Abstract
Objectives
The purpose of this review was to provide a novel perspective utilizing an assessment of biomarkers to evaluate the impact of stress-related disorders on the progression of periodontal disease and evaluate the growing body of evidence of stress as a risk indicator for periodontal disease progression.
Methods
Cross-sectional, case-control, and biomarker studies associating psychological disorders and periodontal disease were included in the literature search. Computational studies, animal studies, reviews, and studies lacking healthy controls were excluded. Electronic and manual literature searches were conducted by two independent reviewers in several databases as well as a manual search for relevant articles published up to January 2018.
Results
Twenty-six articles fulfilled the inclusion criteria and were included in the qualitative synthesis. Relationships between stress-related disorders and serum and salivary biomarkers such as cortisol, dehydroepiandrosterone (DHEA), chromogranin A (CgA), and pro-inflammatory cytokines were identified.
Conclusions
The use of salivary pro-inflammatory cytokines alone is not sufficient for the identification of periodontal disease severity/progression with or without the presence of stress-associated diseases. Keeping in mind the limitations of this review, a positive qualitative correlation was observed in the literature among stress-related biomarkers and the severity of periodontal disease. This correlation may serve as an important reporter of patient susceptibility for periodontal breakdown in the future.
Clinical relevance
Stress-related disorders should be included in the list of globally screened diseases because it can change the biochemistry of both the local periodontal microenvironment as well as the global systemic inflammatory burden.
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References
Denes A, Boldogkoi Z, Uhereczky G et al (2005) Central autonomic control of the bone marrow: multisynaptic tract tracing by recombinant pseudorabies virus. Neuroscience 134(3):947–963
Corr A, Smith J, Baldock P (2017) Neuronal control of bone remodeling. Toxicol Pathol 45(7):894–903
Stein DJ, Naudé PJ, Berk M (2018) Stress, depression, and inflammation: molecular and microglial mechanisms. Biol Psychiatry 83(1):5–6
Genco RJ, Borgnakke WS (2013) Risk factors for periodontal disease. Periodontol 62(1):59–94
Stone PW (2002) Popping the (PICO) question in research and evidence-based practice. Appl Nurs Res 15(3):197–198
Shamseer L, Moher D, Clarke M et al (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 350:g7647
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 62(10):1006–1012
Jaiswal R, Shenoy N, Thomas B (2016) Evaluation of association between psychological stress and serum cortisol levels in patients with chronic periodontitis-estimation of relationship between psychological stress and periodontal status. J Indian Soc Periodontol 20(4):381–385
Fenol A, Jebi S, Krishnan S, Perayil J, Vyloppillil R, Bhaskar A, Menon SM, Mohandas A (2017) Association of stress, salivary cortisol level, and periodontitis among the inmates of a central prison in Kerala. Dent Res J (Isfahan) 14(4):288–292
Mesa F, Magan-Fernandez A, Munoz R et al (2014) Catecholamine metabolites in urine, as chronic stress biomarkers, are associated with higher risk of chronic periodontitis in adults. J Periodontol 85(12):1755–1762
Refulio Z, Rocafuerte M, de la Rosa M, Mendoza G, Chambrone L (2013) Association among stress, salivary cortisol levels, and chronic periodontitis. J Periodontal Implant Sci 43(2):96–100
Mannem S, Chava VK (2012) The effect of stress on periodontitis: A clinicobiochemical study. J Indian Soc Periodontol 16(3):365–369
Seraphim AP, Chiba FY, Pereira RF, Mattera MS, Moimaz SA, Sumida DH (2016) Relationship among periodontal disease, insulin resistance, salivary cortisol, and stress levels during pregnancy. Braz Dent J 27(2):123–127
Haririan H, Andrukhov O, Bottcher M et al (2017) Salivary neuropeptides, stress and periodontitis. J Periodontol:1–15
Aurer A, Aurer-Kozelj J, Stavljenic-Rukavina A et al (1999) Inflammatory mediators in saliva of patients with rapidly progressive periodontitis during war stress induced incidence increase. Coll Antropol 23(1):117–124
Giannopoulou C, Kamma JJ, Mombelli A (2003) Effect of inflammation, smoking and stress on gingival crevicular fluid cytokine level. J Clin Periodontol 30(2):145–153
Kamma JJ, Giannopoulou C, Vasdekis VG, Mombelli A (2004) Cytokine profile in gingival crevicular fluid of aggressive periodontitis: influence of smoking and stress. J Clin Periodontol 31(10):894–902
Mengel R, Bacher M, Flores-De-Jacoby L (2002) Interactions between stress, interleukin-1beta, interleukin-6 and cortisol in periodontally diseased patients. J Clin Periodontol 29(11):1012–1022
Mousavijazi M, Naderan A, Ebrahimpoor M, Sadeghipoor M (2013) Association between psychological stress and stimulation of inflammatory responses in periodontal disease. J Dent (Tehran) 10(1):103–111
Cakmak O, Tasdemir Z, Aral CA, Dundar S, Koca HB (2016) Gingival crevicular fluid and saliva stress hormone levels in patients with chronic and aggressive periodontitis. J Clin Periodontol 43(12):1024–1031
Cakmak O, Alkan BA, Ozsoy S, Sen A, Abdulrezzak U (2014) Association of gingival crevicular fluid cortisol/dehydroepiandrosterone levels with periodontal status. J Periodontol 85(8):e287–e294
Reshma AP, Arunachalam R, Pillai JK, Kurra SB, Varkey VK, Prince MJ (2013) Chromogranin A: novel biomarker between periodontal disease and psychosocial stress. J Indian Soc Periodontol 17(2):214–218
Steer RA, Ranieri WF, Beck AT, Clark DA (1993) Further Evidence for the Validity of the Beck Anxiety Inventory with Psychiatric Outpatients. J Anxiety Disord 7(3):195–205
Beck AT, Erbaugh J, Ward CH, Mock J, Mendelsohn M (1961) An Inventory for Measuring Depression. Arch Gen Psychiatry 4(6):561–&
Beck AT, Weissman A, Lester D, Trexler L (1974) The measurement of pessimism: the hopelessness scale. J Consult Clin Psychol 42(6):861–865
Spielberger CD, Gorsuch RL, Lushene RE (1970) Manual for the state-trait anxiety inventory. Consulting Psychologists Press, Paolo Alto
Savoia MG (1995) Relação entre eventos vitais adversos e mecanismos de “coping” no transtorno de pânico. Universidade de São Paulo, São Paulo
Harding TW, de Arango MV, Baltazar J, Climent CE, Ibrahim HH, Ladrido-Ignacio L, Murthy RS, Wig NN (1980) Mental disorders in primary health care: a study of their frequency and diagnosis in four developing countries. Psychol Med 10(2):231–241
Lipp MEN, Guevara AJH (1994) Validação empírica do Inventário de Sintomas de Stress (ISS). Estud Psicol 11:43–49
Holmes TH, Rahe RH (1967) The Social Readjustment Rating Scale. J Psychosom Res 11(2):213–218
Janke W, Erdmann G, W K (1985) The Stress Coping Questionnaire (SVF) Manual. Verlag für Psychologie, Dr. CJ Hogrefe, Göttingen, pp 7–30
Russell D, Peplau LA, Cutrona CE (1980) The revised UCLA Loneliness Scale: concurrent and discriminant validity evidence. J Pers Soc Psychol 39(3):472–480
Pearlin LI, Schooler C (1978) The structure of coping. J Health Soc Behav 19:2–21
Derogatis LR, Melisaratos N (1983) The Brief Symptom Inventory: an introductory report. Psychol Med 13(3):595–605
Carver CS, Scheier MF, Weintraub JK (1989) Assessing coping strategies—a theoretically based approach. J Pers Soc Psychol 56(2):267–283
Hilgert J, Hugo F, Bandeira D, Bozzetti M (2006) Stress, cortisol, and periodontitis in a population aged 50 years and over. J Dent Res 85(4):324–328
Katuri KK, Dasari AB, Kurapati S, Vinnakota NR, Bollepalli AC, Dhulipalla R (2016) Association of yoga practice and serum cortisol levels in chronic periodontitis patients with stress-related anxiety and depression. J Int Soc Prev Commun Dentistry 6(1):7–14
Canalis E, Mazziotti G, Giustina A, Bilezikian J (2007)Glucocorticoid-induced osteoporosis: pathophysiology and therapy. Osteoporos Int 18(10):1319–1328
Briot K, Roux C (2015)Glucocorticoid-induced osteoporosis. RMD Open 1(1):e000014
Chiodini I, Mascia ML, Muscarella S, Battista C, Minisola S, Arosio M, Santini SA, Guglielmi G, Carnevale V, Scillitani A (2007) Subclinical hypercortisolism among outpatients referred for osteoporosis. Ann Intern Med 147(8):541–548
Dennison E, Hindmarsh P, Fall C, Kellingray S, Barker D, Phillips D, Cooper C (1999) Profiles of endogenous circulating cortisol and bone mineral density in healthy elderly men. J Clin Endocrinol Metab 84(9):3058–3063
Canalis E, Giustina A (2001)Glucocorticoid-induced osteoporosis: summary of a workshop. J Clin Endocrinol Metab 86(12):5681–5685
Westendorf JJ, Kahler RA, Schroeder TM (2004) Wnt signaling in osteoblasts and bone diseases. Gene 341:19–39
Lane NE, Yao W, Balooch M, Nalla RK, Balooch G, Habelitz S, Kinney JH, Bonewald LF (2006)Glucocorticoid-treated mice have localized changes in trabecular bone material properties and osteocyte lacunar size that are not observed in placebo-treated or estrogen-deficient mice. J Bone Miner Res 21(3):466–476
Yao W, Cheng Z, Busse C et al (2008) Glucocorticoid excess in mice results in early activation of osteoclastogenesis and adipogenesis and prolonged suppression of osteogenesis: a longitudinal study of gene expression in bone tissue from glucocorticoid-treated mice. Arthritis Rheum Off J Am Coll Rheumatol 58(6):1674–1686
Kondo T, Kitazawa R, Yamaguchi A, Kitazawa S (2008) Dexamethasone promotes osteoclastogenesis by inhibiting osteoprotegerin through multiple levels. J Cell Biochem 103(1):335–345
Canalis E, Giustina A, Bilezikian JP (2007) Mechanisms of anabolic therapies for osteoporosis. N Engl J Med 357(9):905–916
Duran-Pinedo AE, Solbiati J, Frias-Lopez J (2018) The effect of the stress hormone cortisol on the metatranscriptome of the oral microbiome. Npj Biofilms Microbiomes 4(1):25
Ishisaka A, Ansai T, Soh I, Inenaga K, Yoshida A, Shigeyama C, Awano S, Hamasaki T, Sonoki K, Takata Y, Takehara T (2007) Association of salivary levels of cortisol and dehydroepiandrosterone with periodontitis in older Japanese adults. J Periodontol 78(9):1767–1773
Assies J, Visser I, Nicolson NA et al (2004) Elevated salivary dehydroepiandrosterone-sulfate but normal cortisol levels in medicated depressed patients: preliminary findings. Psychiatry Res 128(2):117–122
Fabian TJ, Dew MA, Pollock BG, Reynolds CF 3rd, Mulsant BH, Butters MA, Zmuda MD, Linares AM, Trottini M, Kroboth PD (2001) Endogenous concentrations of DHEA and DHEA-S decrease with remission of depression in older adults. Biol Psychiatry 50(10):767–774
Vittek J, Kirsch S, Rappaport S, Bergman M, Southren A (1984) Salivary concentrations of steroid hormones in males and in cycling and postmenopausal females with and without periodontitis. J Periodontal Res 19(5):545–555
Mandel ID (1990) The diagnostic uses of saliva. J Oral Pathol Med 19(3):119–125
Kaufman E, Lamster IB (2002) The diagnostic applications of saliva—a review. Crit Rev Oral Biol Med 13(2):197–212
Takuma T, Tanemura T, Hosoda S, Kumegawa M (1978) Effects of thyroxine and 5α-dihydrotesterone on the activities of various enzymes in the mouse submandibular gland. Biochim Biophys Acta Gen Subj 541(2):143–149
Hernandez M, Wenk E, Southren A, Rappaport S, Vittek J (1981) LOCALIZATION OF ANDROGENS-H-3 IN HUMAN GINGIVA BY AUTORADIOGRAPHY. Paper presented at: Journal of Dental Research
Franklin TC, Wohleb ES, Zhang Y, Fogaça M, Hare B, Duman RS (2018) Persistent increase in microglial RAGE contributes to chronic stress–induced priming of depressive-like behavior. Biol Psychiatry 83(1):50–60
Holmes SE, Hinz R, Conen S, Gregory CJ, Matthews JC, Anton-Rodriguez JM, Gerhard A, Talbot PS (2018) Elevated translocator protein in anterior cingulate in major depression and a role for inflammation in suicidal thinking: a positron emission tomography study. Biol Psychiatry 83(1):61–69
Jaedicke KM, Preshaw PM, Taylor JJ (2016) Salivary cytokines as biomarkers of periodontal diseases. Periodontol 70(1):164–183
Funding
This paper was partially supported by the University of Michigan Periodontal Graduate Student Research Fund. AMD is funded by the Tissue Engineering and Regenerative Medicine fellowship (5T32DE007057-42).
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Decker, A., Askar, H., Tattan, M. et al. The assessment of stress, depression, and inflammation as a collective risk factor for periodontal diseases: a systematic review. Clin Oral Invest 24, 1–12 (2020). https://doi.org/10.1007/s00784-019-03089-3
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DOI: https://doi.org/10.1007/s00784-019-03089-3