Longitudinal neurofunctional changes in medication overuse headache patients after mindfulness practice in a randomized controlled trial (the MIND-CM study).


Journal

The journal of headache and pain
ISSN: 1129-2377
Titre abrégé: J Headache Pain
Pays: England
ID NLM: 100940562

Informations de publication

Date de publication:
11 Jun 2024
Historique:
received: 20 02 2024
accepted: 31 05 2024
medline: 11 6 2024
pubmed: 11 6 2024
entrez: 10 6 2024
Statut: epublish

Résumé

Mindfulness practice has gained interest in the management of Chronic Migraine associated with Medication Overuse Headache (CM-MOH). Mindfulness is characterized by present-moment self-awareness and relies on attention control and emotion regulation, improving headache-related pain management. Mindfulness modulates the Default Mode Network (DMN), Salience Network (SN), and Fronto-Parietal Network (FPN) functional connectivity. However, the neural mechanisms underlying headache-related pain management with mindfulness are still unclear. In this study, we tested neurofunctional changes after mindfulness practice added to pharmacological treatment as usual in CM-MOH patients. The present study is a longitudinal phase-III single-blind Randomized Controlled Trial (MIND-CM study; NCT03671681). Patients had a diagnosis of CM-MOH, no history of neurological and severe psychiatric comorbidities, and were attending our specialty headache centre. Patients were divided in Treatment as Usual (TaU) and mindfulness added to TaU (TaU + MIND) groups. Patients underwent a neuroimaging and clinical assessment before the treatment and after one year. Longitudinal comparisons of DMN, SN, and FPN connectivity were performed between groups and correlated with clinical changes. Vertex-wise analysis was performed to assess cortical thickness changes. 177 CM-MOH patients were randomized to either TaU group or TaU + MIND group. Thirty-four patients, divided in 17 TaU and 17 TaU + MIND, completed the neuroimaging follow-up. At the follow-up, both groups showed an improvement in most clinical variables, whereas only TaU + MIND patients showed a significant headache frequency reduction (p = 0.028). After one year, TaU + MIND patients showed greater SN functional connectivity with the left posterior insula (p-FWE = 0.007) and sensorimotor cortex (p-FWE = 0.026). In TaU + MIND patients only, greater SN-insular connectivity was associated with improved depression scores (r = -0.51, p = 0.038). A longitudinal increase in cortical thickness was observed in the insular cluster in these patients (p = 0.015). Increased anterior cingulate cortex thickness was also reported in TaU + MIND group (p-FWE = 0.02). Increased SN-insular connectivity might modulate chronic pain perception and the management of negative emotions. Enhanced SN-sensorimotor connectivity could reflect improved body-awareness of painful sensations. Expanded cingulate cortex thickness might sustain improved cognitive processing of nociceptive information. Our findings unveil the therapeutic potential of mindfulness and the underlying neural mechanisms in CM-MOH patients. Name of Registry; MIND-CM study; Registration Number ClinicalTrials.gov identifier: NCT0367168; Registration Date: 14/09/2018.

Sections du résumé

BACKGROUND BACKGROUND
Mindfulness practice has gained interest in the management of Chronic Migraine associated with Medication Overuse Headache (CM-MOH). Mindfulness is characterized by present-moment self-awareness and relies on attention control and emotion regulation, improving headache-related pain management. Mindfulness modulates the Default Mode Network (DMN), Salience Network (SN), and Fronto-Parietal Network (FPN) functional connectivity. However, the neural mechanisms underlying headache-related pain management with mindfulness are still unclear. In this study, we tested neurofunctional changes after mindfulness practice added to pharmacological treatment as usual in CM-MOH patients.
METHODS METHODS
The present study is a longitudinal phase-III single-blind Randomized Controlled Trial (MIND-CM study; NCT03671681). Patients had a diagnosis of CM-MOH, no history of neurological and severe psychiatric comorbidities, and were attending our specialty headache centre. Patients were divided in Treatment as Usual (TaU) and mindfulness added to TaU (TaU + MIND) groups. Patients underwent a neuroimaging and clinical assessment before the treatment and after one year. Longitudinal comparisons of DMN, SN, and FPN connectivity were performed between groups and correlated with clinical changes. Vertex-wise analysis was performed to assess cortical thickness changes.
RESULTS RESULTS
177 CM-MOH patients were randomized to either TaU group or TaU + MIND group. Thirty-four patients, divided in 17 TaU and 17 TaU + MIND, completed the neuroimaging follow-up. At the follow-up, both groups showed an improvement in most clinical variables, whereas only TaU + MIND patients showed a significant headache frequency reduction (p = 0.028). After one year, TaU + MIND patients showed greater SN functional connectivity with the left posterior insula (p-FWE = 0.007) and sensorimotor cortex (p-FWE = 0.026). In TaU + MIND patients only, greater SN-insular connectivity was associated with improved depression scores (r = -0.51, p = 0.038). A longitudinal increase in cortical thickness was observed in the insular cluster in these patients (p = 0.015). Increased anterior cingulate cortex thickness was also reported in TaU + MIND group (p-FWE = 0.02).
CONCLUSIONS CONCLUSIONS
Increased SN-insular connectivity might modulate chronic pain perception and the management of negative emotions. Enhanced SN-sensorimotor connectivity could reflect improved body-awareness of painful sensations. Expanded cingulate cortex thickness might sustain improved cognitive processing of nociceptive information. Our findings unveil the therapeutic potential of mindfulness and the underlying neural mechanisms in CM-MOH patients.
TRIAL REGISTRATION BACKGROUND
Name of Registry; MIND-CM study; Registration Number ClinicalTrials.gov identifier: NCT0367168; Registration Date: 14/09/2018.

Identifiants

pubmed: 38858629
doi: 10.1186/s10194-024-01803-5
pii: 10.1186/s10194-024-01803-5
doi:

Types de publication

Journal Article Randomized Controlled Trial Clinical Trial, Phase III

Langues

eng

Sous-ensembles de citation

IM

Pagination

97

Subventions

Organisme : European Union - NextGenerationEU
ID : National Recovery and Resilience Plan (NRRP), Mission 4 Component 2 Investment 3.3 - Call for tender No. 117 of 02/03/2023 of Italian Ministry of University and Research
Organisme : Ministero della Salute
ID : RRC
Organisme : Ministero della Salute
ID : RF-2016-02364801
Organisme : Ministero della Salute
ID : RRC
Organisme : Ministero della Salute
ID : RRC
Organisme : Ministero della Salute
ID : RRC
Organisme : Ministero della Salute
ID : RRC

Informations de copyright

© 2024. The Author(s).

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Auteurs

Davide Fedeli (D)

Department of Neuroradiology, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Celoria 11, Milano, Italy.

Giuseppe Ciullo (G)

Department of Neuroradiology, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Celoria 11, Milano, Italy.
Department of Medicine and Surgery, University of Parma, Via Volturno 39, Parma, 43125, Italy.

Greta Demichelis (G)

Department of Neuroradiology, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Celoria 11, Milano, Italy.

Jean Paul Medina Carrion (JP)

Department of Neuroradiology, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Celoria 11, Milano, Italy.

Maria Grazia Bruzzone (MG)

Department of Neuroradiology, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Celoria 11, Milano, Italy.

Emilio Ciusani (E)

Department of Diagnostic and Technology, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milano, Italy.

Alessandra Erbetta (A)

Department of Neuroradiology, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Celoria 11, Milano, Italy.

Stefania Ferraro (S)

Department of Neuroradiology, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Celoria 11, Milano, Italy.
School of Life Science and Technology, MOE Key Laboratory for Neuroinformation, University of Electronic Science and Technology of China, Chengdu, China.

Marina Grisoli (M)

Department of Neuroradiology, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Celoria 11, Milano, Italy.

Erika Guastafierro (E)

Neurology, Public Health and Disability Unit, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milano, Italy.

Domenico D'Amico (D)

Neuroalgology Unit and Headache Center, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milano, Italy.

Alberto Raggi (A)

Neurology, Public Health and Disability Unit, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milano, Italy.

Anna Nigri (A)

Department of Neuroradiology, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Celoria 11, Milano, Italy. anna.nigri@istituto-besta.it.

Licia Grazzi (L)

Neuroalgology Unit and Headache Center, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milano, Italy.

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