Periodontal diseases and stress: A brief review

Journal of Oral Rehabilitation

Volumn 40, Issue 1, 2013, Pages 60-68

  Akcali, A ^a   Huck, O ^b   Tenenbaum, H ^b   Davideau, J L ^b   Buduneli, N ^a  

^a EGE UNIVERSITY   (Turkey)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Cortisol; Periodontal diseases; Psychological stress; Saliva

Indexed keywords

ALPHA AMYLASE SALIVA ISOENZYME; BIOLOGICAL MARKER; CATECHOLAMINE; CHROMOGRANIN A; HYDROCORTISONE; NEUROPEPTIDE;

CHEMISTRY; DISEASE PREDISPOSITION; HUMAN; IMMUNOLOGY; MENTAL STRESS; MICROBIOLOGY; MOUTH MUCOSA; PERIODONTAL DISEASE; PSYCHOLOGICAL ASPECT; REVIEW; RISK FACTOR; SALIVA;

BIOLOGICAL MARKERS; CATECHOLAMINES; CHROMOGRANIN A; DISEASE SUSCEPTIBILITY; HUMANS; HYDROCORTISONE; MOUTH MUCOSA; NEUROPEPTIDES; PERIODONTAL DISEASES; RISK FACTORS; SALIVA; SALIVARY ALPHA-AMYLASES; STRESS, PSYCHOLOGICAL;

EID: 84870922386     PISSN: 0305182X     EISSN: 13652842     Source Type: Journal    
DOI: 10.1111/j.1365-2842.2012.02341.x     Document Type: Review

References (91)

1. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;19:1809-1820.
2. Castillo DM, Sánchez-Beltrán MC, Castellanos JE, Sanz I, Mayorga-Fayad I, Sanz M, Lafaurie GI. Detection of specific periodontal microorganisms from bacteraemia samples after periodontal therapy using molecular-based diagnostics. J Clin Periodontol. 2011;38:418-427.
3. Curtis MA, Slaney JM, Aduse-Opoku J. Critical pathways in microbial virulence. J Clin Periodontol. 2005;32:28-38.
4. Dahan M, Nawrocki B, Elkaïm R et al. Expression of matrix metalloproteinases in healthy and diseased human gingiva. J Clin Periodontol. 2001;28:128-136.
5. Van Dyke TE, Kornman KS. Inflammation and factors that may regulate inflammatory response. Review. J Clin Periodontol. 2008;79:1503-1507.
6. Kiecolt-Glaser JK, Preacher KJ, MacCallum RC, Atkinson C, Malarkey WB, Glaser R. Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proc Natl Acad Sci USA. 2003;100:9090-9095.
7. Leininger M, Tenenbaum H, Davideau JL. Modified periodontal risk assessment score: long-term predictive value of treatment outcomes. A retrospective study. J Clin Periodontol. 2010;37:427-435.
8. Cronin AJ, Claffey N, Stassen LF. Who is at risk? Periodontal disease risk analysis made accessible for the general dental practitioner. Br Dent J. 2008;205:131-137.
9. Peruzzo DC, Benatti BB, Ambrosano GM et al. A systematic review of stress and psychological factors as possible risk factors for periodontal disease. J Periodontol. 2007;78:1491-1504.
10. Leresche L, Dworkin SF. The role of stress in inflammatory disease, including periodontal disease: review of concepts and current findings. Periodontol 2000. 2002;30:91-103.
11. Genco RJ, Ho AW, Grossi SG, Dunford RG, Tedesco LA. Relationship of stress, distress and inadequate coping behaviors to periodontal disease. J Periodontol. 1999;70:711-723.
12. Wimmer G, Janda M, Wieselmann-Penkner K, Jakse N, Polansky R, Pertl C. Coping with stress: its influence on periodontal disease. J Periodontol. 2002;73:1343-1351.
13. Deinzer R, Hilpert D, Bach K, Schawacht M, Herforth A. Effects of academic stress on oral hygiene-a potential link between stress and plaque-associated disease? J Clin Periodontol. 2001;28:459-464.
14. Johannsen A, Bjurshammar N, Gustafsson A. The influence of academic stress on gingival inflammation. Int J Dent Hyg. 2010;8:22-27.
15. Hilgert JB, Hugo FN, Bandeira DR, Bozzetti MC. Stress, cortisol, and periodontitis in a population aged 50 years and over. J Dent Res. 2006;85:324-328.
16. Rai B, Kaur J, Anand SC, Jacobs R. Salivary stress markers, stress, and periodontitis: a pilot study. J Periodontol. 2011;82:287-292.
17. Goyal S, Jajoo S, Nagappa G, Rao G. Estimation of relationship between psychosocial stress and periodontal status using serum cortisol level: a clinico-biochemical study. Indian J Dent Res. 2011;22:6-9.
18. Koolhaas JM, Bartolomucci A, Buwalda B et al. Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev. 2011;35:1291-1301.
19. Dhabbar FS. Stress-induced augmentation of immune function-The role of stress hormones, leukocyte trafficking, and cytokines. Brain Behav Immun. 2002;16:785-798.
20. Culshaw S, Mcinnes IB, Liew FY. What can the periodontal community learn from the pathophysiology of rheumatoid arthritis? J Clin Periodontol. 2011;38:106-113.
21. Chida Y, Hamer M. An association of adverse psychosocial factors with diabetes mellitus: a meta-analytic review of longitudinal cohort studies. Diabetologia. 2008;51:2168-2178.
22. Backé EM, Seidler A, Latza U, Rossnagel K, Schumann B. The role of psychosocial stress at work for the development of cardiovascular diseases: a systematic review. Int Arch Occup Environ Health. 2012;85:67-79.
23. Stabholz A, Soskolne WA, Shapira L. Genetic and environmental risk factors for chronic periodontitis and aggressive periodontitis. Periodontol 2000. 2010;53:138-153.
24. Tsigos C, Chrousos GP. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res. 2002;53:865-871.
25. Sanders VM, Straub RH. Norepinephrine, the beta-adrenergic receptor, and i{dotless}mmunity: review. Brain Behav Immun. 2002;16:290-332.
26. Hamaguchi T, Fukudo S, Kanazawa M, Tomiie T, Shimizu K, Oyama M et al. Changes in salivary physiological stress markers induced by muscle stretching in patients with irritable bowel syndrome. Biopsychosoc Med. 2008;4:2-20.
27. Helle KB. Regulatory peptides from chromogranin A and secretogranin II. Cell Mol Neurobiol. 2010;30:1145-1146.
28. Rosenkranz MA. Substance P at the nexus of mind and body in chronic inflammation and affective disorders. Psychol Bull. 2007;133:1007-1037.
29. Lima DP, Diniz DG, Moimaz SA, Sumida DH, Okamoto AC. Saliva: reflection of the body. Int J Infect Dis. 2010;14:184-188.
30. Papacosta E, Nassis GP. Saliva as a tool for monitoring steroid, peptide and immune markers in sport and exercise science. J Sci Med Sport. 2011;14:424-434.
31. Rohleder N, Nater UM. Determinants of salivary a-amylase in humans and methodological considerations: review. Psychoneuroendocrinology. 2009;34:469-485.
32. Lundy FT, Linden GJ. Neuropeptides and neurogenic mechanisms in oral and periodontal inflammation. Crit Rev Oral Biol Med. 2004;15:82-98.
33. Stanford TW, Rees TD. Acquired immune suppression and other risk factors/indicators for periodontal disease progression. Periodontol 2000. 2003;32:118-135.
34. Ishisaka A, Ansai T, Soh I, Inenaga K, Awano S, Yoshida A et al. Association of cortisol and dehydroepiandrosterone sulphate levels in serum with periodontal status in older Japanese adults. J Clin Periodontol. 2008;35:853-861.
35. Buduneli N, Özçaka Ö, Nalbantsoy A. Salivary and plasma levels of Toll-like receptor 2 and Toll-like receptor 4 in chronic periodontitis. J Periodontol. 2011;82:878-884.
36. Lyte M. Microbial endocrinology and infectious disease in the 21st century. Trends Microbiol. 2004;12:14-20.
37. Kemeny ME, Schedlowski M. Understanding the interaction between psychosocial stress and immune-related diseases: a stepwise progression. Brain Behav Immun. 2007;21:1009-1118.
38. Pani SC, Al Askar AM, Al Mohrij SI, Al Ohali TA. Evaluation of stress in final-year Saudi dental students using salivary cortisol as a biomarker. J Dent Educ. 2011;75:377-384.
39. Poll EM, Kreitschmann-Andermahr I, Langejuergen Y, Stanzel S, Gilsbach JM, Gressner A et al. Saliva collection method affects predictability of serum cortisol. Clin Chim Acta. 2007;382:15-19.
40. Levine A, Zagoory-Sharon O, Feldman R, Lewis JG, Weller A. Measuring cortisol in human psychobiological studies. Physiol Behav. 2007;30:43-53.
41. Dickerson SS, Kemeny ME. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull. 2004;130:355-391.
42. Gatti R, Antonelli G, Prearo M, Spinella P, Cappellin E, De Palo EF. Cortisol assays and diagnostic laboratory procedures in human biological fluids. Clin Biochem. 2009;42:1205-1217.
43. Groer M, Murphy R, Bunnell W, Salomon K, Van Eepoel J, Rankin B et al. Salivary measures of stress and immunity in police officers engaged in simulated critical incident scenarios. J Occup Environ Med. 2010;52:595-602.
44. Taylor CB, Conrad A, Wilhelm FH, Neri E, Delorenzo A, Kramer MA et al. Psychophysiological and cortisol responses to psychological stress in depressed and nondepressed older men and women with elevated cardiovascular disease risk. Psychosom Med. 2006;68:538-546.
45. Kunz-Ebrecht SR, Mohamed-Ali V, Feldman PJ, Kirschbaum C, Steptoe A. Cortisol responses to mild psychological stress are inversely associated with proinflammatory cytokines. Brain Behav Immun. 2003;17:373-383.
46. Webster Marketon JI, Glaser R. Stress hormones and immune function. Cell Immunol. 2008;252:16-26.
47. Hänsel A, Hong S, Cámara RJ, Von Känel R. Inflammation as a psychophysiological biomarker in chronic psychosocial stress. Neurosci Biobehav Rev. 2010;35:115-121.
48. Ben-Eliyahu S, Shakhar G, Page GG, Stefanski V, Shakhar K. Suppression of NK cell activity and of resistance to metastasis by stress: a role for adrenal catecholamines and beta-adrenoceptors. NeuroImmunoModulation. 2000;8:154-164.
49. Padgett DA, Glaser R. How stress influences the immune response. Trends Immunol. 2003;24:444-448.
50. Kennedy B, Dillon E, Mills PJ, Ziegler MG. Catecholamines in human saliva. Life Sci. 2001;25:87-99.
51. Takai N, Yamaguchi M, Aragaki T, Eto K, Uchihashi K, Nishikawa Y. Effect of psychological stress on the salivary cortisol and amylase levels in healthy young adults. Arch Oral Biol. 2004;49:963-968.
52. Nakane H, Asami O, Yamada Y, Ohira H. Effect of negative air ions on computer operation, anxiety and salivary chromogranin A-like immunoreactivity. Int J Psychophysiol. 2002;46:85-89.
53. Saruta J, Tsukinoki K, Sasaguri K, Ishii H, Yasuda M, Osamura YR et al. Expression and localization of chromogranin A gene and protein in human submandibular gland. Cells Tissues Organs. 2005;180:237-244.
54. Cury PR, Canavez F, De Araujo VC, Furuse C, De Araujo NS. Substance P regulates the expression of matrix metalloproteinases and tissue inhibitors of metalloproteinase in cultured human gingival fibroblasts. J Periodontal Res. 2008;43:255-260.
55. Sánchez GA, Miozza V, Delgado A, Busch L. Determination of salivary levels of mucin and amylase in chronic periodontitis patients. J Periodontal Res. 2011;46:221-227.
56. Kabashima H, Nagata K, Maeda K, Lijima T. Involvement of substance P, mast cells, TNF-alpha and ICAM-1 in the infiltration of inflammatory cells in human periapical granulomas. J Oral Pathol Med. 2002;31:175-180.
57. Pradeep AR, Raj S, Aruna G, Chowdhry S. Gingival crevicular fluid and plasma levels of neuropeptide Substance-P in periodontal health, disease and after nonsurgical therapy. J Periodontal Res. 2009;44:232-237.
58. Miller DB, O'callaghan JP. Neuroendocrine aspects of the response to stress. Metabolism. 2002;51:5-10.
59. Soell M, Elkaim R, Tenenbaum H. Cathepsin C, matrix metalloproteinases, and their tissue inhibitors in gingiva and gingival crevicular fluid from periodontitis-affected patients. J Dent Res. 2002;81:174-178.
60. Buduneli N, Biyikoǧlu B, Sherrabeh S, Lappin DF. Saliva concentrations of RANKL and osteoprotegerin in smoker versus non-smoker chronic periodontitis patients. J Clin Periodontol. 2008;35:846-852.
61. Sheiham A, Nicolau B. Evaluation of social and psychological factors in periodontal disease. Periodontol 2000. 2005;39:118-131.
62. Ishisaka A, Ansai T, Soh I, Inenaga K, Yoshida A, Shigeyama C et al. Association of salivary levels of cortisol and dehydroepiandrosterone with periodontitis in older Japanese adults. J Periodontol. 2007;78:1767-1773.
63. Turnbull AV, Rivier CL. Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol Rev. 1999;79:1-71.
64. Baker DG, Ekhator NN, Kasckow JW, Hill KK, Zoumakis E, Dashevsky BA et al. Plasma and cerebrospinal fluid interleukin-6 concentrations in posttraumatic stress disorder. NeuroImmunoModulation. 2001;9:209-217.
65. Furugen R, Hayashida H, Yamaguchi N, Yoshihara A, Ogawa H, Miyazaki H et al. The relationship between periodontal condition and serum levels of resistin and adiponectin in elderly Japanese. J Periodontal Res. 2008;43:556-562.
66. Johannsen A, Rydmark I, Söder B, Asberg M. Gingival inflammation, increased periodontal pocket depth and elevated interleukin-6 in gingival crevicular fluid of depressed women on long-term sick leave. J Periodontal Res. 2007;42:546-552.
67. Ulkar B, Elgun S, Ozmeric N, Ozdemir B, Boynueǧri D. Periodontal nitric oxide pathway alteration due to precompetition anxiety in handball players. J Periodontol. 2012;83:204-210.
68. Giannopoulou C, Kamma JJ, Mombelli A. Effect of inflammation, smoking and stress on gingival crevicular fluid cytokine level. J Clin Periodontol. 2003;30:145-153.
69. Kamma JJ, Giannopoulou C, Vasdekis VG, Mombelli A. Cytokine profile in gingival crevicular fluid of aggressive periodontitis: influence of smoking and stress. J Clin Periodontol. 2004;31:894-902.
70. Mengel R, Bacher M, Flores-De-Jacoby L. Interactions between stress, interleukin-1beta, interleukin-6 and cortisol in periodontally diseased patients. J Clin Periodontol. 2002;29:1012-1022.
71. Soeda R, Tasaka A, Sakurai K. Influence of chewing force on salivary stress markers as indicator of mental stress. J Oral Rehabil. 2012;39:261-269.
72. Shapira L, Houri-Haddad Y, Frolov I, Halabi A, Ben-Nathan D. The effect of stress on the inflammatory response to Porphyromonas gingivalis in a mouse subcutaneous chamber model. J Periodontol. 1999;70:289-293.
73. Houri-Haddad Y, Itzchaki O, Ben-Nathan D, Shapira L. The effect of chronic emotional stress on the humoral immune response to Porphyromonas gingivalis in mice. J Periodontal Res. 2003;38:204-209.
74. Takada T, Yoshinari N, Sugiishi S, Kawase H, Yamane T, Noguchi T. Effect of restraint stress on the progression of experimental periodontitis in rats. J Periodontol. 2004;75:306-315.
75. Kim Y, Hamada N, Takahashi Y, Sasaguri K, Tsukinoki K, Onozuka M et al. Cervical sympathectomy causes alveolar bone loss in an experimental rat model. J Periodontal Res. 2009;44:695-703.
76. Huang S, Lu F, Zhang Z, Yang X, Chen Y. The role of psychologic stress-induced hypoxia-inducible factor-1α in rat experimental periodontitis. J Periodontol. 2011;82:934-941.
77. Semenoff-Segundo A, Porto AN, Semenoff TA, Cortelli JR, Costa FO, Cortelli SC et al. Effects of two chronic stress models on ligature-induced periodontitis in Wistar rats. Arch Oral Biol. 2012;57:66-72.
78. Shapira L, Frolov I. Experimental stress suppresses recruitment of macrophages but enhanced their P. gingivalis LPS-stimulated secretion of nitric oxide. J Periodontol. 2007;71:476-481.
79. Menezes AR, Lavie CJ, Milani RV, O'Keefe J, Lavie TJ. Psychological risk factors and cardiovascular disease: is it all in your head? Postgrad Med. 2011;123:165-176.
80. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2000. 2005;38:135-187.
81. Lyte M. The role of microbial endocrinology in infectious disease. J Endocrinol. 1993;137:343-345.
82. Roberts A, Matthews JB, Socransky SS, Freestone PP, Williams PH, Chapple IL. Stress and the periodontal diseases: effects of catecholamines on the growth of periodontal bacteria in vitro. Oral Microbiol Immunol. 2002;17:296-303.
83. Saito T, Inagaki S, Sakurai K, Okuda K, Ishihara K. Exposure of P. gingivalis to noradrenaline reduces bacterial growth and elevates ArgX protease activity. Arch Oral Biol. 2011;56:244-250.
84. Hardie KR, Heurlier K. Establishing bacterial communities by 'word of mouth': LuxS and autoinducer 2 in biofilm development. Nat Rev Microbiol. 2008;8:635-643.
85. Roberts A, Matthews JB, Socransky SS, Freestone PP, Williams PH, Chapple IL. Stress and the periodontal diseases: growth responses of periodontal bacteria to Escherichia coli stress-associated autoinducer and exogenous Fe. Oral Microbiol Immunol. 2005;20:147-153.
86. Iacopino AM. Relationship between stress, depression and periodontal disease. J Can Dent Assoc. 2009;75:329-330.
87. Kamma JJ, Baehni PC. Five-year maintenance follow-up of early-onset periodontitis patients. J Clin Periodontol. 2003;30:562-572.
88. Forde MD, Koka S, Eckert SE, Carr AB, Wong DT. Systemic assessments utilizing saliva: Part 1. General considerations and current assessments. Int J Prosthodont. 2006;19:43-52.
89. Wolff A, Ofer S, Raviv M, Helft M, Cardash HS. The flow rate of whole and submandibular/sublingual gland saliva in patients receiving replacement complete dentures. J Oral Rehabil. 2004;31:340-343.
90. Doepel M, Söderling E, Ekberg EL, Nilner M, Le Bell Y. Salivary cortisol and IgA levels in patients with myofascial pain treated with occlusal appliances in the short term. J Oral Rehabil. 2009;36:210-216.
91. Offenbacher S, Barros SP, Beck JD. Rethinking periodontal inflammation. Review. J Periodontol. 2008;79:1577-1584.