First report of fowl aviadenovirus serotypes FAdV-8b and FAdV-11 associated with inclusion body hepatitis in commercial broiler and broiler-breeder flocks in Turkey

  • İsmail ŞahindokuyucuEmail author
Original Article


Inclusion body hepatitis (IBH), hydropericardium syndrome (HS), and gizzard erosion (GE) are all economically important diseases in the poultry industry worldwide and are all caused by fowl aviadenovirus (FAdV). It is important to identify the serotype of the virus to differentiate these diseases. In the present study, a total of six recent FAdV serotypes were isolated and identified in broiler and broiler-breeder flocks in Izmir, Manisa, and Aydın provinces of the Aegean region of Turkey between January and March 2019. The viruses were isolated from livers and pooled organs of chickens using primary chicken embryo kidney cell cultures (CEKC). Virus isolates were identified by PCR amplification of the loop 1 (L1) variable region of the hexon gene followed by Sanger sequencing. Sequence analysis revealed the presence of both FAdV-D (serotype 11) and FAdV-E (serotype 8b). The viruses that were isolated were associated with IBH, which is typically characterized by gross lesions such as enlarged and pale yellow liver with multiple petechial hemorrhages. Histopathological examination also showed necrotizing hepatitis with intranuclear inclusion bodies in hepatocytes. This study is the first report of the isolation and identification of FAdV serotypes associated with IBH in commercial broilers and broiler-breeder flocks in Turkey. The results of sequence analysis showed that FAdV-8b and FAdV-11 were the circulating serotypes that caused recent field outbreaks of IBH in the Aegean region between January and March, 2019.



The authors thank Dr. Ozhan Turkyilmaz, Dr. Gulnur Kalayci, Mr. Hasan Huseyin Pala and Mr. Bahtiyar Yılmaz for their contribution and help. The authors also especially thank Dr. Gerald Barry (University College of Dublin, Ireland) for English language editing and scientific advice. This study was supported by the Izmir/Bornova Veterinary Control Institute.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

In this study, the samples were collected after the death of chickens because of virus infections in broiler and broiler-breeder flocks. No chickens were killed for the purpose of the sampling in the present study.


  1. 1.
    Adair BM, McFerran JB (2008) Adenoviruses in a laboratory manual for the isolation, identification and characterization of avian pathogens, 5th edn. In: Zavala LD, Swayne DE, Glisson JR, Pearson JE, Reed WM, Jackwood MW, Woolcock PR (eds) A laboratory manual for the isolation, identification, and characterization of avian pathogens. The American Association of Avian Pathologists, Kennett Square, pp 84–89Google Scholar
  2. 2.
    Adair BM, Smyth JA (2008) Group I Adenovirus infections. In: Saif YM, Fadly AM, Glisson JR, McDougald LR, Nolan LK, Swayne DE (eds) Diseases of poultry, 12th edn. Iowa State University Press, Iowa, pp 252–266Google Scholar
  3. 3.
    Ahmad K, Ahmad I, Muneer MA, Ajmal M (1992) Experimental transmission of Angara disease in broiler fowls. Stud Res Vet Med 1:53–55Google Scholar
  4. 4.
    Akhtar S, Zahid S, Khan MI (1992) Risk factors associated with hydropericardium syndrome in broiler flocks. Vet Rec 131:481–484CrossRefPubMedGoogle Scholar
  5. 5.
    Akhtar S (1995) Lateral spread of the aetiologic agent(s) of hydropericardium syndrome in broiler chickens. Vet Rec 136:118–120CrossRefPubMedGoogle Scholar
  6. 6.
    Choi K, Kye SJ, Kim JY, Jeon WJ, Lee EK, Park KY, Sung HW (2012) Epidemiological investigation of outbreaks of fowl adenovirus infection in commercial chickens in Korea. Poult Sci 91:2502–2506CrossRefPubMedGoogle Scholar
  7. 7.
    Cook JKA (1974) Spread of an avian adenovirus (CELOvirus) to uninoculated fowls. Res Vet Sci 16:156–161CrossRefPubMedGoogle Scholar
  8. 8.
    Dar A, Gomis S, Shirley I, Mutwiri G, Brownlie R, Potter A, Gerdts V, Tikoo SK (2012) Pathotypic and molecular characterization of a fowl adenovirus associated with inclusion body hepatitis in Saskatchewan chickens. Avian Dis 56:73–81CrossRefPubMedGoogle Scholar
  9. 9.
    Helmboldt CF, Frazier MN (1963) Avian hepatic inclusion bodies of unknown significance. Avian Dis 7(4):446–450CrossRefPubMedGoogle Scholar
  10. 10.
    Hess M, Raue R, Prusas C (1999) Epidemiological studies on fowl adenoviruses isolated from cases of infectious hydropericardium. Avian Pathol 28:433–439CrossRefPubMedGoogle Scholar
  11. 11.
    Hess M (2000) Detection and differentiation of avian adenoviruses: a review. Avian Pathol 29:195–206CrossRefPubMedGoogle Scholar
  12. 12.
    Hess M, Prusas C, Bergmann V, Mazaheri A, Raue R (2000) Epizootiology of fowls adenoviruses Berl. Munch Tierarztl Wochenschr 113:202–208Google Scholar
  13. 13.
    Hess M (2013) Diseases of poultry. Aviadenovirus infections, 13th edn. Wiley, Hoboken, pp 290–300Google Scholar
  14. 14.
    Howell J, MacDonald DW, Christian RG (1970) Inclusion body hepatitis in chickens. Can Vet J 11(5):99–101PubMedPubMedCentralGoogle Scholar
  15. 15.
    Kataria JM, Dhama K, Nagarajan S, Chakraborty S, Kaushal A, Deb R (2013) Fowl adenoviruses causing hydropericardium syndrome in poultry. Adv Anim Vet Sci 1(4):5–13Google Scholar
  16. 16.
    Lim TH, Lee HJ, Lee DH, Lee YN, Park JK, Youn HN, Kim MS, Youn HS, Lee JB, Park SY, Choi IS, Song CS (2011) Identification and virulence characterization of fowl adenoviruses in Korea. Avian Dis 55:554–560CrossRefPubMedGoogle Scholar
  17. 17.
    Macpherson I, McDougall JS, Laursen-Jones AP (1974) Inclusion body hepatitis in a broiler integration. Vet Rec 95(13):286–289CrossRefPubMedGoogle Scholar
  18. 18.
    Mase M, Nakamura K, Minami F (2012) Fowl adenoviruses isolated from chickens with inclusion body hepatitis in Japan, 2009–2010. J Vet Med Sci 74:1087–1089CrossRefPubMedGoogle Scholar
  19. 19.
    Matos M, Grafl B, Liebhart D, Hess M (2016) The outcome of experimentally induced inclusion body hepatitis (IBH) by fowl aviadenoviruses (FAdVs) is crucially influenced by the genetic background of the host. Vet Res 47:69CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Mazaheri A, Prusas C, Vossand M, Hess M (2003) Vertical transmission of fowl Adenovirus serotype 4 investigated in specified pathogen-free birds after experimental infection. Archiv für Geflügelkunde 67:6–10Google Scholar
  21. 21.
    McFerran JB, McCracken RM, Connor TJ, Evans RT (1976) Isolation of viruses from clinical outbreaks of inclusion body hepatitis. Avian Pathol 5(4):315–324CrossRefPubMedGoogle Scholar
  22. 22.
    Meulemans G, Boschmans M, Van den Berg TP, Decaesstecker M (2001) Polymerase chain reaction combined with restriction enzyme analysis for detection and differentiation of fowl adenoviruses. Avian Pathol 30(6):655–660. CrossRefPubMedGoogle Scholar
  23. 23.
    Morshed R, Hosseini H, Langeroudi AG, Fard MHB, Charkhkar S (2017) Fowl adenoviruses D and E cause inclusion body hepatitis outbreaks in broiler and broiler-breeder pullet flocks. Avian Dis 61:205–210CrossRefPubMedGoogle Scholar
  24. 24.
    Nakamura K, Mase M, Yamamoto Y, Takizawa K, Kabeya M, Wakuda T, Matsuda M, Chikuba T, Yamamoto Y, Ohyama T, Takahashi K, Sato N, Akiyama N, Honma H, Imai K (2011) Inclusion body hepatitis caused by fowl adenovirus in broiler chickens in Japan, 2009–2010. Avian Dis 55:719–723CrossRefPubMedGoogle Scholar
  25. 25.
    Ojkic D, Martin E, Swinton J, Vaillancourt JP, Boulianne M, Gomis S (2008) Genotyping of Canadian isolates of fowl adenoviruses. Avian Pathol 37:95–100CrossRefPubMedGoogle Scholar
  26. 26.
    Raue R, Hess M (1998) Hexon based PCRs combined with restriction enzyme analysis for rapid detection and differentiation of fowl adenoviruses and egg drop syndrome virus. J Virol Methods 73:211–217CrossRefPubMedGoogle Scholar
  27. 27.
    Sanei B (2009) IBH in ontario broilers. Canadian poultry magazine., Ontario, pp 22–28Google Scholar
  28. 28.
    Senties-Cue CG et al (2010) Epidemiology and effect on production parameters of an outbreak of inclusion body hepatitis in broilers. Avian Dis 54(1):74–78CrossRefPubMedGoogle Scholar
  29. 29.
    Steer PA, O’Rourke D, Ghorashi SA, Noormohammadi AH (2011) Application of high-resolution melting curve analysis for typing of fowl adenoviruses in field cases of inclusion body hepatitis. Aust Vet J 89:184–192CrossRefPubMedGoogle Scholar
  30. 30.
    Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  31. 31.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Toro H, González O, Escobar C, Cerda L, Morales MA, González C (2001) Vertical induction of the inclusion body hepatitis/hydropericardium syndrome with fowl adenovirus and chicken anemia virus. Avian Dis 45:215–222CrossRefPubMedGoogle Scholar
  33. 33.
    Toro H, Gonzalez C, Cerda L, Morales MA, Dooner P, Salamero M (2002) Prevention of inclusion body hepatitis/hydropericardium syndrome in progeny chickens by vaccination of breeders with fowl adenovirus and chicken anemia virus. Avian Dis 46:547–554CrossRefPubMedGoogle Scholar
  34. 34.
    Villegas PC (2006) Laboratory manual avian virus diseases. College of Veterinary Medicine, Athens, pp 5–6Google Scholar
  35. 35.
    Wilson FD, Wills RW, Senties-cue CG, Maslin WR, Stayer PA, Magee DL (2010) High incidence of glomerulonephritis associated with inclusion body hepatitis in broiler chickens: routine histopathology and histomorphometric studies. Avian Dis 54:975–980CrossRefPubMedGoogle Scholar
  36. 36.
    Zadravec M, Slavec B, Krapez U, Kajan GL, Racnik J, Junts P, Cizerl RJ, Benko M, Rojs OZ (2013) Inclusion body hepatitis (IBH) outbreak associated with fowl adenovirus type 8b in broilers. Acta Vet 63:101–110CrossRefGoogle Scholar
  37. 37.
    Zhao J, Zhong Q, Zhao Y, Hu YX, Zhang GZ (2015) Correction: Pathogenicity and complete genome characterization of fowl adenoviruses isolated from chickens associated with inclusion body hepatitis and hydropericardium syndrome in China. PLoS One 11:e0161744CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Izmir/Bornova Veterinary Control InstituteIzmirTurkey

Personalised recommendations