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Effects of Cognitive-Behavioral Therapy (CBT) on Brain Connectivity Supporting Catastrophizing in Fibromyalgia

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Effects of Cognitive-Behavioral Therapy (CBT) on Brain Connectivity Supporting Catastrophizing in Fibromyalgia ORIGINAL ARTICLE Effects of Cognitive-Behavioral Therapy (CBT) on Brain Connectivity Supporting Catastrophizing in Fibromyalgia Asimina Lazaridou, PhD,* Jieun Kim, PhD,wz Christine M. Cahalan, BSc,* Marco L. Loggia, PhD,*w Olivia Franceschelli, BSc,* Chantal Berna, MD,* Peter Schur, MD,y Vitaly Napadow, PhD,*w and Robert R. Edwards, PhD* Discussion: The results add to the growing support for the clinically Objective(s): Fibromyalgia (FM) is a chronic, common pain disorder important associations between S1-insula connectivity, clinical characterized by hyperalgesia. A key mechanism by which cognitive- pain, and catastrophizing, and suggest that CBT may, in part via behavioral therapy (CBT) fosters improvement in pain outcomes is via reductions in catastrophizing, help to normalize pain-related brain reductions in hyperalgesia and pain-related catastrophizing, a dys- responses in FM. functional set of cognitive-emotional processes. However, the neural underpinnings of these CBT effects are unclear. Our aim was to assess Key Words: cognitive behavioral therapy (CBT), insula, fibro- CBT’s effects on the brain circuitry underlying hyperalgesia in FM myalgia, fMRI, catastrophizing patients, and to explore the role of treatment-associated reduction in catastrophizing as a contributor to normalization of pain-relevant (Clin J Pain 2017;33:215–221) brain circuitry and clinical improvement. Methods: In total, 16 high-catastrophizing FM patients were enrolled in the study and randomized to 4 weeks of individual treatment with either CBT or a Fibromyalgia Education (control) ibromyalgia (FM) is a chronic musculoskeletal pain condition. Resting state functional magnetic resonance imaging Fcondition that affects 2% to 4% of the population and is scans evaluated functional connectivity between key pain- characterized by anatomically widespread pain symptoms processing brain regions at baseline and posttreatment. Clinical accompanied by fatigue, disturbed sleep, and mood.1–5 FM outcomes were assessed at baseline, posttreatment, and 6-month pain is experienced predominantly in the muscles and soft follow-up. tissue, although the diverse and widespread symptoms may Results: Catastrophizing correlated with increased resting state also extend to nearly any anatomic region. This breadth of functional connectivity between S1 and anterior insula. The CBT symptomatology is consistent with the view that FM is a group showed larger reductions (compared with the education pervasive nervous system disorder6 involving a complex group) in catastrophizing at posttreatment (P < 0.05), and CBT interaction of biopsychosocial mechanisms. Some of the produced significant reductions in both pain and catastrophizing at hallmarks of FM include: (1) alterations in central pain- the 6-month follow-up (P < 0.05). Patients in the CBT group also showed reduced resting state connectivity between S1 and anterior/ modulatory processes in the spinal cord and brain, (2) a medial insula at posttreatment; these reductions in resting state prominent role of negative affective factors in maintaining connectivity were associated with concurrent treatment-related pain and disability, (3) a relative lack of efficacy of many reductions in catastrophizing. “peripheral” treatments such as local trigger point injections. Although FM is often considered challenging to treat, Received for publication December 5, 2015; revised August 11, 2016; some pharmacologic and nonpharmacologic interventions accepted July 16, 2016. have shown promise in reducing its symptoms and impact. y From the Departments of *Anesthesiology; Medicine, Division of Recent meta-analyses and reviews suggest that cognitive- Rheumatology, Harvard Medical School, Brigham & Women’s Hospital, Chestnut Hill; wMGH/MIT/HMS Athinoula A. Martinos behavioral therapy (CBT), compared with other active Center for Biomedical Imaging, Charlestown, MA; and zClinical treatments, reduces pain intensity, disability, and emo- Research Division, Korea Institute of Oriental Medicine, Daejeon, tional distress among individuals with FM.7 CBT uses Korea. active, structured techniques to alter distorted thoughts V.N. and R.R.E. contributed equally. Supported by NIH grant R01-AR064367, by grants to RRE from the and negative moods, and with as few as 2 to 4 sessions, can Arthritis Foundation and the American College of Rheumatology produce adaptive, lasting changes in pain-related and grant P01-AT006663, R01-AT007550 to VN by the National outcomes.8–10 Center for Complementary and Integrative Health (NCCIH). The Although the mechanisms supporting CBT’s benefits project was carried out in part at the Athinoula A. Martinos Center 11 for Biomedical Imaging at the Massachusetts General Hospital, have not been fully elucidated, it is known that CBT acts Charlestown, MA, using resources provided by the Center for to reduce negative affective responses to pain such as those Functional Neuroimaging Technologies, P41EB015896, a P41 characterized by pain-related catastrophizing.12 Catas- Biotechnology Resource Grant supported by the National Institute trophizing, commonly measured by the Pain Catastroph- of Biomedical Imaging and Bioengineering (NIBIB), National 13 Institutes of Health and the KIOM grant K16051. The authors izing Scale (PCS), is a pain-specific psychosocial construct declare no conflict of interests. comprised of cognitive and emotional processes such as Reprints: Robert R. Edwards, PhD, Brigham & Women’s Hospital, helplessness, pessimism, rumination about pain-related Pain Management Center, 850 Boylston St., Chestnut Hill, MA symptoms, and magnification of pain.10,14 Although cata- 02467 (e-mail: [email protected]). Copyright r 2016 Wolters Kluwer Health, Inc. All rights reserved. strophizing positively correlates with general measures of DOI: 10.1097/AJP.0000000000000422 negative affect such as depressive symptoms and anxiety, it Clin J Pain Volume 33, Number 3, March 2017 www.clinicalpain.com | 215 Copyright r 2017 Wolters Kluwer Health, Inc. All rights reserved. Lazaridou et al Clin J Pain Volume 33, Number 3, March 2017 also has a unique and specific influence on pain-related outcomes.12 Overall, greater catastrophizing is associated with amplified attentional focus on pain,15–17 serves as a risk factor for long-term pain,18 and correlates with the presence of disproportionately negative sequelae of pain (eg, worsening physical and psychological disability and/or higher health care costs).19–21 Process analyses of CBT treatment studies indicate that changes in catastrophizing and negative affect precede changes in clinical pain, and that CBT’s effects on catastrophizing last for months or years.22,23 Despite a recent proliferation of research on CBT for chronic pain, however, there has been very limited investigation of its effects on the central nervous system’s processing of pain-related information in FM.24 Indeed, only 1 controlled, neuroimaging-based, study25 of a CBT treatment has been conducted in FM patients; the CBT group showed changes in activation and connectivity within regions of the prefrontal cortex at posttreatment, and reported reductions in anxiety and pain at the 3-month follow-up. FIGURE 1. Study flow. CBT indicates cognitive behavioral The Jensen et al25 trial represents an important step therapy. toward characterizing the neural mechanisms by which CBT shapes long-term improvements in pain-related out- comes. Unfortunately, there are no published studies of the them were randomized to treatment. The Partners Human role of catastrophizing in contributing to these outcomes. Research Committee approved this study, and written Given that previous non-neuroimaging CBT studies have informed consent was obtained from all participants. After identified catastrophizing as a crucial process variable, it the baseline visit, FM patients were randomly assigned into seems likely that changes in catastrophizing may contribute either a month-long 4-session individual CBT treatment critically to the putative “normalization” of brain function program or a month-long 4-session FM education treat- that CBT produces. Moreover, several recent functional ment program. The education group received CBT fol- magnetic resonance imaging (fMRI) studies have indicated lowing completion of their posttreatment assessment and that catastrophizing in patients with functional pain then both groups were followed up at 6 months conditions such as FM and irritable bowel syndrome is posttreatment. associated with the hyperalgesia that characterizes these Specific trial eligibility criteria were as follows: conditions, and also with alterations in pain-related brain Inclusion criteria: (1) At least 18 years old, (2) activation or functional connectivity.26–28 Specifically, Kim documented presence of rheumatologist-diagnosed et al26 found that pain-evoked increase in primary soma- FM for at least 1 year, (3) meet the revised Wolfe tosensory cortex (S1)-insula connectivity was correlated et al34 ACR criteria for FM, and (4) score on the PCS with catastrophizing—patients with greater PCS scores also of at least 21 (ie, a range that represents the top 50% demonstrated greater pain-evoked increases in S1-insula of FM patients in our earlier samples.27,29 connectivity. Our aim in the present randomized, controlled Exclusion criteria: (1) History of clinically significant trial was to assess CBT’s effects on brain circuitry under- anxiety symptoms interfering with fMRI procedures lying clinical pain and hyperalgesia, and to evaluate the (eg, claustrophobia, panic
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