Discussion
Here, we used milk samples from healthy and C. bovis-infected udder quarters from different dairy cows as well as from the same cow. In this regard, we should highlight that the immune response against C. bovis is primarily restricted to the C. bovis-infected quarter [5, 6, 20], and the interdependence of udder quarters was also regarded in the statistical analysis of the present study, as previously suggested [22, 23].
Although it is difficult to draw consistent conclusions about the role of C. bovis on bovine udder health, there is an increasing evidence that C. bovis is part of udder microbiota [7, 11], which could modulate the local immune response [7, 24]. Thus, a recent study published by Porcellato et al. [7] using milk microbiome analysis associate the presence of the genera Corynebacterium in milk samples with a protective role against bovine mammary gland dysbiosis. In another study that investigated the association of teat canal microbiome analysis and mastitis susceptibility and udder inflammation, Corynebacterium identification was negatively correlated with milk SCC [11]. Additionally, the Corynebacterium genera dominate the bacterial populations of teat apices from healthy quarters [9]. Altogether, although the mechanisms behind these phenomena remain to be fully determined, our findings indicated that C. bovis could positively impact udder health by optimizing mammary gland immunity. In this scenario, for the first time, we observed an augment in the percentage of T cells, especially T CD4+ cells, as well as a higher percentage of milk macrophages that phagocytosed S. aureus and produced RONS in C. bovis-infected quarters.
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The ability of cows to resist the establishment of new intramammary infections or to overcome existing intramammary infections depends on the efficiency the mammary gland immunity. In this context, macrophages play a critical role in the initiation of the innate immune response of the host in case of bacterial (i.e., Streptotoccus uberis) invasion into the mammary gland [25, 26], beyond their role on adaptative immunity, such as antigen processing and presentation [27]. Similarly, T CD4+ lymphocytes have been associated with clearance activity against several bacterial pathogens [28-30]. Furthermore, cows having higher frequency of T CD4+ lymphocytes than T CD8+ lymphocytes in their mammary gland secretions appear to be more resistant to mastitis [31]. Overall, these findings support, at least in part, the potential protective role of C. bovis in the bovine udder.
In the present study, no perturbation on CD8+ T lymphocytes was found in quarters in which C. bovis was isolated, although the percentage of this lymphocyte subpopulation increased during staphylococcal and streptococcal intramammary infections [32]and may play a suppressive and cytotoxic role in the mammary gland [27, 33, 34]. In addition, the percentage of CD4− CD8− T lymphocytes, mainly represented by γδ T cells [35] was not affected by C. bovis. Furthermore, the macrophage apoptosis did not appear to be involved in the inflammatory response during C. bovis-infection.
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Thus, our results corroborate other studies that found a high correlation between isolation of C. bovis from aseptically collected milk samples and the reduction in the occurrence of intramammary infection by other pathogenic bacteria [6, 13, 16-18], although there is no consensus on this assertion [36-39]. In addition to our data regarding the lymphocytic and functional profile of milk macrophages, other factors may be related to the potential protective effect of intramammary infection by C. bovis, such as inhibition of growth by competition, bacterial antagonism, increased activity of milk neutrophils, and the presence of plasmocytes in the parenchymal tissue and the teat apices of quarters colonized with C. bovis [6, 16, 21, 40].
Furthermore, macrophages represent the first line of defense of the mammary gland against invasive pathogens because they make up the predominant leukocyte population in healthy udder quarters [27, 30, 41]. Although the proportion of macrophages usually decreases during intramammary infections due to the rapid and massive influx of neutrophils into the inflammatory site [19, 42], macrophages still represented the predominant leukocyte population in quarters infected by C. bovis in the present study. Besides that, an increase in the number of macrophages per mL was observed in C. bovis-infected quarters.
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