Background and objectives
The human immune system has evolved to balance protection against infection with control of immune-mediated damage and tolerance of commensal microbes. Such tradeoffs between protection and harm almost certainly extend to the immune system of milk.
Methodology
Among breastfeeding mother-infant dyads in Kilimanjaro, Tanzania, we characterized in vitro proinflammatory milk immune responses to Salmonella enterica (an infectious agent) and Escherichia coli (a benign target) as the increase in interleukin-6 after 24 hours of incubation with each bacterium. We characterized incident infectious diseases among infants through passive monitoring. We used Cox proportional hazards models to describe associations between milk immune activity and infant infectious disease.
Results
Among infants, risk for respiratory infections declined with increasing milk in vitro proinflammatory response to S. enterica (HR: 0.68; 95% CI: 0.54, 0.86; p: 0.001), while risk for gastrointestinal infections increased with increasing milk in vitro proinflammatory response to E. coli (HR: 1.44; 95% CI: 1.05, 1.99; p: 0.022). Milk proinflammatory responses to S. enterica and E. coli were positively correlated (Spearman’s rho: 0.60; p: 0.000).
Conclusions and implications
These findings demonstrate a tradeoff in milk immune activity: the benefits of appropriate proinflammatory activity come at the hazard of misdirected proinflammatory activity. This tradeoff is likely to affect infant health in complex ways, depending on prevailing infectious disease conditions. How mother-infant dyads optimize proinflammatory milk immune activity should be a central question in future ecological-evolutionary studies of the immune system of milk.
Lay Summary
While vital to infant health, the immune system of milk (ISOM), like all immune activity, comes with potential for both protection and harm. We described the ISOM’s capacity to respond to bacteria among mother-infant pairs, and found that milk immune activity may both lower and increase infants’ infectious disease risk.
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