Hyperbaric Oxygen Therapy Can Induce Neuroplasticity and Significant Clinical Improvement in Patients Suffering From Fibromyalgia With a History of Childhood Sexual Abuse-Randomized Controlled Trial

Amir Hadanny, Yair Bechor, Merav Catalogna, Shir Daphna-Tekoah, Tal Sigal, Mehrzad Cohenpour, Rachel Lev-Wiesel, Shai Efrati, Amir Hadanny, Yair Bechor, Merav Catalogna, Shir Daphna-Tekoah, Tal Sigal, Mehrzad Cohenpour, Rachel Lev-Wiesel, Shai Efrati

Abstract

Background: Fibromyalgia syndrome (FMS), a condition considered to represent a prototype of central sensitization syndrome, can be induced by different triggers including childhood sexual abuse (CSA). Recent studies have demonstrated hyperbaric oxygen therapy (HBOT) can induce neuroplasticity and improve clinical outcome of FMS. The aim of the current study was to evaluate the effect of HBOT on patients suffering from FMS with a history of CSA. Materials and methods: A prospective randomized clinical trial conducted between July 2015 and November 2017 included women with a history of CSA who fulfilled fibromyalgia diagnosis criteria for at least 5 years prior to inclusion. Included participants (N = 30) were randomly assigned to treatment group, treated with 60 HBOT sessions and a control/crossover group received psychotherapy. After the control period, the control/crossover group was crossed to HBOT. Clinical outcomes were assessed using FMS questioners, post-traumatic stress disorder (PTSD) questioners and quality of life questioners. Objective outcome were assessed using brain function and structure imaging. Findings: Following HBOT, there was a significant improvement in all FMS questionnaires (widespread pain index, Fibromyalgia symptoms severity scale, Fibromyalgia functional impairment), most domains of quality of life, PTSD symptoms and psychological distress. The same significant improvements were demonstrated in the control following crossover to HBOT. Following HBOT, brain SPECT imaging demonstrated significant increase in brain activity in the prefrontal cortex, orbital frontal cortex, and subgenual area (p < 0.05). Brain microstructure improvement was seen by MRI-DTI in the anterior thalamic radiation (p = 0.0001), left Insula (p = 0.001), and the right Thalamus (p = 0.001). Conclusion: HBOT induced significant clinical improvement that correlates with improved brain functionality and brain microstructure in CSA related FMS patients. Trial Registration: www.Clinicaltrials.gov, identifier: NCT03376269. url: https://ichgcp.net/clinical-trials-registry/NCT03376269.

Keywords: CSA; FMS; HBOT; PTSD; childhood sexual abuse; fibromyalgia; hyperbaric oxygen; post trauma.

Figures

Figure 1
Figure 1
Participants flowchart.
Figure 2
Figure 2
The effect of HBOT on FMS diagnosis.
Figure 3
Figure 3
The effect of HBOT on Fibromyalgia impact questionnaire (FIQ).
Figure 4
Figure 4
(A) Projection of the significant changes between groups on the brain maps (B) Projection of the significant changes in the improved compared to non- improved participants on the brain maps.
Figure 5
Figure 5
Significant changes in brain microstructure following HBOT.

References

    1. Ablin J. N., Efrati S., Buskila D. (2016). Building up the pressure on chronic pain. Clin. Exp. Rheumatol. 34(2 Suppl. 96), S3–5.
    1. Amano T., Toichi M. (2016). Possible neural mechanisms of psychotherapy for trauma-related symptoms: cerebral responses to the neuropsychological treatment of post-traumatic stress disorder model individuals. Sci. Rep. 6:34610. 10.1038/srep34610
    1. Andersen S. L., Tomada A., Vincow E. S., Valente E., Polcari A., Teicher M. H. (2008). Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. J. Neuropsychiatry Clin. Neurosci. 20, 292–301. 10.1176/jnp.2008.20.3.292
    1. Benedetti F., Bollettini I., Radaelli D., Poletti S., Locatelli C., Falini A., et al. . (2014). Adverse childhood experiences influence white matter microstructure in patients with bipolar disorder. Psychol. Med. 44, 3069–3082. 10.1017/S0033291714000506
    1. Berthoz S., Armony J. L., Blair R. J., Dolan R. J. (2002). An fMRI study of intentional and unintentional (embarrassing) violations of social norms. Brain 125(Pt 8), 1696–1708. 10.1093/brain/awf190
    1. Bisson J. I., Ehlers A., Matthews R., Pilling S., Richards D., Turner S. (2007). Psychological treatments for chronic post-traumatic stress disorder. Systematic review and meta-analysis. Br. J. Psychiatry 190, 97–104. 10.1192/bjp.bp.106.021402
    1. Boussi-Gross R., Golan H., Fishlev G., Bechor Y., Volkov O., Bergan J., et al. . (2013). Hyperbaric oxygen therapy can improve post concussion syndrome years after mild traumatic brain injury - randomized prospective trial. PLoS ONE 8:e79995. 10.1371/journal.pone.0079995
    1. Boussi-Gross R., Golan H., Volkov O., Bechor Y., Hoofien D., Beeri M. S., et al. . (2015). Improvement of memory impairments in poststroke patients by hyperbaric oxygen therapy. Neuropsychology 29, 610–621. 10.1037/neu0000149
    1. Bremner J. D., Staib L. H., Kaloupek D., Southwick S. M., Soufer R., Charney D. S. (1999). Neural correlates of exposure to traumatic pictures and sound in Vietnam combat veterans with and without posttraumatic stress disorder: a positron emission tomography study. Biol. Psychiatry 45, 806–816. 10.1016/S0006-3223(98)00297-2
    1. Buskila D. (2009). Developments in the scientific and clinical understanding of fibromyalgia. Arthritis Res. Ther. 11:242. 10.1186/ar2720
    1. Buskila D., Neumann L. (1996). Assessing functional disability and health status of women with fibromyalgia: validation of a Hebrew version of the Fibromyalgia Impact Questionnaire. J. Rheumatol. 23, 903–906.
    1. Callahan K. L., Price J. L., Hilsenroth M. J. (2004). A review of interpersonal-psychodynamic group psychotherapy outcomes for adult survivors of childhood sexual abuse. Int. J. Group Psychother. 54, 491–519. 10.1521/ijgp.54.4.491.42770
    1. Cardinal R. N., Parkinson J. A., Hall J., Everitt B. J. (2002). Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev. 26, 321–352. 10.1016/S0149-7634(02)00007-6
    1. Clauw D. J., Arnold L. M., McCarberg B. H. (2011). The science of fibromyalgia. Mayo Clin. Proc. 86, 907–911. 10.4065/mcp.2011.0206
    1. Conversano C., Carmassi C., Bertelloni C. A., Marchi L., Micheloni T., Carbone M. G., et al. . (2018). Potentially traumatic events, PTSD and post-traumatic stress spectrum in patients with fibromyalgia. Clin. Exp. Rheumatol. [Epub ahead of print].
    1. Craig A. D. (2009). How do you feel–now? The anterior insula and human awareness. Nat. Rev. Neurosci. 10, 59–70. 10.1038/nrn2555
    1. Edna B., Foa D. S. R., Constance V., Dancu B., Rothbaum O. (1993). Reliability and validity of a brief instrument for assessing post-traumatic stress disorder. J. Trauma. Stress 6, 459–473. 10.1002/jts.2490060405
    1. Efrati S., Ben-Jacob E. (2014). Reflections on the neurotherapeutic effects of hyperbaric oxygen. Expert Rev. Neurother. 14, 233–236. 10.1586/14737175.2014.884928
    1. Efrati S., Fishlev G., Bechor Y., Volkov O., Bergan J., Kliakhandler K., et al. . (2013). Hyperbaric oxygen induces late neuroplasticity in post stroke patients–randomized, prospective trial. PLoS ONE 8:e53716. 10.1371/journal.pone.0053716
    1. Efrati S., Golan H., Bechor Y., Faran Y., Daphna-Tekoah S., Sekler G., et al. . (2015). Hyperbaric oxygen therapy can diminish fibromyalgia syndrome–prospective clinical trial. PLoS ONE 10:e0127012. 10.1371/journal.pone.0127012
    1. Efrati S., Hadanny A., Daphna-Tekoah S., Bechor Y., Tiberg K., Pik N., et al. . (2018). Recovery of repressed memories in fibromyalgia patients treated with hyperbaric oxygen - case series presentation and suggested bio-psycho-social mechanism. Front. Psychol. 9:848. 10.3389/fpsyg.2018.00848
    1. Ehring T., Welboren R., Morina N., Wicherts J. M., Freitag J., Emmelkamp P. M. (2014). Meta-analysis of psychological treatments for posttraumatic stress disorder in adult survivors of childhood abuse. Clin. Psychol. Rev. 34, 645–657. 10.1016/j.cpr.2014.10.004
    1. Fink L. A., Bernstein D., Handelsman L., Foote J., Lovejoy M. (1995). Initial reliability and validity of the childhood trauma interview: a new multidimensional measure of childhood interpersonal trauma. Am. J. Psychiatry 152, 1329–1335. 10.1176/ajp.152.9.1329
    1. Floresco S. B., Grace A. A. (2003). Gating of hippocampal-evoked activity in prefrontal cortical neurons by inputs from the mediodorsal thalamus and ventral tegmental area. J. Neurosci. 23, 3930–3943. 10.1523/JNEUROSCI.23-09-03930.2003
    1. Frodl T., Reinhold E., Koutsouleris N., Reiser M., Meisenzahl E. M. (2010). Interaction of childhood stress with hippocampus and prefrontal cortex volume reduction in major depression. J. Psychiatr. Res. 44, 799–807. 10.1016/j.jpsychires.2010.01.006
    1. Goldberg R. T., Pachas W. N., Keith D. (1999). Relationship between traumatic events in childhood and chronic pain. Disabil. Rehabil. 21, 23–30. 10.1080/096382899298061
    1. Goldenberg D. L. (2008). Multidisciplinary modalities in the treatment of fibromyalgia. J. Clin. Psychiatry 69 (Suppl 2), 30–34.
    1. Guedj E., Cammilleri S., Niboyet J., Dupont P., Vidal E., Dropinski J. P., et al. . (2008). Clinical correlate of brain SPECT perfusion abnormalities in fibromyalgia. J. Nucl. Med. 49, 1798–1803. 10.2967/jnumed.108.053264
    1. Guedj E., Taieb D., Cammilleri S., Lussato D., de Laforte C., Niboyet J., et al. . (2007). 99mTc-ECD brain perfusion SPECT in hyperalgesic fibromyalgia. Eur. J. Nucl. Med. Mol. Imaging 34, 130–134. 10.1007/s00259-006-0174-7
    1. Hadanny A., Efrati S. (2015). Oxygen–a limiting factor for brain recovery. Crit. Care 19:307. 10.1186/s13054-015-1034-2
    1. Hadanny A., Efrati S. (2016a). The efficacy and safety of hyperbaric oxygen therapy in traumatic brain injury. Expert Rev. Neurother. 16, 359–360. 10.1586/14737175.2016.1157018
    1. Hadanny A., Efrati S. (2016b). Treatment of persistent post-concussion syndrome due to mild traumatic brain injury: current status and future directions. Expert Rev. Neurother. 16, 875–887. 10.1080/14737175.2016.1205487
    1. Hadanny A., Golan H., Fishlev G., Bechor Y., Volkov O., Suzin G., et al. . (2015). Hyperbaric oxygen can induce neuroplasticity and improve cognitive functions of patients suffering from anoxic brain damage. Restor. Neurol. Neurosci. 33, 471–486. 10.3233/RNN-150517
    1. Häuser W., Galek A., Erbslöh-Möller B., Köllner V., Kühn-Becker H., Langhorst J., et al. . (2013). Posttraumatic stress disorder in fibromyalgia syndrome: prevalence, temporal relationship between posttraumatic stress and fibromyalgia symptoms, and impact on clinical outcome. Pain 154, 1216–1223. 10.1016/j.pain.2013.03.034
    1. Imbierowicz K., Egle U. T. (2003). Childhood adversities in patients with fibromyalgia and somatoform pain disorder. Eur. J. Pain 7, 113–119. 10.1016/S1090-3801(02)00072-1
    1. Irish L., Kobayashi I., Delahanty D. L. (2010). Long-term physical health consequences of childhood sexual abuse: a meta-analytic review. J. Pediatr. Psychol. 35, 450–461. 10.1093/jpepsy/jsp118
    1. Jensen K. B., Kosek E., Petzke F., Carville S., Fransson P., Marcus H., et al. . (2009). Evidence of dysfunctional pain inhibition in Fibromyalgia reflected in rACC during provoked pain. Pain 144, 95–100. 10.1016/j.pain.2009.03.018
    1. Kim S. J., Lyoo I. K., Lee Y. S., Kim J., Sim M. E., Bae S. J., et al. . (2007). Decreased cerebral blood flow of thalamus in PTSD patients as a strategy to reduce re-experience symptoms. Acta Psychiatr. Scand. 116, 145–153. 10.1111/j.1600-0447.2006.00952.x
    1. Lanius R. A., Williamson P. C., Hopper J., Densmore M., Boksman K., Gupta M. A., et al. . (2003). Recall of emotional states in posttraumatic stress disorder: an fMRI investigation. Biol. Psychiatry 53, 204–210. 10.1016/S0006-3223(02)01466-X
    1. Leemans A., Jeurissen B., Sijbers J., Jones D. (2009). ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. Proc. Intl. Soc. Mag. Reson. Med. 17, 3537.
    1. Lei D., Li L., Li L., Suo X., Huang X., Lui S., et al. . (2015). Microstructural abnormalities in children with post-traumatic stress disorder: a diffusion tensor imaging study at 3.0T. Sci. Rep. 5:8933. 10.1038/srep08933
    1. Liberzon I., Sripada C. S. (2008). The functional neuroanatomy of PTSD: a critical review. Prog. Brain Res. 167, 151–169. 10.1016/S0079-6123(07)67011-3
    1. Linnman C., Appel L., Söderlund A., Frans O., Engler H., Furmark T., et al. . (2009). Chronic whiplash symptoms are related to altered regional cerebral blood flow in the resting state. Eur. J. Pain 13, 65–70. 10.1016/j.ejpain.2008.03.001
    1. Lupien S. J., McEwen B. S., Gunnar M. R., Heim C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 10, 434–445. 10.1038/nrn2639
    1. Lutz J., Jäger L., de Quervain D., Krauseneck T., Padberg F., Wichnalek M., et al. . (2008). White and gray matter abnormalities in the brain of patients with fibromyalgia: a diffusion-tensor and volumetric imaging study. Arthritis Rheum. 58, 3960–3969. 10.1002/art.24070
    1. Martsolf D. S., Draucker C. B. (2005). Psychotherapy approaches for adult survivors of childhood sexual abuse: an integrative review of outcomes research. Issues Ment. Health Nurs. 26, 801–825. 10.1080/01612840500184012
    1. Matthey A., Cedraschi C., Piguet V., Besson M., Chabert J., Daali Y., et al. . (2013). Dual reuptake inhibitor milnacipran and spinal pain pathways in fibromyalgia patients: a randomized, double-blind, placebo-controlled trial. Pain Phys. 16, E553–562. 10.1016/j.clinthera.2013.07.026
    1. McBeth J., Macfarlane G. J., Benjamin S., Morris S., Silman A. J. (1999). The association between tender points, psychological distress, and adverse childhood experiences: a community-based study. Arthritis Rheum. 42, 1397–1404. 10.1002/1529-0131(199907)42:7<1397::AID-ANR13>;2-7
    1. McHorney C. A., Ware J. E., Jr., Lu J. F., Sherbourne C. D. (1994). The MOS 36-item short-form health survey (SF-36): III. tests of data quality, scaling assumptions, and reliability across diverse patient groups. Med Care 32, 40–66. 10.1097/00005650-199401000-00004
    1. McHorney C. A., Ware J. E., Jr., Raczek A. E. (1993). The MOS 36-item short-form health survey (SF-36): II. Psychometric and clinical tests of validity in measuring physical and mental health constructs. Med Care 31, 247–263. 10.1097/00005650-199303000-00006
    1. Monkul E. S., Silva L. A., Narayana S., Peluso M. A., Zamarripa F., Nery F. G., et al. . (2012). Abnormal resting state corticolimbic blood flow in depressed unmedicated patients with major depression: a (15)O-H(2)O PET study. Hum. Brain Mapp. 33, 272–279. 10.1002/hbm.21212
    1. Niida R., Mimura M. (2017). [The Center of Sadness, Pain, and Recognition]. Brain Nerve 69, 417–426. 10.11477/mf.1416200759
    1. Phillips M. L., Drevets W. C., Rauch S. L., Lane R. (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biol. Psychiatry 54, 504–514. 10.1016/S0006-3223(03)00168-9
    1. Recklitis C. J., Parsons S. K., Shih M. C., Mertens A., Robison L. L., Zeltzer L. (2006). Factor structure of the brief symptom inventory−18 in adult survivors of childhood cancer: results from the childhood cancer survivor study. Psychol. Assess. 18, 22–32. 10.1037/1040-3590.18.1.22
    1. Rogers R. D., Owen A. M., Middleton H. C., Williams E. J., Pickard J. D., Sahakian B. J., et al. . (1999). Choosing between small, likely rewards and large, unlikely rewards activates inferior and orbital prefrontal cortex. J. Neurosci. 19, 9029–9038. 10.1523/JNEUROSCI.19-20-09029.1999
    1. Russo J., Trujillo C. A., Wingerson D., Decker K., Ries R., Wetzler H., et al. . (1998). The MOS 36-Item Short Form Health Survey: reliability, validity, and preliminary findings in schizophrenic outpatients. Med. Care 36, 752–756. 10.1097/00005650-199805000-00015
    1. Sancassiani F., Machado S., Ruggiero V., Cacace E., Carmassi C., Gesi C., et al. . (2017). The management of fibromyalgia from a psychosomatic perspective: an overview. Int. Rev. Psychiatry 29, 473–488. 10.1080/09540261.2017.1320982
    1. Sanchez M. M., Ladd C. O., Plotsky P. M. (2001). Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev. Psychopathol. 13, 419–449. 10.1017/S0954579401003029
    1. Sapolsky R. M. (1985). Glucocorticoid toxicity in the hippocampus: temporal aspects of neuronal vulnerability. Brain Res. 359, 300–305. 10.1016/0006-8993(85)91440-4
    1. Sarzi-Puttini P., Atzeni F., Mease P. J. (2011). Chronic widespread pain: from peripheral to central evolution. Best Pract. Res. Clin. Rheumatol. 25, 133–139. 10.1016/j.berh.2011.04.001
    1. Schmidt-Wilcke T., Clauw D. J. (2011). Fibromyalgia: from pathophysiology to therapy. Nat. Rev. Rheumatol. 7, 518–527. 10.1038/nrrheum.2011.98
    1. Schnurr P. P., Green B. L. (2004). Understanding relationships among trauma, post-tramatic stress disorder, and health outcomes. Adv. Mind Body Med. 20, 18–29. 10.1037/10723-010
    1. Seligman M. E. (1995). The effectiveness of psychotherapy. The consumer reports study. Am. Psychol. 50, 965–974. 10.1037/0003-066X.50.12.965
    1. Storey J. D. (2002). A direct approach to false discovery rates. J. R. Statist. Soc. B 64, 479–498. 10.1111/1467-9868.00346
    1. Tal S., Hadanny A., Berkovitz N., Sasson E., Ben-Jacob E., Efrati S. (2015). Hyperbaric oxygen may induce angiogenesis in patients suffering from prolonged post-concussion syndrome due to traumatic brain injury. Restor. Neurol. Neurosci. 33, 943–951. 10.3233/RNN-150585
    1. Tal S., Hadanny A., Sasson E., Suzin G., Efrati S. (2017). Hyperbaric oxygen therapy can induce angiogenesis and regeneration of nerve fibers in traumatic brain injury patients. Front. Hum. Neurosci. 11:508. 10.3389/fnhum.2017.00508
    1. Taylor M. L., Trotter D. R., Csuka M. E. (1995). The prevalence of sexual abuse in women with fibromyalgia. Arthritis Rheum. 38, 229–234. 10.1002/art.1780380211
    1. Tomoda A., Suzuki H., Rabi K., Sheu Y. S., Polcari A., Teicher M. H. (2009). Reduced prefrontal cortical gray matter volume in young adults exposed to harsh corporal punishment. Neuroimage (47 Suppl. 2), T66–71. 10.1016/j.neuroimage.2009.03.005
    1. Treadway M. T., Grant M. M., Ding Z., Hollon S. D., Gore J. C., Shelton R. C. (2009). Early adverse events, HPA activity and rostral anterior cingulate volume in MDD. PLoS ONE 4:e4887. 10.1371/journal.pone.0004887
    1. Walker E. A., Keegan D., Gardner G., Sullivan M., Katon W. J., Bernstein D. (1997). Psychosocial factors in fibromyalgia compared with rheumatoid arthritis: I. psychiatric diagnoses and functional disability. Psychosom. Med. 59, 565–571. 10.1097/00006842-199711000-00002
    1. Wolfe F., Clauw D. J., Fitzcharles M. A., Goldenberg D. L., Häuser W., Katz R. S., et al. . (2011). Fibromyalgia criteria and severity scales for clinical and epidemiological studies: a modification of the ACR Preliminary Diagnostic Criteria for Fibromyalgia. J. Rheumatol. 38, 1113–1122. 10.3899/jrheum.100594
    1. Wolfe F., Clauw D. J., Fitzcharles M. A., Goldenberg D. L., Katz R. S., Mease P., et al. . (2010). The American College of Rheumatology preliminary diagnostic criteria for fibromyalgia and measurement of symptom severity. Arthritis Care Res. 62, 600–610. 10.1002/acr.20140
    1. Yakov Gologorsky M., Ron Alterman M. D. (2011). Essential neuromodulation. Chapter 3. Cereb. Deep, 47–72. 10.1016/C2009-0-61346-5
    1. Yen C. T., Lu P. L. (2013). Thalamus and pain. Acta Anaesthesiol. Taiwan 51, 73–80. 10.1016/j.aat.2013.06.011
    1. Yildiz S., Kiralp M. Z., Akin A., Keskin I., Ay H., Dursun H., et al. . (2004). A new treatment modality for fibromyalgia syndrome: hyperbaric oxygen therapy. J. Int. Med. Res. 32, 263–267. 10.1177/147323000403200305
    1. Zhang Y., Xie B., Chen H., Li M., Guo X., Chen H. (2016). Disrupted resting-state insular subregions functional connectivity in post-traumatic stress disorder. Medicine95:e4083. 10.1097/MD.0000000000004083

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever