Intestinal Colonization of Campylobacter jejuni and Its Hepatic Dissemination Are Associated with Local and Systemic Immune Responses in Broiler Chickens

Abstract

Campylobacter jejuni is an important foodborne pathogen. Despite the lack of clinical signs associated with its colonization in poultry, it has been reported to interact with the intestinal immune system. However, little is known about the interaction between C. jejuni and the chicken immune system, especially in the context of hepatic dissemination. Therefore, to follow up on our previous study showing intestinal colonization and hepatic spread of C. jejuni, cecal tonsils and liver samples were collected from these birds to determine the mRNA levels of chemokines and cytokines. Serum samples were also collected to determine serum amyloid A (SAA) concentrations and specific IgY titers. Lack of Th17 induction was observed in the cecal tonsils of only the liver-contaminated groups. This hepatic dissemination was accompanied by innate, Th1 and Th2 immune responses in livers, as well as an increase in SAA concentrations and specific IgY levels in sera. Campylobacter appears to be able to restrain the induction of the chicken gut immunity in particular conditions, possibly enhancing its hepatic dissemination and thus eliciting systemic immune responses. Although Campylobacter is often recognized as a commensal-like bacterium in chickens, it seems to modulate the gut immune system and induce systemic immunity.

Investigation of Potential Gut Health Biomarkers in Broiler Chicks Challenged by Campylobacter jejuni and Submitted to a Continuous Water Disinfection Program

“…Particularly, Mortada et al [44] reported that the challenge of broilers by C. jejuni did not significantly affect the IL-10 mRNA levels in the ceca of broilers on 0, 1, 2, 3, and 7 dpi; however, an upregulation of IL-10 was observed at 14 and 21 dpi [44]. Additionally, Chagneau et al [45] observed a significant increase in cecal tonsil IL-10 expression at 21 dpi, suggesting a potential correlation with long-term C. jejuni colonization. The results of our study indicate that IL-10 is not directly involved in the initial response during the first 5 dpi, which is in accordance with the previously mentioned studies.…”

“…Cytokines are generally thought to be rapidly released during infection or other stimuli, remaining at basal levels under physiological conditions, and thus could be used as valuable markers [41]. Regarding C. jejuni infection, previous studies, including Humphrey et al [42], Reid et al [43], Mortada et al [44] and Chagneau et al [45], highlighted the dynamic expression of IL-10 mRNA in tissue sections from various parts of the intestine of birds infected by C. jejuni. Particularly, Mortada et al [44] reported that the challenge of broilers by C. jejuni did not significantly affect the IL-10 mRNA levels in the ceca of broilers on 0, 1, 2, 3, and 7 dpi; however, an upregulation of IL-10 was observed at 14 and 21 dpi [44].…”

“…The results of our study indicate that IL-10 is not directly involved in the initial response during the first 5 dpi, which is in accordance with the previously mentioned studies. Recently, Chagneau et al [45] reported the role of C. jejuni translocation in the increase of IL-10 expression in the liver of the infected birds, suggesting one additional area for increased expression after challenge that could be linked with the increase in serum levels. Finally, the continuous drinking water disinfection using Cid 2000™ (counting at the sampling time: 23 continuous days) had no significant impact on IL-10 levels.…”

Characterizing the Effect of Campylobacter jejuni Challenge on Growth Performance, Cecal Microbiota, and Cecal Short-Chain Fatty Acid Concentrations in Broilers

“…Additionally, different reports emphasized the commensal nature of C. jejuni infection in broilers, highlighting the absence of an effective immune response despite the high colonization rate in the ceca [13,18]. Nonetheless, other papers have challenged the notion of C. jejuni being merely a commensal bacterium, citing observed reduction in performance parameters following the infection of C. jejuni [19][20][21][22].…”