1887

Abstract

serovar Gallinarum has two distinct biovars, Pullorum and Gallinarum. They are host-adapted avian pathogens that infect a number of wild and domesticated species but they pose a particular threat to farmed and backyard chickens and turkeys. Both biovars cause invasive and septicaemic disease, often resulting in high mortality. Pullorum is transmitted in eggs and typically affects birds soon after hatch. Gallinarum may cause disease in any age of bird, which often progresses through mature flocks. The establishment of clean breeding stock has resulted in freedom from the pathogens in many countries although even in these territories sporadic incursions still occur.

Funding
This study was supported by the:
  • Department for Environment, Food and Rural Affairs, UK Government (Award FZ2000)
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001653
2023-02-08
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jmm/72/2/jmm001653.html?itemId=/content/journal/jmm/10.1099/jmm.0.001653&mimeType=html&fmt=ahah

References

  1. Klein E. Über eine epidemische krankheit der Hühner, verursacht durch einen bacillus - bacillus gallinarum. Cent für Bakteriol Parasitenkd 1889; 5:689–693
    [Google Scholar]
  2. Rettger LF. Further studies on fatal septicemia in young chickens, or “white diarrhea.”. J Med Res 1909; 21:115–123
    [Google Scholar]
  3. Bullis KL. The history of avian medicine in the U.S. II. pullorum disease and fowl typhoid. Avian Dis 1977; 21:422–429 [View Article]
    [Google Scholar]
  4. Revolledo L. Vaccines and vaccination against fowl typhoid and pullorum disease: an overview and approaches in developing countries. J Appl Poult Res 2018; 27:279–291 [View Article]
    [Google Scholar]
  5. Cobb SP, McVicar CM, Davies RH, Ainsworth H. Fowl typhoid in caged layer birds. Vet Rec 2005; 157:268 [View Article]
    [Google Scholar]
  6. Shivaprasad HL, Barrow P. Pullorum disease and Fowl typhoid. In Swayne DE, Glisson JR, McDougald LR, Nolan LK, Suarez DL. eds Diseases of Poultry Ames, Iowa: John Wiley & Sons, Inc; 2013 pp 678–693
    [Google Scholar]
  7. Matos M, Sommer F, Liebhart D, Bilic I, Hess M et al. An outbreak of Pullorum disease in a young layer parent flock in Austria presented with central nervous system signs. Avian Dis 2021; 65:159–164 [View Article]
    [Google Scholar]
  8. WOAH Chapter 3.3.11: Fowl typhoid and Pullorum disease. In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals World Organisation for Animal Health (WOAH); 2018 pp 914–930
    [Google Scholar]
  9. Grimont PAD, Weill F-X. Antigenic formulae of the Salmonella serovars, 9th edition. Paris: WHO Collaborating Centre for Reference and Research on Salmonella (WHOCC-Salm), Institut Pasteur; 2007
    [Google Scholar]
  10. Langridge GC, Fookes M, Connor TR, Feltwell T, Feasey N et al. Patterns of genome evolution that have accompanied host adaptation in Salmonella. Proc Natl Acad Sci 2015; 112:863–868 [View Article]
    [Google Scholar]
  11. Thomson NR, Clayton DJ, Windhorst D, Vernikos G, Davidson S et al. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res 2008; 18:1624–1637 [View Article] [PubMed]
    [Google Scholar]
  12. Li J, Smith NH, Nelson K, Crichton PB, Old DC et al. Evolutionary origin and radiation of the avian-adapted non-motile salmonellae. J Med Microbiol 1993; 38:129–139 [View Article]
    [Google Scholar]
  13. Batista DFA, Freitas Neto OC, Barrow PA, de Oliveira MT, Almeida AM et al. Identification and characterization of regions of difference between the Salmonella Gallinarum biovar Gallinarum and the Salmonella Gallinarum biovar Pullorum genomes. Infect Genet Evol 2015; 30:74–81 [View Article] [PubMed]
    [Google Scholar]
  14. Parmar D, Davies R. Fowl typhoid in a small backyard laying flock. Vet Rec 2007; 160:348 [View Article]
    [Google Scholar]
  15. Shivaprasad HL. Fowl typhoid and pullorum disease. Rev Sci Tech 2000; 19:405–424 [View Article]
    [Google Scholar]
  16. Shivaprasad HL, Methner U, Barrow PA. Salmonella infections in the domestic fowl. In Barrow PA, Methner U. eds Salmonella in Domestic Animals Wallingford, UK: CAB International; 2013 pp 162–192
    [Google Scholar]
  17. Berchieri A Jr, Murphy CK, Marston K, Barrow PA. Observations on the persistence and vertical transmission of Salmonella enterica serovars Pullorum and Gallinarum in chickens: effect of bacterial and host genetic background. Avian Pathol 2001; 30:221–231 [View Article] [PubMed]
    [Google Scholar]
  18. Oliveira GH de, Berchieri Junior A, Fernandes AC. Experimental infection of laying hens with Salmonella enterica serovar Gallinarum. Braz J Microbiol 2005; 36:51–56 [View Article]
    [Google Scholar]
  19. Batista DFA, de Freitas Neto OC, de Almeida AM, Barrow PA, de Oliveira Barbosa F et al. Molecular identification of Salmonella enterica subsp. enterica serovar Gallinarum biovars Gallinarum and Pullorum by a duplex PCR assay. J Vet Diagn Invest 2016; 28:419–422 [View Article]
    [Google Scholar]
  20. McDonough PL, Jacobson RH, Timoney JF, Mutalib A, Kradel DC et al. Interpretations of antibody responses to Salmonella enterica serotype Enteritidis gm flagellin in poultry flocks are enhanced by a kinetics-based enzyme-linked immunosorbent assay. Clin Diagn Lab Immunol 1998; 5:550–555 [View Article]
    [Google Scholar]
  21. More S, Bøtner A, Butterworth A, Calistri P, Depner K et al. Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): Salmonella infection in poultry with serotypes of animal health relevance (S. Pullorum, S. Gallinarum and S. arizonae). EFS2 2017; 15: [View Article]
    [Google Scholar]
  22. McCullough N, Eisele CW. Experimental human salmonellosis. IV. Pathogenicity of strains of Salmonella pullorum obtained from spray-dried whole egg. J Infect Dis 1951; 89:259–265 [View Article]
    [Google Scholar]
  23. Barrow PA, Freitas Neto OC. Pullorum disease and fowl typhoid--new thoughts on old diseases: a review. Avian Pathol 2011; 40:1–13 [View Article] [PubMed]
    [Google Scholar]
  24. Celis-Estupiñan ALDP, Batista DFA, Cardozo MV, Secundo de Souza AI, Rodrigues Alves LB et al. Further investigations on the epidemiology of fowl typhoid in Brazil. Avian Pathol 2017; 46:416–425 [View Article] [PubMed]
    [Google Scholar]
  25. Pugliese N, Circella E, Marino M, De Virgilio C, Cocciolo G et al. Circulation dynamics of Salmonella enterica subsp. enterica ser. Gallinarum biovar Gallinarum in a poultry farm infested by Dermanyssus gallinae. Med Vet Entomol 2019; 33:162–170 [View Article] [PubMed]
    [Google Scholar]
  26. Sun Y, Yu P, Cheng Y, Liu J, Chen X et al. The feed additive potassium diformate prevents Salmonella enterica serovar Pullorum infection and affects intestinal flora in chickens. Antibiotics 2022; 11:1265 [View Article]
    [Google Scholar]
  27. Saleem G, Ramzaan R, Khattak F, Akhtar R. Effects of acetic acid supplementation in broiler chickens orally challenged with Salmonella Pullorum. Turk J Vet Anim Sci 2016; 40:434–443 [View Article]
    [Google Scholar]
  28. Al-Tarazi YH, Alshawabkeh K. Effect of dietary formic and propionic acids on Salmonella Pullorum shedding and mortality in layer chicks after experimental infection. J Vet Med B Infect Dis Vet Public Health 2003; 50:112–117 [View Article]
    [Google Scholar]
  29. Al-Natour MQ, Alshawabkeh KM. Using varying levels of formic acid to limit growth of Salmonella gallinarum in contaminated broiler feed. Asian Australas J Anim Sci 2005; 18:390–395 [View Article]
    [Google Scholar]
  30. Alshawabkeh K, Tabbaa MJ. Using dietary propionic acid to limit Salmonella gallinarum colonization in broiler chicks. Asian Australas J Anim Sci 2002; 15:243–246 [View Article]
    [Google Scholar]
  31. Berchieri A, Barrow PA. Reduction in incidence of experimental fowl typhoid by incorporation of a commercial formic acid preparation (Bio-Add) into poultry feed. Poult Sci 1996; 75:339–341 [View Article] [PubMed]
    [Google Scholar]
  32. Kang MS, Kim A, Jung BY, Her M, Jeong W et al. Characterization of antimicrobial resistance of recent Salmonella enterica serovar Gallinarum isolates from chickens in South Korea. Avian Pathol 2010; 39:201–205 [View Article] [PubMed]
    [Google Scholar]
  33. Mechesso AF, Moon DC, Kim S-J, Song H-J, Kang HY et al. Nationwide surveillance on serotype distribution and antimicrobial resistance profiles of non-typhoidal Salmonella serovars isolated from food-producing animals in South Korea. Int J Food Microbiol 2020; 335:108893 [View Article] [PubMed]
    [Google Scholar]
  34. Song Y, Wang F, Liu Y, Song Y, Zhang L et al. Occurrence and characterization of Salmonella isolated from chicken breeder flocks in nine Chinese provinces. Front Vet Sci 2020; 7:479 [View Article]
    [Google Scholar]
  35. Sun F, Li X, Wang Y, Wang F, Ge H et al. Epidemic patterns of antimicrobial resistance of Salmonella enterica serovar Gallinarum biovar Pullorum isolates in China during the past half-century. Poult Sci 2021; 100:100894 [View Article] [PubMed]
    [Google Scholar]
  36. Zhang J-F, Shang K, Park J-Y, Lee Y-J, Choi Y-R et al. Antimicrobial resistance and PFGE molecular typing of Salmonella enterica serovar Gallinarum isolates from chickens in South Korea from 2013 to 2018. Animals 2021; 12:83 [View Article]
    [Google Scholar]
  37. Hu Y, Wang Z, Qiang B, Xu Y, Chen X et al. Loss and gain in the evolution of the Salmonella enterica serovar Gallinarum biovar Pullorum genome. mSphere 2019; 4:e00627-18 [View Article]
    [Google Scholar]
  38. Hafez HM. Salmonella infections in turkeys. In Barrow PA, Methner U. eds Salmonella in Domestic Animals Wallingford, UK: CAB International; 2013 pp 193–220
    [Google Scholar]
  39. Haider G, Chowdhury EH, Hossain M. Mode of vertical transmission of Salmonella enterica sub. enterica serovar pullorum in chickens. Afr J Microbiol Res 2014; 8:1344–1351 [View Article]
    [Google Scholar]
  40. Bunyea H, Hall WJ. Transmission of pullorum disease (bacillary white diarrhea) in incubators. J Agric Res 1930; 40:209–223
    [Google Scholar]
  41. GWATKIN R. Studies in pullorum disease; transmission of infection to healthy birds by contact. Can J Comp Med Vet Sci 1945; 9:335–338 [PubMed]
    [Google Scholar]
  42. Hall WJ, Legenhausen DH, MacDonald AD. Studies on Fowl typhoid I. Nature and dissemination. Poult Sci 1949; 28:344–362 [View Article]
    [Google Scholar]
  43. Lee H-J, Jeong J-Y, Jeong O-M, Youn S-Y, Kim J-H et al. Impact of Dermanyssus gallinae infestation on persistent outbreaks of fowl typhoid in commercial layer chicken farms. Poult Sci 2020; 99:6533–6541 [View Article] [PubMed]
    [Google Scholar]
  44. Jordan FTW. The transmission of Salmonella gallinarum through the egg. Poultry Science 1956; 35:1019–1025 [View Article]
    [Google Scholar]
  45. Basnet HB, Kwon H-J, Cho S-H, Kim S-J, Yoo H-S et al. Reproduction of fowl typhoid by respiratory challenge with Salmonella Gallinarum. Avian Dis 2008; 52:156–159 [View Article] [PubMed]
    [Google Scholar]
  46. Cheng Y, Sihua Z, Lu Q, Zhang W, Wen G et al. Evaluation of young chickens challenged with aerosolized Salmonella Pullorum. Avian Pathol 2020; 49:507–514 [View Article] [PubMed]
    [Google Scholar]
  47. Guiney DG, Fierer J. The role of the spv genes in Salmonella pathogenesis. Front Microbiol 2011; 2:129 [View Article]
    [Google Scholar]
  48. Blondel CJ, Jiménez JC, Leiva LE, Alvarez SA, Pinto BI et al. The type VI secretion system encoded in Salmonella pathogenicity island 19 is required for Salmonella enterica serotype Gallinarum survival within infected macrophages. Infect Immun 2013; 81:1207–1220 [View Article] [PubMed]
    [Google Scholar]
  49. Blondel CJ, Yang H-J, Castro B, Chiang S, Toro CS et al. Contribution of the type VI secretion system encoded in SPI-19 to chicken colonization by Salmonella enterica serotypes Gallinarum and Enteritidis. PLoS One 2010; 5:e11724 [View Article]
    [Google Scholar]
  50. Wigley P. Salmonella enterica serovar Gallinarum: addressing fundamental questions in bacteriology sixty years on from the 9R vaccine. Avian Pathol 2017; 46:119–124 [View Article] [PubMed]
    [Google Scholar]
  51. Lopes PD, Freitas Neto OC, Batista DFA, Denadai J, Alarcon MFF et al. Experimental infection of chickens by a flagellated motile strain of Salmonella enterica serovar Gallinarum biovar Gallinarum. Vet J 2016; 214:40–46 [View Article] [PubMed]
    [Google Scholar]
  52. Feng Y, Liu J, Li Y-G, Cao F-L, Johnston RN et al. Inheritance of the Salmonella virulence plasmids: mostly vertical and rarely horizontal. Infect Genet Evol 2012; 12:1058–1063 [View Article] [PubMed]
    [Google Scholar]
  53. Rychlik I, Gregorova D, Hradecka H. Distribution and function of plasmids in Salmonella enterica. Vet Microbiol 2006; 112:1–10 [View Article] [PubMed]
    [Google Scholar]
  54. Schat KA, Nagaraja KV, Saif YM. Pullorum disease: evolution of the eradication strategy. Avian Dis 2021; 65:227–236 [View Article]
    [Google Scholar]
  55. WOAH Chapter 10.7: Fowl typhoid and Pullorum disease. In Terrestrial Animal Health Code World Organisation for Animal Health (WOAH); 2022
    [Google Scholar]
  56. Guo R, Jiao Y, Li Z, Zhu S, Fei X et al. Safety, protective immunity, and DIVA capability of a rough mutant Salmonella Pullorum vaccine candidate in broilers. Front Microbiol 2017; 8:547 [View Article]
    [Google Scholar]
  57. Psifidi A, Russell KM, Matika O, Sánchez-Molano E, Wigley P et al. The genomic architecture of fowl typhoid resistance in commercial layers. Front Genet 2018; 9:519 [View Article]
    [Google Scholar]
  58. Hutt FB, Scholes JC. Genetics of the fowl: XIII. breed differences in susceptibility to Salmonella pullorum. Poult Sci 1941; 20:342–352 [View Article]
    [Google Scholar]
  59. Pinheiro LAS, De Oliveira GH, Berchieri A. Experimental Salmonella enterica serovar Pullorum infection in two commercial varieties of laying hens. Avian Pathol 2001; 30:129–133 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001653
Loading
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error