Major depressive disorder with melancholia displays robust alterations in resting state heart rate and its variability: Implications for future morbidity and mortality

Frontiers in Psychology

Volumn 5, Issue NOV, 2014, Pages

  Kemp, Andrew H ^a,b,c   Quintana, Daniel S ^b,d,e   Quinn, Candice R ^a   Hopkinson, Patrick ^a   Harris, Anthony W F ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF OSLO   (Norway)

^e OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Ecg; Electrocardiogram; Heart rate; Heart rate variability; Hrv; Melancholia; Non melancholia; Resting state

Indexed keywords

EID: 84923349001     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2014.01387     Document Type: Article

References (72)

1. Åberg, M. A., Nyberg, J., Torén, K., Sörberg, A., Kuhn, H. G., and Waern, M. (2014). Cardiovascular fitness in early adulthood and future suicidal behaviour in men followed for up to 42 years. Psychol. Med. 44, 779-788. doi: 10.1017/S0033291713001207
2. Albinet, C. T., Boucard, G., Bouquet, C. A., and Audiffren, M. (2010). Increased heart rate variability and executive performance after aerobic training in the elderly. Eur. J. Appl. Physiol. 109, 617-624. doi: 10.1007/s00421-010-1393-y
3. Alvares, G. A., Quintana, D. S., Kemp, A. H., Van Zwieten, A., Balleine, B. W., Hickie, I. B.,et al. (2013). Reduced heart rate variability in social anxiety disorder: associations with gender and symptom severity. PLoS ONE 8:e70468. doi: 10.1371/journal.pone.0070468
4. Barzi, F., and Woodward, M. (2004). Imputations of missing values in practice: results from imputations of serum cholesterol in 28 cohort studies. Am. J. Epidemiol. 160, 34-45. doi: 10.1093/aje/kwh175
5. Billman, G. E. (2011). Heart rate variability - a historical perspective. Front. Physiol. 2:86. doi: 10.3389/fphys.2011.00086
6. Britton, A., Shipley, M., Malik, M., and Hnatkova, K. (2007). Changes in heart rate and heart rate variability over time in middle-aged men and women in the general population (from the Whitehall II Cohort Study). Am. J. Cardiol. 100, 524-527. doi: 10.1016/j.amjcard.2007.03.056
7. Brunoni, A. R., Kemp, A. H., Dantas, E. M., Goulart, A. C., Nunes, M. A., Boggio, P. S.,et al. (2013). Heart rate variability is a trait marker of major depressive disorder: evidence from the sertraline vs. electric current therapy to treat depression clinical study. Int. J. Neuropsychopharmacol. 16, 1937-1949. doi: 10.1017/S1461145713000497
8. Brunoni, A. R., Lotufo, P. A., and Benseñor, I. M. (2012). Are antidepressants good for the soul but bad for the matter? Using noninvasive brain stimulation to detangle depression/antidepressants effects on heart rate variability and cardiovascular risk. Biol. Psychiatry 71, e27-e28; author reply e29-e30. doi: 10.1016/j.biopsych.2011.08.026
9. Carney, R. M., Rich, M. W., teVelde, A., Saini, J., Clark, K., and Freedland, K. E. (1988). The relationship between heart rate, heart rate variability and depression in patients with coronary artery disease. J. Psychosom. Res. 32, 159-164. doi: 10.1016/0022-3999(88)90050-5
10. Chalmers, J. A., Quintana, D. S., Abbott, M. J.-A., and Kemp, A. H. (2014). Anxiety disorders are associated with reduced heart rate variability: a meta-analysis. Front. Psychiatry 5:80. doi: 10.3389/fpsyt.2014.00080
11. Cohen, J. (1988). Set correlation and contingency tables. Appl. Psychol. Meas. 12, 425-434. doi: 10.1177/014662168801200410
12. Cooney, M. T., Vartiainen, E., Laakitainen, T., Juolevi, A., Dudina, A., and Graham, I. M. (2010). Elevated resting heart rate is an independent risk factor for cardiovascular disease in healthy men and women. Am. Heart. J. 159, 612-619.e3. doi: 10.1016/j.ahj.2009.12.029
13. de Jonge, P., Mangano, D., and Whooley, M. A. (2007). Differential association of cognitive and somatic depressive symptoms with heart rate variability in patients with stable coronary heart disease: findings from the Heart and Soul Study. Psychosom. Med. 69, 735-739. doi: 10.1097/PSY.0b013e31815743ca
14. Edwards, A. L. (1985). Multiple Regression Analysis and the Analysis of Variance and Covariance. New York, NY: Freeman.
15. Electrophysiology TFotESoCtNASoP. (1996). Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Circulation 93, 1043-1065.
16. Fox, K., Borer, J. S., Camm, A. J., Danchin, N., Ferrari, R., Sendon, J. L. L.,et al. (2007). Resting heart rate in cardiovascular disease. J. Am. Coll. Cardiol. 50, 823-830. doi: 10.1016/j.jacc.2007.04.079
17. Friedman, B. H., and Thayer, J. (1998). Autonomic balance revisited: panic anxiety and heart rate variability. J. Psychosom. Res. 44, 133-151. doi: 10.1016/S0022-3999(97)00202-X
18. Gold, P. S., and Chrousos, G. P. (2002). Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Mol. Psychiatry 7, 254-275. doi: 10.1038/sj.mp.4001032
19. Goldstein, D. S., Bentho, O., Park, M. Y., and Sharabi, Y. (2011). Low-frequency power of heart rate variability is not a measure of cardiac sympathetic tone but may be a measure of modulation of cardiac autonomic outflows by baroreflexes. Exp. Physiol. 96, 1255-1261. doi: 10.1113/expphysiol.2010.056259
20. Gordon, E., Cooper, N., Rennie, C., Hermens, D., and Williams, L. M. (2005). Integrative neuroscience: the role of a standardized database. Clin. EEG Neurosci. 36, 64-75. doi: 10.1177/155005940503600205
21. Hamilton, M. (1960). A rating scale for depression. J. Neurol. Neurosurg. Psychiatry 23, 56-62. doi: 10.1136/jnnp.23.1.56
22. Hansen, A. L., Thayer, J., Johnsen, B. H., Sollers, J. J., and Stenvik, K. (2004). Heart rate variability and its relation to prefrontal cognitive function: the effects of training and detraining. Eur. J. Appl. Physiol. 93, 263-272. doi: 10.1007/s00421-004-1208-0
23. Harte, C. B., and Meston, C. M. (2014). Effects of smoking cessation on heart rate variability among long-term male smokers. Int. J. Behav. Med. 21, 302-309. doi: 10.1007/s12529-013-9295-0
24. Hickie, I. (1996). "Validity of the CORE," in Melancholia: A Disorder of Movement and Mood, eds G. Parker and D. Hazdi-Pavlovic (New York: Cambridge University Press), 149-159.
25. Hill, J. (2004). Reducing Bias in Treatment Effect Estimation in Observational Studies Suffering from Missing Data (No. ISERP Working Paper 04-01). New York: Institute for Social and Economic Research and Policy, Columbia University. Working Papers.
26. Hillebrand, S., Gast, K. B., de Mutsert, R., Swenne, C. A., Jukema, J. W., Middeldorp, S.,et al. (2013). Heart rate variability and first cardiovascular event in populations without known cardiovascular disease: meta-analysis and dose-response meta-regression. Europace 15, 742-749. doi: 10.1093/europace/eus341
27. Kashdan, T., and Rottenberg, J. (2010). Psychological flexibility as a fundamental aspect of health. Clin. Psychol. Rev. 30, 865-878. doi: 10.1016/j.cpr.2010.03.001
28. Kemp, A. H. (2011). Depression, antidepressant treatment and the cardiovascular system. Acta Neuropsychiatr. 23, 82-83. doi: 10.1111/j.1601-5215.2011.00535.x
29. Kemp, A. H. (2012). Are antidepressants good for the soul but bad for the matter? using noninvasive brain stimulation to detangle depression/antidepressants effects on heart rate variability and cardiovascular risk. Biol. Psychiatry 71, e29-e30. doi: 10.1016/j.biopsych.2011.11.002
30. Kemp, A. H., Brunoni, A. R., Santos, I. S., Nunes, M. A., Dantas, E. M., Carvalho de Figueiredo, R.,et al. (2014). Effects of depression, anxiety, comorbidity, and antidepressants on resting-state heart rate and its variability: an ELSA-Brasil cohort baseline study. Am. J. Psychiatry doi: 10.1176/appi.ajp.2014.13121605 [Epub ahead of print].
31. Kemp, A. H., and Quintana, D. S. (2013). The relationship between mental and physical health: insights from the study of heart rate variability. Int. J. Psychophysiol. 89, 288-296. doi: 10.1016/j.ijpsycho.2013.06.018
32. Kemp, A. H., Quintana, D. S., Felmingham, K. L., Matthews, S., and Jelinek, H. F. (2012). Depression, comorbid anxiety disorders, and heart rate variability in physically healthy, unmedicated patients: implications for cardiovascular risk. PLoS ONE 7:e30777. doi: 10.1371/journal.pone.0030777
33. Kemp, A. H., Quintana, D. S., and Gray, M. A. (2011). Is heart rate variability reduced in depression without cardiovascular disease? Biol. Psychiatry 69, e3-e4. doi: 10.1016/j.biopsych.2010.07.030
34. Kemp, A. H., Quintana, D. S., Gray, M. A., Felmingham, K. L., Brown, K., and Gatt, J. M. (2010). Impact of depression and antidepressant treatment on heart rate variability: a review and meta-analysis. Biol. Psychiatry 67, 1067-1074. doi: 10.1016/j.biopsych.2009.12.012
35. Kim, D. H., Lipsitz, L. A., Ferrucci, L., Varadhan, R., Guralnik, J. M., Carlson, M. C.,et al. (2006). Association between reduced heart rate variability and cognitive impairment in older disabled women in the community: Women's Health and Aging Study I. J. Am. Geriatr. Soc. 54, 1751-1757. doi: 10.1111/j.1532-5415.2006.00940.x
36. Kleiger, R. E., Stein, P. K., and Bigger, J. T. (2005). Heart rate variability: measurement and clinical utility. Ann. Noninvasive Electrocardiol. 10, 88-101. doi: 10.1111/j.1542-474X.2005.10101.x
37. Koenig, J., Jarczok, M. N., Warth, M., Ellis, R. J., Bach, C., Hillecke, T. K.,et al. (2014). Body mass index is related to autonomic nervous system activity as measured by heart rate variability-a replication using short term measurements. J. Nutr. Health Aging 18, 300-302. doi: 10.1007/s12603-014-0022-6
38. Krygier, J. R., Heathers, J. A. J., Shahrestani, S., Abbott, M., Gross, J. J., and Kemp, A. H. (2013). Mindfulness meditation, well-being, and heart rate variability: a preliminary investigation into the impact of intensive Vipassana meditation. Int. J. Psychophysiol. 89, 305-313. doi: 10.1016/j.ijpsycho.2013.06.017
39. Lemogne, C., Thomas, F., Consoli, S. M., Pannier, B., Jégo, B., and Danchin, N. (2011). Heart rate and completed suicide: evidence from the IPC cohort study. Psychosom. Med. 73, 731-736. doi: 10.1097/PSY.0b013e3182365dc7
40. Licht, C. M. M., de Geus, E. J. C., van Dyck, R., and Penninx, B. W. J. H. (2010). Longitudinal evidence for unfavorable effects of antidepressants on heart rate variability. Biol. Psychiatry 68, 861-868. doi: 10.1016/j.biopsych.2010.06.032
41. Licht, C. M. M., de Geus, E. J. C., Zitman, F. G., Hoogendijk, W. J. G., van Dyck, R., and Penninx, B. W. J. H. (2008). Association between major depressive disorder and heart rate variability in the Netherlands Study of Depression and Anxiety (NESDA). Arch. Gen. Psychiatry 65, 1358-1367. doi: 10.1001/archpsyc.65.12.1358
42. Licht, C. M. M., Penninx, B. W., and de Geus, E. J. C. (2011). To include or not to include? A response to the meta-analysis of heart rate variability and depression. Biol. Psychiatry 69, e1; author reply e3-e4. doi: 10.1016/j.biopsych.2010.06.034
43. Lovibond, P. F., and Lovibond, S. H. (1995). The structure of negative emotional states: comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behav. Res. Ther. 33, 335-343. doi: 10.1016/0005-7967(94)00075-U
44. Malhi, G. S., Parker, G. B., and Greenwood, J. (2005). Structural and functional models of depression: from sub-types to substrates. Acta Psychiatr. Scand. 111, 94-105. doi: 10.1111/acp.2005.111.issue-2
45. Marshall, A., Altman, D. G., Holder, R. L., and Royston, P. (2009). Combining estimates of interest in prognostic modelling studies after multiple imputation: current practice and guidelines. BMC Med. Res. Methodol. 9:57. doi: 10.1186/1471-2288-9-57
46. Mayberg, H. S., Nemeroff, C., Krahl, S. E., Mcnamara, J., Frazer, A., Henry, T. R.,et al. (2006). VNS therapy in treatment-resistant depression: clinical evidence and putative neurobiological mechanisms. Neuropsychopharmacology 31, 1345-1355. doi: 10.1038/sj.npp.1301082
47. Pan, J., and Tompkins, W. J. (1985). A real-time QRS detection algorithm. IEEE Trans. Biomed. Eng. 32, 230-236. doi: 10.1109/TBME.1985.325532
48. Penttilä, J., Helminen, A., Jartti, T., Kuusela, T., Huikuri, H. V., Tulppo, M. P.,et al. (2001). Time domain, geometrical and frequency domain analysis of cardiac vagal outflow: effects of various respiratory patterns. Clin. Physiol. 21, 365-376. doi: 10.1046/j.1365-2281.2001.00337.x
49. Picard, G., Tan, C. O., Zafonte, R., and Taylor, J. A. (2009). Incongruous changes in heart period and heart rate variability with vagotonic atropine: implications for rehabilitation medicine. PM R 1, 820-826. doi: 10.1016/j.pmrj.2009.07.017
50. Porges, S. W. (2011). The Polyvagal Theory: Neurophysiological Foundations of Emotions, Attachment, Communication, and Self-regulation, 1st Edn. New York: W. W. Norton & Company.
51. Quinn, C. R., Harris, A., Felmingham, K., Boyce, P., and Kemp, A. H. (2012a). The impact of depression heterogeneity on cognitive control in major depressive disorder. Aust. N. Z. J. Psychiatry 46, 1079-1088. doi: 10.1177/0004867412461383
52. Quinn, C., Harris, A., and Kemp, A. H. (2012b). The interdependence of subtype and severity: contributions of clinical and neuropsychological features to melancholia and non-melancholia in an outpatient sample. J. Int. Neuropsychol. Soc. 18, 361-369. doi: 10.1017/S1355617711001858
53. Quintana, D. S., Guastella, A. J., McGregor, I. S., Hickie, I. B., and Kemp, A. H. (2013a). Moderate alcohol intake is related to increased heart rate variability in young adults: implications for health and well-being. Psychophysiology 50, 1202-1208. doi: 10.1111/psyp.12134
54. Quintana, D. S., McGregor, I. S., Guastella, A. J., Malhi, G. S., and Kemp, A. H. (2013b). A meta-analysis on the impact of alcohol dependence on short-term resting-state heart rate variability: implications for cardiovascular risk. Alcohol. Clin. Exp. Res. 37(Suppl. 1), E23-E29. doi: 10.1111/j.1530-0277.2012.01913.x
55. Quintana, D. S., and Heathers, J. A. J. (2014). Considerations in the assessment of heart rate variability in biobehavioral research. Front. Psychol. 5:805. doi: 10.3389/fpsyg.2014.00805
56. Rennie, K. L., Hemingway, H., Kumari, M., Brunner, E., Malik, M., and Marmot, M. (2003). Effects of moderate and vigorous physical activity on heart rate variability in a British study of civil servants. Am. J. Epidemiol. 158, 135-143. doi: 10.1093/aje/kwg120
57. Reyes Del Paso, G. A., Langewitz, W., Mulder, L. J. M., Roon, A., and Duschek, S. (2013). The utility of low frequency heart rate variability as an index of sympathetic cardiac tone: a review with emphasis on a reanalysis of previous studies. Psychophysiology 50, 477-487. doi: 10.1111/psyp.12027
58. Saul, J. P. (1990). Beat-to-beat variations of heart rate reflect modulation of cardiac autonomic outflow. Physiology 5, 32-37.
59. Saxena, A., Minton, D., Lee, D.-C., Sui, X., Fayad, R., Lavie, C. J.,et al. (2013). Protective role of resting heart rate on all-cause and cardiovascular disease mortality. Mayo Clin. Proc. 88, 1420-1426. doi: 10.1016/j.mayocp.2013.09.011
60. Schafer, J. L. (1999). Multiple imputation: a primer. Stat. Methods Med. Res. 8, 3-15. doi: 10.1177/096228029900800102
61. Sheehan, D., Lecrubier, Y., Sheehan, K., Amorim, P., Janavs, J., Weiller, E.,et al. (1998). The Mini-International Neuropsychiatric Interview (MINI): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J. Clin. Psychiatry 59, 22. doi: 10.1016/S0924-9338(99)80239-9
62. Sjoberg, N., and Saint, D. A. (2011). A single 4 mg dose of nicotine decreases heart rate variability in healthy nonsmokers: implications for smoking cessation programs. Nicotine Tob. Res. 13, 369-372. doi: 10.1093/ntr/ntr004
63. Soares-Miranda, L., Sattelmair, J., Chaves, P., Duncan, G. E., Siscovick, D. S., Stein, P. K.,et al. (2014). Physical activity and heart rate variability in older adults: the Cardiovascular Health Study. Circulation 129, 2100-2110. doi: 10.1161/CIRCULATIONAHA.113.005361
64. Stein, P. K., Barzilay, J. I., Domitrovich, P. P., Chaves, P. M., Gottdiener, J. S., Heckbert, S. R.,et al. (2007). The relationship of heart rate and heart rate variability to non-diabetic fasting glucose levels and the metabolic syndrome: the Cardiovascular Health Study. Diabet. Med. 24, 855-863. doi: 10.1111/j.1464-5491.2007.02163.x
65. Tarvainen, M., and Niskanen, J. (2008). Kubios HRV (No. 13779), 2nd Edn, 1-53. Kuopio: Biosignal Analysis and Medical Imaging Group (BSAMIG), Department of Physics, University of Kuopio, Kuopio.
66. Thayer, J., and Fischer, J. E. (2013). Heart rate variability, overnight urinary norepinephrine, and plasma cholesterol in apparently healthy human adults. Int. J. Cardiol. 162, 240-244. doi: 10.1016/j.ijcard.2011.05.058
67. Thayer, J., Hansen, A. L., Saus-Rose, E., and Johnsen, B. H. (2009). Heart rate variability, prefrontal neural function, and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Ann. Behav. Med. 37, 141-153. doi: 10.1007/s12160-009-9101-z
68. Thayer, J. F., and Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. J. Affect. Disord. 61, 201-216. doi: 10.1016/S0165-0327(00)00338-4
69. Thayer, J., Yamamoto, S. S., and Brosschot, J. F. (2010). The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. Int. J. Cardiol. 141, 122-131. doi: 10.1016/j.ijcard.2009.09.543
70. Thoemmes, F. (2012). Propensity score matching in SPSS. arXiv:1201.6385. Available at: http://arxiv.org/ftp/arxiv/papers/1201/1201.6385.pdf
71. van Ginkel, J. R., and Kroonenberg, P. M. (2014). Analysis of variance of multiply imputed data. Multivariate Behav. Res. 49, 78-91. doi: 10.1080/00273171.2013.855890
72. Williams, J. B. (1988). A structured interview guide for the Hamilton Depression Rating Scale. Arch. Gen. Psychiatry 45, 742-747. doi: 10.1007/s12160-009-9101-z