Gastroenterology
Volume 128, Issue 4, Supplement 1 , Pages S92-S97 , April 2005

Neurologic presentation of celiac disease

  • Khalafalla O. Bushara

      Affiliations

    • Corresponding Author InformationAddress requests for reprints to: Khalafalla O. Bushara, MD, 127 Minneapolis VA Medical Center, 1 Veterans Drive, Minneapolis, Minnesota 55417

References 

  1. Luostarinen L , Pirttila T , Collin P . Coeliac disease presenting with neurological disorders . Eur Neurol . 1999;42:132–135
  2. Zelnik N , Pacht A , Obeid R , Lerner A . Range of neurologic disorders in patients with celiac disease . Pediatrics . 2004;113:1672–1676
  3. Cooke W , Smith W . Neurological disorders associated with adult coeliac disease . Brain . 1966;89:683–722
  4. Missen GA . Intestinal malignant lymphoma and cerebellar cortical degeneration complicating idiopathic steatorrhoea (report of a case with a review of the literature) . Guys Hosp Rep . 1966;115:359–385
  5. Finelli PF , McEntee WJ , Ambler M , Kestenbaum D . Adult celiac disease presenting as cerebellar syndrome . Neurology . 1980;30:245–249
  6. Lu CS , Thompson PD , Quinn NP , Parkes JD , Marsden CD . Ramsay Hunt syndrome and coeliac disease (a new association?) . Mov Disord . 1986;1:209–219
  7. Kristoferitsch W , Pointner H . Progressive cerebellar syndrome in adult coeliac disease . J Neurol . 1987;234:116–118
  8. Hermaszewski RA , Rigby S , Dalgleish AG . Coeliac disease presenting with cerebellar degeneration . Postgrad Med J . 1991;67:1023–1024
  9. Harding AE , Muller DP , Thomas PK , Willison HJ . Spinocerebellar degeneration secondary to chronic intestinal malabsorption (a vitamin E deficiency syndrome) . Ann Neurol . 1982;12:419–424
  10. Mauro A , Orsi L , Mortara P , Costa P , Schiffer D . Cerebellar syndrome in adult celiac disease with vitamin E deficiency . Acta Neurol Scand . 1991;84:167–170
  11. Battisti C, Dotti MT, Formichi P, Bonuccelli U, Malandrini A, Carrai M, et al. Disappearance of skin lipofuscin storage and marked clinical improvement in adult onset coeliac disease and severe vitamin E deficiency after chronic vitamin E megatherapy . J Submicrosc Cytol Pathol . 1996;28:339–344
  12. Ward ME , Murphy JT , Greenberg GR . Celiac disease and spinocerebellar degeneration with normal vitamin E status . Neurology . 1985;35:1199–1201
  13. Muller AF , Donnelly MT , Smith CM , Grundman MJ , Holmes GK , Toghill PJ . Neurological complications of celiac disease (a rare but continuing problem) . Am J Gastroenterol . 1996;91:1430–1435
  14. Hadjivassiliou M , Gibson A , Davies-Jones GA , Lobo AJ , Stephenson TJ , Milford-Ward A . Does cryptic gluten sensitivity play a part in neurological illness? . Lancet . 1996;347:369–371
  15. Pellecchia MT , Scala R , Filla A , De Michele G , Ciacci C , Barone P . Idiopathic cerebellar ataxia associated with celiac disease (lack of distinctive neurological features) . J Neurol Neurosurg Psychiatry . 1999;66:32–35
  16. Burk K, Bosch S, Muller CA, Melms A, Zuhlke C, Stern M, et al. Sporadic cerebellar ataxia associated with gluten sensitivity . Brain . 2001;124:1013–1019
  17. Marsh MN . The natural history of gluten sensitivity (defining, refining and re-defining) . QJM . 1995;88:9–13
  18. Wills AJ , Unsworth DJ . The neurology of gluten sensitivity (separating the wheat from the chaff) . Curr Opin Neurol . 2002;15:519–523
  19. Volta U, Molinaro N, De Franchis R, Forzenigo L, Landoni M, Fratangelo D, et al. Correlation between IgA antiendomysial antibodies and subtotal villous atrophy in dermatitis herpetiformis . J Clin Gastroenterol . 1992;14:298–301
  20. Combarros O, Infante J, Lopez-Hoyos M, Bartolome MJ, Berciano J, Corral J, et al. Celiac disease and idiopathic cerebellar ataxia . Neurology . 2000;54:2346
  21. Bushara KO , Goebel SU , Shill H , Goldfarb LG , Hallett M . Gluten sensitivity in sporadic and hereditary cerebellar ataxia . Ann Neurol . 2001;49:540–543
  22. Hadjivassiliou M , Grunewald RA , Davies-Jones GA . Causes of cerebellar degeneration (gluten ataxia in perspective) . J Neurol Sci . 2001;187:S520
  23. Abele M , Schols L , Schwartz S , Klockgether T . Prevalence of antigliadin antibodies in ataxia patients . Neurology . 2003;60:1674–1675
  24. Bushara KO , Nance M , Gomez CM . Antigliadin antibodies in Huntington’s disease . Neurology . 2004;62:132–133
  25. Dick DJ , Abraham D , Falkous G , Hishon S . Cerebellar ataxia in coeliac disease—no evidence of a humoral aetiology . Postgrad Med J . 1995;71:186
  26. Hadjivassiliou M, Boscolo S, Davies-Jones GA, Grunewald RA, Not T, Sanders DS, et al. The humoral response in the pathogenesis of gluten ataxia . Neurology . 2002;58:1221–1226
  27. Chinnery PF , Reading PJ , Milne D , Gardner-Medwin D , Turnbull DM . CSF antigliadin antibodies and the Ramsay Hunt syndrome . Neurology . 1997;49:1131–1133
  28. Pellecchia MT, Scala R, Perretti A, De Michele G, Santoro L, Filla A, et al. Cerebellar ataxia associated with subclinical celiac disease responding to gluten-free diet . Neurology . 1999;53:1606–1608
  29. Bushara KO , Shill H , Hallett M . Open-label trial of gluten-free diet in sporadic and hereditary cerebellar ataxia with gluten sensitivity . (abstr) Mov Disord . 2002;17:S325
  30. Hadjivassiliou M , Davies-Jones GA , Sanders DS , Grunewald RA . Dietary treatment of gluten ataxia . J Neurol Neurosurg Psychiatry . 2003;74:1221–1224
  31. Burk K , Melms A , Schulz JB , Dichgans J . Effectiveness of intravenous immunoglobin therapy in cerebellar ataxia associated with gluten sensitivity . Ann Neurol . 2001;50:827–828
  32. Sander HW, Magda P, Chin RL, Wu A, Brannagan TH, Green PH, et al. Cerebellar ataxia and coeliac disease . Lancet . 2003;362:1548
  33. Cicarelli G, Della Rocca G, Amboni M, Ciacci C, Mazzacca G, Filla A, et al. Clinical and neurological abnormalities in adult celiac disease . Neurol Sci . 2003;24:311–317
  34. Chin RL, Sander HW, Brannagan TH, Green PH, Hays AP, Alaedini A, et al. Celiac neuropathy . Neurology . 2003;60:1581–1585
  35. Banerji NK , Hurwitz LJ . Neurological manifestations in adult steatorrhoea (probable Gluten enteropathy) . J Neurol Sci . 1971;14:125–141
  36. Kaplan JG , Pack D , Horoupian D , DeSouza T , Brin M , Schaumburg H . Distal axonopathy associated with chronic gluten enteropathy (a treatable disorder) . Neurology . 1988;38:642–645
  37. Hadjivassiliou M , Chattopadhyay AK , Davies-Jones GA , Gibson A , Grunewald RA , Lobo AJ . Neuromuscular disorder as a presenting feature of coeliac disease . J Neurol Neurosurg Psychiatry . 1997;63:770–775
  38. Usai P, Usai Satta P, Lai M, Corda MG, Piras E, Calcara C, et al. Autonomic dysfunction and upper digestive functional disorders in untreated adult coeliac disease . Eur J Clin Invest . 1997;27:1009–1015
  39. Alaedini A , Wirguin I , Latov N . Ganglioside agglutination immunoassay for rapid detection of autoantibodies in immune-mediated neuropathy . J Clin Lab Anal . 2001;15:96–99
  40. Alaedini A, Green PH, Sander HW, Hays AP, Gamboa ET, Fasano A, et al. Ganglioside reactive antibodies in the neuropathy associated with celiac disease . J Neuroimmunol . 2002;127:145–148
  41. Henriksson KG , Hallert C , Norrby K , Walan A . Polymyositis and adult coeliac disease . Acta Neurol Scand . 1982;65:301–319
  42. Marie I, Lecomte F, Hachulla E, Antonietti M, Francois A, Levesque H, et al. An uncommon association (celiac disease and dermatomyositis in adults) . Clin Exp Rheumatol . 2001;19:201–203
  43. Polizzi A , Finocchiaro M , Parano E , Pavone P , Musumeci S . Recurrent peripheral neuropathy in a girl with celiac disease . J Neurol Neurosurg Psychiatry . 2000;68:104–105
  44. Tietge UJ , Schmidt HH , Manns MP . Neurological complications in celiac disease . Am J Gastroenterol . 1997;92:540
  45. Simonati A , Battistella PA , Guariso G , Clementi M , Rizzuto N . Coeliac disease associated with peripheral neuropathy in a child (a case report) . Neuropediatrics . 1998;29:155–158
  46. Luostarinen L , Himanen SL , Luostarinen M , Collin P , Pirttila T . Neuromuscular and sensory disturbances in patients with well treated coeliac disease . J Neurol Neurosurg Psychiatry . 2003;74:490–494
  47. Chapman RW , Laidlow JM , Colin-Jones D , Eade OE , Smith CL . Increased prevalence of epilepsy in coeliac disease . BMJ . 1978;2:250–251
  48. Holmes GK . Non-malignant complications of coeliac disease . Acta Paediatr Suppl . 1996;412:68–75
  49. Fois A , Vascotto M , Di Bartolo RM , Di Marco V . Celiac disease and epilepsy in pediatric patients . Childs Nerv Syst . 1994;10:450–454
  50. Cronin CC, Jackson LM, Feighery C, Shanahan F, Abuzakouk M, Ryder DQ, et al. Coeliac disease and epilepsy . QJM . 1998;91:303–308
  51. Luostarinen L, Dastidar P, Collin P, Peraaho M, Maki M, Erila T, et al. Association between coeliac disease, epilepsy and brain atrophy . Eur Neurol . 2001;46:187–191
  52. Pratesi R , Gandolfi L , Martins RC , Tauil PL , Nobrega YK , Teixeira WA . Is the prevalence of celiac disease increased among epileptic patients? . Arq Neuropsiquiatr . 2003;61:330–334
  53. Visakorpi J , Kuitunen P , Pelkonen P . Intestinal malabsorption (a clinical study of 22 children over 2 years of age) . Acta Paediatr Scand . 1970;59:273–280
  54. Garwicz S , Mortensson W . Intracranial calcification mimicking the Sturge-Weber syndrome (a consequence of cerebral folic acid deficiency?) . Pediatr Radiol . 1976;5:5–9
  55. Molteni N , Bardella MT , Baldassarri AR , Bianchi PA . Celiac disease associated with epilepsy and intracranial calcifications (report of two patients) . Am J Gastroenterol . 1988;83:992–994
  56. Ventura A , Bouquet F , Sartorelli C , Barbi E , Torre G , Tommasini G . Coeliac disease, folic acid deficiency and epilepsy with cerebral calcifications . Acta Paediatr Scand . 1991;80:559–562
  57. Gobbi G , Ambrosetto P , Zaniboni MG , Lambertini A , Ambrosioni G , Tassinari CA . Celiac disease, posterior cerebral calcifications and epilepsy . Brain Dev . 1992;14:23–29
  58. Gobbi G, Bouquet F, Greco L, Lambertini A, Tassinari CA, Ventura A, et al. Coeliac disease, epilepsy, and cerebral calcifications . Lancet . 1992;340:439–443
  59. Magaudda A, Dalla Bernardina B, De Marco P, Sfaello Z, Longo M, Colamaria V, et al  Bilateral occipital calcification, epilepsy and coeliac disease (clinical and neuroimaging features of a new syndrome) . J Neurol Neurosurg Psychiatry . 1993;56:885–889
  60. Crosato F , Senter S . Cerebral occipital calcifications in celiac disease . Neuropediatrics . 1992;23:214–217
  61. Arroyo HA , De Rosa S , Ruggieri V , de Davila MT , Fejerman N . Epilepsy, occipital calcifications, and oligosymptomatic celiac disease in childhood . J Child Neurol . 2002;17:800–806
  62. Bye AM , Andermann F , Robitaille Y , Oliver M , Bohane T , Andermann E . Cortical vascular abnormalities in the syndrome of celiac disease, epilepsy, bilateral occipital calcifications, and folate deficiency . Ann Neurol . 1993;34:399–403
  63. Toti P, Balestri P, Cano M, Galluzzi P, Megha T, Farnetani MA, et al. Celiac disease with cerebral calcium and silica deposits (x-ray spectroscopic findings, an autopsy study) . Neurology . 1996;46:1088–1092
  64. Cernibori A , Gobbi G . Partial seizures, cerebral calcifications and celiac disease . Ital J Neurol Sci . 1995;16:187–191
  65. Pratesi R , Modelli IC , Martins RC , Almeida PL , Gandolfi L . Celiac disease and epilepsy (favorable outcome in a child with difficult to control seizures) . Acta Neurol Scand . 2003;108:290–293
  66. Bernasconi A, Bernasconi N, Andermann F, Dubeau F, Guberman A, Gobbi G, et al. Celiac disease, bilateral occipital calcifications and intractable epilepsy (mechanisms of seizure origin) . Epilepsia . 1998;39:300–306
  67. Roche Herrero MC, Arcas Martinez J, Martinez-Bermejo A, Lopez Martin V, Polanco I, Tendero Gormaz A, et al. [The prevalence of headache in a population of patients with coeliac disease] . Rev Neurol . 2001;32:301–309
  68. Gabrielli M, Cremonini F, Fiore G, Addolorato G, Padalino C, Candelli M, et al. Association between migraine and Celiac disease (results from a preliminary case-control and therapeutic study) . Am J Gastroenterol . 2003;98:625–629
  69. Serratrice J , Disdier P , de Roux C , Christides C , Weiller PJ . Migraine and coeliac disease . Headache . 1998;38:627–628
  70. Spina M , Incorpora G , Trigilia T , Branciforte F , Franco G , Di Gregorio F . Headache as atypical presentation of celiac disease (report of a clinical case) . Pediatr Med Chir . 2001;23:133–135
  71. Hadjivassiliou M , Grunewald RA , Lawden M , Davies-Jones GA , Powell T , Smith CM . Headache and CNS white matter abnormalities associated with gluten sensitivity . Neurology . 2001;56:385–388
  72. Battistella PA, Mattesi P, Casara GL, Carollo C, Condini A, Allegri F, et al. Bilateral cerebral occipital calcifications and migraine-like headache . Cephalalgia . 1987;7:125–129
  73. Morris JS , Ajdukiewicz AB , Read AE . Pyridoxine deficiency in celiac disease and the detection of neuropsychiatric disorders . Gut . 1969;10:1057
  74. Goldberg D . A psychiatric study of patients with diseases of the small intestine . Gut . 1970;11:459–465
  75. Hallert C , Astrom J . Psychic disturbances in adult coeliac disease. II. Psychological findings . Scand J Gastroenterol . 1982;17:21–24
  76. Hallert C , Astrom J , Walan A . Reversal of psychopathology in adult coeliac disease with the aid of pyridoxine (vitamin B6) . Scand J Gastroenterol . 1983;18:299–304
  77. Ciacci C , Iavarone A , Mazzacca G , De Rosa A . Depressive symptoms in adult coeliac disease . Scand J Gastroenterol . 1998;33:247–250
  78. Carta MG , Hardoy MC , Boi MF , Mariotti S , Carpiniello B , Usai P . Association between panic disorder, major depressive disorder and celiac disease (a possible role of thyroid autoimmunity) . J Psychosom Res . 2002;53:789–793
  79. Hernanz A , Polanco I . Plasma precursor amino acids of central nervous system monoamines in children with coeliac disease . Gut . 1991;32:1478–1481
  80. Hallert C , Astrom J , Sedvall G . Psychic disturbances in adult coeliac disease. III. Reduced central monoamine metabolism and signs of depression . Scand J Gastroenterol . 1982;17:25–28
  81. Corvaglia L , Catamo R , Pepe G , Lazzari R , Corvaglia E . Depression in adult untreated celiac subjects (diagnosis by the pediatrician) . Am J Gastroenterol . 1999;94:839–843
  82. Pynnonen PA , Isometsa ET , Verkasalo MA , Savilahti E , Aalberg VA . Untreated celiac disease and development of mental disorders in children and adolescents . Psychosomatics . 2002;43:331–334
  83. Addolorato G, Capristo E, Ghittoni G, Valeri C, Masciana R, Ancona C, et al. Anxiety but not depression decreases in coeliac patients after one-year gluten-free diet (a longitudinal study) . Scand J Gastroenterol . 2001;36:502–506
  84. Gillberg C , Wing L . Autism (not an extremely rare disorder) . Acta Psychiatr Scand . 1999;99:399–406
  85. Bailey A, Le Couteur A, Gottesman I, Bolton P, Simonoff E, Yuzda E, et al. Autism as a strongly genetic disorder (evidence from a British twin study) . Psychol Med . 1995;25:63–77
  86. Muhle R , Trentacoste SV , Rapin I . The genetics of autism . Pediatrics . 2004;113:e472–e486
  87. Dohan FC . Is celiac disease a clue to the pathogenesis of schizophrenia? . Ment Hyg . 1969;53:525–529
  88. Panksepp J . A neurochemical theory of autism . Trends Neurosci . 1979;2:174–177
  89. Shattock P , Kennedy A , Rowell F , Berney TP . Role of neuropeptides in autism and their relationships with classical neurotransmitters . Brain Dysfunction . 1991;3:328–345
  90. Reichelt KL, Hole K, Hamberger A, Saelid G, Edminson PD, Braestrup CB, et al. Biologically active peptide-containing fractions in schizophrenia and childhood autism . Adv Biochem Psychopharmacol . 1981;28:627–643
  91. Israngkun PP , Newman HA , Patel ST , Duruibe VA , Abou-Issa H . Potential biochemical markers for infantile autism . Neurochem Pathol . 1986;5:51–70
  92. Hunter LC , O’Hare A , Herron WJ , Fisher LA , Jones GE . Opioid peptides and dipeptidyl peptidase in autism . Dev Med Child Neurol . 2003;45:121–128
  93. Shattock P , Hooper M , Waring R . Opioid peptides and dipeptidyl peptidase in autism . Dev Med Child Neurol . 2004;46:357–358
  94. D’Eufemia P, Celli M, Finocchiaro R, Pacifico L, Viozzi L, Zaccagnini M, et al. Abnormal intestinal permeability in children with autism . Acta Paediatr . 1996;85:1076–1079
  95. Horvath K , Papadimitriou JC , Rabsztyn A , Drachenberg C , Tildon JT . Gastrointestinal abnormalities in children with autistic disorder . J Pediatr . 1999;135:559–563
  96. Horvath K , Stefanatos G , Sokolski KN , Wachtel R , Nabors L , Tildon JT . Improved social and language skills after secretin administration in patients with autistic spectrum disorders . J Assoc Acad Minor Phys . 1998;9:9–15
  97. Sandler AD , Sutton KA , DeWeese J , Girardi MA , Sheppard V , Bodfish JW . Lack of benefit of a single dose of synthetic human secretin in the treatment of autism and pervasive developmental disorder . N Engl J Med . 1999;341:1801–1806
  98. Wakefield AJ, Murch SH, Anthony A, Linnell J, Casson DM, Malik M, et al. Ileal-lymphoid-nodular hyperplasia, non-specific colitis, and pervasive developmental disorder in children . Lancet . 1998;351:637–641
  99. Ashwood P , Anthony A , Pellicer AA , Torrente F , Walker-Smith JA , Wakefield AJ . Intestinal lymphocyte populations in children with regressive autism (evidence for extensive mucosal immunopathology) . J Clin Immunol . 2003;23:504–517
  100. Reichelt WH , Ek J , Stensrud M , Reichelt KL . Peptide excretion in celiac disease . J Pediatr Gastroenterol Nutr . 1998;26:305–309
  101. Pavone L , Fiumara A , Bottaro G , Mazzone D , Coleman M . Autism and celiac disease (failure to validate the hypothesis that a link might exist) . Biol Psychiatry . 1997;42:72–75
  102. Millward C , Ferriter M , Calver S , Connell-Jones G . Gluten- and casein-free diets for autistic spectrum disorder . Cochrane Database Syst Rev . 2004; CD003498
  103. McCarthy DM , Coleman M . Response of intestinal mucosa to gluten challenge in autistic subjects . Lancet . 1979;2:877–878
  104. Lucarelli S, Frediani T, Zingoni AM, Ferruzzi F, Giardini O, Quintieri F, et al. Food allergy and infantile autism . Panminerva Med . 1995;37:137–141
  105. Knivsber AM , Reichelt KL , Nodland M . Reports on dietary intervention in autistic disorders . Nutr Neurosci . 2001;4:25–37
  106. Knivsberg AM , Reichelt KL , Hoien T , Nodland M . A randomised, controlled study of dietary intervention in autistic syndromes . Nutr Neurosci . 2002;5:251–261
  107. Sponheim E . [Gluten-free diet in infantile autism. A therapeutic trial] . Tidsskr Nor Laegeforen . 1991;111:704–707

 Supported by the Bob Allison Ataxia Research Foundation.

PII: S0016-5085(05)00187-3

doi: 10.1053/j.gastro.2005.02.018

Gastroenterology
Volume 128, Issue 4, Supplement 1 , Pages S92-S97 , April 2005