The unrevealed links: periodontal health, human milk composition, and infant gut microbiome dynamics

Abstract

Aim: This review aims to identify the mechanistic relationships related to periodontal diseases and its possible association with changes in human milk composition and the composition and function of infants' gut microbiome.

Background: Maternal health conditions, especially inflammatory, are associated with altered human milk composition. It is not known whether maternal oral inflammatory diseases, including periodontal diseases, deleteriously affect human milk composition.

Methods: A narrative review was conducted according to SANRA, the Scale for the Assessment of Narrative Review Articles, guidelines. PubMed, Google Scholar, and Cochrane database of systematic reviews were searched from September 2019 up to December 2023 using keywords such as breast/human milk, maternal health/infections, and periodontal diseases. Reference lists of relevant articles were also screened. Our primary outcome of interest was human milk composition (i.e., any changes in macronutrients, immunological components, etc.). Secondary outcomes included changes in human milk microbiome and subsequent changes in the infant gut microbiome. Outcomes were synthesized using a narrative approach where the existing evidence and current literature were summarized. No risk of bias assessment of the studies was performed in this review.

Findings: The search yielded no studies investigating the relationship between periodontal diseases in nursing mothers and changes in human milk composition. However, a dose-response relationship exists between the severity of periodontal diseases and the risk of adverse pregnancy outcomes such as preterm birth. Mastitis and diabetes affected milk lipids. Immunoglobulin A (sIgA) was increased in mastitis, whereas reduced concentrations were reported in diabetes. Potential biological pathways through which periodontal diseases can negatively affect human milk composition include the systemic dissemination of inflammatory cytokines like IL-6, PGE2, and tumor necrosis factor (TNF)-β that can be up-regulated by bacterial by-products. This biological plausibility needs to be investigated, given the potentially negative impact on the quality of human milk that could be caused by periodontal inflammation.

Keywords: Breast/human milk; breastfeeding; maternal health/infections; periodontal diseases; periodontitis.

Figure 1.

A diagram showing differences between healthy teeth and teeth with gingivitis and periodontitis. Gingivitis is a reversible inflammation confined to the gingival tissues. The teeth in the oral cavity are supported by a ligament known as the periodontal ligament which attached the teeth to the gingiva and surrounding alveolar bone. The space between the tooth and the gingival tissues is known as the gingival sulcus, and this is where most of the dental plaque accumulates, triggering an inflammatory response. What differentiates gingivitis from periodontitis is that the latter is an irreversible destruction to the periodontal supporting tissues, including the alveolar bone, periodontal ligament, and cementum, which consequently results in tooth loss (Kinane et al., , Tatakis and Kumar, 2005). As sources of inflammation, periodontal diseases contribute to the overall inflammatory burden experienced by individuals (Khoury et al., 2020). Initially, the gingival response to the biofilm is presented in the form of redness, edema, and bleeding. Oral polymorphonuclear neutrophils are then recruited to the sites of inflammation. In a healthy periodontium, oral neutrophils are usually found at the junctional epithelium and base of the sulcus (Khoury et al., 2020) to protect the periodontal tissues by providing a barrier between the junctional epithelium and pathogens within the dental plaque. However, as bacterial counts increase, so does the oral neutrophils count which enhance their activity (Khoury et al., 2020). Any deviation from PMN’s normal production, recruitment, function, or activity can lead to damage in periodontal tissues, and consequently tooth loss. (Prepared using Biorender.com).

Figure 2.

A simplified diagram showing the potential mechanism explaining the impact of periodontal disease on breast milk composition. Maternal diseases/infections (such as diabetes, mastitis, and atopy) can affect the composition of breast milk. Periodontal diseases have been reported to in the literature to be associated with adverse pregnancy outcomes, including preeclampsia, preterm birth, and low birth weight. Potential biological pathways through which periodontal diseases can negatively affect breast milk composition include the systemic dissemination of inflammatory cytokines like IL-1, IL-6, PGE2, and TNF-β in the blood circulation that can be up-regulated by bacterial by-products. Based on results from this review, it can be hypothesized that milk from mothers with periodontal diseases might have low fat content, high levels of inflammatory mediators and fatty acids, changes in levels of immunoglobulins, and higher risk of bacterial dysbiosis, compared to milk from mothers with good periodontal health. (Prepared using Biorender.com).

Figure 3.

A simplified diagram showing the modulation of infant gut microbiota via breast milk microbiome. Infants receive various bacterial communities from breast milk which plays a major role in the development and maturation of the infants’ gut microbiome. Breast milk microbiome shapes the neonate’s intestinal maturation. Infants with mature intestine will have high bacterial diversity in their gut (i.e., low risk of bacterial dysbiosis) which protects them from later infections/diseases and is essential for the infants’ growth/development and optimal health. On the other hand, infants with immature intestine, will have low bacterial diversity in their gut (i.e., high risk of bacterial dysbiosis) which increases the infants’ susceptibility to later disease. (Prepared using Biorender.com).