Changes in salivary microbiota increase volatile sulfur compounds production in healthy male subjects with academic-related chronic stress

Abstract

ObjectiveTo investigate the associations among salivary bacteria, oral emanations of volatile sulfur compounds, and academic-related chronic stress in healthy male subjects.Materials and methodsSeventy-eight healthy male undergraduate dental students were classified as stressed or not by evaluation of burnout, a syndrome attributed to academic-related chronic stress. This evaluation was carried out using the Maslach Burnout Inventory—Student Survey questionnaire. Oral emanations of hydrogen sulfide, methyl mercaptan, and dimethyl sulfide were measured using an Oral Chroma™ portable gas chromatograph. The amounts in saliva of total bacteria and seven bacteria associated with halitosis were quantified by qPCR. The in vitro production of H2S by S. moorei and/or F. nucleatum was also measured with the Oral Chroma™ instrument.ResultsThe stressed students group showed increased oral emanations of hydrogen sulfide and dimethyl sulfide, together with higher salivary Solobacterium moorei levels (p < 0.05, Mann Whitney test). There were moderate positive correlations between the following pairs of variables: Fusobacterium nucleatum and S. moorei; F. nucleatum and hydrogen sulfide; Tannerella forsythia and F. nucleatum; T. forsythia and S. moorei. These correlations only occurred for the stressed group (p < 0.05, Spearman correlation). The in vitro experiment demonstrated that S. moorei increased H2S production by F. nucleatum (p < 0.05, ANOVA and Tukey’s test).ConclusionThe increased amount of S. moorei in saliva, and its coexistence with F. nucleatum and T. forsythia, seemed to be responsible for increased oral hydrogen sulfide in the healthy male stressed subjects.

Stress‐related salivary proteins affect the production of volatile sulfur compounds by oral bacteria

“…In previous work, we found that coculturing of F. nucleatum and S. moorei produced higher H 2 S values than S. moorei or F. nucleatum grown individually (Nani et al., ). It can be concluded from the results obtained here and in our previous data that the two bacteria work together in the process leading to halitosis, with S. moorei probably deglycosylating mucin, which is then degraded by F. nucleatum, promoting the formation of VSCs (Sterer & Rosenberg, ).…”

“…Recently, we showed that healthy stressed male undergraduate students experiencing chronic academic stress presented increased oral H 2 S emanations, which were associated with increased salivary levels of S. moorei and its coexistence with F. nucleatum (Nani et al., ). The findings indicated that the altered saliva composition in chronically stressed subjects provided a more favorable environment for H 2 S production in the oral cavity.…”

“…Hydrogen sulfide (H 2 S), methyl mercaptan (CH 3 SH), and dimethyl sulfide ((CH 3 ) 2 S) are the main oral VSCs (Persson, Edlund, Claesson, & Carlsson, ; Van den Velde, van Steenberghe, Van Hee, & Quirynen, ). Several oral bacterial species are involved in VSC production, such as Porphyromonas gingivalis , Prevotella intermedia , Tannerella forsythia, Fusobacterium nucleatum, Solobacterium moorei (Kurata, Awano, Yoshida, Ansai, & Takehara, ; Nani et al., ; Vancauwenberghe et al., ) , among others.…”

“…Recently, we found that healthy male subjects under chronic academic stress produced higher levels of H 2 S, compared to subjects without stress, and that this phenomenon was associated with an increased amount of S. moorei in the saliva and the coexistence of this organism with F. nucleatum (Nani et al, 2017), leading to the design of this study. Therefore, to improve understanding of the relationship among stress, salivary proteins, and VSCs production, the aim of this study was to determine whether the production of VSCs by S. moorei and F. nucleatum was influenced by the stress-related substances alpha-amylase, beta-defensin-2, and mucin, and the sex hormones estradiol and progesterone.…”

Induction and inhibition of oral malodor

“…It was recently reported in research targeting healthy male dental students that chronic academic‐related stress increases the concentrations of H 2 S and CH 3 SCH 3 , and is associated with higher salivary S . moorei levels (Nani et al, ). Oral dryness and necrotic ulcers in patients with cell carcinoma of the oral cavity also cause oral malodor.…”