Research Article
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Volumetric analysis of pain centers in migraine patients

Year 2024, , 628 - 642, 09.10.2024
https://doi.org/10.31362/patd.1462085

Abstract

Purpose: To investigate patterns of abnormalities in pain centers among patients with chronic pain, particularly
those with migraines. The study aims to explore the potential correlation with pain duration and migraine types,
and to propose new interventions for managing chronic pain.
Materials and methods: Radiologic data of 32 migraine patients and 28 healthy controls underwent threedimensional
iso T1-weighted brain MRI between 2019 and 2023 at our university hospital were examined.
Patients with a minimum migraine duration of three years were included and divided into two groups: patients
without aura (MwoA group) and patients with aura (MwA group). Additionally, patients were categorized based
on the frequency of their migraine attacks, either episodic (EM) or chronic (CM). A control group (Group C) was
also established for comparison. Volumetric analysis, including cortical and subcortical pain-related structures,
was performed using volBrain software.
Results: Significant differences were observed in grey matter (p=0.037), cortical grey matter (p=0.022),
cerebrum grey matter (p=0.026), anterior cingulate cortex (ACC) (p=0.017), middle cingulate cortex (MCC)
(p=0.014), and posterior cingulate cortex (PCC) (p=0.008) volumes among the groups. Group comparisons
revealed significant differences in the ACC, MCC, and PCC between Groups C and MwoA (p=0.047, p=0.040,
and p=0.047, respectively) and PCC between Groups C and MwA (p=0.026), possibly related to aura
pathogenesis. Patients without aura exhibited non-significantly thinner postcentral gyrus (p=0.079), suggesting
potential cortical involvement.
Conclusions: This study provides insights into pain center abnormalities in migraine patients and their potential
relevance to pain duration and migraine type.

Ethical Statement

Trakya University Non-Interventional Clinical Research Ethics Committee (TÜTF-GOBAEK 2023/287)

Supporting Institution

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors

References

  • 1. Treede, RD, Rief W, Barke A, et al. A classification of chronic pain for ICD-11. Pain 2015;156:1003-1007. https://doi.org/10.1097/j.pain.0000000000000160
  • 2. Davis KD, Flor H, Greely HT, et al. Brain imaging tests for chronic pain: medical, legal and ethical issues and recommendations. Nat Rev Neurol 2017;13:624-638. https://doi.org/10.1038/nrneurol.2017.122
  • 3. Kim JH, Suh SI, Seol HY, et al. Regional grey matter changes in patients with migraine: a voxel-based morphometry study. Cephalalgia 2008;28:598-604. https://doi.org/10.1111/j.1468-2982.2008.01550.x
  • 4. Valfrè W, Rainero I, Bergui M, Pinessi L. Voxel‐based morphometry reveals gray matter abnormalities in migraine. Headache 2008;48:109-117. https://doi.org/10.1111/j.1526-4610.2007.00723.x
  • 5. Qin Z, He XW, Zhang J, et al. Structural changes of cerebellum and brainstem in migraine without aura. J Headache Pain 2019;20:93(e1-9). https://doi.org/10.1186/s10194-019-1045-5
  • 6. Palm Meinders IH, Arkink EB, Koppen H, et al. Volumetric brain changes in migraineurs from the general population. Neurology 2017;89:2066-2074. https://doi.org/10.1212/WNL.0000000000004640
  • 7. Schwedt TJ, Dodick DW. Advanced neuroimaging of migraine. Lancet Neurol 2009;8:560-568. https://doi.org/10.1016/S1474-4422(09)70107-3
  • 8. Bashir A, Lipton RB, Ashina S, Ashina M. Migraine and structural changes in the brain: a systematic review and meta-analysis. Neurology 2013;81:1260-1268. https://doi.org/10.1212/WNL.0b013e3182a6cb32
  • 9. Bonanno L, Lo Buono V, De Salvo S, et al. Brain morphologic abnormalities in migraine patients: an observational study. J Headache Pain 2020;21:39(e1-6). https://doi.org/10.1186/s10194-020-01109-2
  • 10. Kreitzer AC, Malenka RC. Striatal plasticity and basal ganglia circuit function. Neuron 2008;60:543-554. https://doi.org/10.1016/j.neuron.2008.11.005
  • 11. Kruit MC, Launer LJ, Overbosch J, van Buchem MA, Ferrari MD. Iron accumulation in deep brain nuclei in migraine: a population-based magnetic resonance imaging study. Cephalalgia 2009;29:351-359. https://doi.org/10.1111/j.1468-2982.2008.01723.x
  • 12. Yuan K, Zhao L, Cheng P, et al. Altered structure and resting-state functional connectivity of the basal ganglia in migraine patients without aura. J Pain 2013;14:836-844. https://doi.org/10.1016/j.jpain.2013.02.010
  • 13. Rocca MA, Messina R, Colombo B, Falini A, Comi G, Filippi M. Structural brain MRI abnormalities in pediatric patients with migraine. J Neurol 2014;261:350-357. https://doi.org/10.1007/s00415-013-7201-y
  • 14. Younis S, Hougaard A, Noseda R, Ashina M. Current understanding of thalamic structure and function in migraine. Cephalalgia 2019;39:1675-1682. https://doi.org/10.1177/0333102418791595
  • 15. Magon S, May A, Stankewitz A, et al. Morphological abnormalities of thalamic subnuclei in migraine: a multicenter MRI study at 3 tesla. J Neurosci 2015;35:13800-13806. https://doi.org/10.1523/JNEUROSCI.2154-15.2015
  • 16. Granziera C, DaSilva AF, Snyder J, Tuch DS, Hadjikhani N. Anatomical alterations of the visual motion processing network in migraine with and without aura. PLoS Med 2006;3:e402(1915-1921). https://doi.org/10.1371/journal.pmed.0030402
  • 17. Chen XY, Chen ZY, Dong Z, Liu MQ, Yu SY. Regional volume changes of the brain in migraine chronification. Neural Regen Res 2020;15:1701-1708. https://doi.org/10.4103/1673-5374.276360
  • 18. Maleki N, Becerra L, Brawn J, McEwen B, Burstein R, Borsook D. Common hippocampal structural and functional changes in migraine. Brain Struct Funct 2013;218:903-912. https://doi.org/S0896-6273(01)00533-5
  • 19. Price DD. Psychological and neural mechanisms of the affective dimension of pain. Science 2000;288:1769-1772. https://doi.org/10.1126/science.288.5472.1769
  • 20. Bliss TV, Collingridge GL, Kaang BK, Zhuo M. Synaptic plasticity in the anterior cingulate cortex in acute and chronic pain. Nat Rev Neurosci 2016;17:485-496. https://doi.org/10.1038/nrn.2016.68
  • 21. Xiao X, Ding M, Zhang YQ. Role of the anterior cingulate cortex in translational pain research. Neurosci Bull 2021;37:405-422. https://doi.org/10.1007/s12264-020-00615-2
  • 22. Davis KD, Taub E, Duffner F, et al. Activation of the anterior cingulate cortex by thalamic stimulation in patients with chronic pain: a positron emission tomography study. Neurosurg Focus 2000;8:1-6. https://doi.org/10.3171/foc.2000.8.2.7
  • 23. Talbot J, Villemure JG, Bushnell MC, Duncan GH. Evaluation of pain perception after anterior capsulotomy: a case report. Somatosens Mot Res 1995;12:115-126. https://doi.org/10.3109/08990229509101503
  • 24. Mo J, Zhang J, Hu W, Luo F, Zhang K. Whole-brain morphological alterations associated with trigeminal neuralgia. J Headache Pain 2021;22:95(e1-10). https://doi.org/10.1186/s10194-021-01308-5
  • 25. Zhang J, Su J, Wang M, et al. The posterior insula shows disrupted brain functional connectivity in female migraineurs without aura based on brainnetome atlas. Sci Rep 2017;7:16868(e1-12). https://doi.org/10.1038/s41598-017-17069-8
  • 26. Tso AR, Trujillo A, Guo CC, Goadsby PJ, Seeley WW. The anterior insula shows heightened interictal intrinsic connectivity in migraine without aura. Neurology 2015;84:1043-1050. https://doi.org/10.1212/WNL.0000000000001330
  • 27. Mammadkhanli O, Kehaya S, Solak S, Yagmurlu K. Insular cortex involvement in migraine subjects with chronic pain: a volumetric radiological and clinical study. Journal of Clinical Neuroscience 2024;123:157-161. https://doi.org/10.1016/j.jocn.2024.03.034
  • 28. Neumann N, Domin M, Schmidt CO, Lotze M. Chronic pain is associated with less grey matter volume in the anterior cingulum, anterior and posterior insula and hippocampus across three different chronic pain conditions. Eur J Pain 2023;27:1239-1248. https://doi.org/10.1002/ejp.2153
  • 29. Yin T, Lan L, Tian Z, et al. Parahippocampus hypertrophy drives gray matter morphological alterations in migraine patients without aura. J Headache Pain 2023;24:53(e1-12). https://doi.org/10.1186/s10194-023-01588-z
  • 30. Silva NO, Maciel NM, Nather JC Jr, et al. White matter lesions identified by magnetic resonance in women with migraine: a volumetric analysis and clinical correlations. Diagnostics (Basel) 2023;13:799(e1-13). https://doi.org/10.3390/diagnostics13040799
  • 31. Chen ZH, Cui YL, Sun JT, et al. The brain structure and function abnormalities of migraineurs: A systematic review and neuroimaging meta-analysis. Front Neurol 2022;13:1022793. https://doi.org/10.3389/fneur.2022.1022793 32. Zhang X, Zhou J, Guo M, et al. A systematic review and meta-analysis of voxel-based morphometric studies of migraine. J Neurol 2023;270:152-170. https://doi.org/10.1007/s00415-022-11363-w
  • 33. Cao Z, Yu W, Zhang Z, et al. Decreased gray matter volume in the frontal cortex of migraine patients with associated functional connectivity alterations: a VBM and rs-FC Study. Pain Res Manag 2022;2022:2115956. https://doi.org/10.1155/2022/2115956
  • 34. Masson R, Demarquay G, Meunier D, et al. Is migraine associated to brain anatomical alterations? New data and coordinate-based meta-analysis. Brain Topogr 2021;34:384-401. https://doi.org/10.1007/s10548-021-00824-6

Migren hastalarında ağrı merkezlerinin volümetrik analizi

Year 2024, , 628 - 642, 09.10.2024
https://doi.org/10.31362/patd.1462085

Abstract

Amaç: Kronik ağrısı olan, özellikle migren hastalarında ağrı merkezlerindeki anormallik paternlerini araştırmak.
Çalışma, ağrı süresi ve migren tipleri ile olası korelasyonu keşfetmeyi ve kronik ağrı yönetimi için yeni
müdahaleler önermeyi amaçlamaktadır.
Gereç ve yöntem: Üniversite hastanemizde 2019-2023 yılları arasında üç boyutlu izo T1 ağırlıklı beyin MRG'si
çekilen 32 migren hastası ve 28 sağlıklı kontrolün radyolojik verileri incelendi. En az 3 yıllık migren süresi
olan hastalar çalışmaya dahil edildi ve aura yokluğu (Grup MwoA) veya varlığına (Grup MwA) göre iki gruba
ayrıldı. Ek olarak hastalar migren ataklarının sıklığına göre epizodik (EM) veya kronik (CM) olarak sınıflandırıldı.
Karşılaştırma için bir kontrol grubu da (Grup C) oluşturuldu. Kortikal ve subkortikal ağrıyla ilişkili yapılar dahil
olmak üzere volümetrik analiz volBrain yazılımı kullanılarak yapıldı.
Bulgular: Gruplar arasında gri madde (p=0,037), kortikal gri madde (p=0,022), serebrum gri maddesi (p=0,026),
ön singulat korteks (ACC) (p=0,017), orta singulat korteks (MCC) (p=0,014) ve arka singulat korteks (PCC)
(p=0,008) hacimlerinde anlamlı farklılıklar gözlendi. Grup karşılaştırmalarında ACC, MCC ve PCC'de Grup C
ve MwoA arasında (sırasıyla p=0,047, p=0,040 ve p=0,047) ve PCC'de Grup C ve MwA arasında (p=0,026)
muhtemelen aura patogeneziyle ilişkili anlamlı farklılıklar ortaya konuldu. Aurası olmayan hastalarda, potansiyel
kortikal tutulumu düşündüren, istatistiksel olarak anlamlı olmayan (p=0,079) daha ince postcentral girus görüldü.
Sonuç: Bu çalışma, migren hastalarında ağrı merkezi anormalliklerine ve bu durumun ağrı süresi ve migren tipi
ile potansiyel ilişkisine dair anlayış sağlamaktadır.

Ethical Statement

Trakya Üniversitesi Girişimsel Olmayan Klinik Araştırmalar Etik Kurulu (TÜTF-GOBAEK 2023/287)

Supporting Institution

Bu araştırmada kamu, ticari veya kâr amacı gütmeyen sektörlerdeki fon sağlayıcı kuruluşlardan herhangi bir özel hibe alınmadı

References

  • 1. Treede, RD, Rief W, Barke A, et al. A classification of chronic pain for ICD-11. Pain 2015;156:1003-1007. https://doi.org/10.1097/j.pain.0000000000000160
  • 2. Davis KD, Flor H, Greely HT, et al. Brain imaging tests for chronic pain: medical, legal and ethical issues and recommendations. Nat Rev Neurol 2017;13:624-638. https://doi.org/10.1038/nrneurol.2017.122
  • 3. Kim JH, Suh SI, Seol HY, et al. Regional grey matter changes in patients with migraine: a voxel-based morphometry study. Cephalalgia 2008;28:598-604. https://doi.org/10.1111/j.1468-2982.2008.01550.x
  • 4. Valfrè W, Rainero I, Bergui M, Pinessi L. Voxel‐based morphometry reveals gray matter abnormalities in migraine. Headache 2008;48:109-117. https://doi.org/10.1111/j.1526-4610.2007.00723.x
  • 5. Qin Z, He XW, Zhang J, et al. Structural changes of cerebellum and brainstem in migraine without aura. J Headache Pain 2019;20:93(e1-9). https://doi.org/10.1186/s10194-019-1045-5
  • 6. Palm Meinders IH, Arkink EB, Koppen H, et al. Volumetric brain changes in migraineurs from the general population. Neurology 2017;89:2066-2074. https://doi.org/10.1212/WNL.0000000000004640
  • 7. Schwedt TJ, Dodick DW. Advanced neuroimaging of migraine. Lancet Neurol 2009;8:560-568. https://doi.org/10.1016/S1474-4422(09)70107-3
  • 8. Bashir A, Lipton RB, Ashina S, Ashina M. Migraine and structural changes in the brain: a systematic review and meta-analysis. Neurology 2013;81:1260-1268. https://doi.org/10.1212/WNL.0b013e3182a6cb32
  • 9. Bonanno L, Lo Buono V, De Salvo S, et al. Brain morphologic abnormalities in migraine patients: an observational study. J Headache Pain 2020;21:39(e1-6). https://doi.org/10.1186/s10194-020-01109-2
  • 10. Kreitzer AC, Malenka RC. Striatal plasticity and basal ganglia circuit function. Neuron 2008;60:543-554. https://doi.org/10.1016/j.neuron.2008.11.005
  • 11. Kruit MC, Launer LJ, Overbosch J, van Buchem MA, Ferrari MD. Iron accumulation in deep brain nuclei in migraine: a population-based magnetic resonance imaging study. Cephalalgia 2009;29:351-359. https://doi.org/10.1111/j.1468-2982.2008.01723.x
  • 12. Yuan K, Zhao L, Cheng P, et al. Altered structure and resting-state functional connectivity of the basal ganglia in migraine patients without aura. J Pain 2013;14:836-844. https://doi.org/10.1016/j.jpain.2013.02.010
  • 13. Rocca MA, Messina R, Colombo B, Falini A, Comi G, Filippi M. Structural brain MRI abnormalities in pediatric patients with migraine. J Neurol 2014;261:350-357. https://doi.org/10.1007/s00415-013-7201-y
  • 14. Younis S, Hougaard A, Noseda R, Ashina M. Current understanding of thalamic structure and function in migraine. Cephalalgia 2019;39:1675-1682. https://doi.org/10.1177/0333102418791595
  • 15. Magon S, May A, Stankewitz A, et al. Morphological abnormalities of thalamic subnuclei in migraine: a multicenter MRI study at 3 tesla. J Neurosci 2015;35:13800-13806. https://doi.org/10.1523/JNEUROSCI.2154-15.2015
  • 16. Granziera C, DaSilva AF, Snyder J, Tuch DS, Hadjikhani N. Anatomical alterations of the visual motion processing network in migraine with and without aura. PLoS Med 2006;3:e402(1915-1921). https://doi.org/10.1371/journal.pmed.0030402
  • 17. Chen XY, Chen ZY, Dong Z, Liu MQ, Yu SY. Regional volume changes of the brain in migraine chronification. Neural Regen Res 2020;15:1701-1708. https://doi.org/10.4103/1673-5374.276360
  • 18. Maleki N, Becerra L, Brawn J, McEwen B, Burstein R, Borsook D. Common hippocampal structural and functional changes in migraine. Brain Struct Funct 2013;218:903-912. https://doi.org/S0896-6273(01)00533-5
  • 19. Price DD. Psychological and neural mechanisms of the affective dimension of pain. Science 2000;288:1769-1772. https://doi.org/10.1126/science.288.5472.1769
  • 20. Bliss TV, Collingridge GL, Kaang BK, Zhuo M. Synaptic plasticity in the anterior cingulate cortex in acute and chronic pain. Nat Rev Neurosci 2016;17:485-496. https://doi.org/10.1038/nrn.2016.68
  • 21. Xiao X, Ding M, Zhang YQ. Role of the anterior cingulate cortex in translational pain research. Neurosci Bull 2021;37:405-422. https://doi.org/10.1007/s12264-020-00615-2
  • 22. Davis KD, Taub E, Duffner F, et al. Activation of the anterior cingulate cortex by thalamic stimulation in patients with chronic pain: a positron emission tomography study. Neurosurg Focus 2000;8:1-6. https://doi.org/10.3171/foc.2000.8.2.7
  • 23. Talbot J, Villemure JG, Bushnell MC, Duncan GH. Evaluation of pain perception after anterior capsulotomy: a case report. Somatosens Mot Res 1995;12:115-126. https://doi.org/10.3109/08990229509101503
  • 24. Mo J, Zhang J, Hu W, Luo F, Zhang K. Whole-brain morphological alterations associated with trigeminal neuralgia. J Headache Pain 2021;22:95(e1-10). https://doi.org/10.1186/s10194-021-01308-5
  • 25. Zhang J, Su J, Wang M, et al. The posterior insula shows disrupted brain functional connectivity in female migraineurs without aura based on brainnetome atlas. Sci Rep 2017;7:16868(e1-12). https://doi.org/10.1038/s41598-017-17069-8
  • 26. Tso AR, Trujillo A, Guo CC, Goadsby PJ, Seeley WW. The anterior insula shows heightened interictal intrinsic connectivity in migraine without aura. Neurology 2015;84:1043-1050. https://doi.org/10.1212/WNL.0000000000001330
  • 27. Mammadkhanli O, Kehaya S, Solak S, Yagmurlu K. Insular cortex involvement in migraine subjects with chronic pain: a volumetric radiological and clinical study. Journal of Clinical Neuroscience 2024;123:157-161. https://doi.org/10.1016/j.jocn.2024.03.034
  • 28. Neumann N, Domin M, Schmidt CO, Lotze M. Chronic pain is associated with less grey matter volume in the anterior cingulum, anterior and posterior insula and hippocampus across three different chronic pain conditions. Eur J Pain 2023;27:1239-1248. https://doi.org/10.1002/ejp.2153
  • 29. Yin T, Lan L, Tian Z, et al. Parahippocampus hypertrophy drives gray matter morphological alterations in migraine patients without aura. J Headache Pain 2023;24:53(e1-12). https://doi.org/10.1186/s10194-023-01588-z
  • 30. Silva NO, Maciel NM, Nather JC Jr, et al. White matter lesions identified by magnetic resonance in women with migraine: a volumetric analysis and clinical correlations. Diagnostics (Basel) 2023;13:799(e1-13). https://doi.org/10.3390/diagnostics13040799
  • 31. Chen ZH, Cui YL, Sun JT, et al. The brain structure and function abnormalities of migraineurs: A systematic review and neuroimaging meta-analysis. Front Neurol 2022;13:1022793. https://doi.org/10.3389/fneur.2022.1022793 32. Zhang X, Zhou J, Guo M, et al. A systematic review and meta-analysis of voxel-based morphometric studies of migraine. J Neurol 2023;270:152-170. https://doi.org/10.1007/s00415-022-11363-w
  • 33. Cao Z, Yu W, Zhang Z, et al. Decreased gray matter volume in the frontal cortex of migraine patients with associated functional connectivity alterations: a VBM and rs-FC Study. Pain Res Manag 2022;2022:2115956. https://doi.org/10.1155/2022/2115956
  • 34. Masson R, Demarquay G, Meunier D, et al. Is migraine associated to brain anatomical alterations? New data and coordinate-based meta-analysis. Brain Topogr 2021;34:384-401. https://doi.org/10.1007/s10548-021-00824-6
There are 33 citations in total.

Details

Primary Language English
Subjects Neurology and Neuromuscular Diseases, Neurosciences (Other)
Journal Section Research Article
Authors

Orkhan Mammadkhanli 0000-0003-3299-4196

Kaan Yagmurlu 0000-0002-7635-2809

Sezgin Kehaya 0000-0002-9608-9278

Erdi Şensöz 0000-0001-6889-3720

Ahmet Tolgay Akıncı 0000-0002-9937-076X

Osman Şimşek 0000-0002-8716-5187

Early Pub Date June 4, 2024
Publication Date October 9, 2024
Submission Date March 31, 2024
Acceptance Date April 16, 2024
Published in Issue Year 2024

Cite

AMA Mammadkhanli O, Yagmurlu K, Kehaya S, Şensöz E, Akıncı AT, Şimşek O. Volumetric analysis of pain centers in migraine patients. Pam Tıp Derg. October 2024;17(4):628-642. doi:10.31362/patd.1462085
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