Cytokine and adipokine alterations in patients with schizophrenia treated with clozapine

Psychiatry Research

Volumn 218, Issue 3, 2014, Pages 277-283

  Klemettilä, Jari Pekka ^a   Kampman, Olli ^b,c   Seppälä, Niko ^d   Viikki, Merja ^b,e   Hämäläinen, Mari ^a,b   Moilanen, Eeva ^a,b   Leinonen, Esa ^a,b  

^a TAMPERE UNIVERSITY HOSPITAL   (Finland)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c SEINÄJOKI CENTRAL HOSPITAL   (Finland)

^d Satakunta Hospital District   (Finland)

^e Tampere Mental Health Centre   (Finland)

Author keywords

Adiponectin; Hs CRP; IL 1Ra; IL 6; Metabolic syndrome

Indexed keywords

ADIPONECTIN; C REACTIVE PROTEIN; CLOZAPINE; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN CHOLESTEROL; ADIPOCYTOKINE; BIOLOGICAL FACTOR; CYTOKINE; NEUROLEPTIC AGENT;

ADULT; AGE DISTRIBUTION; AGED; ARTICLE; BODY MASS; CARDIOMETABOLIC RISK; CHOLESTEROL BLOOD LEVEL; COMORBIDITY; CROSS-SECTIONAL STUDY; DISEASE ASSOCIATION; FEMALE; GLUCOSE BLOOD LEVEL; HUMAN; HYPERTRIGLYCERIDEMIA; INSULIN RESISTANCE; MAJOR CLINICAL STUDY; MALE; METABOLIC SYNDROME X; OBESITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN MODIFICATION; RETROSPECTIVE STUDY; SCHIZOPHRENIA; SEX DIFFERENCE; SMOKING; BLOOD; COMPLICATION; DRUG EFFECTS; MIDDLE AGED;

ADIPOKINES; ADIPONECTIN; ADULT; ANTIPSYCHOTIC AGENTS; BIOLOGICAL FACTORS; CLOZAPINE; CYTOKINES; FEMALE; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-6; MALE; METABOLIC SYNDROME X; MIDDLE AGED; SCHIZOPHRENIA;

EID: 84902083137     PISSN: 01651781     EISSN: 18727123     Source Type: Journal    
DOI: 10.1016/j.psychres.2014.04.049     Document Type: Article

References (63)

1. Ahonen T., Vanhala M., Kautiainen H., Kumpusalo E., Saltevo J. Sex differences in the association of adiponectin and low-grade inflammation with changes in the body mass index from youth to middle age. Gender Medicine 2012, 9:1-8.
2. Alberti K.G., Eckel R.H., Grundy S.M., Zimmet P.Z., Cleeman J.I., Donato K.A., Fruchart J.C., James W.P., Loria C.M., Smith S.C. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the study of obesity. Circulation 2009, 120:1640-1645.
3. Bai Y.M., Chen J.Y., Yang W.S., Chi Y.C., Liou Y.J., Lin C.C., Wang Y.C., Lin C.Y., Su T.P., Chou P. Adiponectin as a potential biomarker for the metabolic syndrome in Chinese patients taking clozapine for schizophrenia. Journal of Clinical Psychiatry 2007, 68:1834-1839.
4. Beary M., Hodgson R., Wildgust H.J. A critical review of major mortality risk factors for all-cause mortality in first-episode schizophrenia: clinical and research implications. Journal of Psychopharmacology 2012, 26:52-61.
5. Beumer W., Drexhage R.C., De Wit H., Versnel M.A., Drexhage H.A., Cohen D. Increased level of serum cytokines, chemokines and adipokines in patients with schizophrenia is associated with disease and metabolic syndrome. Psychoneuroendocrinology 2012, 37:1901-1911.
6. Cartier A., Cote M., Lemieux I., Perusse L., Tremblay A., Bouchard C., Despres J.P. Sex differences in inflammatory markers: what is the contribution of visceral adiposity?. American Journal of Clinical Nutrition 2009, 89:1307-1314.
7. Chen P.Y., Huang M.C., Chiu C.C., Liu H.C., Lu M.L., Chen C.H. Association of plasma retinol-binding protein-4, adiponectin, and high molecular weight adiponectin with metabolic adversities in patients with schizophrenia. Progress in Neuro-psychopharmacology & Biological Psychiatry 2011, 35:1927-1932.
8. De Hert M., van Winkel R., van Eyck D., Hanssens L., Wampers M., Scheen A., Peuskens J. Prevalence of diabetes, metabolic syndrome and metabolic abnormalities in schizophrenia over the course of the illness: a cross-sectional study. Clinical Practice and Epidemiology in Mental Health 2006, 2:14.
9. Dieset I., Hope S., Ueland T., Bjella T., Agartz I., Melle I., Aukrust P., Rossberg J.I., Andreassen O.A. Cardiovascular risk factors during second generation antipsychotic treatment are associated with increased C-reactive protein. Schizophrenia Research 2012, 140:169-174.
10. Fan X., Liu E.Y., Freudenreich O., Park J.H., Liu D., Wang J., Yi Z., Goff D., Henderson D.C. Higher white blood cell counts are associated with an increased risk for metabolic syndrome and more severe psychopathology in non-diabetic patients with schizophrenia. Schizophrenia Research 2010, 118:211-217.
11. Fantuzzi G. Adipose tissue, adipokines, and inflammation. Journal of Allergy and Clinical Immunology 2005, 115:911-919.
12. Fernandez-Egea E., Bernardo M., Donner T., Conget I., Parellada E., Justicia A., Esmatjes E., Garcia-Rizo C., Kirkpatrick B. Metabolic profile of antipsychotic-naïve individuals with non-affective psychosis. British Journal of Psychiatry 2009, 194:434-438.
13. Gustafson B. Adipose tissue, inflammation and atherosclerosis. Journal of Atherosclerosis and Thrombosis 2010, 17:332-341.
14. Hanssens L., van Winkel R., Wampers M., van Eyck D., Scheen A., Reginster J.Y., Collette J., Peuskens J., De Hert M. A cross-sectional evaluation of adiponectin plasma levels in patients with schizophrenia and schizoaffective disorder. Schizophrenia Research 2008, 106:308-314.
15. Harwood H.J. The adipocyte as an endocrine organ in the regulation of metabolic homeostasis. Neuropharmacology 2012, 63:57-75.
16. Himmerich H., Schönherr J., Fulda S., Sheldrick A.J., Bauer K., Sack U. Impact of antipsychotics on cytokine production in-vitro. Journal of Psychiatric Research 2011, 45:1358-1365.
17. Jin H., Meyer J.M., Mudaliar S., Jeste D.V. Impact of atypical antipsychotic therapy on leptin, ghrelin and adiponectin. Schizophrenia Research 2008, 100:70-85.
18. Kane J., Honigfeld G., Singer J., Meltzer H. Clozapine for the treatment-resistant schizophrenic. A double-blind comparison with chlorpromazine. Archives of General Psychiatry 1988, 45:789-796.
19. Kilbourne A.M., Morden N.E., Austin K., Ilgen M., McCarthy J.F., Dalack G., Blow F.C. Excess heart-disease-related mortality in a national study of patients with mental disorders: identifying modifiable risk factors. General Hospital Psychiatry 2009, 31:555-563.
20. Kluge M., Schuld A., Schacht A., Himmerich H., Dalal M.A., Wehmeier P.M., Hinze-Selch D., Kraus T., Dittmann R.W., Pollmächer T. Effects of clozapine and olanzapine on cytokine systems are closely linked to weight gain and drug-induced fever. Psychoneuroendocrinology 2009, 34:118-128.
21. Kuo S-M., Halpern M.M. Lack of association between body mass index and plasma adiponectin levels in healthy adults. International Journal of Obesity 2011, 35:1487-1494.
22. Leonard B.E., Schwarz M., Myint A.M. The metabolic syndrome in schizophrenia: is inflammation a contributing cause?. Journal of Psychopharmacology 2012, 26:33-41.
23. Löffler S., Klimke A., Kronenwett R., Kobbe G., Haas R., Fehsel K. Clozapine mobilizes CD34+ hematopoietic stem and progenitor cells and increases plasma concentration of interleukin 6 in patients with schizophrenia. Journal of Clinical Psychopharmacology 2010, 30:591-595.
24. Löffler S., Löffler-Ensgraber M., Fehsel K., Klimke A. Clozapine therapy raises serum concentrations of high sensitive c-reactive protein in schizophrenic patients. International Clinical Psychopharmacology 2010, 25:101-106.
25. Lu L.X., Guo S.Q., Chen W., Li Q., Cheng J., Guo J.H. Effect of clozapine and risperidone on serum cytokine levels in patients with first-episode paranoid schizophrenia. Di Yi Jun Yi Da Xue Xue Bao 2004, 24:1251-1254. (Abstract, article in Chinese).
26. Luotola K., Pietilä A., Zeller T., Moilanen L., Kähönen M., Nieminen M.S., Kesäniemi Y.A., Blankenberg S., Jula A., Perola M., Salomaa V. Associations between interleukin-1 (IL-1) gene variations or IL-1 receptor antagonist levels and the development of type 2 diabetes. Journal of Internal Medicine 2011, 269:322-332.
27. Maes M., Bosmans E., Kenis G., De Jong R., Smith R.S., Melzer H.Y. in vivo immunomodulatory effects of clozapine in schizophrenia. Schizophrenia Research 1997, 29:221-225.
28. Malo E., Ukkola O., Jokela M., Moilanen L., Kähönen M., Nieminen M.S., Salomaa V., Jula A., Kesäniemi Y.A. Resistin is an indicator of the metabolic syndrome according to five different definitions in the Finnish Health 2000 survey. Metabolic Syndrome and Related Disorders 2011, 9:203-210.
29. Marques-Vidal P., Bastardot F., Von Känel R., Preisig M., Waeber G., Vollenweider P. Association between circulating cytokine levels, diabetes and insulin resistance in a population-based sample (CoLaus study). Clinical Endocrinology 2013, 78:232-241.
30. Matsuda Y., Tanioka T., Yoshioka T., Nagano T., Hiroi T., Yoshikawa K., Okabe K., Nagamine I., Takasaka Y. Gender differences in association of plasma adiponectin with obesity reflect resultant insulin resistance in non-diabetic Japanese patients with schizophrenia. Psychiatry and Clinical Neurosciences 2005, 59:266-273.
31. Matthews D.R., Hosker J.P., Rudenski A.S., Naylor B.A., Teacher D.F., Turner R.C. Homeostasis model assessment: insulin resistance and b cell function from fasting plasma glucose and insulin concentration in man. Diabetologia 1985, 28:412-419.
32. Meltzer H.Y. Update on typical and atypical antipsychotic drugs. Annual Review of Medicine 2013, 64:393-406.
33. Miller B.J., Buckley P., Seabolt W., Mellor A., Kirkpatrick B. Meta-analysis of cytokine alterations in schizophrenia: clinical status and antipsychotic effects. Biological Psychiatry 2011, 70:663-671.
34. Miller B.J., Culpepper N., Rapaport M.H. C-reactive protein levels in schizophrenia. Clinical Schizophrenia & Related Psychoses 2014, 7:223-230.
35. Miller B.J., Mellor A., Buckley P. Total and differential white blood cell counts, high-sensitivity C-reactive protein, and the metabolic syndrome in non-affective psychoses. Brain, Behaviour, and Immunity 2013, 31:82-89.
36. Mitchell A.J., Vancampfort D., Sweers K., van Winkel R., Yu W., De Hert M. Prevalence of metabolic syndrome and metabolic abnormalities in schizophrenia and related disorders - a systematic review and meta-analysis. Schizophrenia Bulletin 2013, 39:306-318.
37. Monteleone P., Fabrazzo M., Tortorella A., Maj M. Plasma levels of interleukin-6 and tumor necrosis factor alpha in chronic schizophrenia: effects of clozapine treatment. Psychiatry Research 1997, 16:11-17.
38. Newcomer J.W. Second-generation (atypical) antipsychotics and metabolic effects: a comprehensive literature review. CNS Drugs 2005, 19:S1-S93. (Suppl. 1).
39. Oh J.E., Cho Y.M., Kwak S.N., Kim J.H., Lee K.W., Jung H., Jeong S.W., Kwon O.J. Inhibition of mouse brown adipocyte differentiation by second- generation antipsychotics. Experimental & Molecular Medicine 2012, 44:545-553.
40. Oriot P., Feys J.L., Mertens de Wilmars S., Misson A., Ayache L., Fagnart O., Gruson D., Luts A., Jamart J., Hermans M.P., Buysschaert M. Insulin sensitivity, adjusted beta-cell function and adiponectinaemia among lean drug-naïve schizophrenic patients treated with atypical antipsychotic drugs: a nine-month prospective study. Diabetes & Metabolism 2008, 34:490-496.
41. Osby U., Correia N., Brandt L., Ekbom A., Sparen P. Mortality and causes of death in schizophrenia in Stockholm county, Sweden. Schizophrenia Research 2000, 45:21-28.
42. Plaisance E.P., Grandjean P.W., Judd R.L., Jones K.W., Taylor J.K. The influence of sex, body composition, and nonesterified fatty acids on serum adipokine concentrations. Metabolism 2009, 58:1557-1563.
43. Pollmächer T., Hinze-Selch D., Mullington J. Effects of clozapine on plasma cytokine and soluble cytokine receptor levels. Journal of Clinical Psychopharmacology 1996, 16:403-409.
44. Potvin S., Stip E., Sepehry A.A., Gendron A., Ramatoulaye B., Kouassi E. Inflammatory cytokine alterations in schizophrenia: a systematic quantitative review. Biological Psychiatry 2008, 63:801-808.
45. Raucci R., Rusolo F., Sharma A., Colonna G., Castello G., Costantini S. Functional and structural features of adipokine family. Cytokine 2013, 61:1-14.
46. Richards A.A., Hickman I.J., Wang A.Y., Jones A.L., Newell F., Mowry B.J., Whitehead J.P., Prins J.B., Macdonald G.A. Olanzapine treatment is associated with reduced high molecular weight adiponectin in serum: a potential mechanism for olanzapine-induced insulin resistance in patients with schizophrenia. Journal of Clinical Psychopharmacology 2006, 26:232-237.
47. Rossi I.A., Bochud M., Bovet P., Paccaud F., Waeber G., Vollenweider P., Taffe P. Sex difference and the role of leptin in the association between high-sensitivity C-reactive protein and adiposity in two different populations. European Journal of Epidemiology 2012, 27:379-384.
48. Ruotsalainen E., Salmenniemi U., Vauhkonen I., Pihlajamäki J., Punnonen K., Kainulainen S., Laakso M. Changes in inflammatory cytokines are related to impaired glucose tolerance in offspring of type 2 diabetic subjects. Diabetes Care 2006, 29:2714-2720.
49. Røge R., Møller B.K., Andersen C.R., Correll C.U., Nielsen J. Immunomodulatory effects of clozapine and their clinical implications: what have we learned so far?. Schizophrenia Research 2012, 140:204-213.
50. Salomaa V., Havulinna A., Saarela O., Zeller T., Jousilahti P., Jula A., Muenzel T., Aromaa A., Evans A., Kuulasmaa K., Blankenberg S. Thirty novel biomarkers as predictors for clinically incident diabetes. PLOS One 2010, 5:e10100.
51. Santaniemi M., Kesäniemi Y.A., Ukkola O. Low plasma adiponectin concentration is an indicator of the metabolic syndrome. European Journal of Endocrinology 2006, 155:745-750.
52. Schmitt A., Bertsch T., Tost H., Bergmann A., Henning U., Klimke A., Falkai P. Increased serum interleukin-1beta and interleukin -6 in elderly, chronic schizophrenic patients on stable antipsychotic medication. Neuropsychiatric Disease and Treatment 2005, 1:171-177.
53. Shen J., Ordovas J.M. Impact of genetic and environmental factors on hsCRP concentrations and response to therapeutic agents. Clinical Chemistry 2009, 55:256-264.
54. Shi H., Seeley R.J., Clegg D.J. Sexual differences in the control of energy homeostasis. Frontiers in Neuroendocrinology 2009, 30:396-404.
55. Steinke J.W., Borish L. Cytokines and chemokines. Journal of Allergy and Clinical Immunology 2006, 117:S441-S445.
56. Sugai T., Suzuki Y., Fukui N., Ono S., Watanabe J., Tsuneyama N., Someya T. Dysregulation of adipocytokines related to second-generation antipsychotics in normal fasting glucose patients with schizophrenia. Journal of Clinical Psychopharmacology 2012, 32:390-393.
57. Sugino H., Futamura T., Mitsumoto Y., Maeda K., Marunaka Y. Atypical antipsychotics suppress production of inflammatory cytokines and up-regulate interleukin-10 in lipopolysaccharide-treated mice. Progress in Neuro-psychopharmacology & Biological Psychiatry 2009, 17:303-307.
58. Suvisaari J.M., Saarni S.I., Perälä J., Suvisaari J.V., Härkänen T., Lönnqvist J., Reunanen A. Metabolic syndrome among persons with schizophrenia and other psychotic disorders in a general population survey. Journal of Clinical Psychiatry 2007, 68:1045-1055.
59. Tiihonen J., Haukka J., Taylor M., Haddad P.M., Patel M.X., Korhonen P. A nationwide cohort study of oral and depot antipsychotics after first hospitalization for schizophrenia. American Journal of Psychiatry 2011, 168:603-609.
60. Togo T., Kojima K., Shoji M., Kase A., Uchikado H., Katsuse O., Iseki E., Kosaka K. Serum adiponectin concentrations during treatment with olanzapine or risperidone: a pilot study. International Clinical Psychopharmacology 2004, 19:37-40.
61. Wampers M., Hanssens L., van Winkel R., Heald A., Collette J., Peuskens J., Reginster J.Y., Scheen A., De Hert M. Differential effects of olanzapine and risperidone on plasma adiponectin levels over time: results from a 3-month prospective open-label study. European Neuropsychopharmacology 2012, 22:17-26.
62. Wang H.C., Yang Y.K., Chen P.S., Lee I.H., Yeh T.L., Lu R.B. Increased plasma leptin in antipsychotic-naïve females with schizophrenia, but not in males. Neuropsychobiology 2007, 56:213-215.
63. Wu M.K., Huang C.Y., Liou Y.J., Wang C.K., Lee S.D. Glucose-insulin homeostasis, lipid profiles and GH-IGF-IGFBP axis in clozapine-treated schizophrenic obesity versus non-psychiatric obesity. International Journal of Obesity 2008, 32:436-442.