Fatigue symptoms relate to systemic inflammation in patients with type 2 diabetes

Brain, Behavior, and Immunity

Volumn 26, Issue 8, 2012, Pages 1211-1219

  Lasselin, Julie ^a,b   Layé, Sophie ^a,b   Dexpert, Sandra ^a,b   Aubert, Agnès ^a,b   Gonzalez, Concepcion ^c   Gin, Henri ^c   Capuron, Lucile ^a,b  

^a NutriNeuro Bordeaux University   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c HAUT LÉVÊQUE HOSPITAL   (France)

Author keywords

Adiposity; C reactive protein; Cytokines; Diabetes; Dimensions; Fatigue; Inflammation; Interleukin 6; Neopterin; Types 1 and 2

Indexed keywords

C REACTIVE PROTEIN; INSULIN; INTERLEUKIN 6; NEOPTERIN; TUMOR NECROSIS FACTOR ALPHA;

ADULT; CLINICAL ARTICLE; COMPARATIVE STUDY; DIABETIC PATIENT; DIET RESTRICTION; DISEASE DURATION; FATIGUE; FEMALE; GLYCEMIC CONTROL; HUMAN; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN TREATMENT; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SCORING SYSTEM; SYMPTOM;

ADIPOSITY; ADULT; AGED; BIOLOGICAL MARKERS; DIABETES MELLITUS, TYPE 2; FATIGUE; FEMALE; HUMANS; INFLAMMATION; INTERLEUKIN-6; MALE; MIDDLE AGED; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84867217210     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2012.03.003     Document Type: Review

References (58)

1. Alexandraki K.I., Piperi C., Ziakas P.D., Apostolopoulos N.V., Makrilakis K., Syriou V., Diamanti-Kandarakis E., Kaltsas G., Kalofoutis A. Cytokine secretion in long-standing diabetes mellitus type 1 and 2: associations with low-grade systemic inflammation. J. Clin. Immunol. 2008, 28:314-321.
2. Baris N., Erdogan M., Sezer E., Saygili F., Mert Ozgonul A., Turgan N., Ersoz B. Alterations in l-arginine and inflammatory markers in type 2 diabetic patients with and without microalbuminuria. Acta Diabetol. 2009, 46:309-316.
3. Baron R.M., Kenny D.A. The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J. Pers. Soc. Psychol. 1986, 51:1173-1182.
4. Basu S., Larsson A., Vessby J., Vessby B., Berne C. Type 1 diabetes is associated with increased cyclooxygenase- and cytokine-mediated inflammation. Diabetes Care 2005, 28:1371-1375.
5. Bower J.E. Cancer-related fatigue: links with inflammation in cancer patients and survivors. Brain Behav. Immun. 2007, 21:863-871.
6. Bower J.E., Ganz P.A., Aziz N., Fahey J.L. Fatigue and proinflammatory cytokine activity in breast cancer survivors. Psychosom. Med. 2002, 64:604-611.
7. Bower J.E., Ganz P.A., Irwin M.R., Kwan L., Breen E.C., Cole S.W. Inflammation and behavioral symptoms after breast cancer treatment: do fatigue, depression, and sleep disturbance share a common underlying mechanism?. J. Clin. Oncol. 2011, 29:3517-3522.
8. Calder P.C. N-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am. J. Clin. Nutr. 2006, 83:1505S-1519S.
9. Capuron L., Gumnick J.F., Musselman D.L., Lawson D.H., Reemsnyder A., Nemeroff C.B., Miller A.H. Neurobehavioral effects of interferon-alpha in cancer patients: phenomenology and paroxetine responsiveness of symptom dimensions. Neuropsychopharmacology 2002, 26:643-652.
10. Capuron L., Pagnoni G., Demetrashvili M.F., Lawson D.H., Fornwalt F.B., Woolwine B., Berns G.S., Nemeroff C.B., Miller A.H. Basal ganglia hypermetabolism and symptoms of fatigue during interferon-alpha therapy. Neuropsychopharmacology 2007, 32:2384-2392.
11. Capuron L., Su S., Miller A.H., Bremner J.D., Goldberg J., Vogt G.J., Maisano C., Jones L., Murrah N.V., Vaccarino V. Depressive symptoms and metabolic syndrome: is inflammation the underlying link?. Biol. Psychiatry 2008, 64:896-900.
12. Capuron L., Schroecksnadel S., Feart C., Aubert A., Higueret D., Barberger-Gateau P., Laye S., Fuchs D. Chronic low-grade inflammation in elderly persons is associated with altered tryptophan and tyrosine metabolism: role in neuropsychiatric symptoms. Biol. Psychiatry 2011, 70:175-182.
13. Capuron L., Poitou C., Machaux-Tholliez D., Frochot V., Bouillot J.L., Basdevant A., Layé S., Clément K. Relationship between adiposity, emotional status and eating behaviour in obese women: role of inflammation. Psychol. Med. 2011, 41:1517-1528.
14. Capuron L., Miller A.H. Immune system to brain signaling: neuropsychopharmacological implications. Pharmacol. Ther. 2011, 130:226-238.
15. Cavelti-Weder, C., Furrer, R., Keller, C., Babians-Brunner, A., Solinger, A.M., Gast, H., Fontana, A., Donath, M.Y., Penner, I.K., 2011. Inhibition of IL-1beta improves fatigue in type 2 diabetes. Diabetes Care 34, e158.
16. Cho H.J., Seeman T.E., Bower J.E., Kiefe C.I., Irwin M.R. Prospective association between C-reactive protein and fatigue in the coronary artery risk development in young adults study. Biol. Psychiatry 2009, 66:871-878.
17. Collado-Hidalgo A., Bower J.E., Ganz P.A., Cole S.W., Irwin M.R. Inflammatory biomarkers for persistent fatigue in breast cancer survivors. Clin. Cancer Res. 2006, 12:2759-2766.
18. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-56.
19. Devaraj S., Glaser N., Griffen S., Wang-Polagruto J., Miguelino E., Jialal I. Increased monocytic activity and biomarkers of inflammation in patients with type 1 diabetes. Diabetes 2006, 55:774-779.
20. Devaraj S., Cheung A.T., Jialal I., Griffen S.C., Nguyen D., Glaser N., Aoki T. Evidence of increased inflammation and microcirculatory abnormalities in patients with type 1 diabetes and their role in microvascular complications. Diabetes 2007, 56:2790-2796.
21. Drivsholm T., de Fine Olivarius N., Nielsen A.B., Siersma V. Symptoms, signs and complications in newly diagnosed type 2 diabetic patients, and their relationship to glycaemia, blood pressure and weight. Diabetologia 2005, 48:210-214.
22. Duncan B.B., Schmidt M.I., Pankow J.S., Ballantyne C.M., Couper D., Vigo A., Hoogeveen R., Folsom A.R., Heiss G. Low-grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes 2003, 52:1799-1805.
23. Festa A., D'Agostino R., Tracy R.P., Haffner S.M. Elevated levels of acute-phase proteins and plasminogen activator inhibitor-1 predict the development of type 2 diabetes: the insulin resistance atherosclerosis study. Diabetes 2002, 51:1131-1137.
24. Flachenecker P., Bihler I., Weber F., Gottschalk M., Toyka K.V., Rieckmann P. Cytokine mRNA expression in patients with multiple sclerosis and fatigue. Mult. Scler. 2004, 10:165-169.
25. Fletcher M.A., Zeng X.R., Barnes Z., Levis S., Klimas N.G. Plasma cytokines in women with chronic fatigue syndrome. J. Transl. Med. 2009, 7:96.
26. Fritschi C., Quinn L. Fatigue in patients with diabetes: a review. J. Psychosom. Res. 2010, 69:33-41.
27. Heesen C., Nawrath L., Reich C., Bauer N., Schulz K.H., Gold S.M. Fatigue in multiple sclerosis: an example of cytokine mediated sickness behaviour?. J. Neurol. Neurosurg. Psychiatry 2006, 77:34-39.
28. Hu F.B., Meigs J.B., Li T.Y., Rifai N., Manson J.E. Inflammatory markers and risk of developing type 2 diabetes in women. Diabetes 2004, 53:693-700.
29. Kabir M., Skurnik G., Naour N., Pechtner V., Meugnier E., Rome S., Quignard-Boulange A., Vidal H., Slama G., Clement K., Guerre-Millo M., Rizkalla S.W. Treatment for 2 mo with n 3 polyunsaturated fatty acids reduces adiposity and some atherogenic factors but does not improve insulin sensitivity in women with type 2 diabetes: a randomized controlled study. Am. J. Clin. Nutr. 2007, 86:1670-1679.
30. Kadoglou N.P., Perrea D., Iliadis F., Angelopoulou N., Liapis C., Alevizos M. Exercise reduces resistin and inflammatory cytokines in patients with type 2 diabetes. Diabetes Care 2007, 30:719-721.
31. Kelley K.W., Bluthe R.M., Dantzer R., Zhou J.H., Shen W.H., Johnson R.W., Broussard S.R. Cytokine-induced sickness behavior. Brain Behav. Immun. 2003, 17(Suppl. 1):S112-118.
32. Lasselin, J., Layé, S., Barreau, J.B., Rivet, A., Dulucq, M.J., Gin, H., Capuron, L., 2012. Fatigue and cognitive symptoms in patients with diabetes: relationship with disease phenotype and insulin treatment. Psychoneuroendocrinology. http://dx.doi.org/10.1016/j.psyneuen.2012.01.016.
33. Majer M., Welberg L.A., Capuron L., Pagnoni G., Raison C.L., Miller A.H. IFN-alpha-induced motor slowing is associated with increased depression and fatigue in patients with chronic hepatitis C. Brain Behav. Immun. 2008, 22:870-880.
34. Miller A.H., Ancoli-Israel S., Bower J.E., Capuron L., Irwin M.R. Neuroendocrine-immune mechanisms of behavioral comorbidities in patients with cancer. J. Clin. Oncol. 2008, 26:971-982.
35. Mraz M., Lacinova Z., Drapalova J., Haluzikova D., Horinek A., Matoulek M., Trachta P., Kavalkova P., Svacina S., Haluzik M. The effect of very-low-calorie diet on mRNA expression of inflammation-related genes in subcutaneous adipose tissue and peripheral monocytes of obese patients with type 2 diabetes mellitus. J. Clin. Endocrinol. Metab. 2011, 96:E606-E613.
36. Orre I.J., Murison R., Dahl A.A., Ueland T., Aukrust P., Fossa S.D. Levels of circulating interleukin-1 receptor antagonist and C-reactive protein in long-term survivors of testicular cancer with chronic cancer-related fatigue. Brain Behav. Immun. 2009, 23:868-874.
37. Orre I.J., Reinertsen K.V., Aukrust P., Dahl A.A., Fossa S.D., Ueland T., Murison R. Higher levels of fatigue are associated with higher CRP levels in disease-free breast cancer survivors. J. Psychosom. Res. 2011, 71:136-141.
38. Pedersen M., Bruunsgaard H., Weis N., Hendel H.W., Andreassen B.U., Eldrup E., Dela F., Pedersen B.K. Circulating levels of TNF-alpha and IL-6-relation to truncal fat mass and muscle mass in healthy elderly individuals and in patients with type-2 diabetes. Mech. Ageing Dev. 2003, 124:495-502.
39. Pham M.N., Hawa M.I., Pfleger C., Roden M., Schernthaner G., Pozzilli P., Buzzetti R., Scherbaum W., Seissler J., Kolb H., Hunter S., Leslie R.D., Schloot N.C. Pro- and anti-inflammatory cytokines in latent autoimmune diabetes in adults, type 1 and type 2 diabetes patients: action LADA 4. Diabetologia 2011, 54:1630-1638.
40. Pickup J.C., Chusney G.D., Thomas S.M., Burt D. Plasma interleukin-6, tumour necrosis factor alpha and blood cytokine production in type 2 diabetes. Life Sci. 2000, 67:291-300.
41. Poudyal H., Panchal S.K., Diwan V., Brown L. Omega-3 fatty acids and metabolic syndrome: effects and emerging mechanisms of action. Prog. Lipid Res. 2011, 50:372-387.
42. Preacher K.J., Hayes A.F. Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behav. Res. Methods 2008, 40:879-891.
43. Raison C.L., Lin J.M., Reeves W.C. Association of peripheral inflammatory markers with chronic fatigue in a population-based sample. Brain Behav. Immun. 2009, 23:327-337.
44. Rief W., Mills P.J., Ancoli-Israel S., Ziegler M.G., Pung M.A., Dimsdale J.E. Overnight changes of immune parameters and catecholamines are associated with mood and stress. Psychosom. Med. 2010, 72:755-762.
45. Rocca M.A., Agosta F., Colombo B., Mezzapesa D.M., Falini A., Comi G., Filippi M. FMRI changes in relapsing-remitting multiple sclerosis patients complaining of fatigue after IFNbeta-1a injection. Hum. Brain Mapp. 2007, 28:373-382.
46. Sam S., Haffner S., Davidson M.H., D'Agostino R.B., Feinstein S., Kondos G., Perez A., Mazzone T. Relation of abdominal fat depots to systemic markers of inflammation in type 2 diabetes. Diabetes Care 2009, 32:932-937.
47. Schmidt M.I., Duncan B.B., Sharrett A.R., Lindberg G., Savage P.J., Offenbacher S., Azambuja M.I., Tracy R.P., Heiss G. Markers of inflammation and prediction of diabetes mellitus in adults (Atherosclerosis Risk in Communities study): a cohort study. Lancet 1999, 353:1649-1652.
48. Sheehan, D.V., Lecrubier, Y., Sheehan, K.H., Amorim, P., Janavs, J., Weiller, E., Hergueta, T., Baker, R., Dunbar, G.C., 1998. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J. Clin. Psychiatry 59(Suppl. 20, 22-33), quiz 34-57.
49. Smets E.M., Garssen B., Bonke B., De Haes J.C. The Multidimensional Fatigue Inventory (MFI) psychometric qualities of an instrument to assess fatigue. J. Psychosom. Res. 1995, 39:315-325.
50. Spranger J., Kroke A., Mohlig M., Hoffmann K., Bergmann M.M., Ristow M., Boeing H., Pfeiffer A.F. Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes 2003, 52:812-817.
51. Storlien L.H., Kraegen E.W., Chisholm D.J., Ford G.L., Bruce D.G., Pascoe W.S. Fish oil prevents insulin resistance induced by high-fat feeding in rats. Science 1987, 237:885-888.
52. Su S.C., Pei D., Hsieh C.H., Hsiao F.C., Wu C.Z., Hung Y.J. Circulating pro-inflammatory cytokines and adiponectin in young men with type 2 diabetes. Acta Diabetol. 2011, 48:113-119.
53. Thomas K.S., Motivala S., Olmstead R., Irwin M.R. Sleep depth and fatigue: role of cellular inflammatory activation. Brain Behav. Immun. 2011, 25:53-58.
54. Trayhurn P., Wood I.S. Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br. J. Nutr. 2004, 92:347-355.
55. Treszl A., Szereday L., Doria A., King G.L., Orban T. Elevated C-reactive protein levels do not correspond to autoimmunity in type 1 diabetes. Diabetes Care 2004, 27:2769-2770.
56. Valentine R.J., Woods J.A., McAuley E., Dantzer R., Evans E.M. The associations of adiposity, physical activity and inflammation with fatigue in older adults. Brain Behav. Immun. 2011, 25:1482-1490.
57. Viardot A., Lord R.V., Samaras K. The effects of weight loss and gastric banding on the innate and adaptive immune system in type 2 diabetes and prediabetes. J. Clin. Endocrinol. Metab. 2010, 95:2845-2850.
58. Wellen K.E., Hotamisligil G.S. Obesity-induced inflammatory changes in adipose tissue. J. Clin. Invest. 2003, 112:1785-1788.