Top

Published in:

01-05-2017 | Functional Neuroradiology

Altered structural connectivity of pain-related brain network in burning mouth syndrome—investigation by graph analysis of probabilistic tractography

Authors: Akihiko Wada, Takashi Shizukuishi, Junko Kikuta, Haruyasu Yamada, Yusuke Watanabe, Yoshiki Imamura, Takahiro Shinozaki, Ko Dezawa, Hiroki Haradome, Osamu Abe

Published in: Neuroradiology | Issue 5/2017

Abstract

Purpose

Burning mouth syndrome (BMS) is a chronic intraoral pain syndrome featuring idiopathic oral pain and burning discomfort despite clinically normal oral mucosa. The etiology of chronic pain syndrome is unclear, but preliminary neuroimaging research has suggested the alteration of volume, metabolism, blood flow, and diffusion at multiple brain regions. According to the neuromatrix theory of Melzack, pain sense is generated in the brain by the network of multiple pain-related brain regions. Therefore, the alteration of pain-related network is also assumed as an etiology of chronic pain. In this study, we investigated the brain network of BMS brain by using probabilistic tractography and graph analysis.

Methods

Fourteen BMS patients and 14 age-matched healthy controls underwent 1.5T MRI. Structural connectivity was calculated in 83 anatomically defined regions with probabilistic tractography of 60-axis diffusion tensor imaging and 3D T1-weighted imaging. Graph theory network analysis was used to evaluate the brain network at local and global connectivity.

Results

In BMS brain, a significant difference of local brain connectivity was recognized at the bilateral rostral anterior cingulate cortex, right medial orbitofrontal cortex, and left pars orbitalis which belong to the medial pain system; however, no significant difference was recognized at the lateral system including the somatic sensory cortex. A strengthened connection of the anterior cingulate cortex and medial prefrontal cortex with the basal ganglia, thalamus, and brain stem was revealed.

Conclusion

Structural brain network analysis revealed the alteration of the medial system of the pain-related brain network in chronic pain syndrome.

Headache Classification Committee of the International Headache Society (IHS) (2013) The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia 33:629–808. doi:10.1177/0333102413485658 CrossRef

Gao J, Chen L, Zhou J, Peng J (2008) A case-control study on etiological factors involved in patients with burning mouth syndrome. J Oral Pathol Med 38:24–28. doi:10.1111/j.1600-0714.2008.00708.x CrossRef

Gorsky M, Silverman S, Chinn H (1991) Clinical characteristics and management outcome in the burning mouth syndrome. An open study of 130 patients. Oral Surg Oral Med Oral Pathol 72:192–195CrossRefPubMed

Gurvits GE, Tan A (2013) Burning mouth syndrome. World J Gastroenterol 19:665–672. doi:10.3748/wjg.v19.i5.665 CrossRefPubMedPubMedCentral

Kohorst JJ, Bruce AJ, Torgerson RR et al (2014) A population-based study of the incidence of burning mouth syndrome. Mayo Clin Proc 89:1545–1552. doi:10.1016/j.mayocp.2014.05.018 CrossRefPubMedPubMedCentral

Renton T (2011) Burning mouth syndrome. Rev Pain 5:12–17. doi:10.1177/204946371100500403 PubMedPubMedCentral

Adamo D, Celentano A, Ruoppo E et al (2015) The relationship between sociodemographic characteristics and clinical features in burning mouth syndrome. Pain Med 16:2171–2179. doi:10.1111/pme.12808 CrossRefPubMed

Forssell H, Jääskeläinen S, Tenovuo O, Hinkka S (2002) Sensory dysfunction in burning mouth syndrome. Pain 99:41–47. doi:10.1016/S0304-3959(02)00052-0 CrossRefPubMed

Grushka M, Epstein JB, Gorsky M (2003) Burning mouth syndrome and other oral sensory disorders: a unifying hypothesis. Pain Res Manag 8:133–135CrossRefPubMed

10.

Albuquerque RJC, de Leeuw R, Carlson CR et al (2006) Cerebral activation during thermal stimulation of patients who have burning mouth disorder: an fMRI study. Pain 122:223–234. doi:10.1016/j.pain.2006.01.020 CrossRefPubMed

11.

Forssell H, Jääskeläinen S, List T et al (2015) An update on pathophysiological mechanisms related to idiopathic oro-facial pain conditions with implications for management. J Oral Rehabil 42:300–322. doi:10.1111/joor.12256 CrossRefPubMed

12.

Lauria G, Majorana A, Borgna M et al (2005) Trigeminal small-fiber sensory neuropathy causes burning mouth syndrome. Pain 115:332–337. doi:10.1016/j.pain.2005.03.028 CrossRefPubMed

13.

Yilmaz Z, Renton T, Yiangou Y et al (2007) Burning mouth syndrome as a trigeminal small fibre neuropathy: increased heat and capsaicin receptor TRPV1 in nerve fibres correlates with pain score. J Clin Neurosci 14:864–871. doi:10.1016/j.jocn.2006.09.002 CrossRefPubMed

14.

Eliav E, Kamran B, Schaham R et al (2007) Evidence of chorda tympani dysfunction in patients with burning mouth syndrome. J Am Dent Assoc 138:628–633CrossRefPubMed

15.

Nasri-Heir C, Gomes J, Heir GM et al (2011) The role of sensory input of the chorda tympani nerve and the number of fungiform papillae in burning mouth syndrome. Oral Surg Oral Med Oral Pathol Oral Radiol Endodontol 112:65–72. doi:10.1016/j.tripleo.2011.02.035 CrossRef

16.

Svensson P, Bjerring P, Arendt-Nielsen L, Kaaber S (1993) Sensory and pain thresholds to orofacial argon laser stimulation in patients with chronic burning mouth syndrome. Clin J Pain 9:207–215CrossRefPubMed

17.

Sinding C, Gransjøen AM, Schlumberger G et al (2016) Grey matter changes of the pain matrix in patients with burning mouth syndrome. Eur J Neurosci 43:997–1005. doi:10.1111/ejn.13156 CrossRefPubMed

18.

Shinozaki T, Imamura Y, Kohashi R et al (2016) Spatial and temporal brain responses to noxious heat thermal stimuli in burning mouth syndrome. J Dent Res 95:1138–1146. doi:10.1177/0022034516653580 CrossRefPubMed

19.

Khan SA, Keaser ML, Meiller TF, Seminowicz DA (2014) Altered structure and function in the hippocampus and medial prefrontal cortex in patients with burning mouth syndrome. Pain 155:1472–1480. doi:10.1016/j.pain.2014.04.022 CrossRefPubMed

20.

Kupers R, Kehlet H (2006) Brain imaging of clinical pain states: a critical review and strategies for future studies. Lancet Neurol 5:1033–1044. doi:10.1016/S1474-4422(06)70624-X CrossRefPubMed

21.

Seifert F, Maihöfner C (2009) Central mechanisms of experimental and chronic neuropathic pain: findings from functional imaging studies. Cell Mol Life Sci 66:375–390. doi:10.1007/s00018-008-8428-0 CrossRefPubMed

22.

Price DD (2000) Psychological and neural mechanisms of the affective dimension of pain. Science 288:1769–1772. doi:10.1126/science.288.5472.1769 CrossRefPubMed

23.

Apkarian AV, Bushnell MC, Treede R-D, Zubieta J-K (2005) Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 9:463–484. doi:10.1016/j.ejpain.2004.11.001 CrossRefPubMed

24.

Melzack R (2001) Pain and the neuromatrix in the brain. J Dent Educ 65:1378–1382PubMed

25.

Van Dijk KRA, Hedden T, Venkataraman A et al (2010) Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J Neurophysiol 103:297–321. doi:10.1152/jn.00783.2009 CrossRefPubMed

26.

Whitfield-Gabrieli S, Nieto-Castanon A (2012) Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connectivity 2:125–141. doi:10.1089/brain.2012.0073 CrossRefPubMed

27.

Behrens TEJ, Woolrich MW, Jenkinson M et al (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50:1077–1088. doi:10.1002/mrm.10609 CrossRefPubMed

28.

Nucifora PGP, Verma R, Lee S-K, Melhem ER (2007) Diffusion-tensor MR imaging and tractography: exploring brain microstructure and connectivity. Radiology 245:367–384. doi:10.1148/radiol.2452060445 CrossRefPubMed

29.

Behrens TEJ, Berg HJ, Jbabdi S et al (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? NeuroImage 34:144–155. doi:10.1016/j.neuroimage.2006.09.018 CrossRefPubMed

30.

Cao Q, Shu N, An L et al (2013) Probabilistic diffusion tractography and graph theory analysis reveal abnormal white matter structural connectivity networks in drug-naive boys with attention deficit/hyperactivity disorder. J Neurosci 33:10676–10687. doi:10.1523/JNEUROSCI.4793-12.2013 CrossRefPubMed

31.

Koike K, Shinozaki T, Hara K et al (2014) Immune and endocrine function in patients with burning mouth syndrome. Clin J Pain 30:168–173. doi:10.1097/AJP.0b013e31828c4bf1 PubMed

32.

Yamada H, Abe O, Shizukuishi T et al (2014) Efficacy of distortion correction on diffusion imaging: comparison of FSL eddy and eddy_correct using 30 and 60 directions diffusion encoding. PLoS One. doi:10.1371/journal.pone.0112411.s009

33.

Daducci A, Gerhard S, Griffa A et al (2012) The connectome mapper: an open-source processing pipeline to map connectomes with MRI. PLoS One 7:e48121. doi:10.1371/journal.pone.0048121 CrossRefPubMedPubMedCentral

34.

Desikan RS, Ségonne F, Fischl B et al (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31:968–980. doi:10.1016/j.neuroimage.2006.01.021 CrossRefPubMed

35.

Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. NeuroImage 52:1059–1069. doi:10.1016/j.neuroimage.2009.10.003 CrossRefPubMed

36.

Rubinov M, Sporns O (2011) Weight-conserving characterization of complex functional brain networks. NeuroImage 56:2068–2079. doi:10.1016/j.neuroimage.2011.03.069 CrossRefPubMed

37.

Boccaletti S, Latora V, Moreno Y, Chavez M (2006) Complex networks: structure and dynamics. Phys Rep 424:175–308. doi:10.1016/j.physrep.2005.10.009 CrossRef

38.

Albert R, Barabási A-L (2002) Statistical mechanics of complex networks. Rev Mod Phys 74:47–97. doi:10.1103/RevModPhys.74.47 CrossRef

39.

Borgatti SP, Mehra A, Brass DJ, Labianca G (2009) Network analysis in the social sciences. Science 323:892–895. doi:10.1126/science.1165821 CrossRefPubMed

40.

Newman M (2003) The structure and function of complex networks. SIAM Rev 45:167–256CrossRef

41.

Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198. doi:10.1038/nrn2575 CrossRefPubMed

42.

Achard S (2006) A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci 26:63–72. doi:10.1523/JNEUROSCI.3874-05.2006 CrossRefPubMed

43.

Watts DJ, Strogatz SH (1998) Collective dynamics of small-world networks. Nature 393:440–442. doi:10.1038/30918 CrossRefPubMed

44.

Woolf CJ (2010) What is this thing called pain? J Clin Invest 120:3742. doi:10.1172/JCI45178 CrossRefPubMedPubMedCentral

45.

Chen J (2011) History of pain theories. Neurosci Bull 27:343–350. doi:10.1007/s12264-011-0139-0 CrossRefPubMed

46.

May A (2007) Neuroimaging: visualising the brain in pain. Neurol Sci 28:S101–S107. doi:10.1007/s10072-007-0760-x CrossRefPubMed

47.

Moisset X, Bouhassira D (2007) Brain imaging of neuropathic pain. NeuroImage 37(Suppl 1):S80–S88. doi:10.1016/j.neuroimage.2007.03.054 CrossRefPubMed

48.

Luo C, Kuner T, Kuner R (2014) Synaptic plasticity in pathological pain. Trends Neurosci 37:343–355. doi:10.1016/j.tins.2014.04.002 CrossRefPubMed

49.

Borsook D, Moulton EA, Schmidt KF, Becerra LR (2007) Neuroimaging revolutionizes therapeutic approaches to chronic pain. Mol Pain 3:1. doi:10.1186/1744-8069-3-25

50.

Rainville P (1997) Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277:968–971. doi:10.1126/science.277.5328.968 CrossRefPubMed

51.

Peyron R, Laurent B, García-Larrea L (2000) Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiol Clin 30:263–288CrossRefPubMed

52.

Ghatan PH, Hsieh JC, Wirsen-Meurling A et al (1995) Brain activation induced by the perceptual maze test: a PET study of cognitive performance. NeuroImage 2:112–124. doi:10.1006/nimg.1995.1014 CrossRefPubMed

53.

Wager TD (2004) Placebo-induced changes in fMRI in the anticipation and experience of pain. Science 303:1162–1167. doi:10.1126/science.1093065 CrossRefPubMed

54.

Amodio DM, Frith CD (2006) Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7:268–277. doi:10.1038/nrn1884 CrossRefPubMed

55.

May A (2008) Chronic pain may change the structure of the brain. Pain 137:7–15. doi:10.1016/j.pain.2008.02.034 CrossRefPubMed

56.

Baliki MN, Geha PY, Jabakhanji R et al (2008) A preliminary fMRI study of analgesic treatment in chronic back pain and knee osteoarthritis. Mol Pain 4:47. doi:10.1186/1744-8069-4-47 CrossRefPubMedPubMedCentral

57.

Apkarian AV, Sosa Y, Sonty S et al (2004) Chronic back pain is associated with decreased prefrontal and thalamic gray matter density. J Neurosci 24:10410–10415. doi:10.1523/JNEUROSCI.2541-04.2004 CrossRefPubMed

58.

Grushka M (1987) Clinical features of burning mouth syndrome. Oral Surg Oral Med Oral Pathol 63:30–36. doi:10.1016/0030-4220(87)90336-7 CrossRefPubMed

59.

Kong J, Jensen K, Loiotile R et al (2013) Functional connectivity of the frontoparietal network predicts cognitive modulation of pain. Pain 154:459–467. doi:10.1016/j.pain.2012.12.004 CrossRefPubMed

60.

Bushnell MC, Čeko M, Low LA (2013) Cognitive and emotional control of pain and its disruption in chronic pain. Nat Rev Neurosci 14:502–511. doi:10.1038/nrn3516 CrossRefPubMedPubMedCentral

61.

Catani M, Thiebaut de Schotten M, Slater D, Dell’Acqua F (2013) Connectomic approaches before the connectome. NeuroImage 80:2–13. doi:10.1016/j.neuroimage.2013.05.109 CrossRefPubMed

62.

Talbot JD, Marrett S, Evans AC et al (1991) Multiple representations of pain in human cerebral cortex. Science 251:1355–1358CrossRefPubMed

63.

Apkarian VA (1995) Functional imaging of pain: new insights regarding the role of the cerebral cortex in human pain perception. Semin Neurosci 7:279–293. doi:10.1006/smns.1995.0031 CrossRef

64.

Hsieh J-C, Ståhle-Bäckdahl M, Hägermark Ö et al (1996) Traumatic nociceptive pain activates the hypothalamus and the periaqueductal gray: a positron emission tomography study. Pain 64:303–314. doi:10.1016/0304-3959(95)00129-8 CrossRefPubMed

65.

Forss N, Raij TT, Seppä M, Hari R (2005) Common cortical network for first and second pain. NeuroImage 24:132–142. doi:10.1016/j.neuroimage.2004.09.032 CrossRefPubMed

66.

Mullins P, Rowland L, Jung R, Sibbittjr W (2005) A novel technique to study the brain’s response to pain: proton magnetic resonance spectroscopy. NeuroImage 26:642–646. doi:10.1016/j.neuroimage.2005.02.001 CrossRefPubMed

67.

Petrovic P, Ingvar M (2002) Imaging cognitive modulation of pain processing. Pain 95:1–5CrossRefPubMed

68.

Gracely RH, Geisser ME, Giesecke T et al (2004) Pain catastrophizing and neural responses to pain among persons with fibromyalgia. Brain 127:835–843. doi:10.1093/brain/awh098 CrossRefPubMed

69.

Schweinhardt P, Bushnell MC (2010) Pain imaging in health and disease—how far have we come? J Clin Invest 120:3788. doi:10.1172/JCI43498 CrossRefPubMedPubMedCentral

70.

Fields H (2004) State-dependent opioid control of pain. Nat Rev Neurosci 5:565–575. doi:10.1038/nrn1431 CrossRefPubMed

71.

Tracey I (2005) Nociceptive processing in the human brain. Curr Opin Neurobiol 15:478–487. doi:10.1016/j.conb.2005.06.010 CrossRefPubMed

72.

Hadjipavlou G, Dunckley P, Behrens TE, Tracey I (2006) Determining anatomical connectivities between cortical and brainstem pain processing regions in humans: a diffusion tensor imaging study in healthy controls. Pain 123:169–178. doi:10.1016/j.pain.2006.02.027 CrossRefPubMed

73.

Tracey I, Mantyh PW (2007) The cerebral signature for pain perception and its modulation. Neuron 55:377–391. doi:10.1016/j.neuron.2007.07.012 CrossRefPubMed

74.

Koch MA, Norris DG, Hund-Georgiadis M (2002) An investigation of functional and anatomical connectivity using magnetic resonance imaging. NeuroImage 16:241–250. doi:10.1006/nimg.2001.1052 CrossRefPubMed

75.

Camchong J, MacDonald AW, Bell C et al (2011) Altered functional and anatomical connectivity in schizophrenia. Schizophr Bull 37:640–650. doi:10.1093/schbul/sbp131 CrossRefPubMed

76.

Damoiseaux JS, Greicius MD (2009) Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity. Brain Struct Funct 213:525–533. doi:10.1007/s00429-009-0208-6 CrossRefPubMed

77.

Messé A, Rudrauf D, Benali H, Marrelec G (2014) Relating structure and function in the human brain: relative contributions of anatomy, stationary dynamics, and non-stationarities. PLoS Comp Biol 10:e1003530. doi:10.1371/journal.pcbi.1003530 CrossRef

78.

Greicius MD, Supekar K, Menon V, Dougherty RF (2008) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19:72–78. doi:10.1093/cercor/bhn059 CrossRefPubMedPubMedCentral

79.

Xiao H, Yang Y, Xi J-H, Chen Z-Q (2015) Structural and functional connectivity in traumatic brain injury. Neural Regen Res 10:2062–2071. doi:10.4103/1673-5374.172328 CrossRefPubMedPubMedCentral

80.

Ray S, Miller M, Karalunas S et al (2014) Structural and functional connectivity of the human brain in autism spectrum disorders and attention-deficit/hyperactivity disorder: a rich club-organization study. Hum Brain Mapp 35:6032–6048. doi:10.1002/hbm.22603 CrossRefPubMedPubMedCentral

81.

Betzel RF, Byrge L, He Y et al (2014) Changes in structural and functional connectivity among resting-state networks across the human lifespan. NeuroImage 102(Pt 2):345–357. doi:10.1016/j.neuroimage.2014.07.067 CrossRefPubMed

Title: Altered structural connectivity of pain-related brain network in burning mouth syndrome—investigation by graph analysis of probabilistic tractography
Authors: Akihiko Wada
Takashi Shizukuishi
Junko Kikuta
Haruyasu Yamada
Yusuke Watanabe
Yoshiki Imamura
Takahiro Shinozaki
Ko Dezawa
Hiroki Haradome
Osamu Abe
Publication date: 01-05-2017
Publisher: Springer Berlin Heidelberg
Published in: Neuroradiology / Issue 5/2017
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI: https://doi.org/10.1007/s00234-017-1830-2

At a glance: The STEP trials

Springer Medicine

Altered structural connectivity of pain-related brain network in burning mouth syndrome—investigation by graph analysis of probabilistic tractography

Abstract

Purpose

Methods

Results

Conclusion

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 5/2017

A semi-automated volumetric software for segmentation and perfusion parameter quantification of brain tumors using 320-row multidetector computed tomography: a validation study

The structural connectome in children: basic concepts, how to build it, and synopsis of challenges for the developing pediatric brain

Radiological imaging features of the basal ganglia that may predict progression to hemicraniectomy in large territory middle cerebral artery infarct

Association between proximal internal carotid artery steno-occlusive disease and diffuse wall thickening in its petrous segment: a magnetic resonance vessel wall imaging study

Cerebral aneurysms and metastases occurring as a delayed complication of resected atrial Myxoma: Imaging findings including high resolution Vessel Wall MRI

Erratum to: Oculo-auriculo-vertebral spectrum: going beyond the first and second pharyngeal arch involvement