Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-28T13:23:36.941Z Has data issue: false hasContentIssue false
  • English
  • Français

The causal nature of the association between resting pulse in late adolescence and risk for internalizing and externalizing disorders: a co-relative analysis in a national male Swedish sample

Published online by Cambridge University Press:  24 March 2020

Kenneth S. Kendler Open the ORCID record for Kenneth S. Kendler [Opens in a new window] ,
Sara L. Lönn ,
Jan Sundquist  and
Kristina Sundquist
Kenneth S. Kendler*
Affiliation:
Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond, VA, USA Department of Psychiatry, Virginia Commonwealth University, Richmond, VA, USA
Sara L. Lönn
Affiliation:
Center for Primary Health Care Research, Lund University, Malmö, Sweden
Jan Sundquist
Affiliation:
Center for Primary Health Care Research, Lund University, Malmö, Sweden Department of Family Medicine and Community Health, Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, USA Department of Functional Pathology, Center for Community-based Healthcare Research and Education (CoHRE), School of Medicine, Shimane University, Izumo, Shimane, Japan
Kristina Sundquist
Affiliation:
Center for Primary Health Care Research, Lund University, Malmö, Sweden Department of Family Medicine and Community Health, Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, USA Department of Functional Pathology, Center for Community-based Healthcare Research and Education (CoHRE), School of Medicine, Shimane University, Izumo, Shimane, Japan
*
Author for correspondence: Kenneth S. Kendler, E-mail: Kenneth.Kendler@vcuhealth.org
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Resting pulse is robustly and inversely associated with the risk for externalizing disorders and may be positively associated with internalizing disorders. We know little about the causal nature of these associations.

Methods

We examined resting pulse at conscription examination in 369 301 males born 1960–80 with a mean (s.d.) follow-up of 29.1 (7.7) years. From pulse rates, we predicted, using Cox models, the risk for criminal behavior (CB), drug abuse (DA), alcohol use disorder (AUD), major depression (MD), and anxiety disorders (AD), assessed from medical, criminal, and pharmacy registries. Co-relative analyses were conducted on the general population, cousin, half-sibling, full-sibling, and monozygotic pairs discordant for the outcome. Twin/sibling modeling for pulse was performed using OpenMX.

Results

Familial resemblance for pulse resulted entirely from genetic factors. In the general population, the risk for externalizing disorders (CB, DA, and AUD) and internalizing disorders (MD and AD) were, respectively, significantly associated with low and high resting pulse rate. For CB, DA, and AUD, co-relative analyses showed that the inverse association with pulse resulted entirely from familial common causes (aka ‘confounders’). By contrast, co-relative analyses found that the association between higher pulse and MD and AD resulted from direct causal effects.

Conclusions

Resting pulse has a negative and positive association with, respectively, the risk for externalizing and for internalizing disorders. Co-relative analyses indicate that the nature of these associations differ, suggesting that elevated pulse appears to directly increase the risk for internalizing disorders while the reduced pulse is a risk index for underlying traits that predispose to externalizing disorders.

Keywords

Causal inferenceexternalizing disordersinternalizing disorderspulse
Type
Original Article
Information
Psychological Medicine , Volume 51 , Issue 11 , August 2021 , pp. 1822 - 1828
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akaike, H. (1987). Factor analysis and AIC. Psychometrika, 52, 317–332.CrossRefGoogle Scholar
Armstrong, T. A., Keller, S., Franklin, T. W., & Macmillan, S. N. (2009). Low resting heart rate and antisocial behavior: A brief review of evidence and preliminary results from a new test. Criminal Justice and Behavior, 36(11), 1125–1140.CrossRefGoogle Scholar
Baker, L. A., Tuvblad, C., Reynolds, C., Zheng, M., Lozano, D. I., & Raine, A. (2009). Resting heart rate and the development of antisocial behavior from age 9 to 14: Genetic and environmental influences. Development and Psychopathology, 21(3), 939–960.CrossRefGoogle ScholarPubMed
Cannon, W. B. (1927). The James-Lange theory of emotions: A critical examination and an alternative theory. The American Journal of Psychology, 39(1/4), 106–124.CrossRefGoogle Scholar
Cicek, Y., Durakoglugil, M. E., Kocaman, S. A., Guveli, H., Cetin, M., Erdogan, T., … Canga, A. (2012). Increased pulse wave velocity in patients with panic disorder: Independent vascular influence of panic disorder on arterial stiffness. Journal of Psychosomatic Research, 73(2), 145–148. doi:10.1016/j.jpsychores.2012.05.012.CrossRefGoogle ScholarPubMed
Hammerton, G., Heron, J., Mahedy, L., Maughan, B., Hickman, M., & Murray, J. (2018). Low resting heart rate, sensation seeking and the course of antisocial behaviour across adolescence and young adulthood. Psychological Medicine, 48(13), 2194–2201. doi:10.1017/S0033291717003683.CrossRefGoogle ScholarPubMed
Kavish, N., Vaughn, M. G., Cho, E., Barth, A., Boutwell, B., Vaughn, S., … Martinez, L. (2017). Physiological arousal and juvenile psychopathy: Is low resting heart rate associated with affective dimensions? Psychiatric Quarterly, 88(1), 103–114. doi:10.1007/s11126-016-9437-z.CrossRefGoogle ScholarPubMed
Kemp, A. H., Brunoni, A. R., Santos, I. S., Nunes, M. A., Dantas, E. M., de Carvalho, F. R., … Lotufo, P. A. (2014a). Effects of depression, anxiety, comorbidity, and antidepressants on resting-state heart rate and its variability: An ELSA-Brasil cohort baseline study. American Journal of Psychiatry, 171(12), 1328–1334. doi:10.1176/appi.ajp.2014.13121605.CrossRefGoogle Scholar
Kemp, A. H., Quintana, D. S., Quinn, C. R., Hopkinson, P., & Harris, A. W. (2014b). 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, 5, 1387. doi:10.3389/fpsyg.2014.01387.CrossRefGoogle Scholar
Kendler, K. S., Neale, M. C., MacLean, C. J., Heath, A. C., Eaves, L. J., & Kessler, R. C. (1993). Smoking and major depression. A causal analysis. Archives of General Psychiatry, 50(1), 36–43. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/8422220.CrossRefGoogle ScholarPubMed
Latvala, A., Kuja-Halkola, R., Almqvist, C., Larsson, H., & Lichtenstein, P. (2015). A longitudinal study of resting heart rate and violent criminality in more than 700000 men. JAMA Psychiatry, 72(10), 971–978.CrossRefGoogle ScholarPubMed
Latvala, A., Kuja-Halkola, R., Ruck, C., D'Onofrio, B. M., Jernberg, T., Almqvist, C., … Lichtenstein, P. (2016). Association of resting heart rate and blood pressure in late adolescence with subsequent mental disorders: A longitudinal population study of more than 1 million men in Sweden. JAMA Psychiatry, 73(12), 1268–1275. doi:10.1001/jamapsychiatry.2016.2717.CrossRefGoogle ScholarPubMed
Lichtenstein, P., Sullivan, P. F., Cnattingius, S., Gatz, M., Johansson, S., Carlstrom, E., … Pedersen, N. L. (2006). The Swedish Twin Registry in the third millennium: An update. Twin Research and Human Genetics, 9(6), 875–882. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/17254424.CrossRefGoogle ScholarPubMed
Miles, D. R., van den Bree, M. B., Gupman, A. E., Newlin, D. B., Glantz, M. D., & Pickens, R. W. (2001). A twin study on sensation seeking, risk taking behavior and marijuana use. Drug and Alcohol Dependence, 62(1), 57–68. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11173168.CrossRefGoogle ScholarPubMed
Neale, M. C., Hunter, M. D., Pritikin, J. N., Zahery, M., Brick, T. R., Kirkpatrick, R. M., … Boker, S. M. (2016). Openmx 2.0: Extended structural equation and statistical modeling. Psychometrika, 81(2), 535–549. doi:10.1007/s11336-014-9435-8.CrossRefGoogle ScholarPubMed
Ohlsson, H., & Kendler, K. S. (2019). Applying causal inference methods in psychiatric epidemiology: A review. JAMA Psychiatry, December 11, 2019([epub]). https://doi.org/10.1001/jamapsychiatry.2019.3758.Google Scholar
Ortiz, J., & Raine, A. (2004). Heart rate level and antisocial behavior in children and adolescents: A meta-analysis. Journal of the American Academy of Child and Adolescent Psychiatry, 43(2), 154–162. doi:10.1097/00004583-200402000-00010.CrossRefGoogle ScholarPubMed
Portnoy, J., & Farrington, D. P. (2015). Resting heart rate and antisocial behavior: An updated systematic review and meta-analysis. Aggression and Violent Behavior, 22, 33–45.CrossRefGoogle Scholar
Portnoy, J., Raine, A., Chen, F. R., Pardini, D., Loeber, R., & Jennings, J. R. (2014). Heart rate and antisocial behavior: The mediating role of impulsive sensation seeking. Criminology; An Interdisciplinary Journal, 52(2), 292–311.Google Scholar
Raine, A. (2002). Annotation: The role of prefrontal deficits, low autonomic arousal, and early health factors in the development of antisocial and aggressive behavior in children. Journal of Child Psychology and Psychiatry, 43(4), 417–434. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12030589.CrossRefGoogle ScholarPubMed
Raine, A., Venables, P. H., & Mednick, S. A. (1997). Low resting heart rate at age 3 years predisposes to aggression at age 11 years: Evidence from the Mauritius Child Health Project. Journal American Academy of Child and Adolescent Psychiatry, 36(10), 1457–1464.CrossRefGoogle ScholarPubMed
Schiweck, C., Piette, D., Berckmans, D., Claes, S., & Vrieze, E. (2019). Heart rate and high frequency heart rate variability during stress as biomarker for clinical depression. A systematic review. Psychological Medicine, 49(2), 200–211. doi:10.1017/S0033291718001988.CrossRefGoogle ScholarPubMed
Sijtsema, J. J., Veenstra, R., Lindenberg, S., Van Roon, A. M., Verhulst, F. C., Ormel, J., & Riese, H. (2010). Mediation of sensation seeking and behavioral inhibition on the relationship between heart rate and antisocial behavior: The TRAILS study. Journal of the American Academy of Child and Adolescent Psychiatry, 49(5), 493–502. doi:10.1097/00004583-201005000-00010.Google ScholarPubMed
Snieder, H., Harshfield, G. A., & Treiber, F. A. (2003). Heritability of blood pressure and hemodynamics in African- and European-American youth. Hypertension, 41(6), 1196–1201. doi:10.1161/01.HYP.0000072269.19820.0D.CrossRefGoogle ScholarPubMed
Stoel, R. D., de Geus, E. J., & Boomsma, D. I. (2006). Genetic analysis of sensation seeking with an extended twin design. Behavior Genetics, 36(2), 229–237. doi:10.1007/s10519-005-9028-5.CrossRefGoogle ScholarPubMed