Advertisement
Clinical Research|Articles in Press

Functional Connectivity Magnetic Resonance Imaging Sequences in Patients With Postsurgical Persistent Spinal Pain Syndrome Type 2 With Implanted Spinal Cord Stimulation Systems: A Safety, Feasibility, and Validity Study

      Abstract

      Background

      Chronic pain has been associated with alterations in brain connectivity, both within networks (regional) and between networks (cross-network connectivity). Functional connectivity (FC) data on chronic back pain are limited and based on heterogeneous pain populations. Patients with postsurgical persistent spinal pain syndrome (PSPS) type 2 are good candidates for spinal cord stimulation (SCS) therapy. We hypothesize that 1) FC magnetic resonance imaging (fcMRI) scans can be safely obtained in patients with PSPS type 2 with implanted therapeutic SCS devices and that 2) their cross-network connectivity patterns are altered and involve emotion and reward/aversion functions.

      Materials and Methods

      Resting-state (RS) fcMRI (rsfcMRI) scans were obtained from nine patients with PSPS type 2 implanted with therapeutic SCS systems and 13 age-matched controls. Seven RS networks were analyzed, including the striatum.

      Results

      Cross-network FC sequences were safely obtained on a 3T MRI scanner in all nine patients with PSPS type 2 with implanted SCS systems. FC patterns involving emotion/reward brain circuitry were altered as compared with controls. Patients with a history of constant neuropathic pain, experiencing longer therapeutic effects of SCS, had fewer alterations in their connectivity patterns.

      Conclusions

      To our knowledge, this is the first report of altered cross-network FC involving emotion/reward brain circuitry in a homogeneous population of patients with chronic pain with fully implanted SCS systems, on a 3T MRI scanner. All rsfcMRI studies were safe and well tolerated by all nine patients, with no detectable effects on the implanted devices.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Rock A.K.
        • Truong H.
        • Park Y.L.
        • Pilitsis J.G.
        Spinal cord stimulation.
        Neurosurg Clin N Am. 2019; 30: 169-194
        • Alizadeh R.
        • Sharifzadeh S.R.
        Pathogenesis, etiology and treatment of failed back surgery syndrome.
        Neurochirurgie. 2022; 68: 426-431
        • Deer T.R.
        • Mekhail N.
        • Provenzano D.
        • et al.
        The appropriate use of neurostimulation of the spinal cord and peripheral nervous system for the treatment of chronic pain and ischemic diseases: the Neuromodulation Appropriateness Consensus Committee.
        Neuromodulation. 2014; 17 ([discussion: 550]): 515-550
        • Pahapill P.A.
        Incidence of revision surgery in a large cohort of patients with thoracic surgical three-column paddle leads: a retrospective case review.
        Neuromodulation. 2015; 18: 367-375
        • Duarte R.V.
        • Houten R.
        • Nevitt S.
        • et al.
        Screening trials of spinal cord stimulation for neuropathic pain in England–a budget impact analysis.
        Front Pain Res (Lausanne). 2022; 3974904https://doi.org/10.3389/fpain.2022.974904
        • Pahapill P.A.
        • Chen G.
        • Arocho-Quinones E.V.
        • Nencka A.S.
        • Li S.J.
        Functional connectivity and structural analysis of trial spinal cord stimulation responders in failed back surgery syndrome.
        PLoS One. 2020; 15e022836
        • Baliki M.N.
        • Mansour A.R.
        • Baria A.T.
        • Apkarian A.V.
        Functional reorganization of the default mode network across chronic pain conditions.
        PLoS One. 2014; 9e106133
        • Baliki M.N.
        • Apkarian A.V.
        Nociception, pain, negative moods, and behavior selection.
        Neuron. 2015; 87: 474-491
        • Baliki M.N.
        • Petre B.
        • Torbey S.
        • et al.
        Corticostriatal functional connectivity predicts transition to chronic back pain.
        Nat Neurosci. 2012; 15: 1117-1119
        • Kucyi A.
        • Davis K.D.
        The dynamic pain connectome.
        Trends Neurosci. 2015; 38: 86-95https://doi.org/10.1016/j.tins.2014.11.006
        • Hashmi J.A.
        • Baliki M.N.
        • Huang L.
        • et al.
        Shape shifting pain: chronification of back pain shifts brain representation from nociceptive to emotional circuits.
        Brain. 2013; 136: 2751-2768
        • Khan S.A.
        • Keaser M.L.
        • Meiller T.F.
        • Seminowicz D.A.
        Altered structure and function in the hippocampus and medial prefrontal cortex in patients with burning mouth syndrome.
        Pain. 2014; 155: 1472-1480
        • Yu R.
        • Gollub R.L.
        • Spaeth R.
        • Napadow V.
        • Wasan A.
        • Kong J.
        Disrupted functional connectivity of the periaqueductal gray in chronic low back pain.
        NeuroImage Clin. 2014; 6: 100-108
        • Seminowicz D.A.
        • Wideman T.H.
        • Naso L.
        • et al.
        Effective treatment of chronic low back pain in humans reverses abnormal brain anatomy and function.
        J Neurosci. 2011; 31: 7540-7550
        • Napadow V.
        • Lacount L.
        • Park K.
        • As-Sanie S.
        • Clauw D.J.
        • Harris R.E.
        Intrinsic brain connectivity in fibromyalgia is associated with chronic pain intensity.
        Arthritis Rheum. 2010; 62: 2545-2555
        • Deogaonkar M.
        • Sharma M.
        • Oluigbo C.
        • et al.
        Spinal cord stimulation (SCS) and functional magnetic resonance imaging (fMRI): modulation of cortical connectivity with therapeutic SCS.
        Neuromodulation. 2016; 19: 142-153
        • De Ridder D.
        • Vanneste S.
        Burst and tonic spinal cord stimulation: different and common brain mechanisms.
        Neuromodulation. 2016; 19: 47-59
        • Hemington K.S.
        • Wu Q.
        • Kucyi A.
        • et al.
        Abnormal cross-network functional connectivity in chronic pain and its association with clinical symptoms.
        Brain Struct Funct. 2016; 221: 4203-4219https://doi.org/10.1007/s00429-015-1161-1
        • Miao J.
        • Ailes I.
        • Krisa L.
        • et al.
        Case report: the promising application of dynamic functional connectivity analysis on an individual with failed back surgery syndrome.
        Front Neurosci. 2022; 16987223
        • Fan X.
        • Ren H.
        • Bu C.
        • et al.
        Alterations in local activity and functional connectivity in patients with postherpetic neuralgia after short-term spinal cord stimulation.
        Front Mol Neurosci. 2022; 15938280
        • Kiriakopoulos E.T.
        • Tasker R.R.
        • Nicosia S.
        • Wood M.L.
        • Mikulis D.J.
        Functional magnetic resonance imaging: a potential tool for the evaluation of spinal cord stimulation: technical case report.
        Neurosurgery. 1997; 41: 501-504
        • Moens M.
        • Droogmans S.
        • Spapen H.
        • et al.
        Feasibility of cerebral magnetic resonance imaging in patients with externalised spinal cord stimulator.
        Clin Neurol Neurosurg. 2012; 114: 135-141
        • De Groote S.
        • De Jaeger M.
        • Van Schuerbeek P.
        • et al.
        Functional magnetic resonance imaging: cerebral function alterations in subthreshold and suprathreshold spinal cord stimulation.
        J Pain Res. 2018; 11: 2517-2526
        • Moens M.
        • Sunaert S.
        • Mariën P.
        • et al.
        Spinal Cord Stimulation Modulates Cerebral Function: an fMRI study.
        Neuroradiology. 2012; 54: 1399-1407
        • De Groote S.
        • Goudman L.
        • Peeters R.
        • et al.
        Magnetic resonance imaging exploration of the human brain during 10 kHz spinal cord stimulation for failed back surgery syndrome: a resting state functional magnetic resonance imaging study.
        Neuromodulation. 2020; 23: 46-55
        • De Groote S.
        • Goudman L.
        • Peeters R.
        • et al.
        The influence of high dose spinal cord stimulation on the descending pain modulatory system in patients with failed back surgery syndrome.
        Neuroimage Clin. 2019; 24102087
        • Thornton J.S.
        Technical challenges and safety of magnetic resonance imaging with in situ neuromodulation from spine to brain.
        Eur J Paediatr Neurol. 2017; 21: 232-241
        • Tzourio-Mazoyer N.
        • Landeau B.
        • Papathanassiou D.
        • et al.
        Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.
        Neuroimage. 2002; 15: 273-289
        • Chen G.
        • Shu H.
        • Chen G.
        • et al.
        Staging Alzheimer’s disease risk by sequencing brain function and structure, cerebrospinal fluid, and cognition biomarkers.
        J Alzheimers Dis. 2016; 54: 983-993
        • Arocho-Quinones E.
        • Chen G.
        • Nencka A.
        • Shu H.
        • Li S.-J.
        • Pahapill P.
        Distinct functional connectivity patterns for constant neuropathic and intermittent pain phenotypes in failed back surgery patients.
        Neuromodulation. 2017; 20: e515
        • Pahapill P.A.
        • Zhang W.
        Restoration of altered somatosensory cortical representation with spinal cord stimulation therapy in a patient with complex regional pain syndrome: a magnetoencephalography case study.
        Neuromodulation. 2014; 17 ([discussion: 26–27]): 22-26
        • Goudman L.
        • De Groote S.
        • Linderoth B.
        • et al.
        Exploration of the supraspinal hypotheses about spinal cord stimulation and dorsal root ganglion stimulation: a systematic review.
        J Clin Med. 2021; 10: 2766

      Comment