Inflammation and iron metabolism in adult patients with epilepsy: Does a link exist?

Epilepsy Research

Volumn 107, Issue 3, 2013, Pages 244-252

  Tombini, M ^a   Squitti, R ^a,b   Cacciapaglia, F ^c   Ventriglia, M ^a,b   Assenza, G ^a   Benvenga, A ^a   Pellegrino, G ^a   Campana, C ^a   Assenza, F ^a   Siotto, M ^f   Pacifici, L ^b   Afeltra, A ^a   Rossini, P M ^b,d,e  

^a UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^b FATEBENEFRATELLI HOSPITAL   (Italy)

^c N Melli Hospital   (Italy)

^d CATHOLIC UNIVERSITY   (Italy)

^e IRCCS SAN RAFFAELE PISANA   (Italy)

^f IRCCS FONDAZIONE DON CARLO GNOCCHI   (Italy)

Author keywords

Cytokines; Epilepsy; IL 6; Inflammation; Iron; TNF

Indexed keywords

CARBAMAZEPINE; CERULOPLASMIN; COPPER; ETIRACETAM; FERRITIN; HEMOGLOBIN; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; IRON; LAMOTRIGINE; OXCARBAZEPINE; PHENOBARBITAL; TOPIRAMATE; TRANSFERRIN; TUMOR NECROSIS FACTOR ALPHA; VALPROIC ACID;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; COPPER BLOOD LEVEL; DISEASE DURATION; ENZYME ACTIVITY; ERYTHROCYTE COUNT; FEMALE; FERRITIN BLOOD LEVEL; FOCAL EPILEPSY; HEMATOCRIT; HEMOGLOBIN DETERMINATION; HUMAN; INFLAMMATION; IRON BLOOD LEVEL; IRON METABOLISM; MALE; MEAN CORPUSCULAR VOLUME; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL;

CYTOKINES; EPILEPSY; IL-6; INFLAMMATION; IRON; TNF-Α;

ACUTE DISEASE; ADULT; AGED; BIOLOGICAL MARKERS; EPILEPSY; FEMALE; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-6; IRON; MALE; MIDDLE AGED; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84888435344     PISSN: 09201211     EISSN: 18726844     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2013.09.010     Document Type: Article

References (67)

1. Abe A., Yamashita S., Noma A. Sensitive, direct colorimetric assay for copper in serum. Clin. Chem. 1989, 35:552-554.
2. Altamura C., Squitti R., Pasqualetti P., Gaudino C., Palazzo P., Tibuzzi F., Lupoi D., Cortesi M., Rossini P.M., Vernieri F. Ceruloplasmin/transferrin system is related to clinical status in acute stroke. Stroke 2009, 40:1282-1288.
3. Alvarez-Hernandez X., Lićeaga J., McKay I.C., Brock J.H. Induction of hypoferremia and modulation of macrophage iron metabolism by tumor necrosis factor. Lab. Invest. 1989, 61:319-322.
4. Balosso S., Ravizza T., Perego C., Peschon J., Campbell I.L., De Simoni M.G., Vezzani A. Tumor necrosis factor-alpha inhibits seizures in mice via p75 receptors. Ann. Neurol. 2005, 57:804-812.
5. Bernardino L., Xapelli S., Silva A.P., Jakobsen B., Poulsen F.R., Oliveira C.R., Vezzani A., Malva J.O., Zimmer J. Modulator effects of interleukin-1beta and tumor necrosis factor-alpha on AMPA-induced excitotoxicity in mouse organotypic hippocampal slice cultures. J. Neurosci. 2005, 25:6734-6744.
6. Bidabadi E., Mashouf M. Association between iron deficiency anemia and first febrile convulsion: a case-control study. Seizure 2009, 18:347-351.
7. Bielli P., Calabrese L. Structure to function relationships in ceruloplasmin: a 'moonlighting' protein. Cell. Mol. Life Sci. 2002, 59:1413-1427.
8. Boyett J.D., Lehmann H.P., Beeler M.F. Automated assay of ceruloplasmin by kinetic analysis of o-dianisidine oxidation. Clin. Chim. Acta 1976, 69:233-241.
9. Campbell K.A., Bank B., Milgram N.W. Epileptogenic effects of electrolytic lesions in the hippocampus: role of iron deposition. Exp. Neurol. 1984, 86:506-514.
10. Castell J.V., Gomez-Lechon M.J., David M., Andus T., Geiger T., Trullenque R., Fabra R., Heinrich P.C. Interleukin-6 is the major regulator of acute phase protein synthesis in adult human hepatocytes. FEBS Lett. 1989, 242:237-239.
11. Daoud A.S., Batieha A., Abu-Ekteish F., Gharaibeh N., Ajlouni S., Hijazi S. Iron status: a possible risk factor for the first febrile seizure. Epilepsia 2002, 43:740-743.
12. De Sarro G., Russo E., Ferreri G., Giuseppe B., Flocco M.A., Di Paola E.D., De Sarro A. Seizure susceptibility to various convulsant stimuli of knockout interleukin-6 mice. Pharmacol. Biochem. Behav. 2004, 77:761-766.
13. DeUngria M., Rao R., Wobken J.D., Luciana M., Nelson C.A., Georgieff M.K. Perinatal iron deficiency decreases cytochrome c oxidase (CytOx) activity in selected regions of neonatal rat brain. Pediatr. Res. 2000, 48:169-176.
14. Dinarello C.A. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 2009, 27:519-550.
15. Duncan J.S., Sander J.W., Sisodiya S.M., Walker M.C. Adult epilepsy. Lancet 2006, 367:1087-1100.
16. Fahmy M., Young S.P. Modulation of iron metabolism in monocyte cell line U937 by inflammatory cytokines: changes in transferrin uptake, iron handling and ferritin mRNA. Biochem. J. 1993, 296:175-181.
17. Finch C.A., Huebers H.A., Cazzola M., Bergamaschi G., Bellotti V. Storage iron. Ferritins and Isoferritins as Biochemical Markers 1984, 3-21. Elsevier Science Publishers, Amsterdam, The Netherlands. A. Albertini, P. Arosio, E. Chiancone, J. Drysdale (Eds.).
18. Higgins T. Novel chromogen for serum iron determinations. Clin. Chem. 1981, 27:1619-1620.
19. Hughes J.T., Oppenheimer D.R. Superficial siderosis of the central nervous system. A report on nine cases with autopsy. Acta Neuropathol. (Berl.) 1969, 13:56-74.
20. Hulkkonen J., Koskikallio E., Rainesalo S., Keränen T., Peltola J. The balance of inhibitory and excitatory cytokines is differently regulated in vivo and in vitro among therapy resistant epilepsy patients. Epilepsy Res. 2004, 59:199-205.
21. Hussain R.I., Ballard C.G., Edwardson J.A., Morris C.M. Transferrin gene polymorphism in Alzheimer's disease and dementia with Lewy bodies in humans. Neurosci. Lett. 2002, 317:13-16.
22. Idro R., Gwer S., Williams T.N., Otieno T., Uyoga S., Fegan G., Kager P.A., Maitland K., Kirkham F., Neville B.G., Newton C.R. Iron deficiency and acute seizures: results from children living in rural Kenya and a meta-analysis. PLoS ONE 2010, 5(11):e14001.
23. Ikeda M. Iron overload without the C282Y mutation in patients with epilepsy. J. Neurol. Neurosurg. Psychiatry 2001, 70:551-553.
24. Kalueff A.V., Lehtimaki K.A., Ylinen A., Honkaniemi J., Peltola J. Intranasal administration of human IL-6 increases the severity of chemically induced seizures in rats. Neurosci. Lett. 2004, 22:106-110.
25. Kobrinsky N.L., Yager J.Y., Cheang M.S., Yatscoff R.W., Tenenbein M. Does iron deficiency raise the seizure threshold?. J. Child Neurol. 1995, 10:105-109.
26. Koorts A.M., Levay P.F., Becker P.J., Viljoen M. Pro- and anti-inflammatory cytokines during immune stimulation: modulation of iron status and red blood cell profile. Mediators Inflamm. 2011, 716301.
27. Kozlov P.M.A.V., Sergienko V.I., Vladimirov I.A., Azizova O.A. The antioxidant system of transferrin-ceruloplasmin in experimental hypercholesterolemia. Biull. Eksp. Biol. Med. 1984, 98:668-671.
28. Lehmann H.P., Schosinsky K.H., Beeler M.F. Standardization of serum ceruloplasmin concentrations in international enzyme units with o-dianisidinedihydrochloride as substrate. Clin. Chem. 1974, 20:1564-1567.
29. Liimatainen S., Fallah M., Kharazmi E., Peltola M., Peltola J. Interleukin-6 levels are increased in temporal lobe epilepsy but not in extra-temporal lobe epilepsy. J. Neurol. 2009, 256:796-802.
30. Lipschitz D.A., Simon M.O., Lynch S.R., Dugard J., Bothwell T.H., Charlton R.W. Some factors affecting the release of iron from reticuloendothelial cells. Br. J. Haematol. 1971, 21:289-303.
31. Lu M.O., Zhang X.M., Mix E., Quezada H.C., Jin T., Zhu J., Adem A. TNF-alpha receptor 1 deficiency enhances kainic acid-induced hippocampal injury in mice?. J. Neurosci. Res. 2008, 86(7):1608-1614.
32. Ludwiczek S., Aigner E., Theurl I., Weiss G. Cytokine-mediated regulation of iron transport in human monocytic cells. Blood 2003, 101:4148-4154.
33. MacEwan D.J. TNF ligands and receptors - a matter of life and death. Br. J. Pharmacol. 2002, 135:855-875.
34. Madan N., Rusia U., Sikka M., Sharma S., Shankar N. Developmental and neurophysiologic deficits in iron deficiency in children. Indian J. Pediatr. 2011, 78:58-64.
35. Martinez-Subiela S., Tecles F., Ceron J.J. Comparison of two automated spectrophotometric methods for ceruloplasmin measurement in pigs. Res. Vet. Sci. 2007, 83:12-19.
36. Miller L.L., Miller S.C., Torti S.V., Tsuji Y., Torti F.M. Iron-independent induction of ferritin H chain by tumor necrosis factor. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:4946-4950.
37. Momen A.A., Hakimzadeh M. Case-control study of the relationship between anemia and febrile convulsion in children between 9 months and 5 years of age. Sci. Med. J. Ahwaz Univ. Med. Sci. 2003, 1:50-54.
38. Naveed-ur-Rehman, Billoo A.G. Association between iron deficiency anemia and febrile seizures. J. Coll. Physicians Surg. Pak. 2005, 15:338L 340.
39. Ounjaijean S., Westermarck T., Partinen M., Plonka-Poltorak E., Kaipainen P., Kaski M., Fucharoen S., Srichairatanakool S., Atroshi F. Increase in non-transferrin bound iron and the oxidative stress status in epilepsy patients treated using valproic acid monotherapy. Int. J. Clin. Pharmacol. Ther. 2011, 49:268L 76.
40. Ozaydin E., Arhan E., Cetinkaya B., Ozdel S., Deǧerliyurt A., Güven A., Köse G. Differences in iron deficiency anemia and mean platelet volume between children with simple and complex febrile seizures. Seizure 2012, 21:211-214.
41. Peltola J., Hurme M., Miettinen A., Keränen T. Elevated levels of interleukin-6 may occur in cerebrospinal fluid from patients with recent epileptic seizures. Epilepsy Res. 1998, 31:129-133.
42. Peltola J., Palmio J., Korhonen L., Suhonen J., Miettinen A., Hurme M., Lindholm D., Keränen T. Interleukin-6 and interleukin-1 receptor antagonist in cerebrospinal fluid from patients with recent tonic-clonic seizures. Epilepsy Res. 2000, 41:205-211.
43. Penkowa M., Molinero A., Carrasco J., Hidalgo J. Interleukin-6 deficiency reduces the brain inflammatory response and increases oxidative stress and neurodegeneration after kainic acid-induced seizures. Neuroscience 2001, 102:805-818.
44. Pisacane A., Sansone R., Impagliazzo N., Coppola A., Rolando P., D'Apuzzo A., Tregrossi C. Iron deficiency anaemia and febrile convulsions: case-control study in children under 2 years. BMJ 1996, 10:313-343.
45. Ramadori G., Van Damme J., Rieder H., Meyer zum Büschenfelde K.H. Interleukin 6, the third mediator of acute-phase reaction, modulates hepatic protein synthesis in human and mouse. Comparison with interleukin 1 beta and tumor necrosis factor-alpha. Eur. J. Immunol. 1988, 18:1259-1264.
46. Riazi K., Galic M.A., Pittman Q.J. Contributions of peripheral inflammation to seizure susceptibility: cytokines and brain excitability. Epilepsy Res. 2010, 89:34-42.
47. Riikonen R. Infantile spasms: therapy and outcome. J. Child Neurol. 2004, 19:401-404.
48. Rogers J.T. Ferritin translation by interleukin-1 and interleukin-6: the role of sequences upstream of the start codons of the heavy and light subunit genes. Blood 1996, 87:2525-2537.
49. Rojas G., Messen L. Generalized cytosiderosis in two cases of progressive myoclonic epilepsy with Lafora inclusion bodies. Histopathological and ultrastructural studies. Neurocirugia 1968, 26:3-11.
50. Scheller J., Chalaris A., Schmidt-Arras D., Rose-John S. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim. Biophys. Acta 2011, 1813:878-888.
51. Schosinsky K.H., Lehmann H.P., Beeler M.F. Measurement of ceruloplasmin from its oxidase activity in serum by use of o-dianisidine dihydrochloride. Clin. Chem. 1974, 20:1556-1563.
52. Shinoda S., Skradski S.L., Araki T., Schindler C.K., Meller R., Lan J.Q., Taki W., Simon R.P., Henshall D.C. Formation of a tumour necrosis factor receptor 1 molecular scaffolding complex and activation of apoptosis signal-regulating kinase 1 during seizure-induced neuronal death. Eur. J. Neurosci. 2003, 17:2065-2076.
53. Simo J.M., Joven J., Cliville X., Sans T. Automated latex agglutination immunoassay of serum ferritin with a centrifugal analyzer. Clin. Chem. 1994, 40:625-629.
54. Skikne B.S., Flowers C.H., Cole J.D. Serum transferrin receptor, a quantitative measure of tissue iron deficiency. Blood 1990, 75:1870-1876.
55. Somani B.L., Ambade V. A kinetic method amenable to automation for ceruloplasmin estimation with inexpensive and stable reagents. Clin. Biochem. 2007, 40:571-574.
56. Squitti R., Salustri C., Siotto M., Ventriglia M., Vernieri F., Lupoi D., Cassetta E., Rossini P.M. Ceruloplasmin/transferrin ratio changes in Alzheimer's disease. Int. J. Alzheimers Dis. 2010, 27:2011-231595.
57. Taher A.T., Musallam K.M., Nasreddine W., Perrine S.P., El-Hajj T.I., Beydoun A. Effects of divalproex sodium on hemoglobin level. Blood Cells Mol. Dis. 2009, 43:49L 52.
58. Vezzani A., Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 2005, 46:1724-1743.
59. Vezzani A., Balosso S., Ravizza T. The role of cytokines in the pathophysiology of epilepsy. Brain Behav. Immun. 2008, 22:797-803.
60. Vezzani A., French J., Bartfai T., Baram T.Z. The role of inflammation in epilepsy. Nat. Rev. Neurol. 2011, 7:31-40.
61. Virta M., Hurme M., Helminen M. Increased plasma levels of pro- and anti-inflammatory cytokines in patients with febrile seizures. Epilepsia 2002, 43:920-923.
62. Wheless J.W., Clarke D.F., Arzimanoglou A., Carpenter D. Treatment of pediatric epilepsy: European expert opinion. Epileptic. Disord. 2007, 9:353-412.
63. Weiss G., Goodnough L.T. Anemia of chronic disease. New England J. Med. 2005, 352:1011-1059.
64. Wirrell E., Farrell K., Whiting S. The epileptic encephalopathies of infancy and childhood. Can. J. Neurol. Sci. 2005, 32:409-418.
65. Wolf P.L. Ceruloplasmin: methods and clinical use. Crit. Rev. Clin. Lab. Sci. 1982, 17:229-245.
66. Worwood M. Ferritin. Blood Rev. 1990, 4:259-269.
67. Zareifar S., Hosseinzadeh H.R., Cohan N. Association between iron status and febrile seizures in children. Seizure 2012, 21:603-605.