Passive maternal exposure to environmental microbes selectively modulates the innate defences of chicken egg white by increasing some of its antibacterial activities

Bedrani, Larbi; Helloin, Emmanuelle; Guyot, Nicolas; Réhault-Godbert, Sophie; Nys, Yves

doi:10.1186/1471-2180-13-128

Cited by 23 publications

(21 citation statements)

References 41 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…However, microbial exposure during the development of the immune system can impact subsequent functioning greatly; for example, neonatal chickens and mice raised in germ-free laboratory environments have a reduced functional immune capacity into adulthood, compared with offspring raised in conventional environments (Bedrani et al, 2013;Lee and Mazmanian, 2010). To some extent, this has also been found in two species of wild bird, where microbial exposure was positively correlated with various measures of the innate immune response (Buehler et al, 2008;Horrocks et al, 2012a,b).…”

Section: Introductionmentioning

confidence: 99%

Impact of nest sanitation on the immune system of parents and nestlings in a passerine bird

Evans

Griffith

Klasing

et al. 2016

Journal of Experimental Biology

View full text Add to dashboard Cite

Bacterial communities are thought to have fundamental effects on the growth and development of nestling birds. The antigen exposure hypothesis suggests that, for both nestlings and adult birds, exposure to a diverse range of bacteria would select for stronger immune defences. However, there are relatively few studies that have tested the immune/bacterial relationships outside of domestic poultry. We therefore sought to examine indices of immunity (microbial killing ability in naive birds, which is a measure of innate immunity, and the antibody response to sheep red blood cells, which measures adaptive immunity) in both adult and nestling zebra finches (Taeniopygia guttata). We did this throughout breeding and between reproductive attempts in nests that were experimentally manipulated to change the intensity of bacterial exposure. Our results suggest that nest sanitation and bacterial load affected measures of the adaptive immune system, but not the innate immune parameters tested. Adult finches breeding in clean nests had a lower primary antibody response to sheep red blood cells, particularly males, and a greater difference between primary and secondary responses. Adult microbial killing of Escherichia coli decreased as parents moved from incubation to nestling rearing for both nest treatments; however, killing of Candida albicans remained consistent throughout. In nestlings, both innate microbial killing and the adaptive antibody response did not differ between nest environments. Together, these results suggest that exposure to microorganisms in the environment affects the adaptive immune system in nesting birds, with exposure upregulating the antibody response in adult birds.

show abstract

Section: Introductionmentioning

confidence: 99%

Impact of nest sanitation on the immune system of parents and nestlings in a passerine bird

Evans

Griffith

Klasing

et al. 2016

Journal of Experimental Biology

View full text Add to dashboard Cite

show abstract

“…Yolk contains IgY (IgG-like) while IgA and IgM are deposited in the egg albumen (Rose et al, 1974;Kovacs-Nolan and Mine, 2012;Bedrani et al, 2013). IgY, if present, occurs in very low concentration in egg albumen (Rose and Orlans, 1981).…”

Section: The Egg Albumenmentioning

confidence: 99%

Scientific Opinion on the public health risks of table eggs due to deterioration and development of pathogens

2014

EFSA Journal

View full text Add to dashboard Cite

Salmonella Enteritidis is considered the only pathogen currently posing a major risk of egg-borne diseases in the European Union (EU). The possible impact of extending the shelf-life of eggs on the risk to consumers posed by S. Enteritidis was estimated by applying a quantitative model and comparing the actual situation regarding the storage of eggs in the EU with different possible scenarios combined, considering the prolongation of the bestbefore and the sell-by date from 7 to a maximum of 70 days. Extending the sell-by date by one week (from 21 to 28 days), but leaving the best-before date unchanged, is estimated to result in a relative risk of illness of 1.4 and 1.5 for uncooked and lightly cooked egg meals respectively, compared to the current situation. If the best-before date is also extended by one week (from 28 to 35 days), the relative risk would be 1.6 and 1.7. In the worst case scenario considered (sell-by date of 42 days, best before date of 70 days), such figures would be 2.9 and 3.5. It should be noted that the absolute risk is greater for uncooked meals compared to lightly cooked meals. An effective way to minimise any increase in risk during extended storage is to keep the eggs refrigerated both at retail and the household. Regarding egg spoilage, such events strongly depend on the hygienic conditions of egg production and practices of egg handling, including storage times and temperatures. Finally, the impact of the prolongation of storage time on the quality criteria for eggs (3-hydroxybutyric acid and lactic acid) destined for manufacturing of egg products is considered negligible. Specifically, EFSA was asked to assess: (i) the public health risk posed by relevant pathogens and in particular by Salmonella in the consumption and handling of table eggs (Term of Reference, or ToR1), (ii) the public health risk deriving from deterioration (ToR2) and (iii) possible consequences for public health of an extended shelf-life of table eggs for the specific freshness criteria for egg products as laid out in the hygiene package (ToR3). © European Food Safety Authority, 2014 KEY WORDSIn order to answer the first ToR, the BIOHAZ Panel based its conclusions on the results of a quantitative model, aimed at describing the behaviour of Salmonella Enteritidis following vertical transmission, since this serovar is recognised to be the major pathogen related to egg-borne disease because of its ability to contaminate the interior of intact eggs during their formation within the body of an infected hen. The possible impact of extending the shelf-life of eggs on other serovars of Salmonella, as well as on other pathogens, is evaluated in a qualitative manner, with no individual serovar other than S. Enteritidis currently posing a major risk of egg-borne salmonellosis in the European Union (EU), although S. Typhimurium has been associated with relatively small outbreaks due to duck eggs. Trans-shell contamination (i.e. secondary contamination) is also discussed, but the impact of a prolongation of the shelf ...

show abstract

“…Enteritidis is known to preferentially colonize the reproductive tract of laying hens and contaminate eggs without inducing overt clinical signs (16,17). S. Enteritidis strains recovered from the field have a higher degree of heterogeneity, especially in the glucosylation in the O-chain of the LPS, than S. Typhimurium strains (19,66).…”

Section: Fig 10mentioning

confidence: 99%

“…Many investigators have argued that the main difference between S. Typhimurium and S. Enteritidis with respect to survival in the chicken host is in the use of stress-induced mechanisms, including outer membrane modulation, and that this accounts for the differences seen in pandemics associated with contaminated poultry products (14,17,19,46). Silent colonization of S. Enteritidis in chicken requires intrinsic abilities to defend against the innate immune system without inducing overt inflammation and damage (16). This report shows that AMPR genes virK and ybjX not only aid in resistance to innate antimicrobial peptides and detergents but are also involved in replication and persistence in chicken tissues and eggs.…”

Section: Fig 10mentioning

confidence: 99%

“…S. Enteritidis has been shown to colonize the ovary and the reproductive tract within laying hens, with a higher recovery from the ovary than from any other reproductive tissue (14,15). Successful S. Enteritidis colonization involves inherent characteristics employed to subvert the reproductive innate immune system: phagocytes, antimicrobial peptides, including avian ␤-defensins, and immunoglobulins (16,17). Persistent reproductive-tract colonization that leads to egg contamination is confined primarily to S. Enteritidis and is partially due to its ability to survive under these harsh conditions without causing overt clinical signs in the chicken host (18,19).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Salmonella enterica Serovar Enteritidis Antimicrobial Peptide Resistance Genes Aid in Defense against Chicken Innate Immunity, Fecal Shedding, and Egg Deposition

et al. 2014

View full text Add to dashboard Cite

c Salmonella enterica serovar Enteritidis (S. Enteritidis) is a major etiologic agent of nontyphoid salmonellosis in the United States. S. Enteritidis persistently and silently colonizes the intestinal and reproductive tract of laying hens, resulting in contaminated poultry products. The consumption of contaminated poultry products has been identified as a significant risk factor for human salmonellosis. To understand the mechanisms S. Enteritidis utilizes to colonize and persist in laying hens, we used selective capture of transcribed sequences to identify genes overexpressed in the HD11 chicken macrophage cell line and in primary chicken oviduct epithelial cells. From the 15 genes found to be overexpressed in both cell types, we characterized the antimicrobial peptide resistance (AMPR) genes, virK and ybjX, in vitro and in vivo. In vitro, AMPR genes were required for natural morphology, motility, secretion, defense against detergents such as EDTA and bile salts, and resistance to antimicrobial peptides polymyxin B and avian ␤-defensins. From this, we inferred the AMPR genes play a role in outer membrane stability and/or modulation. In the intestinal tract, AMPR genes were involved in early intestinal colonization and fecal shedding. In the reproductive tract, virK was required in early colonization whereas a deletion of ybjX caused prolonged ovary colonization and egg deposition. Data from the present study indicate that AMPR genes are differentially utilized in various host environments, which may ultimately assist S. Enteritidis in persistent and silent colonization of chickens.

show abstract

Passive maternal exposure to environmental microbes selectively modulates the innate defences of chicken egg white by increasing some of its antibacterial activities

Cited by 23 publications

References 41 publications

Impact of nest sanitation on the immune system of parents and nestlings in a passerine bird

Impact of nest sanitation on the immune system of parents and nestlings in a passerine bird

Scientific Opinion on the public health risks of table eggs due to deterioration and development of pathogens

Salmonella enterica Serovar Enteritidis Antimicrobial Peptide Resistance Genes Aid in Defense against Chicken Innate Immunity, Fecal Shedding, and Egg Deposition

Contact Info

Product

Resources

About