Neurological complications of gastrointestinal disorders. A review of the literature.

Abstract

This article presents a short review of the literature concerning neurological complications of gastrointestinal disorders. These disorders include the following: inflammatory bowel diseases (ulcerative colitis, Crohn's disease), celiac disease, H. Pylori infection, hepatitis C, Wilson's disease, hepatic failure-liver transplantation, gastroenteritis. The most frequent neurological complications are peripheral neuropathy, cerebellar dysfunction, thromboembolism. The exact pathophysiologic mechanism remains unclear. In most cases neurological manifestations are the first clinical manifestation of the disease.

Keywords

• neurological; complications; gastrointestinal

References

1. Watts DA, Satsangi J. The genetic jigsaw of inflammatory bowel disease. Gut 2002;50:31–6.
2. Elsehety A, Bertorini TE. Neurologic and neuropsychiatric complications of Crohn's disease. South Med J 1997;90: 606–10.
3. Greenstein AJ, Janowitz HD, Sachar DB. The extra-intestinal complications of Crohn's disease and ulcerative colitis: a study of 700 patients. Medicine 1976;55:401–12.
4. Rankin GB, Watts HD, Melnyk CS, Kelley ML Jr. National Cooperative Crohn's Disease Study: extraintestinal manifestations and perianal complications. Gastroenterology 1979;77:914–20.
5. Lossos A, River Y, Eliakim A, Steiner I. Neurologic aspects in inflammatory bowel disease. Neurology 1995;45:416–
6. Maisawa S, Sasaki M, Ida S, Uchida K, Kagimoto S, Shimizu T, et al. Characteristics of inflammatory bowel disease with an onset before eight years of age: a multicenter epidemiological survey in Japan.J Gastroenterol Hepatol 2013;28:499-504.
7. Zois CD, Katsanos KH, Kosmidou M, Tsianos EV. Neurologic manifestations in inflammatory bowel diseases: current knowledge and novel insights. J Crohns Colitis 2010;4:115-24.
8. Green JR, O'Donoghue DP, Edwards CR, Dawson AM. A case of apparent hypopituitarism complicating chronic inflammatory bowel disease in childhood and adolescence. Acta Paediatr Scand 1977;66:643-7.

9. Greco F, Pavone P, Falsaperla R, Sorge G. Peripheral neuropathy as first sign of ulcerative colitis in a child. J Clin Gastroenterol 2004;38:115-7.
10. Ståhlberg D, Bárány F, Einarsson K, Ursing B, Elmqvist D, Persson A. Neurophysiologic studies of patients with Crohn's disease on long-term treatment with metronidazole. Scand J Gastroenterol 1991;26:219–24.
11. Gondim FA, Brannagan TH 3rd, Sander HW, Chin RL, Latov N. Peripheral neuropathy in patients with inflammatory bowel disease. Brain 2005;128:867–79.
12. Yeşilova Z, Naharci I, Uygun A, Ulaş HU, Dağalp K. Motor axonal polyneuropathy in the course of ulcerative colitis: a case report. Turk J Gastroenterol 2006;17:58–61.
13. Berden JH, Hoitsma AJ, Merx JL, Keyser A. Severe central nervous system toxicity associated with cyclosporine. Lancet 1985;1: 219–20.
14. Porges Y, Blumen S, Fireman Z, Sternberg A, Zamir D. Cyclosporineinduced optic neuropathy, ophthalmoplegia and nystagmus in a patient with Crohn's disease. Am J Ophthalmol 1998;126:607–9.
15. Watkinson G. Sulfasalazine: a review of 40 years' experience. Drugs 1986;32:1–
16. Scheid R, Teich N. Neurologic manifestations of ulcerative colitis. Eur J Neurol 2007;14:483–93.
17. Nguyen LT, Laberge JM, Guttman FM, Albert D. Spontaneous deep vein thrombosis in childhood and adolescence. J Pediatr Surg 1986;21:640-3.
18. Goodwin FC, Beattie RM, Millar J, Kirkham FJ. Celiac disease and childhood stroke. Pediatr Neurol 2004;31:139-42.
19. Purrmann J, Arendt G, Cleveland S, Borchard F, Fürst W, Gemsa R, et al. Association of Crohn's disease and multiple sclerosis. Is there a common background? J Clin Gastroenterol 1992;14:43–6.
20. Buccino GP, Corrente G, Visintini D. Crohn's disease and multiple sclerosis:a single case report. Ital J Neurol Sci 1994;15:303–6.
21. Kitchin LI, Knobler RL, Friedman LS. Crohn's disease in a patient with multiple sclerosis. J Clin Gastroenterol 1991;13: 331–
22. Ghezzi A, Zaffaroni M. Neurological manifestations of gastrointestinal disorders, with particular reference to the differential diagnosis of multiple sclerosis. Neurol Sci 2001;22 Suppl 2:117-22.
23. Beaugerie L, Lamy P, Ganne N, Carbonnel F, Le Quintrec Y, Cosnes J, et al. Morbid associations in Crohn's disease. Study of a series of 832 patients. Presse Med 1997;26:892–4.
24. Martin RW, Shah A. Myasthenia Gravis coexistent with Crohn's disease. J Clin Gastroenterol 1991;13:112–3.
25. Gelfenbeyn M, Goodkin R, Kliot M. Sterile recurrent spinal epidural abscess in a patient with Crohn's disease: a case report. Surg Neurol 2006;65:178–84.
26. Marks J, Shuster S, Watson AJ. Small bowel changes in dermatitis herpetiformis. Lancet 1966; 1280–2.
27. Cooke WT, Smith WT. Neurological disorders associated with adult coeliac disease. Brain 1966;89:683–722.
28. Finelli PF, McEntee WJ, Ambler M, Kestenbaum D. Adult celiac disease presenting as cerebellar syndrome. Neurology 1980;30:245–9. Hadjivassiliou M, Sanders DS, Grünewald RA, Woodroofe N, Boscolo S, Aeschlimann D. The neurology of gluten sensitivity. Lancet Neurol 2010; 9: 330–42.
29. Gobbi G, Bouquet F, Greco L, Lambertini A, Tassinari CA, Ventura A, et al. Coeliac disease, epilepsy and cerebral calcifi cations. Lancet 1992; 340: 439–43.
30. Ghezzi A, Filippi M, Falini A, Zaffaroni M. Cerebral involvement in celiac disease: a serial MRI study in a patient with brainstem and cerebellar symptoms. Neurology 1997;49:1447–50.
31. Ward ME, Murphy JT, Greenberg GR. Celiac disease and spinocerebellar degeneration with normal vitamin E status. Neurology 1985;35:1199–1201.
32. Beversdorf D, Moses P, Reeves A, Dunn J. A man with weight loss, ataxia, and confusion for 3 months. Lancet 1996;347:446. Hadjivassiliou M, Aeschlimann P, Strigun A, Sanders DS, Woodroofe N, Aeschlimann D. Autoantibodies in gluten ataxia recognise a novel neuronal transglutaminase. Ann Neurol 2008; 64: 332–43. Hadjivassiliou M, Aeschlimann P, Sanders DS, et al. Antibodies against TG6 as the only serological marker of gluten ataxia. Proceedings of the 13th nternational Coeliac Disease Symposium. Amsterdam; April 6–8, 200 09.1.
33. Wilkinson ID, Hadjivassiliou M, Dickson JM, Wallis L, Grünewald RA, Coley SC, et al. Cerebellar abnormalities on proton MR spectroscopy in gluten ataxia. J Neurol Neurosurg Psychiatry 2005; 76: 1011–13.
34. Luostarinen L, Himanen SL, Luostarinen M, Collin P, Pirttila T. Neuromuscular and sensory disturbances in patients with well treated celiac disease. J Neurol Neurosurg Psychiatry 2003; 74: 490–4.
35. Hadjivassiliou M, Grünewald RA, Kandler RH, Chattopadhyay AK, Jarratt JA, Sanders DS, et al. Neuropathy associated with gluten sensitivity. J Neurol Neurosurg Psychiatry 2006; 77: 1262–6.
36. Chapman RWG, Laidlow JM, ColinJones D, Eade OE, Smith CL. Increased prevalence of epilepsy in coeliac disease BMJ. 1978; 2: 250–1.
37. Fois A, Vascotto M, Di Bartolo RM, Di Marco V. Celiac disease and epilepsy in pediatric patients. Childs Nerv Syst 1994; 10: 450–4.
38. Cronin CC, Jackson LM, Feighery C, Shanahan F, Abuzakouk M, Ryder DQ, et al. Coeliac disease and epilepsy Q JM. 1998; 91: 303–8.
39. Gobbi G, Bouquet F, Greco L, Lambertini A, Tassinari CA, Ventura A, et al. Coeliac disease, epilepsy and cerebral calcifi cations. Lancet 1992; 340: 439–43.
40. Magaudda A, Dalla Bernardina B, De Marco P, Sfaello Z, Longo M, Colamaria V, et al. Bilateral occipital calcifi cation, epilepsy and celiac disease: clinical and neuroimaging features of a new syndrome. J Neurol Neurosurg Psychiatry 1993; 56: 885–9.
41. Toti P, Balestri P, Cano M, et al. Celiac disease with cerebral calcium and silica deposits: X-ray spectroscopic fi ndings, an autopsy study. Neurology 1996; 46: 1088–92.
42. Toti P, Balestri P, Cano M, Galluzzi P, Megha T, Farnetani MA, et al. Hippocampal sclerosis in refractory temporal lobe epilepsy is associated with gluten sensitivity. J Neurol Neurosurg Psychiatry 2009; 80: 626–30.
43. Mavroudi A, Karatza E, Papastavrou T, Panteliadis C, Spiroglou K. Succesful treatment of epilepsy and celiac disease with a gluten-free diet. Pediatr Neurol 2005; 33: 292–5.
44. Harper E, Moses H, Lagrange A. Occult celiac disease presenting as epilepsy and MRI changes that responded to glutenfree diet. Neurology 2007; 68: 533.
45. Hadjivassiliou M, Grünewald RAG, Lawden M, Davies-Jones GAB, Powell T, Smith CML. Headache and CNS white matter abnormalities associated with gluten sensitivity. Neurology 2001; 56: 385–8.
46. Gabrielli M, Cremonini F, Fiore G, Addolorato G, Padalino C, Candelli M, et al. Association between migraine and celiac disease: results from a preliminary casecontrol and therapeutic study. Am J Gastroenterol 2003; 98: 625–9.
47. Addolorato G, Di Giuda D, De Rossi G, Valenza V, Domenicali M, Caputo F, et al. Regional cerebral hypoperfusion in patients with celiac disease. Am J Med 2004; 116: 312–7.
48. Kieslich M, Errazuriz G, Rosselt HG, Moeller-Hartmann W, Zanell BH. Brain white matter lesions in celiac disease: a prospective study in diet treated patients. Paediatrics 2001; 108: 21.
49. Paul F, Pfueller CF, Wuerfel JT, Egerer K, Tanczos B, Baumgart DC, et al. Celiac antibodies in the diagnostic workup of white matter lesions. Neurology 2008; 71: 223–5.
50. Hu WT, Murray JA, Greenway MC, Parisi JE, Josephs KA. Cognitive impairment and celiac disease. Arch Neurol 2006; 63: 1440–6.
51. Frisoni GB, Carabellese N, Longhi M, Geroldi C, Bianchetti A, Govoni S, et al. Is celiac disease associated with Alzheimer’s disease. Acta Neurol Scand 1997; 95: 147–51.
52. Collin P, Pirttilä T, Nurmikko T, Somer H, Erilä T, Keyriläinen O. Celiac disease, brain atrophy, and dementia. Neurology 1991;41:372-5.
53. Hu WT, Murray JA, Greenaway MC, Parisi JE, Josephs KA. Cognitive impairment and celiac disease. Arch Neurol 2006;63:1440-6. Cooke WT. The neurological manifestations of malabsorption. Postgrad Med J 1978;54:760-2.
54. Hadjivassiliou M, Boscolo S, DaviesJones GA, Grünewald RA, Not T, Sanders DS, et al. The humoral response in the pathogenesis of gluten ataxia. Neurology 2002;58:1221-6.
55. Hadjivassiliou M, Mäki M, Sanders DS, Williamson CA, Grünewald RA, Woodroofe NM, et al. Autoantibody targeting of brain and intestinal transglutaminase in gluten ataxia. Neurology 2006;66:373-7.
56. Tan HJ, Goh KL. Extragastrointestinal manifestations of Helicobacter pylori infection: facts or myth? A critical review. J Dig Dis 2012;13:342-9.
57. De Bastiani R, Gabrielli M, Ubaldi E, Benedetto E, Sanna G, Cottone C, et al. High prevalence of Cag-A positive H. pylori strains in ischemic stroke: a primary care multicenter study. Helicobacter 2008; 13: 274–7.
58. Pietroiusti A, Diomedi M, Silvestrini M, Cupini LM, Luzzi I, Gomez-Miguel MJ, et al. Cytotoxin-associated gene-Apositive Helicobacter pylori strains are associated with atherosclerotic stroke. Circulation 2002; 106: 580–4.
59. Diomedi M, Pietroiusti A, Silvestrini M, Rizzato B, Cupini LM, Ferrante F, et al. CagA-positive Helicobacter pylori strains may influence the natural history of atherosclerotic stroke. Neurology 2004; 63: 800–4.
60. Zhang S, Guo Y, Ma Y, Teng Y. Relationship between the cytotoxinassociated gene-A status of H pylori strains and cerebral infarction in European Caucasians and Chinese Han: a meta-analysis. World J Gastroenterol 2008; 14: 1286–92.
61. Pasceri V, Patti G, Cammarota G, Pristipino C, Richichi G, Di Sciascio G. Virulent strains of Helicobacter pylori and vascular diseases: a meta-analysis. Am Heart J 2006; 151: 1215–22.
62. Gabrielli M, Santoliquido A, Cremonini F, Cicconi V, Candelli M, Serricchio M, et al. CagA-positive cytotoxic H. pylori strains as a link between plaque instability and atherosclerotic stroke. Eur Heart J 2004; 25: 64–8.
63. Sung JJ, Sanderson JE. Hyperhomocysteinaemia, Helicobacter pylori, and coronary artery disease. Heart 1996; 76: 305–7.
64. Ozturk A, Ozturk CE, Ozdemirli B, Yucel M, Bahçebaşi T. Helicobacter pylori infection in epileptic patients. Seizure 2007; 16: 147–52.
65. Cacoub P, Saadoun D, Limal N, Léger JM, Maisonobe T. Hepatitis C virus infection and mixed cryoglobulinaemia vasculitis: a review of neurological complications. AIDS 2005; 19: 128-134.
66. Cacoub P, Renou C, Rosenthal E, Cohen P, Loury I, Loustaud-Ratti V, et al. Extrahepatic manifestations associated with hepatitis C virus infection. A prospective multicenter study of 321 patients. The GERMIVIC. Groupe d’Etude et de Recherche en Medecine Interne et Maladies Infectieuses sur le Virus de l’Hepatite C. Medicine 2000; 79: 47-56.
67. Lidove O, Cacoub P, Maisonobe T, Servan J, Thibault V, Piette JC, et al. Hepatitis C virus infection with peripheral neuropathy is not always associated with cryoglobulinaemia. Ann Rheum Dis 2001; 60: 290-2.
68. Paoletti V, Donnarumma L, De Matteis A, Mammarella A, Labbadia G, Musca A, et al. Peripheral neuropathy without cryoglobulinemia in patients with hepatitis C virus infection. Panminerva Med 2000; 42: 175-8.
69. Nemni R, Sanvito L, Quattrini A, Santuccio G, Camerlingo M, Canal N. Peripheral neuropathy in hepatitis C virus infection with and without cryoglobulinaemia. J Neurol Neurosurg Psychiatry 2003; 74: 1267-71.
70. Bonetti B, Scardoni M, Monaco S, Rizzuto N, Scarpa A. Hepatitis C virus infection of peripheral nerves in type II cryoglobulinaemia. Virchows Arch 1999; 434: 533-5.
71. Origgi L, Vanoli M, Carbone A, Grasso M, Scorza R. Central nervous system involvement in patients with HCVrelated cryoglobulinemia. Am J Med Sci 1998; 315: 208-10.
72. Petty GW, Duffy J, Houston J. Cerebral ischemia in patients with hepatitis C virus infection and mixed cryoglobulinemia. Mayo Clin Proc 1996; 71: 671-8.
73. Heckmann JG, Kayser C, Heuss D, Manger B, Blum HE, Neundörfer B. Neurological manifestations of chronic hepatitis C. J Neurol 1999; 246: 486-91. Tembl JI, Ferrer JM, Sevilla MT, Lago A, Mayordomo F, Vilchez JJ. Neurologic complications associated with hepatitis C virus infection. Neurology 1999; 53: 861-4.
74. Jung KH, Ahn TB, Jeon BS. Wilson disease with an initial manifestation of polyneuropathy. Arch Neurol 2005;62:1628-31.
75. Schumacher G, Platz KP, Mueller AR, Neuhaus R, Steinmüller T, Bechstein WO, et al. Liver transplantation: treatment of choice for hepatic and neurological manifestation of Wilson's disease. Clin Transplant 1997;11:217-24.
76. Αdams RD, Foley JM. The neurological disorder associated with liver disease. Res Publ Assoc Res Nerv Ment Dis 1953;32:198-237.
77. Cağ M, Saouli AC, Audet M, Wolf P, Cinqualbre J. Reye syndrome and liver transplantation. Turk J Pediatr 2010;52:662-4.
78. Menegaux F, Keeffe EB, Andrews BT, Egawa H, Monge H, Concepcion W, et al. Neurological complications of liver transplantation in adult versus pediatric patients. Transplantation 1994;58:447–
79. Lewis MB, Howdle PD. Neurologic complications of liver transplantation in adults. Neurology 2003;61:1174–8.
80. Bronster DJ, Emre S, Boccagni P, Sheiner PA, Schwartz ME, Miller CM. Central nervous system complications in liver transplant recipients-incidence, timing, and long-term follow-up. Clin Transplant 2000;14:1–7.
81. Ghaus N, Bohlega S, Rezeig M. Neurological complications in liver transplantation. J Neurol 2001;248:1042–8.
82. Vogt DP, Lederman RJ, Carey WD, Broughan TA. Neurologic complications of liver transplantation. Transplantation 1988;45:1057–61.
83. Stein DP, Lederman RJ, Vogt DP, Carey WD, Broughan TA. Neurological complications following liver transplantation. Ann Neurol 1992;31:644–9.
84. Moreno E, Gómez SR, Gonzalez I, Loinaz C, Garcia I, Perez A, et al. Neurologic complications in liver transplantation. Acta Neurol Scand 1993;87:25–31.
85. Boin IF, Falcão AE, Luzo AC, Cardoso AR, Caruy CA, Leonardi LS. Analysis of neurologic complications within the first 30 days after orthotopic liver transplantation. Transplant Proc 2001;33:3695–6.
86. Vecino MC, Cantisani G, Zanotelli ML, Marrone CA, Brandão AB, Cassal AP, et al. Neurological complications in liver transplantation. Transplant Proc 1999;31:3048–9.
87. Shibolet O, Galun E, Bishara A, Eid A, Birmanns B, Ilan Y, et al. Major neurological complications following liver transplantation. Transplant Proc 2001;33:2959.
88. Gümüş H, Per H, Kumandaş S, Yikilmaz A. Reversible posterior leukoencephalopathy syndrome in childhood: report of nine cases and review of the literature. Neurol Sci 2010;31:125-31.
89. Cosottini M, Lazzarotti G, Ceravolo R, Michelassi MC, Canapicchi R, Murri L. Cyclosporine-related posterior reversible encephalopathy syndrome (PRES) in non-transplant patient: a case report and literature review. Eur J Neurol 2003;10:461-2.
90. Ghosh PS, Hupertz V, Ghosh D. Neurological complications following pediatric liver transplant. J Pediatr Gastroenterol Nutr 2012;54:540-6.
91. Komori H, Wada M, Eto M, Oki H, Aida K, Fujimoto T. Benign convulsions with mild gastroenteritis: a report of 10 recent cases detailing clinical varieties. Brain Dev 1995;17:334-7.
92. Narchi H. Benign afebrile cluster convulsions with gastroenteritis: an observational study. BMC Pediatr 2004 5;4: Hung JJ, Wen HY, Yen MH, Chen HW, Yan DC, Lin KL, et al. Rotavirus gastroenteritis associated with afebrile convulsion in children: clinical analysis of 40 cases. Chang Gung Med J 2003;26:654-9.
93. Goldwater PN, Rowland K, Thesinger M, Abbott K, Grieve A, Palombo EA, et al. Rotavirus encephalopathy: pathogenesis reviewed. J Paediatr Child Health 2001;37:206-9.
94. Morioka S, Otabe O, Uehara H, Yokoi K, Ohmizono Y, Ishimaru Y, Morimoto M, Hosoi H. Recurrence of transient splenial lesions in a child with "benign convulsions with gastroenteritis". No To Hattatsu 2010;42:449-53.
95. Narchi H. Benign afebrile cluster convulsions with gastroenteritis: an observational study. BMC Pediatr 2004 5;4: Verrotti A, Tocco AM, Coppola GG, Altobelli E, Chiarelli F. Afebrile benign convulsions with mild gastroenteritis: a new entity? Acta Neurol Scand 2009;120:73-9.
96. Fasheh Youssef W, Pino Ramírez R, Campistol Plana J, Pineda Marfa M. Benign afebrile convulsions in the course of mild acute gastroenteritis: a study of 28 patients and a literature review. Pediatr Emerg Care 2011;27:1062-4.
97. Matano S, Inamura K, Konishi M, Okumura T, Kawai H, Okamura T, et al. Encephalopathy, disseminated intravascular coagulation, and hemolytic-uremic syndrome after infection with enterohemorrhagic Escherichia coli O J Infect Chemother 2012;18:558-64.
98. Arii J, Tanabe Y, Miyake M, Noda M, Takahashi Y, Hishiki H, et al. Acute encephalopathy associated with nontyphoidal salmonellosis. J Child Neurol 2001;16:539-40.