Med. Anim. Health 2009, 1, 5–10. [Google Scholar]
- Awan, F.N.; Muhammad, A.K.; Muhammad, K.; Rabbani, M.; Younus, M.; Khawaja, R.M. Epidemiological investigation of foot and mouth disease in districts of Punjab. Pak. J. Zool. 2009, 9, 179–185. [Google Scholar]
- Megersa, B.; Beyene, B.; Abunna, F.; Regassa, A.; Amenu, K.; Rufael, T. Risk factors for foot and mouth disease seroprevalence in indigenous cattle in Southern Ethopia: The Effect of Production System. Trop. Anim. Health Prod. 2009, 41, 891–898. [Google Scholar] [CrossRef] [PubMed]
- Mohamoud, A.; Tessema, E.; Degefu, H. Seroprevalence of bovine foot and mouth disease (FMD) in Awbere and Babille districts of Jijiga zone, Somalia Regional State, Eastern Ethiopia. Afr. J. Microbiol. Res. 2011, 5, 3559–3563. [Google Scholar]
- Jenbere, T.S.; Manyahilishal, E.; Haileluel, N. Study on the risk factors of Foot-and-mouth disease in selected districts of afar pas-toral area, Northeast Ethiopia. J. Anim. Vet. Adv. 2011, 10, 1368–1372. [Google Scholar]
- Torsson, E.; Berg, M.; Misinzo, G.; Herbe, I.; Kgotlele, T.; Päärni, M.; Roos, N.; Blomström, A.-L.; Ståhl, K.; Wensman, J.J. Seroprevalence and risk factors for peste des petits ruminants and selected differential diagnosis in sheep and goats in Tanzania. Infect. Ecol. Epidemiol. 2017, 7, 1368336. [Google Scholar] [CrossRef]
- Casey-Bryars, M. The Epidemiology of Foot-and-Mouth Sisease at the Wildlife-Livestock Interface in Northern Tanzania. Ph.D. Thesis, University of Glasgow, Scotland, UK, 2016. [Google Scholar]
- Mannan, M.; Siddique, M.; Uddin, M.; Parvaz, M. Prevalence of foot and mouth disease (FMD) in cattle at Meghna upazila in Comilla in Bangladesh. J. Bangladesh Agric. Univ. 2009, 7, 317–319. [Google Scholar] [CrossRef]
- Chepkwony, E.C.; Gitao, C.G.; Muchemi, G.M. Seroprevalence of foot and mouth disease in the Somali eco-system in Kenya. Int. J. Anim. Vet. Adv. 2012, 4, 198–203. [Google Scholar]
- Balinda, S.N.; Tjørnehøj, K.; Muwanika, V.B.; Sangula, A.K.; Mwiine, F.N.; Ayebazibwe, C.; Masembe, C.; Siegismund, H.R.; Alexandersen, S. Prevalence Estimates of Antibodies Towards Foot-and-Mouth Disease Virus in Small Ruminants in Uganda. Transbound. Emerg. Dis. 2009, 56, 362–371. [Google Scholar] [CrossRef]
- Chepkwony, E.C.; Gitao, G.C.; Muchemi, G.M.; Sangula, A.K.; Kairu-Wanyoike, S.W. Epidemiological study on foot-and-mouth disease in small ruminants: Sero-prevalence and risk factor assessment in Kenya. PLoS ONE 2021, 16, e0234286. [Google Scholar] [CrossRef]
- Beyene, B.; Tolosa, T.; Rufael, T.; Hailu, B.; Teklue, T. Foot and mouth disease in selected districts of western Ethiopia: Seroprevalence and associated risk factors. Rev. Sci. Tech. 2015, 34, 939–952. [Google Scholar] [CrossRef] [PubMed]
- Ehizibolo, D.O.; Ajogi, I.; Umoh, J.U.; Kazeem, H.M.; Ehizibolo, P.O.; Perez, A.M.; Metwally, S.A. Serological survey of Foot-and-mouth disease (FMD) 3rd non-structural proteins using virus-infection associated (VIA) antigen assay in livestock animals from Plateau state, Nigeria. In Proceedings of the 47th Annual Congress of the Nigerian Veterinary Medical Association (NVMA), Benue, Nigeria, 4–8 October 2010; Volume 75. [Google Scholar]
- Rout, M.; Senapati, M.R.; Mohapatra, J.K.; Dash, B.B.; Sanyal, A.; Pattnaik, B. Serosurveillance of foot-and-mouth disease in sheep and goat population of India. Prev. Vet. Med. 2014, 113, 273–277. [Google Scholar] [CrossRef]
- Lazarus, D.D.; Schielen, W.J.G.; Wungak, Y.; Kwange, D.; Fasina, F.O. Sero-epidemiology of Foot-and-mouth disease in some border states of Nigeria. Afr. J. Microbiol. Res. 2012, 6, 1756–1761. [Google Scholar] [CrossRef]
- Al-Majali, A.M.; Jawasreh, K.; Al Nsour, A. Epidemiological studies on foot and mouth disease and paratuberculosis in small ruminants in Tafelah and Ma’an, Jordan. Small Rumin. Res. 2008, 78, 197–201. [Google Scholar] [CrossRef]
- Dion, E.; Eric, F.L. Scenarios of transmission risk of foot and-mouth with climatic, social and landscape changes in southern Africa. Appl. Geophys. 2012, 35, 32–42. [Google Scholar] [CrossRef]
- Hii, Y.L.; Rocklöv, J.; Ng, N. Short Term Effects of Weather on Hand, Foot and Mouth Disease. PLoS ONE 2011, 6, e16796. [Google Scholar] [CrossRef]
- Minhaz Ud-Dean, S.M. Structural explanation for the effect of humidity on persistence of airborne virus: Seasonality of influenza. J. Theor. Biol. 2010, 264, 822–829. [Google Scholar] [CrossRef]
Variables | Cluster | Tested Samples | Positives | Prevalence in % (95% CI) | Odds Ratio (95% CI) | p-Value |
---|---|---|---|---|---|---|
Species | Sheep | 97 | 50 | 51.5 (41.6–61.4) | 1.769 (1.296–2.416) | 0.002 |
Goat Cattle Buffalo (ref) | 142 60 86 | 102 35 71 | 71.8 (64.4–79.2) 58.3 (45.8–70.8) 82.5 (68.0–89.7) | |||
Age | <1 year 1 year | 117 6 | 02 00 | 1.7 (0.0–4.05) 0.0 (0.0–0.0) | 0.655 (0.470–0.914) 0.000 (0.00–0.00) | 0.000 |
2 year | 30 | 30 | 100 (100–100) | |||
3 year >3 year (ref) | 158 74 | 155 71 | 98.1 (96.2–100) 95.9 (90.0–100) | |||
Sex | Male | 151 | 27 | 17.8 (7.6–21.8) | 0.621 (0.491–0.985) | 0.000 |
Female (ref) | 234 | 231 | 98.7 (98.0–100) | |||
Flock/Herd size | <than50 51–100 | 116 10 | 1 5 | 0.86 (0.0–2.5) 50.0 (19.0–80.9) | 0.781 (0.053–4.4) 1.336 (0.187–11.753) | |
101–200 | 20 | 15 | 75.0 (56.0–93.9) | 1.213 (0.158–5.532) | 0.000 | |
201–300 301–500 >than 500 (ref) | 99 140 0 | 98 139 0 | 98.9 (97.6–100.0) 99.2 (98.0–100.0) 0.00 (0.0–0.0) | 1.592 (0.215–11.766) 1.628 (0.225–11.966) | ||
Vaccination status | Non-vaccinated | 385 | 258 | 67.0 (61.2–72.4) | 1.201 (0.301–3.981) | 0.987 |
Outbreak of FMD or FMD affected animals in the area in last 15 days | Yes No | 128 257 | 85 173 | 66.4 (55.5–73.8) 67.3 (61.1–75.1) | 0.901 (0.502–1.521) | 0.254 |
Introduced new animals | Yes | 141 | 97 | 68.7 (59.8–75.8) | 0.983 (0.512–1.821) | 0.591 |
No (ref) | 244 | 161 | 65.9 (59.1–70.6) | |||
Nomadic animals movement in the area in last 15 days | Yes No (ref) | 253 132 | 248 10 | 98.0 (96.3–99.8) 7.5 (0.21–7.1) | 0.701 (0.485–0.924) | 0.002 |
Farming methods | Sedentary | 127 | 13 | 10.2 (4.3–14.7) | 2.990 (0.999–15.001) | 0.001 |
Transhumance | 42 | 34 | 80.9 (63.3–91.8) | |||
Nomadic Mixed (ref) | 210 6 | 206 5 | 98.0 (96.3–100.0) 83.3 (53.5–100) | |||
Clinical sign of FMD | Yes No | 145 240 | 129 129 | 88.9 (83.1–94.3) 53.7 (45.5–58.7) | 0.071 (0.041–0.192) | 0.000 |
Type of flock/herd | Sheep Goat Cattle Buffalo Mixed (ref) | 72 93 36 54 130 | 41 63 24 50 80 | 56.9 (45.5–68.3) 67.7 (58.2–77.2) 66.6 (51.2–82.0) 92.5 (73.9–99.2) 61.5 (53.1–69.9) | 1.028 (0.378–2.800) 1.324 (0.498–3.519) 0.452 (0.125–1.643) 0.288 (0.058–1.420) | 0.081 |
Return of unsold animals from the market | Yes No | 50 335 | 37 221 | 74.0 (50.1–81.4) 65.9 (59.8–70.1) | 1.612 (0.525–4.125) | 0.745 |
Outbreak location | MohmandAgency Khyber Agency Bajuar Agency Swat Chitral Gilgit Shangla (ref) | 60 43 41 85 45 44 67 | 46 20 26 69 21 32 44 | 76.6 (65.9–87.3) 46.5 (31.6–61.4) 63.4 (48.6–78.1) 81.1 (72.4–89.4) 46.6 (32.0–61.2) 72.7 (59.5–85.8) 65.6 (49.7–79.0) | 0.751 (0.165–3.414) 4.918 (1.152–21.007) 1.881 (0.401–8.829) 3.073 (0.747–12.646) 0.837 (0.187–3.739) 0.487 (0.129–1.831) | 0.016 |
Seasons Monsoon Post Monsoon Winter Winter Summer | Aug-Sep Oct-Nov Dec-Jan Feb-March April-June | 48 25 171 117 24 | 40 12 115 78 13 | 83.3 (72.7–93.8) 48.0 (28.4–67.5) 67.2 (59.1–74.03) 66.6 (54.1–71.9) 54.1 (34.2–74.1) | 0.158 (0.037–0.671) 0.436 (0.092–2.071) 0.783 (0.232–2.545) 0.495 (0.142–1.732) | 0.020 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ullah, M.; Li, Y.; Munib, K.; Rahman, H.U.; Zhang, Z. Sero-Epidemiology and Associated Risk Factors of Foot-and-Mouth Disease (FMD) in the Northern Border Regions of Pakistan. Vet. Sci. 2023, 10, 356. https://doi.org/10.3390/vetsci10050356
Ullah M, Li Y, Munib K, Rahman HU, Zhang Z. Sero-Epidemiology and Associated Risk Factors of Foot-and-Mouth Disease (FMD) in the Northern Border Regions of Pakistan. Veterinary Sciences. 2023; 10(5):356. https://doi.org/10.3390/vetsci10050356
Chicago/Turabian StyleUllah, Munib, Yanmin Li, Kainat Munib, Hanif Ur Rahman, and Zhidong Zhang. 2023. "Sero-Epidemiology and Associated Risk Factors of Foot-and-Mouth Disease (FMD) in the Northern Border Regions of Pakistan" Veterinary Sciences 10, no. 5: 356. https://doi.org/10.3390/vetsci10050356