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Applied and Environmental Microbiology, May 2009, p. 3377-3378, Vol. 75, No. 10
0099-2240/09/$08.00+0     doi:10.1128/AEM.00513-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

LETTER TO THE EDITOR

Potential Role for the 4,12 Antigen in the Prevalence of Clonal Salmonella Serovars in Poultry


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LETTER
 
In a recent paper, Huehn et al. (6) examined a large number of poultry-associated Salmonella enterica subspecies enterica type I serovar 4,12:d:– strains which predominate in poultry flocks in Germany but are poorly represented in cases of human disease. The authors examined the clonality and pathogenic gene repertoire of these strains to shed light on this contradiction. They concluded that the epidemiology of this highly clonal strain may be due to a lack of several genes which contribute to human pathogenicity and the presence of "genetic factors" which facilitate broiler colonization. The data presented in this study, together with a number of other published reports from around the world which were not cited by these authors, may provide further insight into this important issue.

In Australia, subspecies type II Salmonella enterica subsp. salamae serovar Sofia is also highly clonal and has similar antigenic determinants (4,12:b–) to those described by Huehn et al. and has long been established as the predominant Salmonella serovar isolated from poultry (8). Furthermore, S. Sofia, like the German Salmonella 4,12:d– strain, is regarded as having relatively low virulence for humans as it is rarely associated with human disease in comparison with subspecies type I serovars such as Salmonella enterica serovar Typhimurium (5). The natural habitat of Salmonella subspecies type II is generally believed to be coldblooded animals and the environment (7), and it is therefore unusual to encounter the bacteria in poultry. Furthermore, in both Senegal and Demark, Salmonella enterica serovar Brancaster, which also has a similar antigenic structure (4,12:b–) to the strains found in Germany, has also been found to commonly occur in poultry. This serotype had an apparently low virulence for humans and displayed a relatively high degree of clonality (3, 4).

Salmonella strains possessing fimbrial markers, such as long polar fimbriae (Lpf) and plasmid-encoded fimbriae (Pef), are often associated with human diseases (1, 2). It has been established that plasmid-encoded phase 2 flagellar regions, which contain the genes lpf and pef, are absent in poultry-associated S. Sofia isolates (7). This correlates with the finding that these regions are absent in the German Salmonella 4,12:d– serovar strains. The complete loss of, or inability to harbor, plasmids in many of the Salmonella 4,12d:– strains (6) and in S. Brancaster (4) could be the main reason for the absence of lpf and pef in these strains. As pointed out by Huehn et al., the lack of fimbrial clusters such as Lpf might be an important reason for the successful spread of the serovar in poultry.

These data taken together add weight to the suggestion of Huehn et al. (6) that the inability to produce a phase 2 flagellar antigen has led to the successful colonization of these serovars in poultry. The presence of the 4,12 somatic antigen in serovars with similar traits from diverse continents, however, introduces a new dimension to understanding these issues. We hypothesize that the 4,12 antigen, in combination with the absence of phase 2 flagellar antigens, strongly favors the persistence of these serovars in poultry. Further work in this area, perhaps taking an international comparative approach, is required to fully test this hypothesis. The dominance of Salmonella serovars with a low human virulence potential and a high prevalence in poultry could result in significant public health benefits.


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REFERENCES
 
    1
  1. Bäumler, A. J., R. M. Tsolis, F. A. Bowe, J. G. Kusters, S. Hoffmann, and F. Heffron. 1996. The pef fimbrial operon of Salmonella typhimurium mediates adhesion to murine small intestine and is necessary for fluid accumulation in the infant mouse. Infect. Immun. 64:61-68.[Abstract]
    2. 2
  2. Bäumler, A. J., R. M. Tsolis, and F. Heffron. 1996. The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer's patches. Proc. Natl. Acad. Sci. USA 93:279-283.[Abstract/Free Full Text]
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  3. Cardinale, E., F. Tall, E. F. Guèye, M. Cisse, and G. Salvat. 2004. Risk factors for Salmonella enterica subsp. enterica infection in Senegalese broiler-chicken flocks. Prev. Vet. Med. 63:151-161.[CrossRef][Medline]
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  4. Chadfield, M., M. Skov, J. Christensen, M. Madsen, and M. Bisgaard. 2001. An epidemiological study of Salmonella enterica serovar 4,12:b:– in broiler chickens in Denmark. Vet. Microbiol. 82:233-247.[CrossRef][Medline]
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  5. Harrington, C. S., J. A. Lanser, P. A. Manning, and C. J. Murray. 1991. Epidemiology of Salmonella sofia in Australia. Appl. Environ. Microbiol. 57:223-227.[Abstract/Free Full Text]
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  6. Huehn, S., C. Bunge, E. Junker, R. Helmuth, and B. Malorny. 2009. Poultry-associated Salmonella enterica subsp. enterica serovar 4,12:d:– reveals high clonality and a distinct pathogenicity gene repertoire. Appl. Environ. Microbiol. 75:1011-1020.[Abstract/Free Full Text]
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  7. Popoff, M. Y., and L. E. Le Minor. 2005. Salmonella, 2nd ed., Springer Science, New York, NY.
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  8. Sexton, M., G. Raven, G. Holds, A. Pointon, A. Kiermeier, and J. Sumner. 2007. Effect of acidified sodium chlorite treatment on chicken carcasses processed in South Australia. Int. J. Food Microbiol. 115:252-255.[CrossRef][Medline]
T. W. Raymond Chia
Narelle Fegan
Gary A. Dykes*
Food Science Australia
P.O. Box 3312
Tingalpa, DC, Queensland 4173, Australia

* Phone: 61 7 3214 2037, Fax: 61 7 3214 2150, E-mail: gary.dykes{at}csiro.au


Authors' Reply


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LETTER 
 
We appreciate the comment about the potential role for the 4,12 antigen in the prevalence of clonal serovars in poultry. The authors raise an interesting hypothesis which is worthwhile to substantiate or to negate by additional investigations. Primarily, it is worthwhile to collect all known data from literature concerning this issue.

In Germany and other Western European countries, another clonal Salmonella enterica diphasic serovar Paratyphi B (d-tartrate positive) (4,12:b:1,2) persists which is also associated with poultry (1, 2). We know that isolates of this serovar can contain the lpf fimbrial cluster. The conclusion is that other serovars with antigen 4,12 and lpf might also be associated with poultry. Additionally, we know that in Denmark, the monophasic serovar 4,5,12:b:– (harboring the lpf cluster) has recently caused outbreaks in humans (Mia Torpdahl, Statens Serum Institute, Copenhagen, Denmark, personal communication). Consequently, a number of factors must be considered to establish a working hypothesis, taking all known data into account.

Nevertheless, we would warn not to eradicate such poultry-associated serovars from flocks despite their low infection rate for humans. It might be possible that they serve as a carrier for resistance determinants and rapidly acquire any genetic determinants, resulting in high virulence.


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REFERENCES 
 
    1
  1. Huehn, S., R. Helmuth, C. Bunge, B. Guerra, E. Junker, R. H. Davies, P. Wattiau, W. van Pelt, and B. Malorny. 17 March 2009, posting date. Characterization of pathogenic and resistant genome repertoire reveals two clonal lines in Salmonella enterica subsp. enterica serovar Paratyphi B (+)-tartrate positive. Foodborne Pathog. Dis. [Epub ahead of print.] doi:10.1089/fpd.2008.0221.[CrossRef]
    2. 2
  2. Miko, A., B. Guerra, A. Schroeter, C. Dorn, and R. Helmuth. 2002. Molecular characterization of multiresistant d-tartrate-positive Salmonella enterica serovar Paratyphi B isolates. J. Clin. Microbiol. 40:3184-3191.[Abstract/Free Full Text]
Stephan Huehn
Cornelia Bunge
Ernst Junker
Reiner Helmuth
Burkhard Malorny*
Federal Institute for Risk Assessment
Diedersdorfer Weg 1
D-12277 Berlin, Germany

* Phone: (49 30) 8412 2237
Fax: (49 30) 8412 2064
E-mail: burkhard.malorny{at}bfr.bund.de

Applied and Environmental Microbiology, May 2009, p. 3377-3378, Vol. 75, No. 10
0099-2240/09/$08.00+0     doi:10.1128/AEM.00513-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.




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