Reduced cardiac autonomic response to deep breathing: A heritable vulnerability trait in patients with schizophrenia and their healthy first-degree relatives

Psychiatry Research

Volumn 243, Issue , 2016, Pages 335-341

  Liu, Yu Wen ^a   Tzeng, Nian Sheng ^a,b   Yeh, Chin Bin ^a   Kuo, Terry B J ^c   Huang, San Yuan ^a   Chang, Chuan Chia ^a   Chang, Hsin An ^a  

^a TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^b NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Cardiac autonomic response; Deep breathing; First degree relatives; Heart rate variability; Schizophrenia

Indexed keywords

ADULT; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; CARDIAC AUTONOMIC NEUROPATHY; CARDIAC AUTONOMIC RESPONSE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FIRST DEGREE RELATIVE; GENETIC TRAIT; HEART INNERVATION; HEART RATE VARIABILITY; HUMAN; HYPERPNEA; MALE; PARASYMPATHETIC TONE; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; SCHIZOPHRENIA; AUTONOMIC NERVOUS SYSTEM; BLOOD PRESSURE; BREATHING; ELECTROCARDIOGRAPHY; EPIDEMIOLOGY; GENETIC PREDISPOSITION; GENETICS; HEART RATE; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; QUANTITATIVE TRAIT; TRENDS;

ADULT; AUTONOMIC NERVOUS SYSTEM; BLOOD PRESSURE; ELECTROCARDIOGRAPHY; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HEART RATE; HUMANS; MALE; MIDDLE AGED; QUANTITATIVE TRAIT, HERITABLE; RESPIRATION; SCHIZOPHRENIA;

EID: 84978481264     PISSN: 01651781     EISSN: 18727123     Source Type: Journal    
DOI: 10.1016/j.psychres.2016.04.076     Document Type: Article

References (57)

1. Agelink, M.W., Majewski, T., Wurthmann, C., Lukas, K., Ullrich, H., Linka, T., Klieser, E., Effects of newer atypical antipsychotics on autonomic neurocardiac function: a comparison between amisulpride, olanzapine, sertindole, and clozapine. J. Clin. Psychopharmacol. 21 (2001), 8–13.
2. Andreasen, N.C., Schizophrenia: the fundamental questions. Brain Res. Brain Res. Rev. 31 (2000), 106–112.
3. Andreasen, N.C., Nopoulos, P., O'Leary, D.S., Miller, D.D., Wassink, T., Flaum, M., Defining the phenotype of schizophrenia: cognitive dysmetria and its neural mechanisms. Biol. Psychiatry 46 (1999), 908–920.
4. Bar, K.J., Letzsch, A., Jochum, T., Wagner, G., Greiner, W., Sauer, H., Loss of efferent vagal activity in acute schizophrenia. J. Psychiatr. Res 39 (2005), 519–527.
5. Bar, K.J., Rachow, T., Schulz, S., Bassarab, K., Haufe, S., Berger, S., Koch, K., Voss, A., The phrenic component of acute schizophrenia-a name and its physiological reality. PLoS One, 7, 2012, e33459.
6. Bar, K.J., Berger, S., Metzner, M., Boettger, M.K., Schulz, S., Ramachandraiah, C.T., Terhaar, J., Voss, A., Yeragani, V.K., Sauer, H., Autonomic dysfunction in unaffected first-degree relatives of patients suffering from schizophrenia. Schizophr. Bull. 36 (2010), 1050–1058.
7. Baumert, M., Lambert, G.W., Dawood, T., Lambert, E.A., Esler, M.D., McGrane, M., Barton, D., Sanders, P., Nalivaiko, E., Short-term heart rate variability and cardiac norepinephrine spillover in patients with depression and panic disorder. Am. J. Physiol. Heart Circ. Physiol. 297 (2009), H674–H679.
8. Ben Lamine, S., Calabrese, P., Perrault, H., Dinh, T.P., Eberhard, A., Benchetrit, G., Individual differences in respiratory sinus arrhythmia. Am. J. Physiol. Heart Circ. Physiol. 286 (2004), H2305–H2312.
9. Bernardi, L., Wdowczyk-Szulc, J., Valenti, C., Castoldi, S., Passino, C., Spadacini, G., Sleight, P., Effects of controlled breathing, mental activity and mental stress with or without verbalization on heart rate variability. J. Am. Coll. Cardiol. 35 (2000), 1462–1469.
10. Castro, M.N., Vigo, D.E., Chu, E.M., Fahrer, R.D., de Achaval, D., Costanzo, E.Y., Leiguarda, R.C., Nogues, M., Cardinali, D.P., Guinjoan, S.M., Heart rate variability response to mental arithmetic stress is abnormal in first-degree relatives of individuals with schizophrenia. Schizophr. Res 109 (2009), 134–140.
11. Chang, C.C., Chang, H.A., Chen, T.Y., Fang, W.H., Huang, S.Y., Brain-derived neurotrophic factor (BDNF) Val66Met polymorphism affects sympathetic tone in a gender-specific way. Psychoneuroendocrinology 47 (2014), 17–25.
12. Chang, C.C., Fang, W.H., Chang, H.A., Chen, T.Y., Huang, S.Y., Sex-specific association between nerve growth factor polymorphism and cardiac vagal modulation. Psychosom. Med. 76 (2014), 638–643.
13. Chang, H.A., Chang, C.C., Kuo, T.B., Huang, S.Y., Distinguishing bipolar II depression from unipolar major depressive disorder: Differences in heart rate variability. World J. Biol. Psychiatry 16 (2015), 351–360.
14. Chang, H.A., Lu, R.B., Shy, M.J., Chang, C.C., Lee, M.S., Huang, S.Y., Brain-derived neurotrophic factor Val66Met polymorphism: association with psychopathological symptoms of schizophrenia?. J. Neuropsychiatry Clin. Neurosci. 21 (2009), 30–37.
15. Cloninger, C.R., The discovery of susceptibility genes for mental disorders. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 13365–13367.
16. Cohen, J., Statistical power analysis. Curr. Dir. Psychol. Sci. 1 (1992), 98–101.
17. Cohen, L., Statistical Power Analysis for the behavioral sciencies, 1988, Lawrence Erlbaum Associates, Hillsdale.
18. Curkendall, S.M., Mo, J., Glasser, D.B., Rose Stang, M., Jones, J.K., Cardiovascular disease in patients with schizophrenia in Saskatchewan, Canada. J. Clin. Psychiatry 65 (2004), 715–720.
19. Dekker, J.M., Crow, R.S., Folsom, A.R., Hannan, P.J., Liao, D., Swenne, C.A., Schouten, E.G., Low heart rate variability in a 2-minute rhythm strip predicts risk of coronary heart disease and mortality from several causes: the ARIC Study. Atherosclerosis Risk In Communities. Circulation 102 (2000), 1239–1244.
20. Driscoll, D., Dicicco, G., The effects of metronome breathing on the variability of autonomic activity measurements. J. Manip. Physiol. Ther. 23 (2000), 610–614.
21. Eckberg, D.L., Sympathovagal balance: a critical appraisal. Circulation 96 (1997), 3224–3232.
22. Endicott, J., Spitzer, R.L., A diagnostic interview: the schedule for affective disorders and schizophrenia. Arch. Gen. Psychiatry 35 (1978), 837–844.
23. Esler, M., Eikelis, N., Schlaich, M., Lambert, G., Alvarenga, M., Kaye, D., El-Osta, A., Guo, L., Barton, D., Pier, C., Brenchley, C., Dawood, T., Jennings, G., Lambert, E., Human sympathetic nerve biology: parallel influences of stress and epigenetics in essential hypertension and panic disorder. Ann. New Y. Acad. Sci. 1148 (2008), 338–348.
24. Garcia, E., Robert, M., Peris, F., Nakamura, H., Sato, N., Terazawa, Y., The efficacy and safety of blonanserin compared with haloperidol in acute-phase schizophrenia: a randomized, double-blind, placebo-controlled, multicentre study. CNS Drugs 23 (2009), 615–625.
25. Glatt, S.J., Stone, W.S., Nossova, N., Liew, C.C., Seidman, L.J., Tsuang, M.T., Similarities and differences in peripheral blood gene-expression signatures of individuals with schizophrenia and their first-degree biological relatives. Am. J. Med. Genet. B Neuropsychiatr. Genet. 156B (2011), 869–887.
26. Goldstein, D.S., Bentho, O., Park, M.Y., Sharabi, Y., 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 (2011), 1255–1261.
27. Hennekens, C.H., Hennekens, A.R., Hollar, D., Casey, D.E., Schizophrenia and increased risks of cardiovascular disease. Am. Heart J. 150 (2005), 1115–1121.
28. Jauregui, O.I., Costanzo, E.Y., de Achaval, D., Villarreal, M.F., Chu, E., Mora, M.C., Vigo, D.E., Castro, M.N., Leiguarda, R.C., Bar, K.J., Guinjoan, S.M., Autonomic nervous system activation during social cognition tasks in patients with schizophrenia and their unaffected relatives., Cognit. Behav. Neurol. 24, 2011, 194–203.
29. Kendler, K.S., Reflections on the relationship between psychiatric genetics and psychiatric nosology. Am. J. Psychiatry 163 (2006), 1138–1146.
30. Kendler, K.S., Gruenberg, A.M., Kinney, D.K., Independent diagnoses of adoptees and relatives as defined by DSM-III in the provincial and national samples of the Danish Adoption Study of Schizophrenia. Arch. Gen. Psychiatry 51 (1994), 456–468.
31. Kuo, T.B., Lin, T., Yang, C.C., Li, C.L., Chen, C.F., Chou, P., Effect of aging on gender differences in neural control of heart rate. Am. J. Physiol. 277 (1999), H2233–H2239.
32. Kupper, N.H., Willemsen, G., van den Berg, M., de Boer, D., Posthuma, D., Boomsma, D.I., de Geus, E.J., Heritability of ambulatory heart rate variability. Circulation 110 (2004), 2792–2796.
33. La Rovere, M.T., Bigger, J.T. Jr., Marcus, F.I., Mortara, A., Schwartz, P.J., Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction. ATRAMI (Autonomic Tone and Reflexes After Myocardial Infarction) Investigators. Lancet 351 (1998), 478–484.
34. Lehrer, P.M., Vaschillo, E., Vaschillo, B., Lu, S.E., Eckberg, D.L., Edelberg, R., Shih, W.J., Lin, Y., Kuusela, T.A., Tahvanainen, K.U., Hamer, R.M., Heart rate variability biofeedback increases baroreflex gain and peak expiratory flow. Psychosom. Med. 65 (2003), 796–805.
35. de Leon, J., Dadvand, M., Canuso, C., White, A.O., Stanilla, J.K., Simpson, G.M., Schizophrenia and smoking: an epidemiological survey in a state hospital. Am. J. Psychiatry 152 (1995), 453–455.
36. Malliani, A., Heart rate variability: from bench to bedside. Eur. J. Intern. Med. 16 (2005), 12–20.
37. Moak, J.P., Goldstein, D.S., Eldadah, B.A., Saleem, A., Holmes, C., Pechnik, S., Sharabi, Y., Supine low-frequency power of heart rate variability reflects baroreflex function, not cardiac sympathetic innervation. Heart Rhythm 4 (2007), 1523–1529.
38. Mothi, S.S., Tandon, N., Padmanabhan, J., Mathew, I.T., Clementz, B., Tamminga, C., Pearlson, G., Sweeney, J., Keshavan, M.S., Increased cardiometabolic dysfunction in first-degree relatives of patients with psychotic disorders. Schizophr. Res. 165 (2015), 103–107.
39. Pagani, M., Mazzuero, G., Ferrari, A., Liberati, D., Cerutti, S., Vaitl, D., Tavazzi, L., Malliani, A., Sympathovagal interaction during mental stress. A study using spectral analysis of heart rate variability in healthy control subjects and patients with a prior myocardial infarction. Circulation 83 (1991), II43–II51.
40. Pearlson, G.D., Folley, B.S., Schizophrenia, psychiatric genetics, and Darwinian psychiatry: an evolutionary framework. Schizophr. Bull. 34 (2008), 722–733.
41. Pitzalis, M.V., Mastropasqua, F., Massari, F., Passantino, A., Colombo, R., Mannarini, A., Forleo, C., Rizzon, P., Effect of respiratory rate on the relationships between RR interval and systolic blood pressure fluctuations: a frequency-dependent phenomenon. Cardiovasc. Res. 38 (1998), 332–339.
42. Pomeranz, B., Macaulay, R.J., Caudill, M.A., Kutz, I., Adam, D., Gordon, D., Kilborn, K.M., Barger, A.C., Shannon, D.C., Cohen, R.J., et al. Assessment of autonomic function in humans by heart rate spectral analysis. Am. J. Physiol. 248 (1985), H151–H153.
43. Przybylska-Felus, M., Furgala, A., Zwolinska-Wcislo, M., Mazur, M., Widera, A., Thor, P., Mach, T., Disturbances of autonomic nervous system activity and diminished response to stress in patients with celiac disease. J. Physiol. Pharmacol.: Off. J. Pol. Physiol. Soc. 65 (2014), 833–841.
44. Sanderson, J.E., Yeung, L.Y., Yeung, D.T., Kay, R.L., Tomlinson, B., Critchley, J.A., Woo, K.S., Bernardi, L., Impact of changes in respiratory frequency and posture on power spectral analysis of heart rate and systolic blood pressure variability in normal subjects and patients with heart failure. Clin. Sci. 91 (1996), 35–43.
45. Sato, N., Miyake, S., Akatsu, J., Kumashiro, M., Power spectral analysis of heart rate variability in healthy young women during the normal menstrual cycle. Psychosom. Med. 57 (1995), 331–335.
46. Schulz, S., Haueisen, J., Bar, K.J., Andreas, V., High-resolution joint symbolic analysis to enhance classification of the cardiorespiratory system in patients with schizophrenia and their relatives. Philosophical transactions. Ser. A Math. Phys. Eng. Sci., 2015, 373.
47. Singh, J.P., Larson, M.G., O'Donnell, C.J., Tsuji, H., Evans, J.C., Levy, D., Heritability of heart rate variability: the Framingham Heart Study. Circulation 99 (1999), 2251–2254.
48. Sklar, P., Linkage analysis in psychiatric disorders: the emerging picture. Annu. Rev. Genom. Hum. Genet. 3 (2002), 371–413.
49. Snieder, H., Boomsma, D.I., Van Doornen, L.J., De Geus, E.J., Heritability of respiratory sinus arrhythmia: dependency on task and respiration rate. Psychophysiology 34 (1997), 317–328.
50. Stein, P.K., Rottman, J.N., Kleiger, R.E., Effect of 21 mg transdermal nicotine patches and smoking cessation on heart rate variability. Am. J. Cardiol. 77 (1996), 701–705.
51. Sullivan, P.F., Kendler, K.S., Neale, M.C., Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies. Arch. Gen. Psychiatry 60 (2003), 1187–1192.
52. Tank, J., Jordan, J., Diedrich, A., Stoffels, M., Franke, G., Faulhaber, H.D., Luft, F.C., Busjahn, A., Genetic influences on baroreflex function in normal twins. Hypertension 37 (2001), 907–910.
53. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology, Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 93 (1996), 1043–1065.
54. Voss, A., Schulz, S., Baer, K.J., Linear and nonlinear analysis of autonomic regulation of heart rate variability in healthy first-degree relatives of patients with schizophrenia. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2010 (2010), 5395–5398.
55. Williams, L.M., Das, P., Harris, A.W., Liddell, B.B., Brammer, M.J., Olivieri, G., Skerrett, D., Phillips, M.L., David, A.S., Peduto, A., Gordon, E., Dysregulation of arousal and amygdala-prefrontal systems in paranoid schizophrenia. Am. J. Psychiatry 161 (2004), 480–489.
56. Yang, C.C., Chao, T.C., Kuo, T.B., Yin, C.S., Chen, H.I., Preeclamptic pregnancy is associated with increased sympathetic and decreased parasympathetic control of HR. Am. J. Physiol. Heart Circ. Physiol. 278 (2000), H1269–H1273.
57. Zhong, J., Colicino, E., Lin, X., Mehta, A., Kloog, I., Zanobetti, A., Byun, H.M., Bind, M.A., Cantone, L., Prada, D., Tarantini, L., Trevisi, L., Sparrow, D., Vokonas, P., Schwartz, J., Baccarelli, A.A., Cardiac autonomic dysfunction: particulate air pollution effects are modulated by epigenetic immunoregulation of Toll-like receptor 2 and dietary flavonoid intake. J. Am. Heart Assoc., 4, 2015, e001423.