Commensal or pathogen – a challenge to fulfil Koch’s Postulates

References

• Abe, T., Nakamura, K., Tojo, H., Mase, M., Shibahara, T., Yamaguchi, S. & Yuasa, N. (1998) Histology, immunohistochemistry, and ultrastructure of hydropericardium syndrome in adult broiler breeders and broiler chicks. Avian Diseases, 42: 606–612. doi:10.2307/1592690
   PubMed Web of Science ®Google Scholar
• Addo, P.B. & Mohan, K. (1985) Atypical Pasteurella haemolytica type A from poultry. Avian Diseases, 29: 214–217. doi:10.2307/1590710
   PubMed Web of Science ®Google Scholar
• Al-Sheikhly, F. & Mutalib, A.A. (1979) Inclusion body hepatitis in broiler chickens in Iraq. Avian Diseases, 23: 763–767. doi:10.2307/1589755
   PubMed Web of Science ®Google Scholar
• Anjum, A.D. (1990) Experimental transmission of hydropericardium syndrome and protection against it in commercial broiler chickens. Avian Pathology, 19: 655–660. doi:10.1080/03079459008418721
   PubMed Web of Science ®Google Scholar
• Anjum, A.D., Sabri, M.A. & Iqbal, Z. (1989) Hydropericarditis syndrome in broiler chickens in Pakistan. Veterinary Record, 124: 247–248. doi:10.1136/vr.124.10.247
   PubMed Web of Science ®Google Scholar
• Asthana, M., Chandra, R. & Kumar, R. (2013) Hydropericardium syndrome: current state and future developments. Archives of Virology, 158: 921–931. doi:10.1007/s00705-012-1570-x
   PubMed Web of Science ®Google Scholar
• Bager, R.J., Nesta, B., Pors, S.E., Soriani, M., Serino, L., Boyce, J.D., Adler, B. & Bojesen, A.M. (2013) The fimbrial protein FlfA from Gallibacterium anatis is a virulence factor and vaccine candidate. Infection and Immunity, 81: 1964–1973. doi:10.1128/IAI.00059-13
   PubMed Web of Science ®Google Scholar
• Balamurugan, V. & Kataria, J.M. (2004) The hydropericardium syndrome in poultry – a current scenario. Veterinary Research Communications, 28: 127–148. doi:10.1023/B:VERC.0000012115.86894.1e
   PubMed Web of Science ®Google Scholar
• Bayon, H.P. & Bishop, A. (1937) Cultivation of Histomonas meleagridis from the liver lesions of a hen. Nature, 139: 370–371. doi:10.1038/139370b0
   Google Scholar
• Bilic, I., Jaskulska, B., Souillard, R., Liebhart, D. & Hess, M. (2014) Multi-locus typing of Histomonas meleagridis isolates demonstrates the existence of two different genotypes. PLoS One, 9: e92438. doi:10.1371/journal.pone.0092438
   PubMed Web of Science ®Google Scholar
• Bisgaard, M. (1977) Incidence of Pasteurella haemolytica in the respiratory tract of apparently healthy chickens and chickens with infectious bronchitis. characterisation of 213 strains. Avian Pathology, 6: 285–292. doi:10.1080/03079457708418238
   PubMed Web of Science ®Google Scholar
• Bisgaard, M., Korczak, B.M., Busse, H.-J., Kuhnert, P., Bojesen, A.M. & Christensen, H. (2009) Classification of the taxon 2 and taxon 3 complex of Bisgaard within Gallibacterium and description of Gallibacterium melopsittaci sp. nov., Gallibacterium trehalosifermentans sp. nov. and Gallibacterium salpingitidis sp. nov. International Journal of Systematic and Evolutionary Microbiology, 59: 735–744. doi:10.1099/ijs.0.005694-0
   PubMed Web of Science ®Google Scholar
• Bishop, A. (1938) Histomonas meleagridis in domestic fowls (Gallus gallus) cultivation and experimental infection. Parasitology, 30: 181–194. doi:10.1017/S0031182000025749
   Google Scholar
• Bojesen, A.M., Nielsen, O.L., Christensen, J.P. & Bisgaard, M. (2004) In vivo studies of Gallibacterium anatis infection in chickens. Avian Pathology, 33: 145–152. doi:10.1080/03079450310001652059
   PubMed Web of Science ®Google Scholar
• Bojesen, A.M., Nielsen, S.S. & Bisgaard, M. (2003) Prevalence and transmission of haemolytic Gallibacterium species in chicken production systems with different biosecurity levels. Avian Pathology, 32: 503–510. doi:10.1080/0307945031000154107
   PubMed Web of Science ®Google Scholar
• Bradley, R.E. & Reid, W.M. (1966) Histomonas meleagridis and several bacteria as agents of infectious enterohepatitis in gnotobiotic turkeys. Experimental Parasitology, 19: 91–101. doi:10.1016/0014-4894(66)90057-9
   PubMed Web of Science ®Google Scholar
• Byrd, A.L. & Segre, J.A. (2016) Infectious disease. Adapting Koch’s postulates. Science, 351: 224–226. doi:10.1126/science.aad6753
   PubMed Web of Science ®Google Scholar
• Cepicka, I., Hampl, V. & Kulda, J. (2010) Critical taxonomic revision of Parabasalids with description of one new genus and three new species. Protist, 161: 400–433. doi:10.1016/j.protis.2009.11.005
   PubMed Web of Science ®Google Scholar
• Chandra, R., Shukla, S.K., Kumar, M. & Garg, S.K. (1997) Electron microscopic demonstration of an adenovirus in the hepatocytes of birds experimentally infected with hydropericardium syndrome. Veterinary Record, 140: 70–71. doi:10.1136/vr.140.3.70-b
   PubMed Web of Science ®Google Scholar
• Chen, H., Dou, Y., Zheng, X., Tang, Y., Zhang, M., Zhang, Y., Wang, Z. & Diao, Y. (2016) Hydropericardium hepatitis syndrome emerged in cherry valley ducks in China. Transboundary and Emerging Diseases. doi:10.1111/tbed.12500
   Web of Science ®Google Scholar
• Chester, F.D. & Robin, M.D. (1900) Entero-hepatitis or blackhead of fowls, pp. 60–66 (Deleware College Agricultural Experimental Station).
   Google Scholar
• Choi, K.S., Kye, S.J., Kim, J.Y., Jeon, W.J., Lee, E.K., Park, K.Y. & Sung, H.W. (2012) Epidemiological investigation of outbreaks of fowl adenovirus infection in commercial chickens in Korea. Poultry Science, 91: 2502–2506. doi:10.3382/ps.2012-02296
   PubMed Web of Science ®Google Scholar
• Christensen, H., Bisgaard, M., Bojesen, A.M., Mutters, R. & Olsen, J.E. (2003) Genetic relationships among avian isolates classified as Pasteurella haemolytica, ‘Actinobacillus salpingitidis’ or Pasteurella anatis with proposal of Gallibacterium anatis gen. nov., comb. nov. and description of additional genomospecies within Gallibacterium gen. nov. International Journal of Systemic and Evolutionary Microbiology, 53: 275–287.
   PubMed Web of Science ®Google Scholar
• Christensen, N.H. & Saifuddin, M. (1989) A primary epidemic of inclusion body hepatitis in broilers. Avian Diseases, 33: 622–630. doi:10.2307/1591135
   PubMed Web of Science ®Google Scholar
• Clemmer, D.I. (1972) Age-associated changes in fecal excretion patterns of strain 93 chick embryo lethal orphan virus in chicks. Infection and Immunity, 5: 60–64.
   PubMed Web of Science ®Google Scholar
• Clemmer, D.L. (1965) Experimental enteric infection of chickens with an avian adeno-virus (strain 93). Proceedings of the Society for Experimental Biology and Medicine, 118: 943–948. doi:10.3181/00379727-118-30013
   PubMed Web of Science ®Google Scholar
• Cook, J.K. (1974a) Pathogenicity of avian adenoviruses for day-old chicks. Journal of Comparative Pathology, 84: 505–515. doi:10.1016/0021-9975(74)90043-7
   PubMed Web of Science ®Google Scholar
• Cook, J.K. (1974b) Spread of an avian adenovirus (CELO virus) to uninoculated fowls. Research in Veterinary Science, 16: 156–161.
   PubMed Web of Science ®Google Scholar
• Cook, J.K. (1983) Fowl adenoviruses: studies on aspects of the pathogenicity of six strains for 1-day-old chicks. Avian Pathology, 12: 35–43. doi:10.1080/03079458308436147
   PubMed Web of Science ®Google Scholar
• Cortes, P.L., Chin, R.P., Bland, M.C., Crespo, R. & Shivaprasad, H.L. (2004) Histomoniasis in the bursa of fabricius of chickens. Avian Diseases, 48: 711–715. doi:10.1637/7175-030404R
   PubMed Web of Science ®Google Scholar
• Cushman, S. (1893) The production of turkeys. Rhode Island Agricultural Experiment Station Bulletin, 25: 89–123.
   Google Scholar
• Dar, A., Gomis, S., Shirley, I., Mutwiri, G., Brownlie, R., Potter, A., Gerdts, V. & Tikoo, S.K. (2012) Pathotypic and molecular characterization of a fowl adenovirus associated with inclusion body hepatitis in Saskatchewan chickens. Avian Diseases, 56: 73–81. doi:10.1637/9764-041911-Reg.1
   PubMed Web of Science ®Google Scholar
• Daş, G., Abel, H., Humburg, J., Schwarz, A., Rautenschlein, S., Breves, G. & Gauly, M. (2011) Non-starch polysaccharides alter interactions between Heterakis gallinarum and Histomonas meleagridis. Veterinary Parasitology, 176: 208–216. doi:10.1016/j.vetpar.2010.11.004
   PubMed Web of Science ®Google Scholar
• Delappe, I.P. (1953) Studies on Histomonas meleagridis. I. Use of antibiotics to facilitate in vitro isolation. Experimental Parasitology, 2: 79–86. doi:10.1016/0014-4894(53)90006-X
   Web of Science ®Google Scholar
• Devolt, H.M. (1950) The different effect of artificially and naturally induced blackhead (infectious enterohepatitis) of turkeys on the prophylactic action of one quinoline derivative. Poultry Science, 29: 924–926. doi:10.3382/ps.0290924
   Web of Science ®Google Scholar
• Dolka, B., Żbikowski, A., Dolka, I. & Szeleszczuk, P. (2015) Histomonosis – an existing problem in chicken flocks in Poland. Veterinary Research Communications, 39: 189–195. doi:10.1007/s11259-015-9637-2
   PubMed Web of Science ®Google Scholar
• Doll, J.P. & Franker, C.K. (1963) Experimental histomoniasis in gnotobiotic turkeys. I. Infection and histopathology of the bacteria-free host. The Journal of Parasitology, 49: 411–414. doi:10.2307/3275809
   PubMed Web of Science ®Google Scholar
• Domanska-Blicharz, K., Tomczyk, G., Smietanka, K., Kozaczynski, W. & Minta, Z. (2011) Molecular characterization of fowl adenoviruses isolated from chickens with gizzard erosions. Poultry Science, 90: 983–989. doi:10.3382/ps.2010-01214
   PubMed Web of Science ®Google Scholar
• Dwyer, D.M. (1972) Analysis of the antigenic relationships among trichomonas, histomonas, dientamoeba, and entamoeba. I. Quantitative fluorescent antibody methods. The Journal of Protozoology, 19: 316–325. doi:10.1111/jeu.1972.19.issue-2
   PubMedGoogle Scholar
• Eregae, M.E., Dewey, C.E., Mcewen, S.A., Ouckama, R., Ojkić, D. & Guerin, M.T. (2014) Flock prevalence of exposure to avian adeno-associated virus, chicken anemia virus, fowl adenovirus, and infectious bursal disease virus among Ontario broiler chicken flocks. Avian Diseases, 58: 71–77. doi:10.1637/10612-071113-Reg.1
   PubMed Web of Science ®Google Scholar
• Erny, K.M., Barr, D.A. & Fahey, K.J. (1991) Molecular characterization of highly virulent fowl adenoviruses associated with outbreaks of inclusion body hepatitis. Avian Pathology, 20: 597–606. doi:10.1080/03079459108418799
   PubMed Web of Science ®Google Scholar
• Esquenet, C., De Herdt, P., De Bosschere, H., Ronsmans, S., Ducatelle, R. & Van Erum, J. (2003) An outbreak of histomoniasis in free-range layer hens. Avian Pathology, 32: 305–308. doi:10.1080/0307945031000097903
   PubMed Web of Science ®Google Scholar
• EFSA. (2012) EFSA recommends use of animal-based measures when assessing welfare. Veterinary Record, 170: 112. doi:10.1136/vr.e776
   PubMed Web of Science ®Google Scholar
• Eveleth, D.F. (1943) Histomoniasis in broilers. Veterinary Medicine, 38: 148–149.
   Google Scholar
• Fadly, A.M., Winterfield, R.W. & Olander, H.J. (1976) Role of the bursa of Fabricius in the pathogenicity of inclusion body hepatitis and infectious bursal disease viruses. Avian Diseases, 20: 467–477. doi:10.2307/1589379
   PubMed Web of Science ®Google Scholar
• Ganapathy, K., Salamat, M.H., Lee, C.C. & Johara, M.Y. (2000) Concurrent occurrence of salmonellosis, colibaccillosis and histomoniasis in a broiler flock fed with antibiotic-free commercial feed. Avian Pathology, 29: 639–642. doi:10.1080/03079450020016000
   PubMed Web of Science ®Google Scholar
• Ganas, P., Liebhart, D., Glösmann, M., Hess, C. & Hess, M. (2012) Escherichia coli strongly supports the growth of Histomonas meleagridis, in a monoxenic culture, without influence on its pathogenicity. International Journal for Parasitology, 42: 893–901. doi:10.1016/j.ijpara.2012.07.007
   PubMed Web of Science ®Google Scholar
• Ganesh, K. & Raghavan, R. (2000) Hydropericardium hepatitis syndrome of broiler poultry: current status of research. Research in Veterinary Science, 68: 201–206. doi:10.1053/rvsc.1999.0365
   PubMed Web of Science ®Google Scholar
• Gerbod, D., Edgcomb, V.P., Noel, C., Zenner, L., Wintjens, R., Delgado-Viscogliosi, P., Holder, M.E., Sogin, M.L. & Viscogliosi, E. (2001) Phylogenetic position of the trichomonad parasite of turkeys, Histomonas meleagridis (Smith) Tyzzer, inferred from small subunit rRNA sequence. The Journal of Eukaryotic Microbiology, 48: 498–504. doi:10.1111/jeu.2001.48.issue-4
   PubMed Web of Science ®Google Scholar
• Gerlach, H. (1977) Significance of Pasteurella haemotytica in poultry. Der Praktische Tierarzt, 58: 324–328.
   Google Scholar
• Gerth, C., Rudiger-Boesch, B., Schmidt, U., Mumme, J. & Friedhoff, K.T. (1985) [Histomoniasis in pullet stock and its effect on later laying performance]. Tierärztliche Praxis, 13: 519–527.
   PubMedGoogle Scholar
• Gjevre, A.-G., Kaldhusdal, M. & Eriksen, G.S. (2013) Gizzard erosion and ulceration syndrome in chickens and turkeys: a review of causal or predisposing factors. Avian Pathology, 42: 297–303. doi:10.1080/03079457.2013.817665
   PubMed Web of Science ®Google Scholar
• Goedbloed, E. & Bool, P.H. (1962) The protozoan etiology of blackhead. Avian Diseases, 6: 302–315. doi:10.2307/1587900
   Web of Science ®Google Scholar
• Gomis, S., Goodhope, A.R., Ojkic, A.D. & Willson, P. (2006) Inclusion body hepatitis as a primary disease in broilers in Saskatchewan, Canada. Avian Diseases, 50: 550–555. doi:10.1637/7577-040106R.1
   PubMed Web of Science ®Google Scholar
• Goodwin, M.A., Hill, D.L., Dekich, M.A. & Putnam, M.R. (1993) Multisystemic adenovirus infection in broiler chicks with hypoglycemia and spiking mortality. Avian Diseases, 37: 625–627. doi:10.2307/1591701
   PubMed Web of Science ®Google Scholar
• Gordon, R.F. (1967) The economic effect of disease on the poultry industry. Veterinary Record, 80: 101–107. doi:10.1136/vr.80.3.101
   PubMed Web of Science ®Google Scholar
• Gordon, R.F. (1971) The economic effect of ill health. Veterinary Record, 89: 496–500. doi:10.1136/vr.89.19.496
   PubMed Web of Science ®Google Scholar
• Gordon, R.F. (1973) Houghton poultry research station. Nutrition & Food Science, 73: 15–18. doi:10.1108/eb058561
   Google Scholar
• Gradmann, C. (2014) A spirit of scientific rigour: Koch’s postulates in twentieth-century medicine. Microbes and Infection, 16: 885–892. doi:10.1016/j.micinf.2014.08.012
   PubMed Web of Science ®Google Scholar
• Grafl, B., Aigner, F., Liebhart, D., Marek, A., Prokofieva, I., Bachmeier, J. & Hess, M. (2012) Vertical transmission and clinical signs in broiler breeders and broilers experiencing adenoviral gizzard erosion. Avian Pathology, 41: 599–604. doi:10.1080/03079457.2012.740614
   PubMed Web of Science ®Google Scholar
• Grafl, B., Liebhart, D., Günes, A., Wernsdorf, P., Aigner, F., Bachmeier, J. & Hess, M. (2013) Quantity of virulent fowl adenovirus serotype 1 correlates with clinical signs, macroscopical and pathohistological lesions in gizzards following experimental induction of gizzard erosion in broilers. Veterinary Research, 44: 38. doi:10.1186/1297-9716-44-38
   PubMed Web of Science ®Google Scholar
• Grafl, B., Liebhart, D., Windisch, M., Ibesich, C. & Hess, M. (2011) Seroprevalence of Histomonas meleagridis in pullets and laying hens determined by ELISA. Veterinary Record, 168: 160–164. doi:10.1136/vr.c6479
   PubMed Web of Science ®Google Scholar
• Grafl, B., Prokofieva, I., Wernsdorf, P., Steinborn, R. & Hess, M. (2014) Infection with an apathogenic fowl adenovirus serotype-1 strain (CELO) prevents adenoviral gizzard erosion in broilers. Veterinary Microbiology, 172: 177–185. doi:10.1016/j.vetmic.2014.05.020
   PubMed Web of Science ®Google Scholar
• Graybill, H.W. & Smith, T. (1920) Production of fatal blackhead in turkeys by feeding embryonated eggs of Heterakis papillosa. Journal of Experimental Medicine, 31: 647–655. doi:10.1084/jem.31.5.647
   PubMedGoogle Scholar
• Greenham, L.W. & Hill, T.J. (1962) Observation on an avian strain of Pasteurella haemolytica. Veterinary Record, 74: 861–863.
   Google Scholar
• Grgic, H., Philippe, C., Ojkic, D. & Nagy, E. (2006) Study of vertical transmission of fowl adenoviruses. Canadian Journal of Veterinary Research, 70: 230–233.
   PubMed Web of Science ®Google Scholar
• Grimes, T.M., King, D.J., Kleven, S.H. & Fletcher, O.J. (1977) Involvement of a type-8 avian adenovirus in the etiology of inclusion body hepatitis. Avian Diseases, 21: 26–38. doi:10.2307/1589361
   PubMed Web of Science ®Google Scholar
• Hacking, W.C. & Pettit, J.R. (1974) Pasteurella hemolytica in pullets and laying hens. Avian Diseases, 18: 483–486. doi:10.2307/1589119
   PubMed Web of Science ®Google Scholar
• Hafez, H.M. (2001) Aktuelle Gefügelkrankheiten bei Legehennen im Zusammenhang mit alternativen Haltungssystemen. Tierärztliche Praxis, 29: 168–174.
   Google Scholar
• Harbourne, J.F. (1962) A haemolytic cocco-bacillus recovered from poultry. Veterinary Record, 74: 566–577.
   Google Scholar
• Harrach, B., Benkö, M., Both, G.W., Brown, M., Davison, A.J., Echavarria, M., Hess, M., Jones, M.S., Kajon, A., Lehmkuhl, H.D., Mautner, V., Mittal, S.K. & Wadell, G. (2011) Family adenoviridae, in: King, A.M.Q., Adams, M.J., Carstens, E.B. & Lefkowitz, E.J. (Eds) Virus taxonomy: classification and nomenclature of viruses. Ninth report of the international committee on taxonomy of viruses, pp. 95–111 (San Diego, CA, Elsevier).
   Google Scholar
• Harry, E.G. (1962) A haemolytic coccobacillus recovered from poultry. Veterinary Record, 74: 640.
   Google Scholar
• Hauck, R., Balczulat, S. & Hafez, H.M. (2010) Detection of DNA of Histomonas meleagridis and Tetratrichomonas gallinarum in German poultry flocks between 2004 and 2008. Avian Diseases, 54: 1021–1025. doi:10.1637/9261-012910-Reg.1
   PubMed Web of Science ®Google Scholar
• Hauck, R. & Hafez, H.M. (2013) Experimental infections with the protozoan parasite Histomonas meleagridis: a review. Parasitology Research, 112: 19–34. doi:10.1007/s00436-012-3190-5
   PubMed Web of Science ®Google Scholar
• Helmboldt, C.F. & Frazier, M.N. (1963) Avian hepatic inclusion bodies of unknown significance. Avian Diseases, 7: 446–450. doi:10.2307/1587881
   PubMed Web of Science ®Google Scholar
• Hess, M. (2000) Detection and differentiation of avian adenoviruses: a review. Avian Pathology, 29: 195–206. doi:10.1080/03079450050045440
   PubMed Web of Science ®Google Scholar
• Hess, M. (2013) Aviadenovirus infections, in: Glisson, J.R., McDougald, L.R., Nolan, L.K., Suarez, D.L., Swayne, D. & Nair, V. (Eds) Diseases of poultry, 13th edn., pp. 290–300 (Ames, Wiley-Blackwell). ISBN:978-0-470-95899-5.
   Google Scholar
• Hess, M., Blöcker, H. & Brandt, P. (1997) The complete nucleotide sequence of the egg drop syndrome virus: an intermediate between mastadenoviruses and aviadenoviruses. Virology, 238: 145–156. doi:10.1006/viro.1997.8815
   PubMed Web of Science ®Google Scholar
• Hess, M., Grabensteiner, E. & Liebhart, D. (2006) Rapid transmission of the protozoan parasite Histomonas meleagridis in turkeys and specific pathogen free chickens following cloacal infection with a mono-eukaryotic culture. Avian Pathology, 35: 280–285. doi:10.1080/03079450600815507
   PubMed Web of Science ®Google Scholar
• Hess, M., Liebhart, D., Bilic, I. & Ganas, P. (2015) Histomonas meleagridis–new insights into an old pathogen. Veterinary Parasitology, 208: 67–76. doi:10.1016/j.vetpar.2014.12.018
   PubMed Web of Science ®Google Scholar
• Hess, M., Raue, R. & Prusas, C. (1999) Epidemiological studies on fowl adenoviruses isolated from cases of infectious hydropericardium. Avian Pathology, 28: 433–439. doi:10.1080/03079459994443
   PubMed Web of Science ®Google Scholar
• Homer, B.L. & Butcher, G.D. (1991) Histomoniasis in Leghorn pullets on a Florida farm. Avian Diseases, 35: 621–624. doi:10.2307/1591231
   PubMed Web of Science ®Google Scholar
• Horton-Smith, C. & Long, P.L. (1956) Studies in histomoniasis 1. The infection of chickens (Gallus gallus) with histomonad suspensions. Parasitology, 46: 79–90.
   PubMed Web of Science ®Google Scholar
• Jones, H.G. & Owen, D.M. (1981) Reproductive tract lesions of the laying fowl with particular reference to bacterial infection. Veterinary Record, 108: 36–37. doi:10.1136/vr.108.2.36
   PubMed Web of Science ®Google Scholar
• Jones, K.H., Thornton, J.K., Zhang, Y. & Mauel, M.J. (2013) A 5-year retrospective report of Gallibacterium anatis and Pasteurella multocida isolates from chickens in Mississippi. Poultry Science, 92: 3166–3171. doi:10.3382/ps.2013-03321
   PubMed Web of Science ®Google Scholar
• Jung, A. (2012) Hepatitis bei Legehennen, verursacht durch gleichzeitige Infektion mit Gallibacterium anatis und Ascaridia galli – Fallbericht. Praktischer Tierarzt, 93: 246–250.
   Google Scholar
• Kaján, G.L., Kecskeméti, S., Harrach, B. & Benkő, M. (2013) Molecular typing of fowl adenoviruses, isolated in Hungary recently, reveals high diversity. Veterinary Microbiology, 167: 357–363. doi:10.1016/j.vetmic.2013.09.025
   PubMed Web of Science ®Google Scholar
• Kaufmann-Bart, M. & Hoop, R.K. (2009) Diseases in chicks and laying hens during the first 12 years after battery cages were banned in Switzerland. Veterinary Record, 164: 203–207. doi:10.1136/vr.164.7.203
   PubMed Web of Science ®Google Scholar
• Kim, J.N., Byun, S.H., Kim, M.J., Kim, J., Sung, H.W. & Mo, I.P. (2008) Outbreaks of hydropericardium syndrome and molecular characterization of Korean fowl adenoviral isolates. Avian Diseases, 52: 526–530. doi:10.1637/8178-112207-Case
   PubMed Web of Science ®Google Scholar
• Kjos-Hanssen, B. (1950) Egg peritonitis in hens caused by pathogenic “cloacal bacteria”. Nordisk Veterinaermedicin, 2: 523–531.
   Google Scholar
• Lesser, E. (1961) In vitro cultivation of Histomonas meleagridis free of demonstrable bacteria. The Journal of Protozoology, 8: 228–230. doi:10.1111/jeu.1961.8.issue-2
   Google Scholar
• Liebhart, D., Ganas, P., Sulejmanovic, T. & Hess, M. (2016) Histomonosis in poultry: previous and current strategies for prevention and therapy. Avian Pathology, 1–43. in press. doi:10.1080/03079457.2016.1229458
   PubMed Web of Science ®Google Scholar
• Lim, T.-H., Lee, H.-J., Lee, D.-H., Lee, Y.-N., Park, J.-K., Youn, H.-N., Kim, M.-S., Youn, H.-S., Lee, J.-B., Park, S.-Y., Choi, I.-S. & Song, C.-S. (2011) Identification and virulence characterization of fowl adenoviruses in Korea. Avian Diseases, 55: 554–560. doi:10.1637/9730-032011-Reg.1
   PubMed Web of Science ®Google Scholar
• Lund, E.E. (1958) Growth and development of Heterakis gallinae in turkeys and chickens infected with Histomonas meleagridis. The Journal of Parasitology, 44: 297–301. doi:10.2307/3274594
   PubMed Web of Science ®Google Scholar
• Lund, E.E. (1969) Histomoniasis. Advances in Veterinary Science and Comparative Medicine, 13: 355–390.
   PubMedGoogle Scholar
• Lund, E.E., Augustine, P.C. & Ellis, D.J. (1966) Immunizing action of in vitro-attenuated Histomonas meleagridis in chickens and turkeys. Experimental Parasitology, 18: 403–407. doi:10.1016/0014-4894(66)90041-5
   PubMed Web of Science ®Google Scholar
• Maartens, L.H., Joubert, H.W., Aitchison, H. & Venter, E.H. (2015) Inclusion body hepatitis associated with an outbreak of fowl adenovirus type 2 and type 8b in broiler flocks in South Africa. Journal of the South African Veterinary Association, 85: e1–e5.
   Google Scholar
• Matos, M., Grafl, B., Liebhart, D. & Hess, M. (2016a) The outcome of experimentally induced inclusion body hepatitis (IBH) by fowl aviadenoviruses (FAdVs) is crucially influenced by the genetic background of the host. Veterinary Research, 47: 69. doi:10.1186/s13567-016-0350-0
   PubMed Web of Science ®Google Scholar
• Matos, M., Grafl, B., Liebhart, D., Schwendenwein, I. & Hess, M. (2016b) Selected clinical chemistry analytes correlate with the pathogenesis of inclusion body hepatitis (IBH) experimentally induced by fowl aviadenoviruses (FAdVs). Avian Pathology, 45: 1–32.
   PubMed Web of Science ®Google Scholar
• Matthes, S., Löliger, H.-C. & Schubert, H.J. (1969) Enzootisches Auftreten der Pasteurella haemolytica beim Huhn. Deutsche Tierärztliche Wochenschrift, 89: 98–102.
   Google Scholar
• Mazaheri, A., Prusas, C., Voß, M. & Hess, M. (1998) Some strains of serotype 4 fowl adenoviruses cause inclusion body hepatitis and hydropericardium syndrome in chickens. Avian Pathology, 27: 269–276. doi:10.1080/03079459808419335
   PubMed Web of Science ®Google Scholar
• Mcdougald, L.R. (2005) Blackhead disease (histomoniasis) in poultry: a critical review. Avian Diseases, 49: 462–476. doi:10.1637/7420-081005R.1
   PubMed Web of Science ®Google Scholar
• Mcferran, J.B. & Adair, B.M. (1977) Avian adenoviruses – a review. Avian Pathology, 6: 189–217. doi:10.1080/03079457708418228
   PubMedGoogle Scholar
• Mendelson, C., Nothelfer, H.B. & Monreal, G. (1995) Identification and characterization of an avian adenovirus isolated from a ‘spiking mortality syndrome’ field outbreak in broilers on the Delmarva Peninsula, USA. Avian Pathology, 24: 693–706. doi:10.1080/03079459508419108
   PubMed Web of Science ®Google Scholar
• Mirle, C., Schöngarth, M., Meinhart, H. & Olm, U. (1991) Untersuchungen zu Auftreten und Bedeutung von Pasteurella haemolytica-Infektionen bei Hennen unter besonderer Berücksichtigung von Erkrankungen des Legeapparates. Monatshefte Veterinärmedizin, 46: 545–549.
   Google Scholar
• Mittal, D., Jindal, N., Tiwari, A.K. & Khokhar, R.S. (2014) Characterization of fowl adenoviruses associated with hydropericardium syndrome and inclusion body hepatitis in broiler chickens. Virusdisease, 25: 114–119. doi:10.1007/s13337-013-0183-7
   PubMedGoogle Scholar
• Müller, H. (1990) Enzootische Typhlohepatitis bei intensiv gehaltenen Junghennen. Monatshefte Veterinärmedizin, 45: 464–467.
   Google Scholar
• Mushin, R., Weisman, Y. & Singer, N. (1980) Pasteurella haemolytica found in the respiratory tract of fowl. Avian Diseases, 24: 162–168. doi:10.2307/1589775
   Web of Science ®Google Scholar
• Naeem, K. & Akram, H.S. (1995) Hydropericardium syndrome outbreak in a pigeon flock. Veterinary Record, 136: 296–297. doi:10.1136/vr.136.12.296
   PubMed Web of Science ®Google Scholar
• Nakamura, K., Mase, M., Yamaguchi, S., Shibahara, T. & Yuasa, N. (1999) Pathologic study of specific-pathogen-free chicks and hens inoculated with adenovirus isolated from hydropericardium syndrome. Avian Diseases, 43: 414–423. doi:10.2307/1592638
   PubMed Web of Science ®Google Scholar
• Nakamura, K., Mase, M., Yamaguchi, S. & Yuasa, N. (2000) Induction of hydropericardium in one-day-old specific-pathogen-free chicks by adenoviruses from inclusion body hepatitis. Avian Diseases, 44: 192–196. doi:10.2307/1592524
   PubMed Web of Science ®Google Scholar
• 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 Diseases, 55: 719–723. doi:10.1637/9813-052511-Case.1
   PubMed Web of Science ®Google Scholar
• Nakamura, K., Ohyama, T., Yamada, M., Abe, T., Tanaka, H. & Mase, M. (2002) Experimental gizzard erosions in specific-pathogen-free chicks by serotype 1 group I avian adenoviruses from broilers. Avian Diseases, 46: 893–900. doi:10.1637/0005-2086(2002)046[0893:EGEISP]2.0.CO;2
   PubMed Web of Science ®Google Scholar
• Nakamura, K., Shoyama, T., Mase, M., Imada, T. & Yamada, M. (2003) Reproduction of hydropericardium syndrome in three-week-old cyclophosphamide-treated specific-pathogen-free chickens by adenoviruses from inclusion body hepatitis. Avian Diseases, 47: 169–174. doi:10.1637/0005-2086(2003)047[0169:ROHSIT]2.0.CO;2
   PubMed Web of Science ®Google Scholar
• Neubauer, C., De Souza-Pilz, M., Bojesen, A.M., Bisgaard, M. & Hess, M. (2009) Tissue distribution of haemolytic Gallibacterium anatis isolates in laying birds with reproductive disorders. Avian Pathology, 38: 1–7. doi:10.1080/03079450802577848
   PubMed Web of Science ®Google Scholar
• Nguyen, D.T., Bilic, I., Jaskulska, B., Hess, M., Le, D.Q., Le Hua, L.N., Huynh, V.V., Nguyen, S.T. & Vu-Khac, H. (2015) Prevalence and genetic characterization of Histomonas meleagridis in chickens in Vietnam. Avian Diseases, 59: 309–314. doi:10.1637/10964-102414-Reg
   PubMed Web of Science ®Google Scholar
• Niczyporuk, J.S. (2016) Phylogenetic and geographic analysis of fowl adenovirus field strains isolated from poultry in Poland. Archives of Virology, 161: 33–42. doi:10.1007/s00705-015-2635-4
   PubMed Web of Science ®Google Scholar
• Ojkic, D., Krell, P.J., Tuboly, T. & Nagy, E. (2008a) Characterization of fowl adenoviruses isolated in Ontario and Quebec, Canada. Canadian Journal of Veterinary Research, 72: 236–241.
   PubMed Web of Science ®Google Scholar
• Ojkic, D., Martin, E., Swinton, J., Vaillancourt, J.-P., Boulianne, M. & Gomis, S. (2008b) Genotyping of Canadian isolates of fowl adenoviruses. Avian Pathology, 37: 95–100. doi:10.1080/03079450701805324
   PubMed Web of Science ®Google Scholar
• Okuda, Y., Ono, M., Shibata, I. & Sato, S. (2004) Pathogenicity of serotype 8 fowl adenovirus isolated from gizzard erosions of slaughtered broiler chickens. Journal of Veterinary Medical Science, 66: 1561–1566. doi:10.1292/jvms.66.1561
   PubMed Web of Science ®Google Scholar
• Okuda, Y., Ono, M., Yazawa, S., Imai, Y., Shibata, I. & Sato, S. (2001a) Pathogenicity of serotype 1 fowl adenovirus in commercial broiler chickens. Avian Diseases, 45: 819–827. doi:10.2307/1592862
   PubMed Web of Science ®Google Scholar
• Okuda, Y., Ono, M., Yazawa, S., Shibata, I. & Sato, S. (2001b) Experimental infection of specific-pathogen-free chickens with serotype-1 fowl adenovirus isolated from a broiler chicken with gizzard erosions. Avian Diseases, 45: 19–25. doi:10.2307/1593007
   PubMed Web of Science ®Google Scholar
• Olsen, R.H., Stockholm, N.M., Permin, A., Christensen, J.P., Christensen, H. & Bisgaard, M. (2011) Multi-locus sequence typing and plasmid profile characterization of avian pathogenic Escherichia coli associated with increased mortality in free-range layer flocks. Avian Pathology, 40: 437–444. doi:10.1080/03079457.2011.592822
   PubMed Web of Science ®Google Scholar
• Ono, M., Okuda, Y., Shibata, I., Sato, S. & Okada, K. (2004) Pathogenicity by parenteral injection of fowl adenovirus isolated from gizzard erosion and resistance to reinfection in adenoviral gizzard erosion in chickens. Veterinary Pathology, 41: 483–489. doi:10.1354/vp.41-5-483
   PubMed Web of Science ®Google Scholar
• Ono, M., Okuda, Y., Shibata, I., Sato, S. & Okada, K. (2007) Reproduction of adenoviral gizzard erosion by the horizontal transmission of fowl adenovirus serotype 1. Journal of Veterinary Medical Science, 69: 1005–1008. doi:10.1292/jvms.69.1005
   PubMed Web of Science ®Google Scholar
• Ono, M., Okuda, Y., Yazawa, S., Shibata, I., Sato, S. & Okada, K. (2003) Outbreaks of adenoviral gizzard erosion in slaughtered broiler chickens in Japan. Veterinary Record, 153: 775–779.
   PubMed Web of Science ®Google Scholar
• Ono, M., Okuda, Y., Yazawa, S., Shibata, I., Tanimura, N., Kimura, K., Haritani, M., Mase, M. & Sato, S. (2001) Epizootic outbreaks of gizzard erosion associated with adenovirus infection in chickens. Avian Diseases, 45: 268–275. doi:10.2307/1593040
   PubMed Web of Science ®Google Scholar
• Pallister, J., Wright, P.J. & Sheppard, M. (1996) A single gene encoding the fiber is responsible for variations in virulence in the fowl adenoviruses. Journal of Virology, 70: 5115–5122.
   PubMed Web of Science ®Google Scholar
• Paudel, S., Alispahic, M., Liebhart, D., Hess, M. & Hess, C. (2013) Assessing pathogenicity of Gallibacterium anatis in a natural infection model: the respiratory and reproductive tracts of chickens are targets for bacterial colonization. Avian Pathology, 42: 527–535. doi:10.1080/03079457.2013.843160
   PubMed Web of Science ®Google Scholar
• Paudel, S., Hess, C., Wernsdorf, P., Käser, T., Meitz, S., Jensen-Jarolim, E., Hess, M. & Liebhart, D. (2015) The systemic multiplication of Gallibacterium anatis in experimentally infected chickens is promoted by immunosuppressive drugs which have a less specific effect on the depletion of leukocytes. Veterinary Immunology and Immunopathology, 166: 22–32. doi:10.1016/j.vetimm.2015.05.001
   PubMed Web of Science ®Google Scholar
• Paudel, S., Liebhart, D., Aurich, C., Hess, M. & Hess, C. (2014a) Pathogenesis of Gallibacterium anatis in a natural infection model fulfils Koch’s postulates: 2. Epididymitis and decreased semen quality are the predominant effects in specific pathogen free cockerels. Avian Pathology, 43: 529–534. doi:10.1080/03079457.2014.967176
   PubMed Web of Science ®Google Scholar
• Paudel, S., Liebhart, D., Hess, M. & Hess, C. (2014b) Pathogenesis of Gallibacterium anatis in a natural infection model fulfils Koch’s postulates: 1. Folliculitis and drop in egg production are the predominant effects in specific pathogen free layers. Avian Pathology, 43: 443–449. doi:10.1080/03079457.2014.955782
   PubMed Web of Science ®Google Scholar
• Pedersen, I.J., Pors, S.E., Bager Skjerning, R.J., Nielsen, S.S. & Bojesen, A.M. (2015) Immunogenic and protective efficacy of recombinant protein GtxA-N against Gallibacterium anatis challenge in chickens. Avian Pathology, 44: 386–391. doi:10.1080/03079457.2015.1069259
   PubMed Web of Science ®Google Scholar
• Persson, G. & Bojesen, A.M. (2015) Bacterial determinants of importance in the virulence of Gallibacterium anatis in poultry. Veterinary Research, 46: 57. doi:10.1186/s13567-015-0206-z
   PubMed Web of Science ®Google Scholar
• Pettit, J.R. & Carlson, H.C. (1972) Inclusion-body hepatitis in broiler chickens. Avian Diseases, 16: 858–863. doi:10.2307/1588767
   PubMed Web of Science ®Google Scholar
• Popp, C., Hauck, R., Balczulat, S. & Hafez, H.M. (2011) Recurring histomonosis on an organic farm. Avian Diseases, 55: 328–330. doi:10.1637/9596-110810-Case.1
   PubMed Web of Science ®Google Scholar
• Pors, S.E., Skjerning, R.B., Flachs, E.M. & Bojesen, A.M. (2016) Recombinant proteins from Gallibacterium anatis induces partial protection against heterologous challenge in egg-laying hens. Veterinary Research, 47: 36. doi:10.1186/s13567-016-0320-6
   PubMed Web of Science ®Google Scholar
• Reid, W.M. (1967) Etiology and dissemination of the blackhead disease syndrome in turkeys and chickens. Experimental Parasitology, 21: 249–275. doi:10.1016/0014-4894(67)90087-2
   PubMed Web of Science ®Google Scholar
• Saifuddin, M. & Wilks, C.R. (1991) Pathogenesis of an acute viral hepatitis: inclusion body hepatitis in the chicken. Archives of Virology, 116: 33–43. doi:10.1007/BF01319229
   PubMed Web of Science ®Google Scholar
• Saifuddin, M., Wilks, C.R. & Murray, A. (1992) Characterisation of avian adenoviruses associated with inclusion body hepatitis. Newzealand Veterinary Journal, 40: 52–55. doi:10.1080/00480169.1992.35697
   PubMed Web of Science ®Google Scholar
• Schachner, A., Marek, A., Grafl, B. & Hess, M. (2016) Detailed molecular analyses of the hexon loop-1 and fibers of fowl aviadenoviruses reveal new insights into the antigenic relationship and confirm that specific genotypes are involved in field outbreaks of inclusion body hepatitis. Veterinary Microbiology, 186: 13–20. doi:10.1016/j.vetmic.2016.02.008
   PubMed Web of Science ®Google Scholar
• Schonewille, E., Singh, A., Göbel, T.W., Gerner, W., Saalmüller, A. & Hess, M. (2008) Fowl adenovirus (FAdV) serotype 4 causes depletion of B and T cells in lymphoid organs in specific pathogen-free chickens following experimental infection. Veterinary Immunology and Immunopathology, 121: 130–139. doi:10.1016/j.vetimm.2007.09.017
   PubMed Web of Science ®Google Scholar
• Schulze, H.W. (1975) Über das Auftreten von Schwarzkopfkrankheit bei Legehennenaufzuchten in Norddeutschland. Der Praktische Tierarzt, 3: 164–168.
   Google Scholar
• Smith, T. (1895) An infectious disease among turkeys caused by protozoa (infectious entero-hepatitis). US Department of Agriculture, Bureau of Animal Industry Bulletin, 8: 1–38.
   Google Scholar
• Springer, W.T., Johnson, J. & Reid, W.M. (1970) Histomoniasis in gnotobiotic chickens and turkeys: biological aspects of the role of bacteria in the etiology. Experimental Parasitology, 28: 383–392. doi:10.1016/0014-4894(70)90106-2
   PubMed Web of Science ®Google Scholar
• Steer, P.A., O’rourke, D., Ghorashi, S.A. & Noormohammadi, A.H. (2011) Application of high-resolution melting curve analysis for typing of fowl adenoviruses in field cases of inclusion body hepatitis. Australian Veterinary Journal, 89: 184–192. doi:10.1111/j.1751-0813.2011.00695.x
   PubMed Web of Science ®Google Scholar
• Steer, P.A., Sandy, J.R., O’rourke, D., Scott, P.C., Browning, G.F. & Noormohammadi, A.H. (2015) Chronological analysis of gross and histological lesions induced by field strains of fowl adenovirus serotypes 1, 8b and 11 in one-day-old chickens. Avian Pathology, 44: 106–113. doi:10.1080/03079457.2015.1007919
   PubMed Web of Science ®Google Scholar
• Stokholm, N.M., Permin, A., Bisgaard, M. & Christensen, J.P. (2010) Causes of mortality in commercial organic layers in Denmark. Avian Diseases, 54: 1241–1250. doi:10.1637/9375-041910-Reg.1
   PubMed Web of Science ®Google Scholar
• Swayne, D., Glisson, J.R., Mcdougald, L.R., Nolan, L.K., Suarez, D.L. & Nair, V. (Eds). (2013) Diseases of poultry, 13th edn. (Ames, Wiley-Blackwell). ISBN:978-0-470-95899-5.
   Google Scholar
• Tanimura, N., Nakamura, K., Imai, K., Maeda, M., Gobo, T., Nitta, S., Ishihara, T. & Amano, H. (1993) Necrotizing pancreatitis and gizzard erosion associated with adenovirus infection in chickens. Avian Diseases, 37: 606–611. doi:10.2307/1591697
   PubMed Web of Science ®Google Scholar
• Toro, H., Gonzalez, O., Escobar, C., Cerda, L., Morales, M.A. & Gonzalez, C. (2001) Vertical induction of the inclusion body hepatitis/hydropericardium syndrome with fowl adenovirus and chicken anemia virus. Avian Diseases, 45: 215–222. doi:10.2307/1593031
   PubMed Web of Science ®Google Scholar
• Tyzzer, E.E. (1920) The flagellate character and reclassification of the parasite producing “blackhead” in turkeys-Histomonas (gen.nov.) meleagridis (Smith). The Journal of Parasitology, 6: 124–131. doi:10.2307/3271065
   Google Scholar
• Tyzzer, E.E. (1934) Studies on histomoniasis, or “Blackhead” infection, in the chicken and the turkey. Proceedings of the American Academy of Arts and Sciences, 69: 189–264. doi:10.2307/20023041
   Google Scholar
• Van Der Heijden, H.M. & Landman, W.J. (2011) High seroprevalence of Histomonas meleagridis in Dutch layer chickens. Avian Diseases, 55: 324–327. doi:10.1637/9609-120610-ResNote.1
   PubMed Web of Science ®Google Scholar
• Von Bülow, V., Rudolph, R. & Fuchs, B. (1986) [Sequelae of concomitant infection of chicks with adenovirus or reovirus and the agent of avian infectious anemia (CAA)]. Zentralblatt Veterinärmedizin B, 33: 717–726.
   PubMedGoogle Scholar
• Wilson, F.D., Wills, R.W., Senties-Cue, C.G., Maslin, W.R., Stayer, P.A. & Magee, D.L. (2010) High incidence of glomerulonephritis associated with inclusion body hepatitis in broiler chickens: routine histopathology and histomorphometric studies. Avian Diseases, 54: 975–980. doi:10.1637/9050-090709-Reg.1
   PubMed Web of Science ®Google Scholar
• Yates, V.J. & Fry, D.E. (1957) Observations on a chicken embryo lethal orphan (CELO) virus. American Journal of Veterinary Research, 18: 657–660.
   PubMed Web of Science ®Google Scholar
• Zepeda, V.A., Calderón-Apodaca, N.L., Paasch, M.L., Martín, P.G., Paredes, D.A., Ramírez-Apolinar, S. & Soriano-Vargas, E. (2010) Histopathologic findings in chickens experimentally infected with Gallibacterium anatis by nasal instillation. Avian Diseases, 54: 1306–1309. doi:10.1637/9423-061410-ResNote.1
   PubMed Web of Science ®Google Scholar
• Zhao, J., Zhong, Q., Zhao, Y., Hu, Y.-X., Zhang, G.-Z. & Devlin, J. (2015) Pathogenicity and complete genome characterization of fowl adenoviruses isolated from chickens associated with inclusion body hepatitis and hydropericardium syndrome in China. PLoS One, 10: e0133073. doi:10.1371/journal.pone.0133073
   PubMed Web of Science ®Google Scholar
• Zsak, L. & Kisary, J. (1981) Studies on egg drop syndrome (EDS) and chick embryo lethal orphan (CELO) avian adenovirus DNAs by restriction endonucleases. Journal of General Virology, 56: 87–95. doi:10.1099/0022-1317-56-1-87
   PubMed Web of Science ®Google Scholar