Syndromic surveillance of infectious bursal disease in chickens using lesion indicators: Analysis of clinical records (2008-2018)

Abstract

Infectious bursal disease (IBD) outbreaks significantly undermine chicken production. Syndromic surveillance based on lesion indicators is an established tool for monitoring the disease following reports of morbidity and mortality. This study aimed to develop an epidemiological profile of the IBD burden, including syndromic outbreak prevalence rates, yearly trends, mortality rates, and lesion patterns, used for surveillance. Records of IBD outbreaks from two veterinary hospitals in Maiduguri, Nigeria, were extracted from all reported disease outbreaks in chicken flocks between 2008 and 2018. IBD outbreaks accounted for 493 cases (7.6%; 95% confidence interval [CI]: 7.0-8.3%) of 6,486 recorded disease outbreaks. Annual prevalence ranged from 1.6% (95% CI: 0.9-2.3%) to 17.3% (95% CI: 12.9-21.7%) and showed a linear trend (r = −0.73; p < 0.01), with a significant association across years (p < 0.001). Prevalence varied significantly with chicken type (p < 0.05), with the highest rate observed in Noilers (25.0%), followed by cockerels (17.5%), local chickens (9.1%), broilers (7.2%), and layers (7.1%). Affected chickens were aged 2-27 weeks, with a modal age of 4-5 weeks and a mean age of 5.0 ± 1.7 weeks. The overall mortality rate was 12.6% (95% CI: 12.3-12.9) based on a total flock size of 38,485 from 2015 to 2018, the period for which flock size and mortality records were available. Key lesions used for syndromic detection of acute IBD included inflammatory swelling of the bursa of Fabricius (90.9%), hemorrhages in thigh, leg, and/or breast muscles (72.2%), mucosal hemorrhages at the proventriculus-ventriculus junction, with and without enteritis (24.9%), and kidney lesions (7.7%). This syndromic surveillance system enables outbreak monitoring and can inform the planning of control measures to reduce disease-associated production losses.

Keywords

Infectious bursal disease / Outbreak detection / Syndromic surveillance / Lesion indicator / Chicken / Nigeria

Acknowledgments

The authors appreciate the support and permission to access data from the Veterinary Teaching Hospital, University of Maiduguri, and the Ali Modu Sherriff Veterinary Hospital, both in Maiduguri, Nigeria.

Funding

The project received no direct funding. Ikechukwu Onyebuchi Igbokwe, serving as the principal investigator, received a small research grant from the Centre for Research and Innovation, University of Maiduguri under the TETFund Institution-Based Research Fund scheme to conduct a study on Infectious bursal disease.

Conflict of interest

The authors declare that they have no competing interests.

Author contributions

Conceptualization: Samaila Jonathan Badau, Ikechukwu Onyebuchi Igbokwe

Formal analysis: All authors

Investigation: Samaila Jonathan Badau, Ikechukwu Onyebuchi Igbokwe

Methodology: All authors

Supervision: Ikechukwu Onyebuchi Igbokwe, Shehu Usman Hassan, Abdul-Dahiru El-Yuguda

Writing-original draft: Samaila Jonathan Badau

Writing - review & editing: All authors

Ethics approval and consent to participate

The research was approved by the Postgraduate Committee on Research (University of Maiduguri; approval no.: PGA/16/11/04/09900), and the institutional Ethics Committee confirmed that no ethical approval was required after permission to obtain data was granted.

Consent for publication

Not applicable.

Availability of data

The raw data for the study are available upon request, subject to permission from the veterinary hospitals that maintain the passive surveillance data.

Further disclosure

Findings of this study have been uploaded as preprint versions on Research Square:

(i) Badau SJ, Igbokwe IO, Hassan SU, El-Yuguda AD. Outbreaks of acute infectious bursal disease of chickens in Maiduguri, Nigeria (2008-2018): retrospective survey, 23 February 2023, PREPRINT (Version 1) available at Research Square [https://doi.org/10.21203/rs.3.rs-2305788/v1]

(ii) Badau SJ, Hassan SU, El-Yuguda AD, Igbokwe IO. Syndromic surveillance using lesion indicators for infectious bursal disease in chickens: insight from data summary and analysis from clinic records (2008- 2018), 07 September 2025, PREPRINT (Version 1) available at Research Square [https://doi.org/10.21203/rs.3.rs-5200288/v1]

References

[1] Adamu J, Owoade AA, Abdu PA, Kazeem HM, Fatihu MY. Characterization of field and vaccine infectious bursal disease viruses from Nigeria revealing possible virulence and regional markers in the VP 2 minor hydrophilic peaks. Avian Pathol. 2013; 42(5):420-433. doi:10.1080/03079457.2013.822055

[2] Nwagbo IO, Shittu I, Nwosuh CI, et al. Molecular characterization of field infectious bursal disease virus isolates from Nigeria. Vet World. 2016; 9(12):1420-1428. doi: 10.14202/vetworld.2016.1420-1428

[3] Igbokwe IO, Salako MA, Rabo JS, Hassan SU. Outbreak of infectious bursal disease associated with acute septicaemic colibacillosis in adult prelayer hens. Rev Elev Med Vet Pays Trop. 1996; 49(2):110-113.

[4] Igbokwe IO, Adawaren EO, Abba Y. Concurrent outbreak of staphylococcal pneumonia with infectious bursal disease in broiler chickens. Comp Clin Pathol. 2012; 21(6):1571-1575. doi: 10.1007/s00580-011-1329-x

[5] Ojo MO, Oduye OO, Noibi LM, et al. Gumboro-like disease in Nigeria. Trop Anim Health Prod. 1973; 5:52-56. doi: 10.1007/BF02239686

[6] Onunkwo O. An outbreak of infectious bursal disease (IBD) of chickens in Nigeria. Vet Rec. 1975; 97(22):433. doi: 10.1136/vr.97.22.433

[7] Okoye JO, Uzoukwu M. An outbreak of infectious bursal disease among chickens between 16 and 20 weeks old. Avian Dis. 1981; 25(4):1034-1038. doi: 10.2307/1590079

[8] Okoye JOA, Uzoukwu M. Characterization of Nigerian strains of infectious bursal disease virus of chickens: Clinicopathological manifestations of naturally occurring field outbreaks. Bull Anim Health Prod Afr. 1982; 30:193-197.

[9] Okoye JO. Infectious bursal disease in vaccinated flocks in Nigeria. Bull Anim Health Prod Afr. 1984; 32:193-196.

[10] Durojaiye OA, Ajibade HA, Olafimiham GO. An outbreak of infectious bursal disease in 20-week old birds. Trop Vet. 1984; 2:175-776.

[11] Durojaiye OA, Adene DF, Owoade AA. Counter immunoelectroosmophoresis in the diagnosis of infectious bursal disease of poultry. Trop Anim Health Prod. 1985; 17(4):225-229. doi: 10.1007/BF02356981

[12] Abdu PA. Infectious bursal disease immunisation failures in chickens in Nigeria. Trop Anim Health Prod. 1986; 18(2):123-125. doi: 10.1007/BF02359726

[13] Abdu PA. Infectious bursal disease in a flock of broilers and local chickens in Nigeria. Bull Anim Health Prod Afr. 1986; 18(2):123-125.

[14] Nwosuh CI, Okewole PA, Aba-Adulugba A, Adeyeni PS. Outbreak of infectious bursal disease in vaccinated flock in Kano. Trop Vet. 1989; 7:32-34.

[15] Onunkwo O, Okoye JO. First report of an IBD outbreak in a vaccinated chicken flock in Anambra State, Nigeria. Rev Elev Med Vet Pays Trop. 1991; 44(4):411-414. doi: 10.19182/remvt.9144

[16] Awolaja OA, Adene DF. Infectious bursal disease outbreak in a vaccinated poultry flock. Trop Vet. 1995; 13:37-43.

[17] Owoade AA, Durojaiye OA. Infectious bursal disease in 14-week-old turkeys in Nigeria. Trop Anim Health Prod. 1995; 27(1):47-49. doi: 10.1007/bf02236337

[18] Ibrahim UI, Ambali AG, Geidam YA, Gulani IA. Outbreak of infectious bursal disease in a vaccinated flock of chickens in Maiduguri, Nigeria. Sahel J Vet Sci. 2003; 2:35-37.

[19] Oluwayelu DO, Emikpe BO, Ikheloa JO, Fagbohun OA, Adeniran GA. The pathology of infectious bursal disease in cross breads of Harco cocks and indigenous Nigerian hens. Afr J Clin Exp Microbiol. 2002; 3(2):91. doi: 10.4314/ajcem.v3i2.7336

[20] El-Yuguda AD, Baba SS. An outbreak of infectious bursal disease in eight weeks old IBD vaccinated commercial poultry flock in Maiduguri, Nigeria. Trop Vet. 2006; 22(3). doi: 10.4314/tv.v22i3.4558

[21] Hassan SU, El-Yuguda AD, Gambo HI, Dzuel YM. Outbreak of infectious bursal disease (IBD) associated with hydropericardium syndrome among experimental chickens in Maiduguri, Nigeria. Sahel J Vet Sci. 2011; 10(1):23-27.

[22] Musa IW, Sa’idu L, Abalaka ES. Economic impact of recurrent outbreaks of infectious bursal disease in a commercial poultry farm in Kano, Nigeria. Asian J Poult Sci. 2012; 6(4):152-159. doi: 10.3923/ajpsaj.2012.152.159

[23] Shekaro A, Josiah IE. Infectious bursal disease outbreak in fifteen weeks old pullets in Kaduna, Nigeria. J Anim Prod Adv. 2015; 5(3):636-644. doi: 10.5455/JAPA.20150315015216

[24] Aliyu HB, Sa’idu L, Jamilu A, Andamin AD, Akpavie SO. Outbreaks of Virulent Infectious Bursal Disease in Flocks of Battery Cage Brooding System of Commercial Chickens. J Vet Med. 2016; 2016:1-7. doi: 10.1155/2016/8182160

[25] Igwe AO, Nwachukwu OJ, Chinyere CN, Shittu I. Evaluation of pathological changes of natural infectious bursal disease virus infection in lymphoid organs of Black Harco pullets. Sokoto J Vet Sci. 2017; 15(2):18-28. doi: 10.4314/sokjvs.v15i2.3

[26] Enurah LU, Nwosuh CI, Ehizibolo DO, et al. Gross and Histopathological Changes in Chickens Infected with Infectious Bursal Disease Virus (IBDV) in a Farm in Vom, Plateau State, Nigeria. Asian J Res Animal Vet Sci. 2019; 1(4):288-296. doi: 10.9734/AJRAVS/2018/46193

[27] Mohammed UM, Garba S, Armiya’u R. Outbreak of infectious bursal disease in a flock of 14 weeks old ISA brown pullets, Sokoto State, Nigeria. GSC Biol Pharm Sci. 2019; 9(2):001-008. doi: 10.30574/gscbps.2019.9.2.0182

[28] Abalaka SE, Sani NA, Idoko SI, et al. Pathologic diagnosis of infectious bursal disease outbreak in vaccinated 3-week old pullet chicks on a small scale commercial poultry farm. J Vet Biomed Sci. 2019; 1(2):1-8. doi: 10.36108/jvbs/8102.10.0210

[29] Ogbe AO, Audu Z, Kwaja EZ. Pathological diagnosis of infectious bursal disease in 24 weeks old vaccinated commercial laying hens in Kagarko, Nigeria: a case report. J Dairy Vet Anim Res. 2020; 9(6):172-176. doi: 10.15406/jdvar.2020.09.00300

[30] Owolodun OA, Yakubu B, Jambol AR, et al. Further evidence for very virulent infectious bursal disease virus in vaccinated chickens in Nigeria. Trop Anim Health Prod. 2015; 47:1437-1441. doi: 10.1007/s11250-015-0880-x

[31] Bosha JA, Nongo NN. Common breaches in poultry vaccine handling and administration in Makurdi metropolis: A recurrent phenomena in the tropics. Vom J Vet Sci. 2012; 9:11-16. Available from https://www.ejmanager.com/mnstemps/98/98-1365025156.pdf [Last accessed on 9 April 2026].

[32] Igbokwe IO, Maduka CV, Igbokwe NA, Ogbaji SJ, Onah CC, Atsanda NN. Adoption and failure rates of vaccinations for disease prevention in chicken farms in Jos, Nigeria. Trop Anim Health Prod. 2020; 52(6):3113-3121. doi: 10.1007/s11250-020-02335-1

[33] Ekiri AB, Armson B, Adebowale K, et al. Evaluating Disease Threats to Sustainable Poultry Production in Africa: Newcastle Disease, Infectious Bursal Disease, and Avian Infectious Bronchitis in Commercial Poultry Flocks in Kano and Oyo States, Nigeria. Front Vet Sci. 2021; 8:730159. doi: 10.3389/fvets.2021.730159

[34] Arowolo OA, George UE, Luka PD, et al. Infectious bursal disease in Nigeria: continuous circulation of reassortant viruses. Trop Anim Health Prod. 2021; 53(2):271. doi: 10.1007/s11250-021-02719-x

[35] Nwagbo I, Shittu I, Qasim A, Joannis T. Continuous circulation and mutation at the hypervariable region of the VP2 gene of very virulent infectious bursal disease virus in Nigeria. Niger Vet J. 2018; 39(2):143-150. doi: 10.4314/nvj.v39i2.6

[36] Teshome M, Admassu TFB. Infectious bursal disease (Gumboro disease) in chickens. Br J Poult Sci. 2015; 4:22-28. doi: 10.5829/idosi.bjps.2015.4.1.95172

[37] Igbokwe IO. Postmortem examination of carcasses. Zariya Vet. 1989; 4:145-152. doi: 10.6084/m9.figshare.19102754

[38] Salami JO, Egbulem BN, Kwaga JKP, Yusufu HI, Abdu PA. Nigeria. Disease diagnosed in poultry in Kaduna State, Bull Anim Health Prod Afr. 1989; 18(2):123-125.

[39] Tong JC, Umoh JU, Abdu PA, Sa’idu L. Retrospective studies of Gumboro disease seen in Ahmadu Bello University Veterinary Teaching Hospital, Zaria, Nigeria (1985- 1990). Bull Anim Health Prod Afr. 1993; 41:173-179.

[40] Halle PD, Umoh JU, Saidu L, Abdu PA. Diseases of poultry in Zaria, Nigeria: A ten year analysis of clinic records. Niger J Anim Prod. 2021; 25(1):88-92. doi: 10.51791/njap.v25i1.2269

[41] Ambali AG, Abubakar MB, James TE. An assessment of poultry health problems in Maiduguri, Borno State, Nigeria. Trop Vet. 2004; 21(3). doi: 10.4314/tv.v21i3.4534

[42] Igbokwe IO, Dagwannah NA, Ibrahim UI. Prevalence of endemic viral disease of poultry in Maiduguri, Borno State. In: Proceedings of the 42nd Congress of Nigerian Veterinary Medical Association. November 14-18, 2005; Maiduguri, Nigeria. 2005:206-207.

[43] Adamu AY, Ahmed AB, Abubakar MB, Lawal MD. A retrospective study (2004-2008) of poultry diseases diagnosed in veterinary teaching hospital (VTH), Usmanu Danfodio University, Sokoto (UDUS) and Sokoto Veterinary Centre (SVC), Sokoto State, Nigeria. Int J Anim Vet Adv. 2009; 1(1):15-17.

[44] Mbuko IJ, Abdu PA, Saidu L, Oladele SB, Kazeem H. Investigation of outbreaks of infectious bursa disease in Zaria, Nigeria. Inter J Trop Dis Hlth. 2014; 4(4):411-426. doi: 10.9734/ijtdh/2014/6118

[45] Balami AG, Ndahi JJ, Zaifada AU, et al. A retrospective study of poultry diseases diagnosed in Maiduguri, North- East, Nigeria. Poult Fish Wildlife Sci. 2014; 2:113. doi: 10.4172/2375-446x.1000113

[46] Mshelia IT, Atsanda NN, Bitrus AA, et al. Retrospective study of selected endemic viral diseases of poultry diagnosed in Maiduguri, North-Eastern Nigeria. J Anim Health Prod. 2016; 4(2):60-64. doi: 10.14737/journal.jahp/2016/4.2.60.64

[47] Dorea FC, Vial F. Animal health syndromic surveillance: a systematic literature review of the progress in the last 5 years (2011-2016). Vet Med (Auckl). 2016; 7:157-170. doi: 10.2147/VMRR.S90182

[48] Alba A, Dorea FC, Arinero L, et al. Exploring the surveillance potential of mortality data: nine years of bovine fallen stock data collected in Catalonia (Spain). PLoS One. 2015; 10(4):e0122547. doi: 10.1371/journal.pone.0122547

[49] Dorea FC, Sanchez J, Revie CW. Veterinary syndromic surveillance: Current initiatives and potential for development. Prev Vet Med. 2011; 101(1-2):1-17. doi: 10.1016/j.prevetmed.2011.05.004

[50] Murray J, Cohen AL. Infectious Disease Surveillance. In: International Encyclopedia of Public Health. Vol 4. 2nd ed. 2017:222-229. doi: 10.1016/B978-0-12-803678-5.00517-8

[51] Zhuang QY, Wang SC, Li JP, et al. A clinical survey of common avian infectious diseases in China. Avian Dis. 2014; 58(2):297-302. doi: 10.1637/10709-110113-ResNote.1

[52] Rahman MA, Rahman MM, Abdullah MS, et al. Epidemiological assessment of clinical poultry cases through the government veterinary hospital-based passive surveillance system in Bangladesh: a case study. Trop Anim Health Prod. 2019; 51(4):967-975. doi: 10.1007/s11250-018-1782-5

[53] George J, Hasler B, Komba EVG, Rweyemamu M, Kimera SI, Mlangwa JED. Mechanisms and Contextual Factors Affecting the Implementation of Animal Health Surveillance in Tanzania: A Process Evaluation. Front Vet Sci. 2022; 8:790035. doi: 10.3389/fvets.2021.790035

[54] Huneau-Salaun A, Stark KD, Mateus A, Lupo C, Lindberg A, Le Bouquin-Leneveu S. Contribution of Meat Inspection to the surveillance of poultry health and welfare in the European Union. Epidemiol Infect. 2015; 143(11):2459-2472. doi: 10.1017/S0950268814003379

[55] Abubakar AT, Ogundijo OA, Al-Mustapha AI. Animal disease surveillance system key to understanding disease dynamics. Nature Africa. 2022. doi: 10.1038/d44148-022-00142-4

[56] Al-Mustapha AI, Adetunji V, Ogundijo OA, et al.Animal Disease Burden in Nigeria,2006-2023. Transbound Emerg Dis. 2025; 2025(1): 1694850. doi: 10.1155/tbed/1694850

[57] Haruna ES, Adene DE, Gerrit VJ. Detection of infectious bursal disease virus (IBDV) in naturally infected chickens in Nigeria by reverse transcription-polymerase chain reaction (RT-PCR). Niger Vet J. 2005; 24(2):1-9. doi: 10.1016/0167-5877(89)90004-4

[58] Ogundipe GAT, Oluokun SB, Esuruoso GO. The development and efficiency of the animal health and information system in Nigeria. Prev Vet Med. 1989;7(2):121-135. doi: 10.4314/nvj.v24i2.3448

[59] Sheikh AM, Onyiche ET, Chul SA, Yunus H, Aji AM. A preliminary study on poultry production and the effect of Boko Haram insurgency in Maiduguri. Sahel J Vet Sci. 2022; 19(4):16-19. doi: 10.54058/saheljvs.v19i4.342

[60] Maduka CV, Igbokwe IO, Atsanda NN. Appraisal of Chicken Production with Associated Biosecurity Practices in Commercial Poultry Farms Located in Jos, Nigeria. Scientifica. 2016; 2016:1-9. doi: 10.1155/2016/1914692

[61] Ahmed M, Sarker A, Rahman M. Prevalence of infectious diseases of broiler chickens in Gazipur district. Bangl J Vet Med. 1970; 7(2):326-331. doi: 10.3329/bjvm.v7i2.5999

[62] Rashid MH, Xue C, Islam MR, Islam MT, Cao Y. A longitudinal study on the incidence of mortality of infectious diseases of commercial layer birds in Bangladesh. Prev Vet Med. 2013; 109(3-4):354-358. doi: 10.1016/j.prevetmed.2012.10.012

[63] Chakma S. Epidemiology of infectious bursal disease in broiler birds of three districts in Bangladesh. Asian J Med Biol Res. 2015; 1(1):59-64. doi: 10.3329/ajmbr.v1i1.25499

[64] Jindal N, Mahajan NK, Mittal D, Gupta SL, Khokhar RS. Some epidemiological studies on infectious bursal disease in broiler chickens in parts of Haryana, India. Int J Poult Sci. 2004; 3(7):478-482. doi: 10.3923/ijps.2004.478.482

[65] Khan RW, Khan FA, Farid K, Khan I, Tariq M. Prevalence of infectious bursal disease in broilers in district Peshawar. ARPN J Agric Biol Sci. 2009; 4(1):1-5.

[66] Mor SK, Narang G, Jindal N, Mahajan NK, Sharma PC, Rakha NK. Epidemiological studies on infectious bursal disease in broiler chickens in Haryana, India. Int J Poult Sci. 2010; 9(4):395-400. doi: 10.3923/ijps.2010.395.400

[67] Bhutia LD, Rajkhowa TK, Ravindran R, et al. Infectious bursal disease (IBD) outbreaks in poultry population of Mizoram, India. Indian J Vet Pathol. 2017; 14(1):63-66. doi: 10.5958/0973-970X.2017.00015.3

[68] Rashid MH, Xue C, Islam MT, Islam MR, She Z, Cao Y. Comparative epidemiological study of infectious bursal disease of commercial broiler birds in Bangladesh and China. Pak Vet J. 2013; 33(2):160-164.

[69] Okoye JO, Aba-Adulugba EP, Ezeokonkwo RC, Udem SC, Orajaka LJ. Susceptibility of local Nigerian and exotic chickens to infectious bursal disease by contact exposure. Trop Anim Health Prod. 1999; 31(2):75-81. doi: 10.1023/a:1005159522203

[70] Sa e Silva M, Rissi DR, Swayne DE. Very virulent infectious bursal disease virus produces more-severe disease and lesions in Specific-Pathogen-Free (SPF) Leghorns than in SPF broiler chickens. Avian Dis. 2016; 60(1):63-66. doi: 10.1637/11230-070615-ResNote.1

[71] Ajayi FO, Bamidele O, Hassan WA, et al. Production performance and survivability of six dual-purpose breeds of chicken under smallholder farmers’ management practices in Nigeria. Arch Anim Breed. 2020; 63(2):387-408. doi: 10.5194/aab-63-387-2020

[72] Yakubu A, Bamidele O, Hassan WA, et al. Farmers’ choice of genotypes and trait preferences in tropically adapted chickens in five agro-ecological zones in Nigeria. Trop Anim Health Prod. 2020; 52(1):95-107. doi: 10.1007/s11250-019-01993-0

[73] Okoye JOA. The pathology of infectious bursal disease in indigenous Nigerian chickens. Rev Elev Med Vet Pays Trop. 1987; 40(1):13-16. doi: 10.19182/remvt.8682

[74] Abdel-Moneim AS, Abdel-Gawad MM. Genetic variations in maternal transfer and immune responsiveness to infectious bursal disease virus. Vet Microbiol. 2006; 114(1-2):16-24. doi: 10.1016/j.vetmic.2005.10.037

[75] Juul-Madsen HR, Dalgaard TS, Rontved CM, Jensen KH, Bumstead N. Immune response to a killed infectious bursal disease virus vaccine in inbred chicken lines with different major histocompatibility complex haplotypes. Poult Sci. 2006; 85(6):986-998. doi: 10.1093/ps/85.6.986

[76] El-Kady MF, Dahshan AM, Madbouly HM. Studies on infectious bursal disease maternal immunity decay curve in native and Lohmann chicken breeds. J Vet Med Res. 2008; 18(1):34-40. doi: 10.21608/jvmr.2008.77840

[77] Aricibasi M, Jung A, Heller ED, Rautenschlein S. Differences in genetic background influence the induction of innate and acquired immune responses in chickens depending on the virulence of the infecting infectious bursal disease virus (IBDV) strain. Vet Immunol Immunopathol. 2010; 135(1-2):79-92. doi: 10.1016/j.vetimm.2009.11.005

[78] Kundu P, Narang G, Mahajan NK. Retrospective study on epidemiology of infectious bursal disease in broiler chickens in Haryana, India. Int J Curr Microbiol App Sci. 2018; 7(6):1279-1290. doi: 10.20546/ijcmas.2018.706.150

[79] Panisup AS, Verma KC, Mohanty GC. Age resistance in chickens against infectious bursal disease. Acta Vet Scand. 1984; 25(4):561-567. doi: 10.1186/BF03546923

[80] Ismail NM, Fadly AM, Chang TS. Effect of bursal cell number on the pathogenesis of infectious bursal disease in chickens. Avian Dis. 1987; 31(3):546-555. doi: 10.2307/1590738

[81] Ingrao F, Rauw F, Lambrecht B, van den Berg T. Infectious Bursal Disease: a complex host-pathogen interaction. Dev Comp Immunol. 2013; 41(3):429-438. doi: 10.1016/j.dci.2013.03.017

[82] Bickford AA, Kuney DR, Zander DV, McMartin DA. Histologic characterization of the involuting bursa of Fabricius in single-comb white Leghorn chickens. Avian Dis. 1985; 29(3):778-797. doi: 10.2307/1590670

[83] Ley DH, Storm N, Bickford AA, Yamamoto R. An infectious bursal disease virus outbreak in 14- and 15-week-old chickens. Avian Dis. 1979; 23(1):235-240. doi: 10.2307/1589692

[84] Stoute ST, Jackwood DJ, Sommer-Wagner SE, et al. The diagnosis of very virulent infectious bursal disease in California pullets. Avian Dis. 2009; 53(2):321-326. doi: 10.1637/8684-030909-Case.1

[85] Schat KA, Lucio B, Carlisle JC. Pathogenesis of infectious bursal disease in embryonally bursectomized chickens. Avian Dis. 1981; 25(4):996-1004. doi: 10.2307/1590075

[86] Van den Berg TP, Gonze M, Meulemans G. Acute infectious bursal disease in poultry: Isolation and characterisation of a highly virulent strain. Avian Pathol. 1991; 20(1):133-143. doi: 10.1080/03079459108418748

[87] Neto HS, Ito NMK, Miyaji CI, et al. Infectious bursal disease virus: case report and experimental studies in vaccinated and unvaccinated SPF chickens and commercial broiler chicks. Braz J Poult Sci. 2004; 6(1):41-54. doi: 10.1590/S1516-635X2004000100006

[88] Cheggag M, Sebbar G, Zro K, et al. Pathologic, molecular, and serologic response of specific-pathogen-free chickens inoculated by three very virulent infectious bursal disease virus strains. J World Poult Res. 2021; 11(4):457-467. doi: 10.36380/jwpr.2021.54

[89] Ezeibe MCO, Okoye JOA, Ogunniran TM, et al. Mortality rates from a Nigerian isolate of the Infectious Bursa Disease Virus and passive haemagglutination antibody titer that protects chicks against challenge with the virus isolate. Health. 2013; 5:1355-1359. doi: 10.4236/health.2013.59184

[90] Omer MG, Khalafalla AI. Epidemiology and laboratory diagnosis of very virulent infectious bursal disease virus in vaccinated chickens in Khartoum, Sudan. Open Vet J. 2022; 12(1):33-43. doi: 10.5455/OVJ.2022.v12.i1.5

[91] Wang A, Liu F, Wang Z, et al. Pathological study of SPF chickens experimentally infected with Chinese IBDV strain BC6/85. Asian J Anim Vet Adv. 2011; 6:36-50. doi: 10.3923/ajava.2011.36.50

[92] Skeeles JK, Lukert PD, De Buysscher EV, Fletcher OJ, Brown J. Infectious bursal disease viral infection. I. Complement and virus neutralizing antibody response following infection of susceptible chickens. Avian Dis. 1979; 23(1):95-106. doi: 10.2307/1589676

[93] Skeeles JK, Lukert PD, De Buysscher EV, Fletcher OJ, Brown J. Infectious bursal disease viral infections. II. The relationship of age, complement levels, virus-neutralizing antibody, clotting, and lesions. Avian Dis. 1979; 23(1):107-117. doi: 10.2307/1589677

[94] Skeeles JK, Slavik M, Beasley JN, et al. An age-related coagulation disorder associated with experimental with infectious bursal disease virus. Am J Vet Res. 1980; 41(9):1458-1461. doi: 10.2460/ajvr.1980.41.09.1458

[95] Zeryehum T, Hair-Bejo M, Rasedee A. Hemorrhagic and clotting abnormalities in infectious bursal disease in specific pathogen- free chicks. World Appl Sci J. 2012; 16(8):1123-1130.

[96] Li L, Kubasova T, Rychlik I, Hoerr FJ, Rautenschlein S. Infectious bursal disease virus infection leads to changes in the gut associated-lymphoid tissue and the microbiota composition. PLoS One. 2018; 13(2):e0192066. doi: 10.1371/journal.pone.0192066

[97] Ley DH, Storm N, Bickford AA, Yamamoto R. Immune complex involvement in the pathogenesis of infectious bursal disease virus in chickens. Avian Dis. 1979; 23(1):219-224. doi: 10.2307/1589689

[98] Ley DH, Yamamoto R, Bickford AA. The pathogenesis of infectious bursal disease: serologic, histopathologic, and clinical chemical observations. Avian Dis. 1983; 27(4):1060-1085. doi: 10.2307/1590207

[99] Mwenda R, Changula K, Hang’ombe BM, et al. Characterization of field infectious bursal disease viruses in Zambia: evidence of co-circulation of multiple genotypes with predominance of very virulent strains. Avian Pathol. 2018; 47(3):300-313. doi: 10.1080/03079457.2018.1449941

[100] Oluwayelu DO. Diagnosis and epidemiology of chicken infectious anemia in Africa. Afr J Biotechnol. 2010; 9:2043-2049.

[101] Kristeen-Teo YW, Yeap SK, Tan SW, et al. The effects of different velogenic NDV infections on the chicken bursa of Fabricius. BMC Vet Res. 2017; 13:151. doi: 10.1186/s12917-017-1071-y

[102] Tang X, Qi J, Sun L, Zhao J, Zhang G, Zhao Y. Pathological effect of different avian infectious bronchitis virus strains on the bursa of Fabricius of chickens. Avian Pathol. 2022; 51(4):339-348. doi: 10.1080/03079457.2022.2063710

[103] Schat KA. The importance of the bursa of Fabricius, B Cells and T Cells for the pathogenesis of Marek’s disease: a review. Viruses. 2022; 14(9):2015. doi: 10.3390/v14092015

[104] Wu B, Cui H, Peng X, Fang J, Cui W, Liu X. Pathology of bursae of Fabricius in methionine-deficient broiler chickens. Nutrients. 2013; 5(3):877-886. doi: 10.3390/nu5030877

[105] Shah SWA, Ishfaq M, Nasrullah M, et al. Ammonia inhalation-induced inflammation and structural impairment in the bursa of fabricius and thymus of broilers through NF-κB signaling pathway. Environ Sci Pollut Res. 2020; 27:11596-11607. doi: 10.1007/s11356-020-07743-2

[106] Wang L, Zheng Y, Zhang G, Han X, Li S, Zhao H. Lead exposure induced inflammation in bursa of Fabricius of Japanese quail (C. Japonica) via NF-κB pathway activation and Wnt/β-catenin signaling inhibition. J Inorg Biochem. 2021; 224:111587. doi: 10.1016/j.jinorgbio.2021.111587

[107] Bai Y, Zhang R, Liu Q, et al. Selenium deficiency causes inflammatory Injury in the bursa of Fabricius of broiler chickens by activating the Toll-like receptor signaling pathway. Biol Trace Elem Res. 2022; 200(2):780-789. doi: 10.1007/s12011-021-02688-0

[108] Gopal S, Manoharan P, Kathaperumal K, Chidambaram B, Divya KC. Differential detection of avian oncogenic viruses in poultry layer farms and Turkeys by use of multiplex PCR. J Clin Microbiol. 2012; 50(8):2668-2673. doi: 10.1128/JCM.00457-12

[109] Oluigbo F, Enurah LU. Infectious bursal disease (IBD) and coccidiosis concurrent infections in Nigerian indigenous chickens. A case report. Rev Elev Med Vet Pays Trop. 1989; 42(3):330.

[110] Adedeji AJ, Sati NM, Pewan SB, et al. Concurrent infections of chicken infectious anemia and infectious bursal disease in 5 week old pullets in Jos, Plateau State, Nigeria. Vet Sci Res Rev. 2016; 2(3):60-65. doi: 10.17582/journal.vsrr/2016.2.3.60.65

[111] Van NTB, Yen NTP, Nhung NTO, et al. Characterization of viral, bacterial and parasitic causes of disease in small scale chicken flocks in Mekong Delta of Vietnam. Poult Sci. 2020; 99(2):783-790. doi: 10.1016/j.psj.2019.10.033

[112] El-Yuguda AD, Baba SS. Prevalence of selected viral infections in various age groups of village chickens in Borno State, Nigeria. Niger J Anim Prod. 2002; 29(2):245-250. doi: 10.51791/njap.v29i2.1568

[113] Ngwira A, Manda S, Karimuribo ED, Kimera SI, Stanley C. Spatial analysis of livestock disease in Sub-Saharan Africa: A scoping review. Sci Afr. 2024; 23:e02113. doi: 10.1016/j.sciaf.2024.e02113