Is salivary alpha-amylase an indicator of autonomic nervous system dysregulations in mental disorders?-A review of preliminary findings and the interactions with cortisol

Psychoneuroendocrinology

Volumn 38, Issue 6, 2013, Pages 729-743

  Schumacher, Sarah ^a,b   Kirschbaum, Clemens ^c   Fydrich, Thomas ^b   Ströhle, Andreas ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Autonomic nervous system; Hypothalamus pituitary adrenal system; Mental disorders; Review; Salivary alpha amylase; Stress response

Indexed keywords

ALPHA AMYLASE SALIVA ISOENZYME; HYDROCORTISONE;

ADRENERGIC SYSTEM; ANXIETY DISORDER; AUTONOMIC NEUROPATHY; CLINICAL PROTOCOL; CLINICAL RESEARCH; DEPRESSION; DISEASE MARKER; EATING DISORDER; HUMAN; MENTAL DISEASE; NON INVASIVE PROCEDURE; NONHUMAN; PATHOLOGICAL GAMBLING; PERSONALITY DISORDER; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; STRESS; SYMPATHETIC TONE;

ALPHA-AMYLASES; AUTONOMIC NERVOUS SYSTEM DISEASES; BIOLOGICAL MARKERS; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MENTAL DISORDERS; PITUITARY-ADRENAL SYSTEM; SALIVA;

EID: 84877056338     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2013.02.003     Document Type: Review

References (81)

1. Adam E.K., Kumari M. Assessing salivary cortisol in large-scale, epidemiological research. Psychoneuroendocrinology 2009, 34:1423-1436.
2. Ali N., Pruessner J.C. The salivary alpha amylase over cortisol ratio as a marker to assess dysregulations of the stress systems. Physiol. Behav. 2012, 106:65-72.
3. Allwood M.A., Handwerger K., Kivlighan K.T., Granger D.A., Stroud L.R. Direct and moderating links of salivary alpha-amylase and cortisol stress-reactivity to youth behavioral and emotional adjustment. Biol. Psychol. 2011, 88:57-64.
4. Almela M., Hidalgo V., Villada C., van der Meij L., Espin L., Gomez-Amor J., Salvador A. Salivary alpha-amylase response to acute psychosocial stress: the impact of age. Biol. Psychol. 2011, 87:421-429.
5. Andor T., Gerlach A.L., Rist F. Superior perception of phasic physiological arousal and the detrimental consequences of the conviction to be aroused on worrying and metacognitions in GAD. J. Abnorm. Psychol. 2008, 117:193-205.
6. Bagley S.L., Weaver T.L., Buchanan T.W. Sex differences in physiological and affective responses to stress in remitted depression. Physiol. Behav. 2011, 104:180-186.
7. Bakvis P., Spinhoven P., Giltay E.J., Kuyk J., Edelbroek P.M., Zitman F.G., Roelofs K. Basal hypercortisolism and trauma in patients with psychogenic nonepileptic seizures. Epilepsia 2010, 51:752-759.
8. Balodis I.M., Wynne-Edwards K.E., Olmstead M.C. The other side of the curve: examining the relationship between pre-stressor physiological responses and stress reactivity. Psychoneuroendocrinology 2010, 35:1363-1373.
9. Bauer A.M., Quas J.A., Boyce W.T. Associations between physiological reactivity and children's behavior: advantages of a multisystem approach. J. Dev. Behav. Pediatr. 2002, 23:102-113.
10. Borkovec T.D., Lyonfields J.D., Wiser S.L., Deihl L. The role of worrisome thinking in the suppression of cardiovascular response to phobic imagery. Behav. Res. Ther. 1993, 31:321-324.
11. Bosch J.A., de Geus E.J.C., Veerman E.C.I., Hoogstraten J., Nieuw Amerongen A.V. Innate secretory immunity in response to laboratory stressors that evoke distinct patterns of cardiac autonomic activity. Psychosom. Med. 2003, 65:245-258.
12. Bosch J.A., Veerman E.C.I., de Geus E.J., Proctor G.B. α-Amylase as a reliable and convenient measure of sympathetic activity: do not start salivating just yet!. Psychoneuroendocrinology 2011, 36:449-453.
13. Carroll B.J., Cassidy F., Naftolowitz D., Tatham N.E., Wilson W.H., Iranmanesh A., Liu P.Y., Veldhuis J.D. Pathophysiology of hypercortisolism in depression. Acta Psychiatr. Scand. 2007, 115:90-103.
14. Chatterton R.T., Vogelsong K.M., Lu Y.C., Ellman A.B., Hudgens G.A. Salivary alpha-amylase as a measure of endogenous adrenergic activity. Clin. Physiol. 1996, 16:433-448.
15. Chida Y., Steptoe A. Cortisol awakening response and psychosocial factors: a systematic review and meta-analysis. Biol. Psychol. 2009, 80:265-278.
16. Chrousos G.P. Stress and disorders of the stress system. Nat. Rev. Endocrinol. 2009, 5:374-381.
17. Coupland N.J., Wilson S.J., Potokar J.P., Bell C., Nutt D.J. Increased sympathetic response to standing in panic disorder. Psychiatry Res. 2003, 118:69-79.
18. Ehlert U., Erni K., Hebisch G., Nater U. Salivary alpha-amylase levels after yohimbine challenge in healthy men. J. Clin. Endocrinol. Metab. 2006, 91:5130-5133.
19. El-Sheikh M., Erath S., Buckhalt J., Granger D., Mize J. Cortisol and children's adjustment: the moderating role of sympathetic nervous system activity. J. Abnorm. Child Psychol. 2008, 36:601-611.
20. Engert V., Vogel S., Efanov S.I., Duchesne A., Corbo V., Ali N., Pruessner J.C. Investigation into the cross-correlation of salivary cortisol and alpha-amylase responses to psychological stress. Psychoneuroendocrinology 2011, 36:1294-1302.
21. Fisher A.J., Granger D.A., Newman M.G. Sympathetic arousal moderates self-reported physiological arousal symptoms at baseline and physiological flexibility in response to a stressor in generalized anxiety disorder. Biol. Psychol. 2010, 83:191-200.
22. Foley P., Kirschbaum C. Human hypothalamus-pituitary-adrenal axis responses to acute psychosocial stress in laboratory settings. Neurosci. Biobehav. Rev. 2010, 35:91-96.
23. Frankenhaeuser M., Lundberg U., Forsman L. Dissociation between sympathetic-adrenal and pituitary-adrenal responses to an achievement situation characterized by high controllability: comparison between type A and type B males and females. Biol. Psychol. 1980, 10:79-91.
24. Gaul-Alacova P., Boucek J., Stejskal P., Kryl M., Pastucha P., Pavlik F. Assessment of the influence of exercise on heart rate variability in anxiety patients. Neuroendocrinol. Lett. 2005, 26:713-718.
25. Gillespie C.F., Nemeroff C.B. Hypercortisolemia and depression. Psychosom. Med. 2005, 67:S26-S28.
26. Gordis E.B., Granger D.A., Susman E.J., Trickett P.K. Asymmetry between salivary cortisol and alpha-amylase reactivity to stress: relation to aggressive behavior in adolescents. Psychoneuroendocrinology 2006, 31:976-987.
27. Gordis E.B., Granger D.A., Susman E.J., Trickett P.K. Salivary alpha amylase-cortisol asymmetry in maltreated youth. Horm. Behav. 2008, 53:96-103.
28. Granger D.A., Kivlighan K.T., Blair C., El-Sheikh M., Mize J., Lisonbee J.A., Buckhalt J.A., Stroud L.R., Handwerger K., Schwartz E.B. Integrating the measurement of salivary α-amylase into studies of child health, development, and social relationships. J. Soc. Pers. Relat. 2006, 23:267-290.
29. Granger D.A., Kivlighan K.T., El-Sheikh M., Gordis E.B., Stroud L.R. Salivary alpha-amylase in biobehavioral research: recent developments and applications. Ann. N.Y. Acad. Sci. 2007, 1098:122-144.
30. Grillon C., Duncko R., Covington M.F., Kopperman L., Kling M.A. Acute stress potentiates anxiety in humans. Biol. Psychiatry 2007, 62:1183-1186.
31. Guglielminotti J., Dehoux M., Mentré F., Bedairia E., Montravers P., Desmonts J.M., Longrois D. Assessment of salivary amylase as a stress biomarker in pregnant patients. Int. J. Obstet. Anesth. 2012, 21:35-39.
32. Humphrey S.P., Williamson R.T. A review of saliva: normal composition, flow, and function. J. Prosthet. Dent. 2001, 85:162-169.
33. Iizuka N., Awano S., Ansai T. Salivary alpha-amylase activity and stress in Japan air self-defense force cargo pilots involved in Iraq reconstruction. Am. J. Hum. Biol. 2012, 24(4):468-472.
34. Inagaki T., Miyaoka T., Okazaki S., Yasuda H., Kawamukai T., Utani E., Wake R., Hayashida M., Horiguchi J., Tsuji S. High salivary alpha-amylase levels in patients with schizophrenia: a pilot study. Prog. Neuropsychopharmacol. Biol. Psychiatry 2010, 34:688-691.
35. Ito T., Inoue Y., Sugihara T., Yamada H., Katayama S., Kawahara R. Autonomic function in the early stage of panic disorder: power spectral analysis of heart rate variability. Psychiatry Clin. Neurosci. 1999, 53:667-672.
36. Kang Y. Psychological stress-induced changes in salivary alpha-amylase and adrenergic activity. Nurs. Health Sci. 2010, 12:477-484.
37. Keller P.S., El-Sheikh M. Salivary alpha-amylase as a longitudinal predictor of children's externalizing symptoms: respiratory sinus arrhythmia as a moderator of effects. Psychoneuroendocrinology 2009, 34:633-643.
38. Kirschbaum C., Hellhammer D.H. Salivary cortisol in psychobiological research: an overview. Neuropsychobiology 1989, 22:150-169.
39. Kirschbaum C., Hellhammer D.H. Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 1994, 19:313-333.
40. Kirschbaum C., Hellhammer D.H. Salivary cortisol. Encyclopedia of Stress 2000, 424-429. Academic Press, San Diego. G. Fink (Ed.).
41. Kirschbaum C., Pirke K.M., Hellhammer D.H. The 'Trier Social Stress Test' - a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 1993, 28:76-81.
42. Kop W.J., Stein P.K., Tracy R.P., Barzilay J.I., Schulz R., Gottdiener J.S. Autonomic nervous system dysfunction and inflammation contribute to the increased cardiovascular mortality risk associated with depression. Psychosom. Med. 2010, 72:626-635.
43. Labudda K., Wolf O.T., Markowitsch H.J., Brand M. Decision-making and neuroendocrine responses in pathological gamblers. Psychiatry Res. 2007, 153:233-243.
44. Lord C., Hall G., Soares C.N., Steiner M. Physiological stress response in postpartum women with obsessive-compulsive disorder: a pilot study. Psychoneuroendocrinology 2011, 36:133-138.
45. Lundberg U., Frankenhaeuser M. Pituitary-adrenal and sympathetic-adrenal correlates of distress and effort. J. Psychosom. Res. 1980, 24:125-130.
46. McGirr A., Diaconu G., Berlim M.T., Pruessner J.C., Sable R., Cabot S., Turecki G. Dysregulation of the sympathetic nervous system, hypothalamic-pituitary-adrenal axis and executive function in individuals at risk for suicide. J. Psychiatry Neurosci. 2010, 35:399-408.
47. Meyerbroeker K., Powers M.B., van Stegeren A., Emmelkamp P.M.G. Does yohimbine hydrochloride facilitate fear extinction in virtual reality treatment of fear of flying? A randomized placebo-controlled trial. Psychother. Psychosom. 2012, 81:29-37.
48. Monteleone P., Scognamiglio P., Canestrelli B., Serino I., Monteleone A.M., Maj M. Asymmetry of salivary cortisol and a-amylase responses to psychosocial stress in anorexia nervosa but not in bulimia nervosa. Psychol. Med. 2011, 41:1963-1969.
49. Monteleone P., Scognamiglio P., Monteleone A.M., Mastromo D., Steardo L., Serino I., Maj M. Abnormal diurnal patterns of salivary alpha-amylase and cortisol secretion in acute patients with anorexia nervosa. World J. Biol. Psychiatry 2011, 12:455-461.
50. Nater U.M., Bohus M., Abbruzzese E., Ditzen B., Gaab J., Kleindienst N., Ebner-Priemer U., Mauchnik J., Ehlert U. Increased psychological and attenuated cortisol and alpha-amylase responses to acute psychosocial stress in female patients with borderline personality disorder. Psychoneuroendocrinology 2010, 35:1565-1572.
51. Nater U.M., La Marca R., Florin L., Moses A., Langhans W., Koller M.M., Ehlert U. Stress-induced changes in human salivary alpha-amylase activity - associations with adrenergic activity. Psychoneuroendocrinology 2006, 31:49-58.
52. Nater U.M., Rohleder N. Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: current state of research. Psychoneuroendocrinology 2009, 34:486-496.
53. Nater U.M., Rohleder N., Gaab J., Berger S., Jud A., Kirschbaum C., Ehlert U. Human salivary alpha-amylase reactivity in a psychosocial stress paradigm. Int. J. Psychophysiol. 2005, 55:333-342.
54. Nater U.M., Rohleder N., Schlotz W., Ehlert U., Kirschbaum C. Determinants of the diurnal course of salivary alpha-amylase. Psychoneuroendocrinology 2007, 32:392-401.
55. Noto Y., Sato T., Kudo M., Kurata K., Hirota K. The relationship between salivary biomarkers and state-trait anxiety inventory score under mental arithmetic stress: a pilot study. Anesth. Analg. 2005, 101:1873-1876.
56. Pruessner J.C., Wolf O.T., Hellhammer D.H., Buske-Kirschbaum A., von Auer K., Jobst S., Kaspers F., Kirschbaum C. Free cortisol levels after awakening: a reliable biological marker for the assessment of adrenocortical activity. Life Sci. 1997, 61:2539-2549.
57. Robles T.F., Shetty V., Zigler C.M., Glover D.A., Elashoff D., Murphy D., Yamaguchi M. The feasibility of ambulatory biosensor measurement of salivary alpha amylase: relationships with self-reported and naturalistic psychological stress. Biol. Psychol. 2011, 86:50-56.
58. Rohleder N., Chen E., Wolf J.M., Miller G.E. The psychobiology of trait shame in young women: extending the social self preservation theory. Health Psychol. 2008, 27:523-532.
59. Rohleder N., Nater U.M. Determinants of salivary alpha-amylase in humans and methodological considerations. Psychoneuroendocrinology 2009, 34:469-485.
60. Rohleder N., Nater U.M., Wolf J.M., Ehlert U., Kirschbaum C. Psychosocial stress-induced activation of salivary alpha-amylase: an indicator of sympathetic activity?. Ann. N.Y. Acad. Sci. 2004, 1032:258-263.
61. Rohleder N., Wolf J.M., Maldonado E.F., Kirschbaum C. The psychosocial stress-induced increase in salivary alpha-amylase is independent of saliva flow rate. Psychophysiology 2006, 43:645-652.
62. Southwick S.M., Bremner J.D., Rasmusson A., Morgan Iii C.A., Arnsten A., Charney D.S. Role of norepinephrine in the pathophysiology and treatment of posttraumatic stress disorder. Biol. Psychiatry 1999, 46:1192-1204.
63. Strahler J., Berndt C., Kirschbaum C., Rohleder N. Aging diurnal rhythms and chronic stress: distinct alteration of diurnal rhythmicity of salivary α-amylase and cortisol. Biol. Psychol. 2010, 84:248-256.
64. Strahler J., Kirschbaum C., Rohleder N. Association of blood pressure and antihypertensive drugs with diurnal alpha-amylase activity. Int. J. Psychophysiol. 2011, 81:31-37.
65. Strahler J., Mueller A., Rosenloecher F., Kirschbaum C., Rohleder N. Salivary α-amylase stress reactivity across different age groups. Psychophysiology 2010, 47:587-595.
66. 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.
67. Tanaka Y., Ishitobi Y., Maruyama Y., Kawano A., Ando T., Imanaga J., Okamoto S., Kanehisa M., Higuma H., Ninomiya T., Tsuru J., Hanada H., Isogawa K., Akiyoshi J. Salivary alpha-amylase and cortisol responsiveness following electrical stimulation stress in panic disorder patients. Neurosci. Res. 2012, 73:80-84.
68. Tanaka Y., Ishitobi Y., Maruyama Y., Kawano A., Ando T., Okamoto S., Kanehisa M., Higuma H., Ninomiya T., Tsuru J., Hanada H., Kodama K., Isogawa K., Akiyoshi J. Salivary alpha-amylase and cortisol responsiveness following electrical stimulation stress in major depressive disorder patients. Prog. Neuropsychopharmacol. Biol. Psychiatry 2012, 36:220-224.
69. Thoma M.V., Joksimovic L., Kirschbaum C., Wolf J.M., Rohleder N. Altered salivary alpha-amylase awakening response in Bosnian War refugees with posttraumatic stress disorder. Psychoneuroendocrinology 2012, 37:810-817.
70. van Stegeren A., Rohleder N., Everaerd W., Wolf O.T. Salivary alpha amylase as marker for adrenergic activity during stress: effect of betablockade. Psychoneuroendocrinology 2006, 31:137-141.
71. van Stegeren A.H., Wolf O.T., Kindt M. Salivary alpha amylase and cortisol responses to different stress tasks: impact of sex. Int. J. Psychophysiol. 2008, 69:33-40.
72. van Veen J.F., van Vliet I.M., de Rijk R.H., van Pelt J., Mertens B., Fekkes D., Zitman F.G. Tryptophan depletion affects the autonomic stress response in generalized social anxiety disorder. Psychoneuroendocrinology 2009, 34:1590-1594.
73. van Veen J.F., van Vliet I.M., DeRijk R.H., van Pelt J., Mertens B., Zitman F.G. Elevated alpha-amylase but not cortisol in generalized social anxiety disorder. Psychoneuroendocrinology 2008, 33:1313-1321.
74. Vigil J.M., Geary D.C., Granger D.A., Flinn M.V. Sex differences in salivary cortisol, alpha-amylase, and psychological functioning following Hurricane Katrina. Child Dev. 2010, 81:1228-1240.
75. Voss A., Schulz S., Koschke M., Bar K.J. Linear and nonlinear analysis of autonomic regulation in depressed patients. Conference Proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Conference 2008 2008, 2653-2656.
76. Wessa M., Rohleder N., Kirschbaum C., Flor H. Altered cortisol awakening response in posttraumatic stress disorder. Psychoneuroendocrinology 2006, 31:209-215.
77. Wingenfeld K., Schulz M., Damkroeger A., Philippsen C., Rose M., Driessen M. The diurnal course of salivary alpha-amylase in nurses: an investigation of potential confounders and associations with stress. Biol. Psychol. 2010, 85:179-181.
78. Wolf J.M., Nicholls E., Chen E. Chronic stress, salivary cortisol, and alpha-amylase in children with asthma and healthy children. Biol. Psychol. 2008, 78:20-28.
79. Yamaguchi M., Deguchi M., Wakasugi J., Ono S., Takai N., Higashi T., Mizuno Y. Hand-held monitor of sympathetic nervous system using salivary amylase activity and its validation by driver fatigue assessment. Biosens. Bioelectron. 2006, 21:1007-1014.
80. Yamaguchi M., Wakasugi J., Sakakima J. Evaluation of driver stress using biomarker in motor-vehicle driving simulator. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Conference 1 2006, 1834-1837.
81. Zakowski J.J., Bruns D.E. Biochemistry of human alpha amylase isoenzymes. Crit. Rev. Clin. Lab. Sci. 1985, 21:283-322.