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Stress as a Determinant of Saliva-Mediated Adherence and Coadherence of Oral and Nonoral Microorganisms

From Department of Dental Basic Sciences (J.A.B, M.T., K.N., E.C.I.V., A.V.N.A), Section Oral Biochemistry, Academic Centre for Dentistry Amsterdam, Amsterdam, The Netherlands; Department of Oral Biology (J.A.B), The Ohio State University, Columbus, Ohio; Faculty of Psychology, Department of Biological Psychology (E.J.C.D.G.), Vrije Universiteit, Amsterdam, The Netherlands.

Address reprint requests to: Jos A. Bosch, PhD, The Ohio State University, Department of Oral Biology, 4151 Postle hall, 305 West 12th Ave., Columbus, OH 43218. Email: bosch.18{at}osu.edu

Received for publication April 26, 2002; revision received January 23, 2003.

OBJECTIVE: The mucosal secretory proteins, such as the salivary proteins, play a key role in the acquisition and regulation of the mucosal microflora. Most notably, some microorganisms utilize the host’s secretory proteins to adhere to the mucosa; a first step in colonization and infection. The secretory proteins also influence colonization by affecting the binding among microorganisms, a process denoted as coadherence. Previously we reported that acute stressors cause specific changes in saliva composition. The present study investigated to what extent these changes influence saliva-mediated microbial adherence and coadherence (ex vivo).

METHODS: Thirty-two male undergraduates provided unstimulated saliva before and during a control condition and two stressors: A memory test and a surgery video presentation. We used saliva-coated microplates to test the adherence of bacteria for which the oral cavity is either a natural reservoir (eg, viridans streptococci) or a portal of entry (eg, Helicobacter pylori). We also tested the saliva-mediated co-adherence between Streptococcus gordonii and the yeast Candida albicans. Correlation analyses were performed to determine the relationships between changes in microbial adherence and the concentrations of potential salivary ligands, viz. cystatin S, the mucins MUC5B and MUC7, S-IgA, lactoferrin, -amylase, and total salivary protein.

RESULTS: During the memory test, saliva-mediated adhesion of Streptococcus sanguis, Streptococcus gordonii, and H. pylori increased, whereas the coadherence of C. albicans with S. gordonii decreased. During the surgical video presentation the saliva-mediated adherence of H. pylori, S. sanguis, and Streptococcus mitis increased. These changes were independent of salivary flow rate, but correlated with specific changes in salivary protein composition.

CONCLUSION: The results show that even moderate stressors, by altering the activity of the mucosal secretory glands, may affect microbial colonization processes such as adherence and coadherence. This study hereby presents a mechanism by which stress may affect the mucosal microflora and susceptibility to infectious disease.

Key Words: laboratory stressor, • oral health, • psychoneuroimmunology, • microbiology, • MG1, MG2.

Abbreviations: CHS = cleared human saliva;; DNA = deoxyribonucleic acid;; ELISA = enzyme-linked immunosorbent assay;; GEB = Gibbons & Etherden buffer;; MANOVA = multivariate analysis of variance;; OD = optical density;; PBS = phosphate-buffered saline;; S-IgA = secretory immunoglobulin A.