Exposure of Porphyromonas gingivalis to cortisol increases bacterial growth
Introduction
Periodontal diseases are inflammatory diseases of tooth supporting tissues induced by oral bacterial biofilms.1 Development of these diseases involves several bacterial species such as Porphyromonas gingivalis (P. gingivalis), Prevotella intermedia, Treponema denticola or Aggregatibacter actinomycetemcomitans within subgingival biofilm as well as host response.2 Several local, systemic and environmental risk factors such as oral hygiene, smoking, diabetes mellitus are known to affect subgingival biofilm's composition and increase the severity of periodontal destruction.3 Additionally, consequences of stress on lifestyle (less oral hygiene, high-fat diet) are indirect effects that could worsen different types of manifestations such as plaque accumulation and gingival inflammation.4 In a clinical study, academic stress was suggested to affect periodontal health, as shown by more plaque accumulation and more pronounced gingival inflammation during the examination period of students.5
In response to stressful events, several stress markers such as cortisol, catecholamines, chromogranin A, salivary alpha-amylase are released after the stimulation of central and autonomous nervous system.6 These stress markers are found in blood, saliva and gingival crevicular fluid (GCF) and may influence the inflammatory processes and development of periodontal diseases.7
Cortisol is one of the most extensively studied stress-related hormone. Cortisol is a glucocorticoid hormone and is secreted by the stimulation of hypothalamus-pituitary-adrenal (HPA) axis in response to psychological stress. Salivary level of cortisol reliably reflects HPA axis activity and is used as a biological marker of stress in human psychological studies.8 In a recent clinical study including individuals with salivary cortisol levels varying between 0.006 and 0.015 μg/mL depending on the severity of periodontitis and depression, it was suggested that a high salivary cortisol level may show an increased risk for chronic periodontitis.9 Interestingly, significant associations between serum cortisol levels and periodontitis severity characterized by increased pocket depth, clinical attachment loss and bleeding on probing10 but also increased secretion of pro-inflammatory cytokines particularly interleukin-6 (IL-6) has also been reported.11
Since the introduction of the microbial endocrinology concept,12 studies have focused on the effects of stress hormones on bacterial growth and virulence.13, 14 Analysis of the effect of catecholamines15 and cortisol16 on the growth of periodontal bacteria has demonstrated the direct role of stress hormones on bacterial growth in subgingival biofilm. Noradrenalin reduces growth of P. gingivalis and Aggregatibacter actinomycetemcomitans but increases growth of other species such as Eikenella corrodens.15 Although growth reduction of P. gingivalis occurred, it has been shown that cathecolamines induce bacterial phenotypic change and increase in vitro activity of virulence factors.17 Bacteria in dental plaque have been recognized as the primary etiological agents of periodontal diseases.1 The concept of microbial endocrinology12 was introduced several decades after this recognition and possible correlations between elevated hormone levels and composition of subgingival microbiota have received attention by the field of periodontology. Mechanisms involved in these interactions remain so far unclear. The aim of the present study was to investigate the effect of exposure to cortisol on P. gingivalis growth over time.
Section snippets
Bacterial strain
The P. gingivalis strain ATCC 33277 was purchased from ATCC and was cultivated under strict anaerobic conditions at 37 °C in Brain Heart infusion1 supplemented with hemin (5 μg ml−1) and menadione (1 μg ml−1) both from Sigma.
Influence of cortisol on bacterial growth
Prior to the growth test, P. gingivalis culture was evaluated by OD600 nm. First, a pilot study was conducted in order to determine the optimum hydrocortisone1 concentrations to be used. A total of 15 different hydrocortisone
Influence of cortisol on bacterial growth
First, we assessed the effect of cortisol on bacterial growth. P. gingivalis cultures were challenged by hydrocortisone at different concentrations. At 12-h, all the hydrocortisone concentrations tested (0.04–10 μg ml−1) resulted in an increase in the bacterial growth in comparison with the control. This increase was between 24% and 45% depending on the hydrocortisone concentration at this time. Hydrocortisone increased bacterial growth in a dose-independent manner (p = 0.967) (Fig. 1).
Effect of hydrocortisone on P. gingivalis growth decreases with time
The effect
Discussion
In the present study, we investigated possible effects of cortisol on the growth of P. gingivalis. The growth rate of P. gingivalis was significantly increased after addition of cortisol in the culture medium at 12 h and 24 h in a dose-independent manner. This finding suggests that stress-induced hormone cortisol may have a specific effect on the growth of P. gingivalis. Despite the increase in growth rate, HPLC experiments demonstrated that total amount of cortisol was stable at all time-points
Funding
This study has been support by author's institution.
Competing interests
None.
Ethical approval
Not required.
Author contributions
Aliye Akcali and Olivier Huck contributed to the design of the study, the experiments and manuscript writing. Nurcan Buduneli, Jean-Luc Davideau and Henri Tenenbaum contributed to the design of the study and the manuscript writing. Timur Köse performed statistical analysis.
Acknowledgement
The authors thank Dr. Cynthia Atindehou for her help in HPLC analysis.
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