Restless legs syndrome in multiple sclerosis

Sleep Medicine Reviews

Volumn 22, Issue , 2015, Pages 15-22

  Sieminski, Mariusz ^a   Losy, Jacek ^b,c   Partinen, Markku ^d,e  

^a MEDICAL UNIVERSITY OF GDANSK   (Poland)

^b POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

^c MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

^d Vitalmed Research Centre   (Finland)

^e UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Demyelination; Iron metabolism; Multiple sclerosis; Restless legs syndrome

Indexed keywords

DOPAMINE; FERRITIN; INTERLEUKIN 6; NITRIC OXIDE SYNTHASE; SOLUBLE TRANSFERRINE RECEPTOR; TRANSFERRIN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

CHRONIC INFLAMMATION; CLINICAL FEATURE; COMORBIDITY; DEMYELINATION; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; ENZYME ACTIVATION; EXPANDED DISABILITY STATUS SCALE; FALSE POSITIVE RESULT; FAMILY HISTORY; FATIGUE; FERRITIN BLOOD LEVEL; FRACTIONAL ANISOTROPY; GENETIC ASSOCIATION; HIGH RISK POPULATION; HUMAN; IRON DEFICIENCY; IRON METABOLISM; MULTIPLE SCLEROSIS; NONHUMAN; PREMENOPAUSE; PREVALENCE; QUALITY OF LIFE; RESTLESS LEGS SYNDROME; REVIEW; SLEEP QUALITY; SLEEP TIME; COMPLICATION; INFLAMMATION; IRON DEFICIENCY ANEMIA;

ANEMIA, IRON-DEFICIENCY; HUMANS; INFLAMMATION; MULTIPLE SCLEROSIS; RESTLESS LEGS SYNDROME;

EID: 84937975074     PISSN: 10870792     EISSN: 15322955     Source Type: Journal    
DOI: 10.1016/j.smrv.2014.10.002     Document Type: Review

References (84)

1. Allen R.P., Picchietti D., Hening W.A., Trenkwalder C., Walters A.S., Montplaisi J. Restless legs syndrome: diagnostic criteria, special considerations, and epidemiology. A report from the restless legs syndrome diagnosis and epidemiology workshop at the National Institutes of Health. Sleep Med 2003, 4:101-119.
2. Hornyak M., Feige B., Riemann D., Voderholzer U. Periodic leg movements in sleep and periodic limb movement disorder: prevalence, clinical significance and treatment. Sleep Med Rev 2006, 10:169-177.
3. Partinen M. Epidemiology of sleep disorders. Handb Clin Neurol 2011, 98:275-314.
4. Ohayon M.M., O'Hara R., Vitiello M.V. Epidemiology of restless legs syndrome: a synthesis of the literature. Sleep Med Rev 2012, 16:283-295.
5. Manconi M., Ulfberg J., Berger K., Ghorayeb I., Wesström J., Fulda S., et al. When gender matters: restless legs syndrome. Report of the "RLS and woman" workshop endorsed by the European RLS Study Group. Sleep Med Rev 2012, 16:297-307.
6. Winkelmann J., Ferini-Strambi L. Genetics of restless legs syndrome. Sleep Med Rev 2006, 10:179-183.
7. Stefansson H., Rye D.B., Hicks A., Petursson H., Ingason A., Thorgeirsson T.E., et al. A genetic risk factor for periodic limb movements in sleep. N Engl J Med 2007, 357:639-647.
8. Winkelmann J., Schormair B., Lichtner P., Ripke S., Xiong L., Jalilzadeh S., et al. Genome-wide association study of restless legs syndrome identifies common variants in three genomic regions. Nat Genet 2007, 39:1000-1006.
9. Schormair B., Kemlink D., Roeske D., Eckstein G., Xiong L., Lichtner P., et al. PTPRD (protein tyrosine phosphatase receptor type delta) is associated with restless legs syndrome. Nat Genet 2008, 40:946-948.
10. Allen R.P., Earley C.J. The role of iron in restless legs syndrome. Mov Disord 2007, 22(Suppl. 18):S440-S448.
11. Clemens S., Rye D., Hochman S. Restless legs syndrome: revisiting the dopamine hypothesis from the spinal cord perspective. Neurology 2006, 67:125-130.
12. Qu S., Le W., Zhang X., Xie W., Zhang A., Ondo W.G. Locomotion is increased in a11-lesioned mice with iron deprivation: a possible animal model for restless legs syndrome. J Neuropathol Exp Neurol 2007, 66:383-388.
13. Rijsman R.M., Stam C.J., de Weerd A.W. Abnormal H-reflexes in periodic limb movement disorder; impact on understanding the pathophysiology of the disorder. Clin Neurophysiol 2005, 116:204-210.
14. Bara-Jimenez W., Aksu M., Graham B., Sato S., Hallett M. Periodic limb movements in sleep: state-dependent excitability of the spinal flexor reflex. Neurology 2000, 54:1609-1616.
15. Allen R.P., Auerbach S., Bahrain H., Auerbach M., Earley C.J. The prevalence and impact of restless legs syndrome on patients with iron deficiency anemia. Am J Hematol 2013, 88:261-264.
16. Manconi M., Govoni V., De Vito A., Economou N.T., Cesnik E., Casetta I., et al. Restless legs syndrome and pregnancy. Neurology 2004, 63:1065-1069.
17. Lee J., Nicholl D.D.M., Ahmed S.B., Loewen A.H.S., Hemmelgarn B.R., Beecroft J.M., et al. The prevalence of restless legs syndrome across the full spectrum of kidney disease. J Clin Sleep Med 2013, 9:455-459.
18. Rajabally Y.A., Shah R.S. Restless legs syndrome in chronic inflammatory demyelinating polyneuropathy. Muscle Nerve 2010, 42:252-256.
19. D' Onofrio F., Bussone G., Cologno D., Petretta V., Buzzi M.G., Tedeschi G., et al. Restless legs syndrome and primary headaches: a clinical study. Neurol Sci 2008, 29(Suppl. 1):S169-S172.
20. Sieminski M., Bilińska M., Nyka W.M. Increased frequency of restless legs syndrome in myasthenia gravis. Eur Neurol 2012, 68:166-170.
21. Taylor-Gjevre R.M., Gjevre J.A., Skomro R., Nair B. Restless legs syndrome in a rheumatoid arthritis patient cohort. J Clin Rheumatol 2009, 15:12-15.
22. Moccia M., Pellecchia M.T., Erro R., Zingone F., Marelli S., Barone D.G., et al. Restless legs syndrome is a common feature of adult celiac disease. Mov Disord 2010, 25:877-881.
23. Franco R.A., Ashwathnarayan R., Deshpandee A., Knox J., Daniel J., Eastwood D., et al. The high prevalence of restless legs syndrome symptoms in liver disease in an academic-based hepatology practice. J Clin Sleep Med 2008, 4:45-49.
24. Brass S.D., Duquette P., Proulx-Therrien J., Auerbach S. Sleep disorders in patients with multiple sclerosis. Sleep Med Rev 2010, 14:121-129.
25. Rae-Grant A.D., Eckert N.J., Bartz S., Reed J.F. Sensory symptoms of multiple sclerosis: a hidden reservoir of morbidity. Mult Scler 1999, 5:179-183.
26. Auger C., Montplaisir J., Duquette P. Increased frequency of restless legs syndrome in a French-Canadian population with multiple sclerosis. Neurology 2005, 65:1652-1653.
27. Manconi M., Fabbrini M., Bonanni E., Filippi M., Rocca M., Murri L., et al. High prevalence of restless legs syndrome in multiple sclerosis. Eur J Neurol 2007, 14:534-539.
28. Manconi M., Ferini-Strambi L., Filippi M., Bonanni E., Iudice A., Murri L., et al. Multicenter case-control study on restless legs syndrome in multiple sclerosis: the REMS study. Sleep 2008, 31:944-952. Italian REMS Study Group.
29. Moreira N.C.V., Damasceno R.S., Medeiros C.A.M., PFC de Bruin, Teixeira C.A.C., Horta W.G., et al. Restless leg syndrome, sleep quality and fatigue in multiple sclerosis patients. Braz J Med 2008, 41:932-937.
30. Deriu M., Cossu G., Molari A., Murgia D., Mereu A., Ferrigno P., et al. Restless legs syndrome in multiple sclerosis: a case-control study. Mov Disord 2009, 24:697-701.
31. Fragoso Y.D., Finkelsztejn A., Gomes S., Kaimen-Maciel D.R., Oliveira C.L.S., Lopes J., et al. Restless legs syndrome and multiple sclerosis: a Brazilian multicenter study and meta-analysis of the literature. Arq Neuropsiquiatr 2011, 69:180-183.
32. Aydar G., Kurt S., Karaer Unaldi H., Erkorkmaz U. Restless legs syndrome in multiple sclerosis. Eur Neurol 2011, 65:302-306.
33. Douay X., Waucquier N., Hautecoeur P., Vermersch P. G-SEP (Groupe Septentrional d'Etudes et de Recherche sur la Sclérose en Plaques). [High prevalence of restless legs syndrome in multiple sclerosis]. Rev Neurol (Paris) 2009, 165:194-196.
34. Miri S., Rohani M., Sahraian M.A., Zamani B., Shahidi G.A., Sabet A., et al. Restless legs syndrome in Iranian patients with multiple sclerosis. Neurol Sci 2013, 34:1105-1108.
35. Vávrová J., Kemlink D., Sonka K., Havrdová E., Horáková D., Pardini B., et al. Restless legs syndrome in Czech patients with multiple sclerosis: an epidemiological and genetic study. Sleep Med 2012, 13:848-851.
36. Li Y., Munger K.L., Batool-Anwar S., De Vito K., Ascherio A., Gao X. Association of multiple sclerosis with restless legs syndrome and other sleep disorders in women. Neurology 2012, 78:1500-1506.
37. Shaygannejad V., Ardestani P.E., Ghasemi M., Meamar R. Restless legs syndrome in Iranian multiple sclerosis patients: a case-control study. Int J Prev Med 2013, 4:S189-S193.
38. Gómez-Choco M.J., Iranzo A., Blanco Y., Graus F., Santamaria J., Saiz A. Prevalence of restless legs syndrome and REM sleep behavior disorder in multiple sclerosis. Mult Scler 2007, 13:805-808.
39. Manconi M., Rocca M.A., Ferini-Strambi L., Tortorella P., Agosta F., Comi G., et al. Restless legs syndrome is a common finding in multiple sclerosis and correlates with cervical cord damage. Mult Scler 2008, 14:86-93.
40. Becker P.M., Novak M. Diagnosis, comorbidities, and management of restless legs syndrome. Curr Med Res Opin 2014, 30:1441-1460.
41. Weinstock L.B., Walters A.S., Paueksakon P. Restless legs syndrome - theoretical roles of inflammatory and immune mechanisms. Sleep Med Rev 2012, 16:341-354.
42. Bruno E., Nicoletti A., Messina S., Lo Fermo S., Raciti L., Quattrocchi G., et al. Restless legs syndrome and multiple sclerosis: a population based case-control study in Catania, Sicily. Eur J Neurol 2014, 10.1111/ene.12409.
43. Paulus W., Schomburg E.D. Dopamine and the spinal cord in restless legs syndrome: does spinal cord physiology reveal a basis for augmentation?. Sleep Med Rev 2006, 10:185-196.
44. Yokota T., Hirose K., Tanabe H., Tsukagoshi H. Sleep-related periodic leg movements (nocturnal myoclonus) due to spinal cord lesion. J Neurol Sci 1991, 104:13-18.
45. Lee M.S., Choi Y.C., Lee S.H., Lee S.B. Sleep-related periodic leg movements associated with spinal cord lesions. Mov Disord 1996, 11:719-722.
46. Brown L.K., Heffner J.E., Obbens E.A. Transverse myelitis associated with restless legs syndrome and periodic movements of sleep responsive to an oral dopaminergic agent but not to intrathecal baclofen. Sleep 2000, 23:591-594.
47. Hartmann M., Pfister R., Pfadenhauer K. Restless legs syndrome associated with spinal cord lesions. J Neurol Neurosurg Psychiatry 1999, 66:688-689.
48. Telles S.C.L., Alves R.C., Chadi G. Periodic limb movements during sleep and restless legs syndrome in patients with ASIA A spinal cord injury. J Neurol Sci 2011, 303:119-123.
49. Humanes-Valera D., Aguilar J., Foffani G. Reorganization of the intact somatosensory cortex immediately after spinal cord injury. PloS One 2013, 8:e69655.
50. Wrigley P.J., Press S.R., Gustin S.M., Macefield V.G., Gandevia S.C., Cousins M.J., et al. Neuropathic pain and primary somatosensory cortex reorganization following spinal cord injury. Pain 2009, 141:52-59.
51. Birgegård G., Schneider K., Ulfberg J. High incidence of iron depletion and restless leg syndrome (RLS) in regular blood donors: intravenous iron sucrose substitution more effective than oral iron: Iron depletion and RLS in blood donors. Vox Sang 2010, 99:354-361.
52. Araujo S.M.H.A., Bruin VMS de, Nepomuceno L.A., Maximo M.L., Daher E.de F., Correia Ferrer D.P., et al. Restless legs syndrome in end-stage renal disease: clinical characteristics and associated comorbidities. Sleep Med 2010, 11:785-790.
53. Lin C.-H., Wu V.-C., Li W.-Y., Sy H.-N., Wu S.-L., Chang C.-C., et al. Restless legs syndrome in end-stage renal disease: a multicenter study in Taiwan. Eur J Neurol 2013, 20:1025-1031.
54. Neau J.-P., Porcheron A., Mathis S., Julian A., Meurice J.-C., Paquereau J., et al. Restless legs syndrome and pregnancy: a questionnaire study in the Poitiers District, France. Eur Neurol 2010, 64:268-274.
55. Chen P.-H., Liou K.-C., Chen C.-P., Cheng S.-J. Risk factors and prevalence rate of restless legs syndrome among pregnant women in Taiwan. Sleep Med 2012, 13:1153-1157.
56. O'Keeffe S.T., Gavin K., Lavan J.N. Iron status and restless legs syndrome in the elderly. Age Ageing 1994, 23:200-203.
57. Mizuno S., Mihara T., Miyaoka T., Inagaki T., Horiguchi J. CSF iron, ferritin and transferrin levels in restless legs syndrome. J Sleep Res 2005, 14:43-47.
58. Earley C., Connor J.R., Beard J.L., Clardy S.L., Allen R.P. Ferritin levels in the cerebrospinal fluid and restless legs syndrome: effects of different clinical phenotypes. Sleep 2005, 28:1069-1075.
59. Clardy S.L., Earley C.J., Allen R.P., Beard J.L., Connor J.R. Ferritin subunits in CSF are decreased in restless legs syndrome. J Lab Clin Med 2006, 147:67-73.
60. Earley C.J., Connor J.R., Beard J.L., Malecki E.A., Epstein D.K., Allen R.P. Abnormalities in CSF concentrations of ferritin and transferrin in restless legs syndrome. Neurology 2000, 54:1698-1700.
61. Earley C.J., Barker P B., Horská A., Allen R.P. MRI-determined regional brain iron concentrations in early- and late-onset restless legs syndrome. Sleep Med 2006, 7:458-461.
62. Schmidauer C., Sojer M., Seppi K., Stockner H., Högl B., Biedermann B., et al. Transcranial ultrasound shows nigral hypoechogenicity in restless legs syndrome. Ann Neurol 2005, 58:630-634.
63. Connor J.R., Boyer P.J., Menzies S.L., Dellinger B., Allen R.P., Ondo W.G., et al. Neuropathological examination suggests impaired brain iron acquisition in restless legs syndrome. Neurology 2003, 61:304-309.
64. Connor J.R., Ponnuru P., Wang X.-S., Patton S.M., Allen R.P., Earley C.J. Profile of altered brain iron acquisition in restless legs syndrome. Brain 2011, 134:959-968.
65. Jellen L.C., Lu L., Wang X., Unger E.L., Earley C.J., Allen R.P., et al. Iron deficiency alters expression of dopamine-related genes in the ventral midbrain in mice. Neuroscience 2013, 252:13-23.
66. Rodrigo L., Hernández-Lahoz C., Fuentes D., Alvarez N., López-Vázquez A., González S. Prevalence of celiac disease in multiple sclerosis. BMC Neurol 2011, 11:31.
67. Kang J.-H., Chen Y.-H., Lin H.-C. Comorbidities amongst patients with multiple sclerosis: a population-based controlled study. Eur J Neurol 2010, 17:1215-1219.
68. Sfagos C., Makis A.C., Chaidos A., Hatzimichael E.C., Dalamaga A., Kosma K., et al. Serum ferritin, transferrin and soluble transferrin receptor levels in multiple sclerosis patients. Mult Scler 2005, 11:272-275.
69. Hogl B., Kiechl S., Willeit J., Saletu M., Frauscher B., Seppi K., et al. Restless legs syndrome: a community-based study of prevalence, severity, and risk factors. Neurology 2005, 64:1920-1924.
70. Ortiz E., Pasquini J.M., Thompson K., Felt B., Butkus G., Beard J., et al. Effect of manipulation of iron storage, transport, or availability on myelin composition and brain iron content in three different animal models. J Neurosci Res 2004, 77:681-689.
71. Algarín C., Peirano P., Garrido M., Pizarro F., Lozoff B. Iron deficiency anemia in infancy: long-lasting effects on auditory and visual system functioning. Pediatr Res 2003, 53:217-223.
72. Haacke E.M., Makki M., Ge Y., Maheshwari M., Sehgal V., Hu J., et al. Characterizing iron deposition in multiple sclerosis lesions using susceptibility weighted imaging. J Magn Reson Imaging 2009, 29:537-544.
73. Haacke E.M., Garbern J., Miao Y., Habib C., Liu M. Iron stores and cerebral veins in MS studied by susceptibility weighted imaging. Int Angiol 2010, 29:149-157.
74. Khalil M., Enzinger C., Langkammer C., Tscherner M., Wallner-Blazek M., Jehna M., et al. Quantitative assessment of brain iron by R(2)* relaxometry in patients with clinically isolated syndrome and relapsing-remitting multiple sclerosis. Mult Scler 2009, 15:1048-1054.
75. Bakshi R., Shaikh Z.A., Janardhan V. MRI T2 shortening ('black T2') in multiple sclerosis: frequency, location, and clinical correlation. Neuroreport 2000, 11:15-21.
76. Zhang Y., Zabad R.K., Wei X., Metz L.M., Hill M.D., Mitchell J.R. Deep grey matter "black T2" on 3 tesla magnetic resonance imaging correlates with disability in multiple sclerosis. Mult Scler 2007, 13:880-883.
77. Neema M., Arora A., Healy B.C., Guss Z.D., Brass S.D., Duan Y., et al. Deep gray matter involvement on brain MRI scans is associated with clinical progression in multiple sclerosis. J Neuroimaging 2009, 19:3-8.
78. Ge Y., Jensen J.H., Lu H., Helpern J.A., Miles L., Inglese M., et al. Quantitative assessment of iron accumulation in the deep gray matter of multiple sclerosis by magnetic field correlation imaging. AJNR Am J Neuroradiol 2007, 28:1639-1644.
79. Hametner S., Wimmer I., Haider L., Pfeifenbring S., Brück W., Lassmann H. Iron and neurodegeneration in the multiple sclerosis brain. Ann Neurol 2013, 74:848-861.
80. Rathore K.I., Redensek A., David S. Iron homeostasis in astrocytes and microglia is differentially regulated by TNF-α and TGF-β1. Glia 2012, 60:738-750.
81. Connor J.R., Ponnuru P., Lee B.-Y., Podskalny G.D., Alam S., Allen R.P., et al. Postmortem and imaging based analyses reveal CNS decreased myelination in restless legs syndrome. Sleep Med 2011, 12:614-619.
82. Patton S.M., Ponnuru P., Snyder A.M., Podskalny G.D., Connor J.R. Hypoxia-inducible factor pathway activation in restless legs syndrome patients. Eur J Neurol 2011, 18:1329-1335.
83. Winkelmann J., Lichtner P., Schormair B., Uhr M., Hauk S., Stiasny-Kolster K., et al. Variants in the neuronal nitric oxide synthase (nNOS, NOS1) gene are associated with restless legs syndrome. Mov Disord 2008, 23:350-358.
84. Jana M., Pahan K. Down-regulation of myelin gene expression in human oligodendrocytes by nitric Oxide: implications for demyelination in multiple sclerosis. J Clin Cell Immunol 2013, 4.