Brain perfusion patterns are altered in chronic knee pain: a spatial covariance analysis of arterial spin labelling MRI.
Journal
Pain
ISSN: 1872-6623
Titre abrégé: Pain
Pays: United States
ID NLM: 7508686
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
pubmed:
19
2
2020
medline:
15
5
2021
entrez:
19
2
2020
Statut:
ppublish
Résumé
Chronic musculoskeletal pain is a common problem globally. Current evidence suggests that maladapted central pain pathways are associated with pain chronicity, for example, in postoperative pain after knee replacement. Other factors such as low mood, anxiety, and tendency to catastrophize are also important contributors. We aimed to investigate brain imaging features that underpin pain chronicity based on multivariate pattern analysis of cerebral blood flow (CBF), as a marker of maladaptive brain changes. This was achieved by identifying CBF patterns that discriminate chronic pain from pain-free conditions and by exploring their explanatory power for factors thought to drive pain chronification. In 44 chronic knee pain and 29 pain-free participants, we acquired both CBF and T1-weighted data. Participants completed questionnaires related to affective processes and pressure and cuff algometry to assess pain sensitization. Two factor scores were extracted from these scores representing negative affect and pain sensitization. A spatial covariance principal component analysis of CBF identified 5 components that significantly discriminated chronic pain participants from controls, with the unified network achieving 0.83 discriminatory accuracy (area under the curve). In chronic knee pain, significant patterns of relative hypoperfusion were evident in anterior default-mode and salience network hubs, while hyperperfusion was seen in posterior default mode, thalamus, and sensory regions. One component correlated positively with the pain sensitization score (r = 0.43, P = 0.006), suggesting that this CBF pattern reflects neural activity changes encoding pain sensitization. Here, we report a distinct chronic knee pain-related representation of CBF, pointing toward a brain signature underpinning central aspects of pain sensitization.
Identifiants
pubmed: 32068664
doi: 10.1097/j.pain.0000000000001829
pii: 00006396-202006000-00013
doi:
Substances chimiques
Spin Labels
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1255-1263Subventions
Organisme : Versus Arthritis
ID : 20777
Pays : United Kingdom
Références
Ab Aziz CB, Ahmad AH. The role of the thalamus in modulating pain. Malays J Med Sci 2006;13:11–18.
Alsop DC, Detre JA, Golay X, Gunther M, Hendrikse J, Hernandez-Garcia L, Lu HZ, MacIntosh BJ, Parkes LM, Smits M, van Osch MJP, Wang DJJ, Wong EC, Zaharchuk G. Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European Consortium for ASL in Dementia. Magnet Reson Med 2015;73:102–16.
Baliki MN, Geha PY, Apkarian AV, Chialvo DR. Beyond feeling: chronic pain hurts the brain, disrupting the default-mode network dynamics. J Neurosci 2008;28:1398–403.
Baliki MN, Mansour AR, Baria AT, Apkarian AV. Functional reorganization of the default mode network across chronic pain conditions. PLoS One 2014;9:e106133.
Basbaum AI, Fields HL. Endogenous pain control mechanisms: review and hypothesis. Ann Neurol 1978;4:451–62.
Beck A, Steer R, Brown G. Manual for the Beck depression inventory-II. San Antonio: Psychological Corporation, 1996.
Boissoneault J, Letzen J, Lai S, Robinson ME, Staud R. Static and dynamic functional connectivity in patients with chronic fatigue syndrome: use of arterial spin labelling fMRI. Clin Physiol Funct Imag 2018;38:128–37.
Breivik H, Collett B, Ventafridda V, Cohen R, Gallacher D. Survey of chronic pain in Europe: prevalence, impact on daily life, and treatment. Eur J pain 2006;10:287–333.
Ceko M, Shir Y, Ouellet JA, Ware MA, Stone LS, Seminowicz DA. Partial recovery of abnormal insula and dorsolateral prefrontal connectivity to cognitive networks in chronic low back pain after treatment. Hum Brain Mapp 2015;36:2075–92.
Cheriyan J, Sheets PL. Altered excitability and local connectivity of mPFC-PAG neurons in a mouse model of neuropathic pain. J Neurosci 2018;38:4829–39.
Cottam WJ, Condon L, Alshuft H, Reckziegel D, Auer DP. Associations of limbic-affective brain activity and severity of ongoing chronic arthritis pain are explained by trait anxiety. NeuroImage Clin 2016;12:269–76.
Dahlhamer J, Lucas J, Zelaya C, Nahin R, Mackey S, DeBar L, Kerns R, Von Korff M, Porter L, Helmick C. Prevalence of chronic pain and high-impact chronic pain among adults—United States, 2016. MMWR Morbid Mortal Wkly Rep 2018;67:1001–6.
Dai W, Garcia D, de Bazelaire C, Alsop DC. Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn Reson Med 2008;60:1488–97.
Fayaz A, Croft P, Langford RM, Donaldson LJ, Jones GT. Prevalence of chronic pain in the UK: a systematic review and meta-analysis of population studies. BMJ Open 2016;6:e010364.
Fernandes GS, Sarmanova A, Warner S, Harvey H, Akin-Akinyosoye K, Richardson H, Frowd N, Marshall L, Stocks J, Hall M, Valdes AM, Walsh D, Zhang W, Doherty M. Knee pain and related health in the community study (KPIC): a cohort study protocol. BMC Musculoskelet Disord 2017;18:404.
Fernandes GS, Valdes AM, Walsh DA, Zhang W, Doherty M. Neuropathic-like knee pain and associated risk factors: a cross-sectional study in a UK community sample. Arthritis Res Ther 2018;20:215.
Graven-Nielsen T, Arendt-Nielsen L. Assessment of mechanisms in localized and widespread musculoskeletal pain. Nat Rev Rheumatol 2010;6:599–606.
Gwilym SE, Filippini N, Douaud G, Carr AJ, Tracey I. Thalamic atrophy associated with painful osteoarthritis of the hip is reversible after arthroplasty A longitudinal voxel-based morphometric study. Arthritis Rheum 2010;62:2930–40.
Gwilym SE, Keltner JR, Warnaby CE, Carr AJ, Chizh B, Chessell I, Tracey I. Psychophysical and functional imaging evidence supporting the presence of central sensitization in a cohort of osteoarthritis patients. Arthritis Rheum 2009;61:1226–34.
Hodkinson DJ, Veggeberg R, Wilcox SL, Scrivani S, Burstein R, Becerra L, Borsook D. Primary somatosensory cortices contain altered patterns of regional cerebral blood flow in the interictal phase of migraine. PLoS One 2015;10:e0137971.
Howard MA, Sanders D, Krause K, O'Muircheartaigh J, Fotopoulou A, Zelaya F, Thacker M, Massat N, Huggins JP, Vennart W, Choy E, Daniels M, Williams SC. Alterations in resting-state regional cerebral blood flow demonstrate ongoing pain in osteoarthritis: an arterial spin-labeled magnetic resonance imaging study. Arthritis Rheum 2012;64:3936–46.
Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM. FSL. Neuroimage 2012;62:782–90.
Kambeitz J, Cabral C, Sacchet MD, Gotlib IH, Zahn R, Serpa MH, Walter M, Falkai P, Koutsouleris N. Detecting neuroimaging biomarkers for depression: a meta-analysis of multivariate pattern recognition studies. Biol Psychiatry 2017;82:330–8.
Keszthelyi D, Aziz Q, Ruffle JK, O'Daly O, Sanders D, Krause K, Williams SCR, Howard MA. Delineation between different components of chronic pain using dimension reduction—an ASL fMRI study in hand osteoarthritis. Eur J Pain 2018;22:1245–54.
Kucyi A, Salomons TV, Davis KD. Mind wandering away from pain dynamically engages antinociceptive and default mode brain networks. Proc Natl Acad Sci U S A 2013;110:18692–7.
Kulkarni B, Bentley DE, Elliott R, Julyan PJ, Boger E, Watson A, Boyle Y, El-Deredy W, Jones AKP. Arthritic pain is processed in brain areas concerned with emotions and fear. Arthritis Rheum 2007;56:1345–54.
Liang X, Zou Q, He Y, Yang Y. Coupling of functional connectivity and regional cerebral blood flow reveals a physiological basis for network hubs of the human brain. Proc Natl Acad Sci U S A 2013;110:1929–34.
Lincoln N, Moreton B, Turner K, Walsh D. The measurement of psychological constructs in people with osteoarthritis of the knee: a psychometric evaluation. Disabil Rehabil 2017;39:372–84.
Linnman C, Moulton EA, Barmettler G, Becerra L, Borsook D. Neuroimaging of the periaqueductal gray: state of the field. NeuroImage 2012;60:505–22.
Loggia ML, Kim J, Gollub RL, Vangel MG, Kirsch I, Kong J, Wasan AD, Napadow V. Default mode network connectivity encodes clinical pain: an arterial spin labeling study. PAIN 2013;154:24–33.
Melzer TR, Watts R, MacAskill MR, Pearson JF, Rueger S, Pitcher TL, Livingston L, Graham C, Keenan R, Shankaranarayanan A, Alsop DC, Dalrymple-Alford JC, Anderson TJ. Arterial spin labelling reveals an abnormal cerebral perfusion pattern in Parkinson's disease. Brain 2011;134:845–55.
Murphy K, Harris AD, Diukova A, Evans CJ, Lythgoe DJ, Zelaya F, Wise RG. Pulsed arterial spin labeling perfusion imaging at 3 T: estimating the number of subjects required in common designs of clinical trials. Magn Reson Imag 2011;29:1382–9.
O'Muircheartaigh J, Marquand A, Hodkinson DJ, Krause K, Khawaja N, Renton TF, Huggins JP, Vennart W, Williams SC, Howard MA. Multivariate decoding of cerebral blood flow measures in a clinical model of on-going postsurgical pain. Hum Brain Mapp 2015;36:633–42.
Ossipov MH, Morimura K, Porreca F. Descending pain modulation and chronification of pain. Curr Opin Support Palliat Care 2014;8:143–51.
Petersen KK, Arendt-Nielsen L, Finocchietti S, Hirata RP, Simonsen O, Laursen MB, Graven-Nielsen T. Age interactions on pain sensitization in patients with severe knee osteoarthritis and controls. Clin J Pain 2017;33:1081–7.
Phillips CJ. The cost and burden of chronic pain. Rev Pain 2009;3:2–5.
Rathleff MS, Petersen KK, Arendt-Nielsen L, Thorborg K, Graven-Nielsen T. Impaired conditioned pain modulation in young female adults with long-standing patellofemoral pain: a single blinded cross-sectional study. Pain Med 2016;17:980–8.
Schnack HG, Kahn RS. Detecting neuroimaging biomarkers for psychiatric disorders: sample size matters. Front Psychiatr 2016;7:50.
Segerdahl AR, Mezue M, Okell TW, Farrar JT, Tracey I. The dorsal posterior insula subserves a fundamental role in human pain. Nat Neurosci 2015;18:499–500.
Soni A, Wanigasekera V, Mezue M, Cooper C, Javaid MK, Price AJ, Tracey I. Central sensitization in knee osteoarthritis: relating presurgical brainstem neuroimaging and PainDETECT-based patient stratification to arthroplasty outcome. Arthritis Rheumatol 2019;71:550–60.
Spetsieris PG, Ma Y, Dhawan V, Eidelberg D. Differential diagnosis of parkinsonian syndromes using PCA-based functional imaging features. NeuroImage 2009;45:1241–52.
Spielberger C, Gorsuch R, Lushene R, Vagg PR, Jacobs GA. Manual for the State-Trait Anxiety Inventory. Palo Alto: Consulting Psychologists Press, 1983.
Sullivan MJL, Bishop SR, Pivik J. The pain catastrophizing scale: development and validation. Psychol Assess 1995;7:524–32.
Vaegter HB, Graven-Nielsen T. Pain modulatory phenotypes differentiate subgroups with different clinical and experimental pain sensitivity. PAIN 2016;157:1480–8.
Wager TD, Atlas LY, Lindquist MA, Roy M, Woo CW, Kross E. An fMRI-based neurologic signature of physical pain. N Engl J Med 2013;368:1388–97.
Wartolowska KA, Bulte DP, Chappell MA, Jenkinson M, Okell TW, Webster M, Carr AJ. Using arterial spin labelling to investigate spontaneous and evoked ongoing musculoskeletal pain. bioRxiv 2018:163196.
Wasan AD, Loggia ML, Chen LQ, Napadow V, Kong J, Gollub RL. Neural correlates of chronic low back pain measured by arterial spin labeling. Anesthesiology 2011;115:364–74.
Zaharchuk G, Straka M, Marks MP, Albers GW, Moseley ME, Bammer R. Combined arterial spin label and dynamic susceptibility contrast measurement of cerebral blood flow. Magnet Reson Med 2010;63:1548–56.