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Neurological Sciences

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01-03-2021 | Magnetic Resonance Imaging | Review Article

Imaging and depression in multiple sclerosis: a historical perspective

Authors: Fabio Giuseppe Masuccio, Giulia Gamberini, Massimiliano Calabrese, Claudio Solaro

Published in: Neurological Sciences | Issue 3/2021

Abstract

Purpose

Patients affected with multiple sclerosis suffer from depression more frequently than the general population. Beyond psychosocial, genetic and immune-inflammatory factors, also the brain damage which is peculiar of multiple sclerosis has been claimed to have a role in the aetiology of depression in those patients. The study of this interesting relation has been implemented with both conventional and advanced magnetic resonance imaging techniques. The aim of this review is to provide a historical perspective on the link between multiple sclerosis-related depression and structural and functional brain damage.

Methods

In this review, the results of the MRI studies regarding multiple sclerosis-related brain damage and the presence of depression are presented.

Results

The findings of the reports reveal a link between brain pathology and depressive symptoms or the diagnosis of depression in multiple sclerosis.

Conclusions

Although a multifactorial aetiology has been theorized for depression and depressive symptoms in patients with multiple sclerosis, this review supports the hypothesis that the structural and functional brain impairment might substantially be amongst those factors. Thus, depression itself might be a symptom with a neuro-biological basis and not only the consequence of the disability derived from the neurological impairment.

Solaro C, Gamberini G, Masuccio FG (2018) Depression in multiple sclerosis: epidemiology, aetiology, diagnosis and treatment. CNS Drugs 32:117–133. https://doi.org/10.1007/s40263-018-0489-5CrossRefPubMed

Solaro C, Trabucco E, Signori A, Martinelli V, Radaelli M, Centonze D, Rossi S, Grasso MG, Clemenzi A, Bonavita S, D’Ambrosio A, Patti F, D’Amico E, Cruccu G, Truini A (2016) Depressive symptoms correlate with disability and disease course in multiple sclerosis patients: an Italian multi-center study using the Beck Depression Inventory. PLoS One 11:1–9. https://doi.org/10.1371/journal.pone.0160261CrossRef

Alba Palé L, León Caballero J, Samsó Buxareu B, Salgado Serrano P, Pérez Solà V (2017) Systematic review of depression in patients with multiple sclerosis and its relationship to interferonβ treatment. Mult Scler Relat Disord 17:138–143. https://doi.org/10.1016/j.msard.2017.07.008CrossRefPubMed

Feinstein A, Magalhaes S, Richard J et al (2014) The link between multiple sclerosis and depression. Nat Publ Gr 10:507–517. https://doi.org/10.1038/nrneurol.2014.139CrossRef

Wattjes MP, Rovira À, Miller D et al (2015) Evidence-based guidelines: MAGNIMS consensus guidelines on the use of MRI in multiple sclerosis - establishing disease prognosis and monitoring patients. Nat Rev Neurol 11:597–606. https://doi.org/10.1038/nrneurol.2015.157CrossRefPubMed

Honer WG, Hurwitz T, Li DKB, Palmer M, Paty DW (1987) Temporal lobe involvement in multiple sclerosis patients with psychiatric disorders. Arch Neurol 44:187–190. https://doi.org/10.1001/archneur.1987.00520140053017CrossRefPubMed

Reischies FM, Baum K, Bräu H et al (1988) Cerebral magnetic resonance imaging findings in multiple sclerosis. Arch Neurol 8:8–10

Ron MA, Logsdail SJ (1989) Psychiatric morbidity in multiple sclerosis: a clinical and MRI study. Psychol Med 19:887–895. https://doi.org/10.1017/S0033291700005602CrossRefPubMed

Millefiorini E, Paduvani A, Pozzili C et al (1992) Depression in the early phase of MS: influence of functional disability, cognitive impairment and brain abnormalities. Acta Neurol Scand 86:354–358CrossRef

10.

Sabatini U, Pozzilli C, Pantano P, Koudriavtseva T, Padovani A, Millefiorini E, Biasi CD, Gualdi GF, Salvetti M, Lenzi GL (1996) Involvement of the limbic system in multiple sclerosis patients with depressive disorders. Biol Psychiatry 39:970–975. https://doi.org/10.1016/0006-3223(95)00291-XCrossRefPubMed

11.

George MS, Kellner CH, Bernstein H, Goust JM (1994) A magnetic resonance imaging investigation into mood disorders in multiple sclerosis: a pilot study. J Nerv Ment Dis 182:410–412CrossRef

12.

Pujol J, Bello J, Deus J, Marti-Vilalta JL, Capdevila A (1997) Lesions in the left arcuate fasciculus region and depressive symptoms in multiple sclerosis. Neurology 49:1105–1110. https://doi.org/10.1212/WNL.49.4.1105CrossRefPubMed

13.

Pujol J, Bello J, Deus J, Cardoner Ń, Martı́-Vilalta JL, Capdevila A (2000) Beck Depression Inventory factors related to demyelinating lesions of the left arcuate fasciculus region. Psychiatry Res - Neuroimaging 99:151–159. https://doi.org/10.1016/S0925-4927(00)00061-5CrossRef

14.

Berg D, Supprian T, Thomae J, Warmuth-Metz M, Horowski A, Zeiler B, Magnus T, Rieckmann P, Becker G (2000) Lesion pattern in patients with multiple sclerosis and depression. Mult Scler 6:156–162. https://doi.org/10.1177/135245850000600304CrossRefPubMed

15.

Bakshi R, Czarnecki CAD, Shaikh ZA et al (2000) Brain MRI lesions and atrophy are related to depression in multiple sclerosis. Neuroreport 11:1153–1158. https://doi.org/10.1097/00001756-200004270-00003

16.

Möller A, Wiedemann G, Rohde U, Backmund H, Sonntag A (1994) Correlates of cognitive impairment and depressive mood disorder in multiple sclerosis. Acta Psychiatr Scand 89:117–121. https://doi.org/10.1111/j.1600-0447.1994.tb01497.xCrossRefPubMed

17.

Kallaur AP, Lopes J, Oliveira SR, Simão ANC, Reiche EMV, de Almeida ERD, Morimoto HK, de Pereira WLCJ, Alfieri DF, Borelli SD, Kaimen-Maciel DR, Maes M (2016) Immune-inflammatory and oxidative and nitrosative stress biomarkers of depression symptoms in subjects with multiple sclerosis : increased peripheral inflammation but less acute neuroinflammation. Mol Neurobiol 53:5191–5202. https://doi.org/10.1007/s12035-015-9443-4CrossRefPubMed

18.

Rossi S, Studer V, Motta C, Polidoro S, Perugini J, Macchiarulo G, Giovannetti AM, Pareja-Gutierrez L, Calò A, Colonna I, Furlan R, Martino G, Centonze D (2017) Neuroinflammation drives anxiety and depression in relapsing-remitting multiple sclerosis. Neurology 89:1338–1347. https://doi.org/10.1212/WNL.0000000000004411CrossRefPubMed

19.

Calabrese M, Magliozzi R, Ciccarelli O, Geurts JJG, Reynolds R, Martin R (2015) Exploring the origins of grey matter damage in multiple sclerosis. Nat Rev Neurosci 16:147–158. https://doi.org/10.1038/nrn3900CrossRefPubMed

20.

Zorzon M, de Masi R, Nasuelli D, Ukmar M, Pozzi Mucelli R, Cazzato G, Bratina A, Zivadinov R (2001) Depression and anxiety in multiple sclerosis. A clinical and MRI study in 95 subjects. J Neurol 248:416–421. https://doi.org/10.1007/s004150170184CrossRefPubMed

21.

Zorzon M, Zivadinov R, Nasuelli D et al (2002) Depressive symptoms and MRI changes in multiple sclerosis. Eur J Neurol 9:491–496. https://doi.org/10.1046/j.1468-1331.2002.00442.x

22.

Feinstein A, Roy P, Lobaugh N et al (2004) Structural brain abnormalities in multiple sclerosis patients with major depression. Neurology 62:586–590. https://doi.org/10.1212/01.wnl.0000110316.12086.0c

23.

Stuke H, Hanken K, Hirsch J et al (2016) Cross-sectional and longitudinal relationships between depressive symptoms and brain atrophy in MS patients. 10:1–8. https://doi.org/10.3389/fnhum.2016.00622

24.

Pravatà E, Rocca MA, Valsasina P et al (2017) Gray matter trophism, cognitive impairment, and depression in patients with multipls sclerosis. Mult Scler J 23:1864–1874. https://doi.org/10.1177/2040620717690316CrossRef

25.

Nygaard GO, Walhovd KB, Sowa P, Chepkoech JL, Bjørnerud A, Due-Tønnessen P, Landrø NI, Damangir S, Spulber G, Storsve AB, Beyer MK, Fjell AM, Celius EG, Harbo HF (2015) Cortical thickness and surface area relate to specific symptoms in early relapsing–remitting multiple sclerosis. Mult Scler J 21:402–414. https://doi.org/10.1177/1352458514543811CrossRef

26.

Koolschijn PCMP, Van Haren NEM, Lensvelt-Mulders GJLM et al (2009) Brain volume abnormalities in major depressive disorder: a meta-analysis of magnetic resonance imaging studies. Hum Brain Mapp 30:3719–3735. https://doi.org/10.1002/hbm.20801CrossRefPubMedPubMedCentral

27.

Gold SM, Kern KC, O’Connor MF et al (2010) Smaller cornu ammonis 23/dentate gyrus volumes and elevated cortisol in multiple sclerosis patients with depressive symptoms. Biol Psychiatry 68:553–559. https://doi.org/10.1016/j.biopsych.2010.04.025CrossRefPubMedPubMedCentral

28.

Kiy G, Lehmann P, Hahn HK, Eling P, Kastrup A, Hildebrandt H (2011) Decreased hippocampal volume, indirectly measured, is associated with depressive symptoms and consolidation deficits in multiple sclerosis. Mult Scler J 17:1088–1097. https://doi.org/10.1177/1352458511403530CrossRef

29.

Gobbi C, Rocca MA, Pagani E, Riccitelli GC, Pravatà E, Radaelli M, Martinelli-Boneschi F, Falini A, Copetti M, Comi G, Filippi M (2014) Forceps minor damage and co-occurrence of depression and fatigue in multiple sclerosis. Mult Scler J 20:1633–1640. https://doi.org/10.1177/1352458514530022CrossRef

30.

Gold SM, Connor MO, Gill R et al (2014) Detection of altered hippocampal morphology in multiple sclerosis-associated depression using automated surface mesh modeling. 37:30–37. https://doi.org/10.1002/hbm.22154

31.

Feinstein A, O’Connor P, Akbar N et al (2010) Diffusion tensor imaging abnormalities in depressed multiple sclerosis patients. Mult Scler 16:189–196. https://doi.org/10.1177/1352458509355461CrossRefPubMed

32.

Shen Y, Bai L, Gao Y, Cui F, Tan Z, Tao Y, Sun C, Zhou L (2014) Depressive symptoms in multiple sclerosis from an in vivo study with TBSS. 2014: https://doi.org/10.1155/2014/148465

33.

Nigro S, Passamonti L, Riccelli R, Toschi N, Rocca F, Valentino P, Nisticò R, Fera F, Quattrone A (2015) Structural ‘connectomic’ alterations in the limbic system of multiple sclerosis patients with major depression. Mult Scler J 21:1003–1012. https://doi.org/10.1177/1352458514558474CrossRef

34.

Rojas JI, Sanchez F, Patrucco L, Miguez J, Besada C, Cristiano E (2017) Brain structural changes in patients in the early stages of multiple sclerosis with depression. Neurol Res 39:596–600. https://doi.org/10.1080/01616412.2017.1298279CrossRefPubMed

35.

Rocca MA, Pravatà E, Valsasina P, Radaelli M, Colombo B, Vacchi L, Gobbi C, Comi G, Falini A, Filippi M (2015) Hippocampal-DMN disconnectivity in MS is related to WM lesions and depression. Hum Brain Mapp 36:5051–5063. https://doi.org/10.1002/hbm.22992CrossRefPubMedPubMedCentral

36.

Bonavita S, Sacco R, Esposito S et al (2017) Default mode network changes in multiple sclerosis : a link between depression and cognitive impairment?:27–36. https://doi.org/10.1111/ene.13112

37.

van Geest Q, Boeschoten RE, Keijzer MJ, Steenwijk MD, Pouwels PJW, Twisk JWR, Smit JH, Uitdehaag BMJ, Geurts JJG, van Oppen P, Hulst HE (2019) Fronto-limbic disconnection in patients with multiple sclerosis and depression. Mult Scler J 25:715–726. https://doi.org/10.1177/httpsCrossRef

38.

Riccelli R, Passamonti L, Cerasa A, Nigro S, Cavalli SM, Chiriaco C, Valentino P, Nisticò R, Quattrone A (2016) Individual differences in depression are associated with abnormal function of the limbic system in multiple sclerosis patients. Mult Scler J 22:1094–1105. https://doi.org/10.1177/1352458515606987CrossRef

39.

Fassbender K, Schmidt R, Mo R, Ku J (2017) Mood disorders and dysfunction of the hypothalamic-pituitary-adrenal axis in multiple sclerosis. Arch Neurol 55:66–72CrossRef

40.

Kantorová E, Poláček H, Bittšanský M, Baranovičová E, Hnilicová P, Čierny D, Sivák Š, Nosáľ V, Zeleňák K, Kurča E (2017) Hypothalamic damage in multiple sclerosis correlates with disease activity, disability , depression , and fatigue. Neurol Res 6412:1–8. https://doi.org/10.1080/01616412.2016.1275460CrossRef

41.

Yaldizli PIK, Yonekawa T et al (2016) The association between olfactory bulb volume, cognitive dysfunction, physical disability and depression in multiple sclerosis. Eur J Neurol 23:510–519. https://doi.org/10.1111/ene.12891CrossRefPubMed

42.

Zivadinov R, Zorzon M, Bragadin LM et al (1999) Olfactory loss in multiple sclerosis. J Neurol Sci 168:127–130CrossRef

43.

Gobbi C, Rocca M, Riccitelli G, Pagani E, Messina R, Preziosa P, Colombo B, Rodegher M, Falini A, Comi G, Filippi M (2014) Influence of the topography of brain damage on depression and fatigue in patients with multiple sclerosis. Mult Scler J 20:192–201. https://doi.org/10.1177/1352458513493684CrossRef

44.

Leonard BE (2018) Inflammation and depression: a causal or coincidental link to the pathophysiology ? Acta Neuropsychiatr 30:1–16. https://doi.org/10.1017/neu.2016.69CrossRefPubMed

45.

Grech LB, Butler E, Stuckey S, Hester R (2019) Neuroprotective benefits of antidepressants in multiple sclerosis: are we missing the mark? J Neuropsychiatry Clin Neurosci. https://doi.org/10.1176/appi.neuropsych.18070164

Title: Imaging and depression in multiple sclerosis: a historical perspective
Authors: Fabio Giuseppe Masuccio
Giulia Gamberini
Massimiliano Calabrese
Claudio Solaro
Publication date: 01-03-2021
Publisher: Springer International Publishing
Keywords: Magnetic Resonance Imaging
Magnetic Resonance Imaging
Multiple Sclerosis
Affective Disorder
Affective Disorder
Published in: Neurological Sciences / Issue 3/2021
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-020-04951-z

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Springer Medicine

Imaging and depression in multiple sclerosis: a historical perspective

Abstract

Purpose

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

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