Skip to main content
Top
Published in: Archives of Virology 11/2018

Open Access 01-11-2018 | Original Article

A comparative pathogenicity analysis of two adenovirus strains, 1/A and 8a/E, isolated from poultry in Poland

Authors: Jowita Samanta Niczyporuk, Hanna Czekaj

Published in: Archives of Virology | Issue 11/2018

Login to get access

Abstract

Fowl adenoviruses (FAdVs) are the causative agents of multietiological syndromes and diseases in poultry flocks. During a routine diagnostic examination, two FAdVs strains were isolated. Molecular typing of these isolates based on the partial loop L1 HVR1-4 region of the hexon gene sequence revealed the presence of different FAdV isolates: 1/A-61/11z (GenBank accession number KX247012, APP94082), and 8a/E-6/12j (GenBank accession number: KP890032, ALB00550), and comparative genome analysis indicated small differences between these two viruses. The next step of the study was the estimation of the pathogenicity of these isolates in specific-pathogen-free (SPF) chickens. Chickens were divided into three groups, with 20 chickens per group infected intraperitoneally on the first day after hatching. Group I consisted of chickens infected with strain FAdV-1/A-61/11z, group II consisted of chickens infected with strain FAdV-8a/E-6/12j, and group III consisted of uninfected birds. Clinical signs observed in infected chickens included poor growth, apathy, prostration, ruffled feathers, crouching position, and huddling behavior. The mortality rate in chickens infected with FAdV-1/A-61/11z was 10% at 10 days postinfection (dpi), and no mortality was observed in chickens infected with the FAdV-8a-6/12j strain. The mean real-time PCR threshold cycle (Ct) value was 39.70%. The detection limit of these assays was 8 copies, with an efficiency of 91.03% and 95.17% and regression square (R2) values of 0.991 and 0.997, respectively, with a mean pathogen load of 4.8 × 106.0 copies/µl. The assays did not demonstrate cross-reactivity between types 1/A and 8a/E and non-targeted poultry viruses. Adenoviral DNA was detected in the liver, spleen, kidney, gizzard, intestine, bursa of Fabricius, and thymus of every examined dead and euthanized chicken from groups I and II between the third and fourth week postinfection. This is the first study conducted on the pathogenic and apathogenic strains FAdV-1/A and FAdV-8a/E, showing the presence of the virus in multiple tissues in chickens in Poland. This study revealed that it is very likely that the FAdV-1/A-61/11z strain is able to cause clinical inclusion body hepatitis (IBH) in chickens and that it is slightly more virulent than the FAdV-8a/E-6/12j strain, although both are primary pathogens of the disease.
Literature
1.
go back to reference Ballman M, Harrach B (2016) Detection and partial genetic characterisation of novel avi- and siadenoviruses in racing and fancy pigeons (Columba livia domestica). Acta Veta Hung 64:514–528CrossRef Ballman M, Harrach B (2016) Detection and partial genetic characterisation of novel avi- and siadenoviruses in racing and fancy pigeons (Columba livia domestica). Acta Veta Hung 64:514–528CrossRef
2.
go back to reference Carrie J, Markowski G, Miller MM, Schat KA (2002) Development of strain- specific real-time PCR and RT-PCR assays for quantitation of chicken anemia virus. J Virol Methods 101:135–147CrossRef Carrie J, Markowski G, Miller MM, Schat KA (2002) Development of strain- specific real-time PCR and RT-PCR assays for quantitation of chicken anemia virus. J Virol Methods 101:135–147CrossRef
3.
go back to reference Cook JK (1983) Fowl adenoviruses: studies on aspects of the pathogenicity of six strains for 1-day-old chicks. Avian Pathol 12:35–43CrossRefPubMed Cook JK (1983) Fowl adenoviruses: studies on aspects of the pathogenicity of six strains for 1-day-old chicks. Avian Pathol 12:35–43CrossRefPubMed
4.
go back to reference Choi KS, Kye SJ, Kim JY, Jeon WJ, Lee EK, Park KY (2012) Epidemiological investigation of outbreaks of fowl adenovirus infection in commercial chickens in Korea. Poult Sci 91:2502–2506CrossRefPubMed Choi KS, Kye SJ, Kim JY, Jeon WJ, Lee EK, Park KY (2012) Epidemiological investigation of outbreaks of fowl adenovirus infection in commercial chickens in Korea. Poult Sci 91:2502–2506CrossRefPubMed
5.
go back to reference Dar A, Gomis S, Shirle I, Mutwiri G, Brownlie R, Potter A, Gerdts V, Tikoo SK (2012) Pathotypic and molecular characterization of fowl adenovirus associated with inclusion body hepatitis in Saskatchewan chickens. Avian Dis 56:73–81CrossRefPubMed Dar A, Gomis S, Shirle I, Mutwiri G, Brownlie R, Potter A, Gerdts V, Tikoo SK (2012) Pathotypic and molecular characterization of fowl adenovirus associated with inclusion body hepatitis in Saskatchewan chickens. Avian Dis 56:73–81CrossRefPubMed
6.
go back to reference Fitzgerald SD (2008) Adenovirus infections. In: Saif YM, Fadly AM, Glisson JR, McDougald LR, Nolan LK, Swayne DE (eds) Diseases of poultry, 12th edn. Blackwell, Ames, pp 251–252 Fitzgerald SD (2008) Adenovirus infections. In: Saif YM, Fadly AM, Glisson JR, McDougald LR, Nolan LK, Swayne DE (eds) Diseases of poultry, 12th edn. Blackwell, Ames, pp 251–252
7.
go back to reference Ganesh K, Suryanarayana V, Raghavan R, Gowda S (2001) Nucleotide sequence of L1 and part of P1 of hexon gene of fowl adenovirus associated with hydropericardium hepatitis syndrome differs with the corresponding region of other fowl adenoviruses. Vet Microbiol 7:1–11CrossRef Ganesh K, Suryanarayana V, Raghavan R, Gowda S (2001) Nucleotide sequence of L1 and part of P1 of hexon gene of fowl adenovirus associated with hydropericardium hepatitis syndrome differs with the corresponding region of other fowl adenoviruses. Vet Microbiol 7:1–11CrossRef
8.
go back to reference Gjevre AG, Kaldhusdal M, Eriksen GS (2013) Gizzard erosion and ulceration syndrome in chickens and turkeys: a review of causal or predisposing factors. Avian Pathol 42:297–303CrossRefPubMed Gjevre AG, Kaldhusdal M, Eriksen GS (2013) Gizzard erosion and ulceration syndrome in chickens and turkeys: a review of causal or predisposing factors. Avian Pathol 42:297–303CrossRefPubMed
9.
go back to reference Günes A, Marek A, Grafl B, Berger E, Hess M (2012) Real-time PCR assay for universal detection and quantitation of all five species of fowl adenoviruses (FAdV-A to FAdV-E). J Virol Methods 183:147–153CrossRefPubMed Günes A, Marek A, Grafl B, Berger E, Hess M (2012) Real-time PCR assay for universal detection and quantitation of all five species of fowl adenoviruses (FAdV-A to FAdV-E). J Virol Methods 183:147–153CrossRefPubMed
10.
go back to reference Grafl B, Liebhart D, Gunes 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. Vet Res 38:1–8 Grafl B, Liebhart D, Gunes 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. Vet Res 38:1–8
11.
go back to reference Grgic H, Yang DH, Nagy E (2011) Pathogenicity and complete genome sequence of a fowl adenovirus serotype 8 isolate. Virus Res 156:91–97CrossRefPubMed Grgic H, Yang DH, Nagy E (2011) Pathogenicity and complete genome sequence of a fowl adenovirus serotype 8 isolate. Virus Res 156:91–97CrossRefPubMed
12.
go back to reference Harrach B (2008) Adenoviruses: General Features. In: Mahy BWJ, Van Regenmortel RMH (eds) Encyclopedia of virology (third edition). Academic Press of Elsevier, Oxford, pp 1–9 Harrach B (2008) Adenoviruses: General Features. In: Mahy BWJ, Van Regenmortel RMH (eds) Encyclopedia of virology (third edition). Academic Press of Elsevier, Oxford, pp 1–9
13.
go back to reference Harrach B, Kaján GL (2011) Aviadenovirus. Adenoviridae. In: Tidona CA, Darai G (eds) Springer index of viruses. Springer, New York, pp 13–28CrossRef Harrach B, Kaján GL (2011) Aviadenovirus. Adenoviridae. In: Tidona CA, Darai G (eds) Springer index of viruses. Springer, New York, pp 13–28CrossRef
14.
go back to reference Kajan GL, Kecskemeti S, Harrach B, Benko M (2013) Molecular typing of fowl adenoviruses, isolated in Hungary recently, reveals high diversity. Vet Microbiol 167:357–363CrossRefPubMed Kajan GL, Kecskemeti S, Harrach B, Benko M (2013) Molecular typing of fowl adenoviruses, isolated in Hungary recently, reveals high diversity. Vet Microbiol 167:357–363CrossRefPubMed
15.
go back to reference Kecskemeti S, Bistyak A, Matiz K, Rt Glavits, Kajan GL, Benko M (2012) Observations on gizzard ulcers caused by adenovirus in chickens. Magyar Allatorvosk Lapia 134:145–149 Kecskemeti S, Bistyak A, Matiz K, Rt Glavits, Kajan GL, Benko M (2012) Observations on gizzard ulcers caused by adenovirus in chickens. Magyar Allatorvosk Lapia 134:145–149
16.
go back to reference Lim TH, Kim BY, Kim MS, Jang JH, Lee DH, Kwon YK, Lee JB, Park SY, Choi IS, Song CS (2012) Outbreak of gizzard erosion associated with fowl adenovirus infection in Korea. Poultry Science Association Inc, Fayetteville Lim TH, Kim BY, Kim MS, Jang JH, Lee DH, Kwon YK, Lee JB, Park SY, Choi IS, Song CS (2012) Outbreak of gizzard erosion associated with fowl adenovirus infection in Korea. Poultry Science Association Inc, Fayetteville
17.
go back to reference Manarolla G, Pisoni G, Moroni P, Gallazzi D, Sironi G, Rampin T (2009) Adenoviral gizzard erosions in Italian chicken flocks. Vet Res 164:754–756 Manarolla G, Pisoni G, Moroni P, Gallazzi D, Sironi G, Rampin T (2009) Adenoviral gizzard erosions in Italian chicken flocks. Vet Res 164:754–756
18.
go back to reference Marek A, Nolte V, Schachner A, Berger E, Schlötterer C, Hess M (2012) Two fiber genes of nearly equal lengths are a common and distinctive feature of fowl adenovirus C members. Vet Microbiol 156:411–417CrossRefPubMed Marek A, Nolte V, Schachner A, Berger E, Schlötterer C, Hess M (2012) Two fiber genes of nearly equal lengths are a common and distinctive feature of fowl adenovirus C members. Vet Microbiol 156:411–417CrossRefPubMed
19.
go back to reference Marek A, Schulz E, Hess C, Hess M (2010) Comparison of the fibers of Fowl adenovirus A serotype 1 isolates from chickens with gizzard erosions in Europe and apathogenic reference strains. J Vet Diagn Investig 22:937–941CrossRef Marek A, Schulz E, Hess C, Hess M (2010) Comparison of the fibers of Fowl adenovirus A serotype 1 isolates from chickens with gizzard erosions in Europe and apathogenic reference strains. J Vet Diagn Investig 22:937–941CrossRef
20.
go back to reference Marek A, Kaján GL, Kosiol C, Harrach B, Schlötterer C, Hess M (2014) Complete genome sequences of pigeon adenovirus 1 and duck adenovirus 2 extend the number of species within the genus Aviadenovirus. Virology 463:107–114CrossRef Marek A, Kaján GL, Kosiol C, Harrach B, Schlötterer C, Hess M (2014) Complete genome sequences of pigeon adenovirus 1 and duck adenovirus 2 extend the number of species within the genus Aviadenovirus. Virology 463:107–114CrossRef
21.
go back to reference Mase M, Nakamura K, Minami F (2012) Fowl adenoviruses isolated from chickens with inclusion body hepatitis in Japan, 2009–2010. J Vet Med Sci 74:1087–1089CrossRefPubMed Mase M, Nakamura K, Minami F (2012) Fowl adenoviruses isolated from chickens with inclusion body hepatitis in Japan, 2009–2010. J Vet Med Sci 74:1087–1089CrossRefPubMed
22.
go back to reference Matczuk AK, Niczyporuk JS, Kuczkowski M, Woźniakowski G, Nowak M, Wieliczko A (2017) Whole genome sequencing of fowl aviadenovirus A—a causative agent of gizzard erosion and ulceration, in adult laying hens. Infect Genet Evol 48:47CrossRefPubMed Matczuk AK, Niczyporuk JS, Kuczkowski M, Woźniakowski G, Nowak M, Wieliczko A (2017) Whole genome sequencing of fowl aviadenovirus A—a causative agent of gizzard erosion and ulceration, in adult laying hens. Infect Genet Evol 48:47CrossRefPubMed
23.
go back to reference McConnell BA, Fitzgerald AS (2008) Group I adenovirus infections. In: Saif YM (ed) Diseases of poultry, 12th edn. Blackwell/Iowa State Press, Ames, pp 252–266 McConnell BA, Fitzgerald AS (2008) Group I adenovirus infections. In: Saif YM (ed) Diseases of poultry, 12th edn. Blackwell/Iowa State Press, Ames, pp 252–266
24.
go back to reference McFerran JB, Adair BM (2008) Group I Adenovirus Infections. In: Saif YM, Barnes HJ, Glisson JR (eds) Diseases of poultry, 12th edn. Blackwell, Ames, pp 214–227 McFerran JB, Adair BM (2008) Group I Adenovirus Infections. In: Saif YM, Barnes HJ, Glisson JR (eds) Diseases of poultry, 12th edn. Blackwell, Ames, pp 214–227
26.
go back to reference Meulemans G, Couvreur B, Decaesstecker M, Boschmans M, Van den Berg TP (2004) Phylogenetic analysis of fowl adenoviruses. Avian Pathol 33:164–170CrossRefPubMed Meulemans G, Couvreur B, Decaesstecker M, Boschmans M, Van den Berg TP (2004) Phylogenetic analysis of fowl adenoviruses. Avian Pathol 33:164–170CrossRefPubMed
27.
go back to reference Mittal D, Jindal N, Tiwari AK, Khokhar RS (2014) Characterization of fowl adenoviruses associated with hydropericardium syndrome and inclusion body hepatitis in broiler chickens. Virus Dis 25:114–119CrossRef Mittal D, Jindal N, Tiwari AK, Khokhar RS (2014) Characterization of fowl adenoviruses associated with hydropericardium syndrome and inclusion body hepatitis in broiler chickens. Virus Dis 25:114–119CrossRef
28.
go back to reference Niczyporuk JS (2014) Molecular characteristic on occurrence of fowl adenovirus field strains and effect of efficiency on prophylactic vaccinations against Marek’s disease. Doctoral dissertation, National Veterinary Research Institute, Pulawy, pp 1–148 Niczyporuk JS (2014) Molecular characteristic on occurrence of fowl adenovirus field strains and effect of efficiency on prophylactic vaccinations against Marek’s disease. Doctoral dissertation, National Veterinary Research Institute, Pulawy, pp 1–148
29.
go back to reference Niczyporuk JS (2016) Phylogenetic and geographic analysis of fowl adenovirus field strains isolated from poultry in Poland. Arch Virol 1:32–42 Niczyporuk JS (2016) Phylogenetic and geographic analysis of fowl adenovirus field strains isolated from poultry in Poland. Arch Virol 1:32–42
30.
go back to reference Okuda Y, Ono M, Shibata I, Sato S, Akashi H (2006) Comparison of the polymerase chain reaction restriction fragment length polymorphism pattern of the fiber gene and pathogenicity of serotype-1 fowl adenovirus isolates from gizzard erosions and room feces of clinically healthy chickens in Japan. J Vet Diagn Investig 18:162–167CrossRef Okuda Y, Ono M, Shibata I, Sato S, Akashi H (2006) Comparison of the polymerase chain reaction restriction fragment length polymorphism pattern of the fiber gene and pathogenicity of serotype-1 fowl adenovirus isolates from gizzard erosions and room feces of clinically healthy chickens in Japan. J Vet Diagn Investig 18:162–167CrossRef
31.
go back to reference Okuda Y, Ono M, Shibata I, Sato S (2004) Pathogenicity of serotype 8 fowl adenovirus isolated from gizzard erosions of slaughtered broiler chickens. J Vet Med Sci 66:1561–1566CrossRefPubMed Okuda Y, Ono M, Shibata I, Sato S (2004) Pathogenicity of serotype 8 fowl adenovirus isolated from gizzard erosions of slaughtered broiler chickens. J Vet Med Sci 66:1561–1566CrossRefPubMed
32.
go back to reference Ono M, Okuda Y, Yazawa S, Shibata I, Tanimura N, Kimura K, Haritani M, Mase M, Sato S (2001) Epizotic outbreaks of gizzard erosion associated with adenovirus infection in chickens. Avian Dis 45:268–275CrossRefPubMed Ono M, Okuda Y, Yazawa S, Shibata I, Tanimura N, Kimura K, Haritani M, Mase M, Sato S (2001) Epizotic outbreaks of gizzard erosion associated with adenovirus infection in chickens. Avian Dis 45:268–275CrossRefPubMed
33.
go back to reference Pallister J, Wright PJ, Sheppard M (1996) A single gene encoding the fiber is responsible for variations in virulence in the fowl adenoviruses. J Virol 70:5115–5122PubMedPubMedCentral Pallister J, Wright PJ, Sheppard M (1996) A single gene encoding the fiber is responsible for variations in virulence in the fowl adenoviruses. J Virol 70:5115–5122PubMedPubMedCentral
34.
go back to reference Reed L, Muench JH (1938) A simple method of estimating fifty per cent endpoinds. Am J Epidemiol 27:493–497CrossRef Reed L, Muench JH (1938) A simple method of estimating fifty per cent endpoinds. Am J Epidemiol 27:493–497CrossRef
35.
go back to reference Schonewille E, Singh A, Gobel TW, Gerner W, Saalmuller 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. Vet Immunol Immunopathol 121:130–139CrossRefPubMed Schonewille E, Singh A, Gobel TW, Gerner W, Saalmuller 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. Vet Immunol Immunopathol 121:130–139CrossRefPubMed
36.
go back to reference Steer PA, Sandy JR, O’Rourke D, Scott PC, Browning GF, Noormohammadi AH (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 Pathol 44:106–113CrossRefPubMed Steer PA, Sandy JR, O’Rourke D, Scott PC, Browning GF, Noormohammadi AH (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 Pathol 44:106–113CrossRefPubMed
37.
go back to reference Steer PA, Rourke DO, 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 89:184–192CrossRefPubMed Steer PA, Rourke DO, 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 89:184–192CrossRefPubMed
38.
go back to reference Tomás G, Hernández M, Marandino A, Techera C, Grecco S, Hernández D, Banda A, Panzera Y, Pérez R (2017) Development of an RT-qPCR assay for the specific detection of a distinct genetic lineage of the infectious bursal disease virus. Avian Pathol 2:150–156CrossRef Tomás G, Hernández M, Marandino A, Techera C, Grecco S, Hernández D, Banda A, Panzera Y, Pérez R (2017) Development of an RT-qPCR assay for the specific detection of a distinct genetic lineage of the infectious bursal disease virus. Avian Pathol 2:150–156CrossRef
39.
go back to reference Woźniakowski G, Niczyporuk JS, Samorek-Salamonowicz E, Gaweł A (2015) The development and evaluation of cross-priming amplification for the detection of avian reovirus. J Appl Microbiol 118:528–536CrossRefPubMed Woźniakowski G, Niczyporuk JS, Samorek-Salamonowicz E, Gaweł A (2015) The development and evaluation of cross-priming amplification for the detection of avian reovirus. J Appl Microbiol 118:528–536CrossRefPubMed
40.
go back to reference Zadravec M, Slavec B, Krapež U, Kaján GL, Račnik J, Juntes P, Rojs OZ (2011) Inclusion body hepatitis associated with fowl adenovirus type 8b in broiler flock in Slovenia—a case report. Slov Vet Res 48:107–113 Zadravec M, Slavec B, Krapež U, Kaján GL, Račnik J, Juntes P, Rojs OZ (2011) Inclusion body hepatitis associated with fowl adenovirus type 8b in broiler flock in Slovenia—a case report. Slov Vet Res 48:107–113
41.
go back to reference Zadravec M, Brigita Slavec, Krapež U, Gl Kaján, Račnik J, Polona Juntes, Rahela Juršič-Cizerl, Mária Benkõ, Olga Zorman-Rojs (2013) Inclusion body hepatitis (IBH) outbreak associated with fowl adenovirus type 8b in broilers. Acta Vet 63:101–110CrossRef Zadravec M, Brigita Slavec, Krapež U, Gl Kaján, Račnik J, Polona Juntes, Rahela Juršič-Cizerl, Mária Benkõ, Olga Zorman-Rojs (2013) Inclusion body hepatitis (IBH) outbreak associated with fowl adenovirus type 8b in broilers. Acta Vet 63:101–110CrossRef
Metadata
Title
A comparative pathogenicity analysis of two adenovirus strains, 1/A and 8a/E, isolated from poultry in Poland
Authors
Jowita Samanta Niczyporuk
Hanna Czekaj
Publication date
01-11-2018
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 11/2018
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-018-3965-9

Other articles of this Issue 11/2018

Archives of Virology 11/2018 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.