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Adverse childhood experiences predict autonomic indices of emotion dysregulation and negative emotional cue-elicited craving among female opioid-treated chronic pain patients

  • Eric L. Garland (a1), Sarah E. Reese (a1), Carter E. Bedford (a1) and Anne K. Baker (a1)

Abstract

Through autonomic and affective mechanisms, adverse childhood experiences (ACEs) may disrupt the capacity to regulate negative emotions, increasing craving and exacerbating risk for opioid use disorder (OUD) among individuals with chronic pain who are receiving long-term opioid analgesic pharmacotherapy. This study examined associations between ACEs, heart rate variability (HRV) during emotion regulation, and negative emotional cue-elicited craving among a sample of female opioid-treated chronic pain patients at risk for OUD. A sample of women (N = 36, mean age = 51.2 ± 9.5) with chronic pain receiving long-term opioid analgesic pharmacotherapy (mean morphine equivalent daily dose = 87.1 ± 106.9 mg) were recruited from primary care and pain clinics to complete a randomized task in which they viewed and reappraised negative affective stimuli while HRV and craving were assessed. Both ACEs and duration of opioid use significantly predicted blunted HRV during negative emotion regulation and increased negative emotional cue-elicited craving. Analysis of study findings from a multiple-levels-of-analysis approach suggest that exposure to childhood abuse occasions later emotion dysregulation and appetitive responding toward opioids in negative affective contexts among adult women with chronic pain, and thus this vulnerable clinical population should be assessed for OUD risk when initiating a course of extended, high-dose opioids for pain management.

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Corresponding author

Author for Correspondence: Eric L. Garland, 395 South, 1500 East, University of Utah, Salt Lake City, UT 84112; E-mail: elgarlan@gmail.com.

References

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American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Washington, DC: Author.
Appelhans, B. M., & Luecken, L. J. (2006). Heart rate variability as an index of regulated emotional responding. Review of General Psychology, 10, 229240.
Barahmand, U., Khazaee, A., & Hashjin, G. S. (2016). Emotion dysregulation mediates between childhood emotional abuse and motives for substance use. Archives of Psychiatric Nursing, 30, 653659. doi:10.1016/j.apnu.2016.02.007
Beauchaine, T. P. (2015). Future directions in emotion dysregulation and youth psychopathology. Journal of Clinical Child and Adolescent Psychology, 44, 875896.
Beauchaine, T. P., & Thayer, J. F. (2015). Heart rate variability as a transdiagnostic biomarker of psychopathology. International Journal of Psychophysiology, 98, 338350.
Becker, J. B. (2016). Sex differences in addiction. Dialogues in Clinical Neuroscience, 18, 395402.
Berntson, G. G., Bigger, J. T. Jr., Eckberg, D. L., Grossman, P., Kaufman, P. G., Malik, M., … van der Molen, M. W. (1997). Heart rate variability: Origins, methods, and interpretive caveats. Psychophysiology, 34, 623648.
Berridge, K. C., & Robinson, T. E. (2016). Liking, wanting, and the incentive-sensitization theory of addiction. American Psychologist, 71, 670.
Boscarino, J. A., Hoffman, S. N., & Han, J. J. (2015). Opioid-use disorder among patients on long-term opioid therapy: Impact of final DSM-5 diagnostic criteria on prevalence and correlates. Substance Abuse and Rehabilitation, 6, 8391.
Brown, R., Deyo, B., Riley, C., Quanbeck, A., Glass, J. E., Turpin, R., … Agarwal, S. (2017). Screening in Trauma for Opioid Misuse Prevention (STOMP): Study protocol for the development of an opioid risk screening tool for victims of injury. Addiction Science & Clinical Practice, 12, 28.
Burr, R. L. (2007). Interpretation of normalized spectral heart rate variability indices in sleep research: A critical review. Sleep, 30, 913919.
Butler, E. A., Wilhelm, F. H., & Gross, J. J. (2006). Respiratory sinus arrhythmia, emotion, and emotion regulation during social interaction. Psychophysiology, 43, 612622.
Carter, B. L., & Tiffany, S. T. (1999). Meta-analysis of cue-reactivity in addiction research. Addiction, 94, 327340.
Case, A., & Deaton, A. (2015). Rising morbidity and mortality in midlife among white non-Hispanic Americans in the 21st century. Proceedings of the National Academy of Sciences, 112, 1507815083.
Centers for Disease Control and Prevention. (2018). Annual surveillance report of drug-related risks and outcomes—United States. Retrieved from https://www.cdc.gov/drugoverdose/pdf/pubs/2018-cdc-drug-surveillance-report.pdf
Chou, R., Fanciullo, G. J., Fine, P. G., Adler, J. A., Ballantyne, J. C., Davies, P., … American Pain Society—American Academy of Pain Medicine Opioid Guidelines Panel. (2009). Clinical guidelines for the use of chronic opioid therapy in chronic noncancer pain. Journal of Pain, 10, 113130.
Cicchetti, D., & Dawson, G. (2002). Multiple levels of analysis. Development and Psychopathology, 14, 417420.
Cohen, R. A., Grieve, S., Hoth, K. F., Paul, R. H., Sweet, L., Tate, D., … Williams, L. M. (2006). Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biological Psychiatry, 59, 975982.
Cole, P. M., Hall, S. E., & Hajal, N. J. (2013). Emotion dysregulation as a risk factor for psychopathology. In Beauchaine, T. P. & Hinshaw, S. P. (Eds.), Child and adolescent psychopathology (2nd ed., pp. 341373). Hoboken, NJ: Wiley.
Danese, A., & McEwen, B. S. (2012). Adverse childhood experiences, allostasis, allostatic load, and age-related disease. Physiology & Behavior, 106, 2939. doi:10.1016/j.physbeh.2011.08.019
Degenhardt, L., Bruno, R., Lintzeris, N., Hall, W., Nielsen, S., Larance, B., … Campbell, G. (2015). Agreement between definitions of pharmaceutical opioid use disorders and dependence in people taking opioid for chronic non-cancer pain (POINT): A cohort study. Lancet Psychiatry, 2, 314322.
Di Simplicio, M., Costoloni, G., Western, D., Hanson, B., Taggart, P., & Harmer, C. J. (2012). Decreased heart rate variability during emotion regulation in subjects at risk for psychopathology. Psychological Medicine, 42, 17751783.
Dube, S. R., Felitti, V. J., Dong, M., Chapman, D. P., Giles, W. H., & Anda, R. F. (2003). Childhood abuse, neglect, and household dysfunction and the risk of illicit drug use: The Adverse Childhood Experiences Study. Pediatrics, 111, 564572.
Dvir, Y., Ford, J. D., Hill, M., & Frazier, J. A. (2014). Childhood maltreatment, emotional dysregulation, and psychiatric comorbidities. Harvard Review of Psychiatry, 22, 149161.
Epstein, D. H., Wilner-Reid, J., Vahabzadeh, M., Mezghanni, M., Lin, J. L., & Preston, K. L. (2009). Real-time electronic diary reports of cue exposure and mood in the hours before cocaine and heroin craving and use. Archives of General Psychiatry, 66, 8894.
Felitti, V., Anda, R., Nordenberg, D., Williamson, D., Spitz, A., Edwards, V., … Marks, J. (1998). Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. American Journal of Prevention Medicine, 14, 245258.
Gallo, L. C. (2009). The reserve capactiy model as a framework for understanding psychosocial factors in health disparities. Applied Psychology: Health and Well-Being, 1, 6272.
Garland, E. L., Brown, S. M., & Howard, M. O. (2016). Thought suppression as a mediator of the association between depressed mood and prescription opioid craving among chronic pain patients. Journal of Behavioral Medicine, 39, 128138.
Garland, E. L., Bryan, C. J., Nakamura, Y., Froeliger, B., & Howard, M. O. (2017). Deficits in autonomic indices of emotion regulation and reward processing associated with prescription opioid use and misuse. Psychopharmacology, 234, 621629.
Garland, E. L., Carter, K., Ropes, K., & Howard, M. O. (2012). Thought suppression, impaired regulation of urges, and Addiction-Stroop predict affect-modulated cue-reactivity among alcohol dependent adults. Biological Psychology, 89, 8793.
Garland, E. L., Froeliger, B., & Howard, M. O. (2014). Effects of mindfulness-oriented recovery enhancement on reward responsiveness and opioid cue-reactivity. Psychopharmacology, 231, 32293238. doi:10.1007/s00213-014-3504-7
Garland, E. L., Froeliger, B., Zeidan, F., Partin, K., & Howard, M. O. (2013). The downward spiral of chronic pain, prescription opioid misuse, and addiction: Cognitive, affective, and neuropsychopharmacologic pathways. Neuroscience & Biobehavioral Reviews, 37, 25972607.
Garland, E. L., Hanley, A. W., Riquino, M. R., Reese, S. E., Baker, A. K., Bryan, M. A., … Howard, M. O. (2019). Mindfulness-oriented recovery enhancement reduces opioid misuse risk via analgesic and positive psychological mechanisms: A randomized controlled trial. Journal of Consulting and Clinical Psychology. Advance online publication.
Garland, E. L., Hanley, A. W., Thomas, E. A., Knoll, P., & Ferraro, J. (2015). Low dispositional mindfulness predicts self-medication of negative emotion with prescription opioids. Journal of Addiction Medicine, 9, 6167.
Garland, E. L., Manusov, E. G., Froeliger, B., Kelly, A., Williams, J. M., & Howard, M. O. (2014). Mindfulness-oriented recovery enhancement for chronic pain and prescription opioid misuse: Results from an early-stage randomized controlled trial. Journal of Consulting and Clinical Psychology, 82, 448.
Garland, E. L., Pettus-Davis, C., & Howard, M. O. (2013). Self-medication among traumatized youth: Structural equation modeling of pathways between trauma history, substance misuse, and psychological distress. Journal of Behavioral Medicine, 36, 175185.
Garland, E. L., Roberts-Lewis, A., Tronnier, C. D., Graves, R., & Kelley, K. (2016b). Mindfulness-oriented recovery enhancement versus CBT for co-occurring substance dependence, traumatic stress, and psychiatric disorders: Proximal outcomes from a pragmatic randomized trial. Behaviour Research and Therapy, 77, 716.
Gillie, B. L., & Thayer, J. F. (2014). Individual differences in resting heart rate variability and cognitive control in posttraumatic stress disorder. Frontiers in Psychology, 5, 758.
Gross, J. J., & John, O. P. (2003). Individual differences in two emotion regulation processes: Implications for affect, relationships, and well-being. Journal of Personality and Social Psychology, 85, 348362.
Hassan, A. N., Foll, B. L., Imtiaz, S., & Rehm, J. (2017). The effect of post-traumatic stress disorder on the risk of developing prescription opioid use disorder: Results from the National Epidemiologic Survey on Alcohol and Related Conditions III. Drug and Alcohol Dependence, 179, 260266.
Heckman, B. W., Kovacs, M. A., Marquinez, N. S., Meltzer, L. R., Tsambarlis, M. E., Drobes, D. J., & Brandon, T. H. (2013). Influence of affective manipulations on cigarette craving: A meta-analysis. Addiction, 108, 20682078.
Heim, C., & Nemeroff, C. B. (2002). Neurobiology of early life stress: Clinical studies. Seminar in Clinical Neuropsychiatry, 7, 147159.
Heim, C., Newport, D. J., Heit, S., Graham, Y. P., Wilcox, M., Bonsall, R., … Nemeroff, C. B. (2000). Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. Journal of the American Medical Association, 284, 592597.
Holzman, J. B., & Bridgett, D. J. (2017). Heart rate variability indices as bio-markers of top-down self-regulatory mechanisms: A meta-analytic review. Neuroscience and Biobehavioral Reviews, 74, 233255.
Hovland, A., Pallesen, S., Hammar, A., Hansen, A. L., Thayer, J. F., Tarvainen, M. P., & Nordhus, I. H. (2012). The relationship among heart rate variability, executive functions, and clinical variables in patients with panic disorder. Intervnational Journal of Psychophysiology, 86, 269275.
Huhn, A. S., Meyer, R. E., Harris, J. D., Ayaz, H., Deneke, E., Stankoski, D. M., & Bunce, S. C. (2016). Evidence of anhedonia and differential reward processing in prefrontal cortex among post-withdrawal patients with prescription opiate dependence. Brain Research Bulletin, 123, 102109.
Ingjaldsson, J. T., Laberg, J. C., & Thayer, J. F. (2003). Reduced heart rate variability in chronic alcohol abuse: Relationship with negative mood, chronic thought suppression, and compulsive drinking. Biological Psychiatry, 54, 14271436.
Jackson, D. C., Malmstadt, J. R., Larson, C. L., & Davidson, R. J. (2000). Suppression and enhancement of emotional responses to unpleasant pictures. Psychophysiology, 37, 515522.
Jarrahi, B., Johnson, K., & Mackey, S. (2018). Effect of opioids on brain morphometrics in patients with chronic low back pain: A pilot MRI study. Journal of Pain, 19, S7.
Jovanovic, T., Blanding, N. Q., Norrholm, S. D., Duncan, E., Bradley, B., & Ressler, K. J. (2009). Childhood abuse is associated with increased startle reactivity in adulthood. Depression and Anxiety, 26, 10181026.
Kim, J., & Cicchetti, D. (2010). Longitudinal pathways linking child maltreatment, emotion regulation, peer relations, and psychopathology. Journal of Child Psychology and Psychiatry, 51, 706716.
Koob, G. F., & Volkow, N. D. (2016). Neurobiology of addiction: A neurocircuitry analysis. Lancet Psychiatry, 3, 760773.
Lang, P., Bradley, M., & Cuthbert, B. (1997). International Affective Picture System (IAPS): Technical manual and affective ratings. Rockville, MD: NIMH Center for the Study of Emotion and Attention.
Lazarus, R., & Folkman, S. (1984). Stress, appraisal, and coping. New York: Springer.
Malliani, A., Lombardi, F., & Pagani, M. (1994). Power spectrum analysis of heart rate variability: A tool to explore neural regulatory mechanisms. British Heart Journal, 71, 12.
Martel, M. O., Dolman, A. J., Edwards, R. R., Jamison, R. N., & Wasan, A. D. (2014). The association between negative affect and prescription opioid misuse in patients with chronic pain: The mediating role of opioid craving. Journal of Pain, 15, 90100.
McCauley, J., Kern, D. E., Kolodner, K., Dill, L., Schroeder, A. F., DeChant, H. K., … Bass, E. B. (1997). Clinical characteristics of women with a history of childhood abuse: Unhealed wounds. Journal of the American Medical Association, 277, 13621368.
McEwen, B. S. (2003). Interacting mediators of allostasis and allostatic load: Towards an understanding of resilience in aging. Metabolism, 52, 1016.
McHugh, R. K., Fitzmaurice, G. M., Carroll, K. M., Griffin, M. L., Hill, K. P., Wasan, A. D., & Weiss, R. D. (2014). Assessing craving and its relationship to subsequent prescription opioid use among treatment-seeking prescroption opioid dependent patients. Drug & Alcohol Dependence, 145, 121126.
Meyer, P. W., Müller, L. E., Zastrow, A., Schmidinger, I., Bohus, M., Herpertz, S. C., & Bertsch, K. (2016). Heart rate variability in patients with post-traumatic stress disorder or borderline personality disorder: Relationship to early life maltreatment. Journal of Neural Transmission, 123(9), 11071118.
Mullen, P. E., Martin, J. L., Anderson, J. C., Romans, S. E., & Herbison, G. P. (1996). The long-term impact of the physical, emotional, and sexual abuse of children: A community study. Child Abuse & Neglect, 20, 721. doi:10.1016/0145-2134(95)00112-3
Naqvi, N. H., Gaznick, N., Tranel, D., & Bechara, A. (2014). The insula: A critical neural substrate for craving and drug seeking under conflict and risk. Annals of the New York Academy of Sciences, 1316, 5370. doi:10.1111/nyas.12415
Nemeroff, C. (2016). Paradise lost: The neurobiological and clinical consequences of child abuse and neglect. Neuron, 89, 892909.
Ochsner, K. N., Bunge, S. A., Gross, J. J., & Gabrieli, J. D. E. (2002). Rethinking feelings: An fMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience, 14, 12151229.
Quintana, D. S., McGregor, I. S., Guastella, A. J., Malhi, G. S., & Kemp, A. H. (2013). A meta-analysis on the impact of alcohol dependence on short-term resting-state heart rate variability: Implications for cardiovascular risk. Alcoholism: Clinical and Experimental Research, 37, E23E29.
Radley, J., Morilak, D., Viau, V., & Campeau, S. (2015). Chronic stress and brain plasticity: Mechanisms underlying adaptive and maladaptive changes and implications for stress-related CNS disorders. Neuroscience & Biobehavioral Reviews, 58, 7991. doi:10.1016/j.neubiorev.2015.06.018
Sachs-Ericsson, N. J., Sheffler, J. L., Stanley, I. H., Piazza, J. R., & Preacher, K. J. (2017). When emotional pain becomes physical: Adverse childhood experiences, pain, and the role of mood and anxiety disorders. Journal of Clinical Psychology, 73, 14021428.
Segerstrom, S. C., & Nes, L. S. (2007). Heart rate variability reflects self-regulatory strength, effort, and fatigue. Psychological Science, 18, 275281.
Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., … Dunbar, G. C. (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry, 59(Suppl. 20), 2233; quiz 34–57.
Stein, E. M., Gennuso, K. P., Ugboaja, D. C., & Remington, P. L. (2017). The epidemic of despair among White Americans: Trends in the leading causes of premature death, 1999–2015. American Journal of Public Health, 107, 15411547.
Stein, M. D., Conti, M. T., Kenney, S., Anderson, B. J., Flori, J. N., Risi, M. M., & Bailey, G. L. (2017b). Adverse childhood experience effects on opioid use initiation, injection drug use, and overdose among persons with opioid use disorder. Drug and Alcohol Dependence, 179, 325329.
Thayer, J. F., Åhs, F., Fredrikson, M., Sollers, J. J. III, & Wager, T. D. (2012). A meta-analysis of heart rate variability and neuroimaging studies: Implications for heart rate variability as a marker of stress and health. Neuroscience & Biobehavioral Reviews, 36, 747756. doi:10.1016/j.neubiorev.2011.11.009
Thayer, J. F., & Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61, 201216.
Thayer, J. F., & Lane, R. D. (2009). Claude Bernard and the heart-brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience and Biobehavioral Reviews, 33, 8188.
Tiffany, S. T., & Wray, J. M. (2012). The clinical significance of drug craving. Annals of the New York Academy of Sciences, 1248, 117.
Tsui, J. I., Lira, M. C., Cheng, D. M., Winter, M. R., Alford, D. P., Liebschutz, J. M., … Samet, J. H. (2016). Chronic pain, craving, and illicity opioid use among patients receiving opioid agonist therapy. Drug and Alcohol Dependence, 166, 2631.
Upadhyay, J., Maleki, N., Potter, J., Elman, I., Rudrauf, D., Knudsen, J., … Borsook, D. (2010). Alterations in brain structure and functional connectivity in prescription opioid-dependent patients. Brain, 133, 20982114. doi:10.1093/brain/awq138
van Hammelen, A. L., van Tol, M. J., van der Wee, N. J., Veltman, D. J., Aleman, A., Spinhoven, P., … Elzinga, B. M. (2010). Reduced medial prefrontal cortex volume in adults reporting childhood emotional maltreatment. Biological Psychiatry, 68, 832838. doi:10.1016/j.biopsych.2010.06.011
Wasan, A. D., Butler, S. F., Budman, S. H., Fernandez, K., Weiss, R. D., Greenfield, S. F., & Jamison, R. N. (2009). Does report of craving opioid medication predict aberrant drug behavior among chronic pain patients? Clinical Journal of Pain, 25, 193198.
Wasan, A. D., Ross, E. L., Michna, E., Chibnik, L., Greenfield, S. F., Weiss, R. D., & Jamison, R. N. (2012). Craving of prescription opioids in patients with chronic pain: A longitudinal outcomes trial. Journal of Pain, 13, 146154.
Williams, D. P., Cash, C., Rankin, C., Bernardi, A., Koenig, J., & Thayer, J. F. (2015). Resting heart rate variability predicts self-reported difficulties in emotion regulation: A focus on different facets of emotion regulation. Emotion Science, 6, 261. doi:10.3389/fpsyg.2015.00261
Younger, J. W., Chu, L. F., D'Arcy, N. T., Trott, K. E., Jastrzab, L. E., & Mackey, S. C. (2011). Prescription opioid analgesics rapidly change the human brain. Pain, 152, 18031810. doi:10.1016/j.pain.2011.03.028

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