Association between serum amyloid A and obesity: A meta-analysis and systematic review

Inflammation Research

Volumn 59, Issue 5, 2010, Pages 323-334

  Zhao, Yulan ^a   He, Xuelian ^b   Shi, Xuegui ^a   Huang, Chengjin ^c   Liu, Jie ^a   Zhou, Shuli ^a   Heng, Chew Kiat ^d  

^a EAST CHINA NORMAL UNIVERSITY   (China)

^b Wuhan Children's Hospital   (China)

^c PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Adipose; BMI; Obesity; Serum amyloid A; Weight loss

Indexed keywords

AMYLOID A PROTEIN; BIOLOGICAL MARKER; C REACTIVE PROTEIN; FIBRINOGEN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PADGEM PROTEIN; PROTEIN PAI 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ATHEROSCLEROSIS; BODY MASS; CARDIOVASCULAR DISEASE; COMPUTER PROGRAM; CORRELATION COEFFICIENT; DIABETES MELLITUS; DISEASE ASSOCIATION; HUMAN; INFLAMMATION; INSULIN RESISTANCE; MEDICAL LITERATURE; OBESITY; PROSPECTIVE STUDY; REVIEW; STATISTICAL ANALYSIS; SYSTEMATIC REVIEW; WEIGHT REDUCTION;

BODY MASS INDEX; CROSS-SECTIONAL STUDIES; DATABASES, FACTUAL; FEMALE; HUMANS; MALE; OBESITY; PROSPECTIVE STUDIES; SERUM AMYLOID A PROTEIN;

EID: 77953362682     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-010-0163-y     Document Type: Review

References (88)

1. Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444:860-867
2. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest. 2005;115:1111-1119
3. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor-necrosis-factor-alpha\direct role in obesity-linked insulin resistance. Science. 1993;259:87-91.
4. Visser M, Bouter LM, McQuillan GM, Wener MH, Harris TB. Elevated C-reactive protein levels in overweight and obese adults. JAMA. 1999;282:2131-2135
5. Wallenius V, Wallenius K, Ahren B, Rudling M, Carlsten H, Dickson SL, et al. Interleukin-6-deficient mice develop mature-onset obesity. Nat Med. 2002;8:75-79
6. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest. 2003;112:1796-1808
7. Xu HY, Barnes GT, Yang Q, Tan Q, Yang DS, Chou CJ, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest. 2003;112:1821-1830
8. Malle E, de Beer FC. Human serum amyloid A (SAA) protein: a prominent acute-phase reactant for clinical practice. Eur J Clin Invest. 1996;26:427-435
9. Gabay C, Kushner I. Mechanisms of disease: acute-phase proteins and other systemic responses to inflammation. N Engl J Med. 1999;340:448-454
10. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epi-demiology\a proposal for reporting. JAMA. 2000;283:2008-2012
11. Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol. 2005;5:13.
12. Kraja AT, Province MA, Arnett D, Wagenknecht L, Tang W, Hopkins PN, et al. Do inflammation and procoagulation bio-markers contribute to the metabolic syndrome cluster? Nutr Metab (Lond). 2007;4:28.
13. Liu J, Young TK, Zinman B, Harris SB, Connelly PW, Hanley AJG. Lifestyle variables, non-traditional cardiovascular risk factors, and the metabolic syndrome in an aboriginal Canadian population. Obesity (Silver Spring). 2006;14:500-508
14. Panagiotakos DB, Pitsavos C, Yannakoulia M, Chrysohoou C, Stefanadis C. The implication of obesity and central fat on markers of chronic inflammation: the ATTICA study. Atherosclerosis. 2005;183:308-315
15. Thorand B, Baumert J, Doring A, Herder C, Kolb H, Rathmann W, et al. Sex differences in the relation of body composition to markers of inflammation. Atherosclerosis. 2006;184:216-224
16. Tannock LR, O'Brien KD, Knopp RH, Retzlaff B, Fish B, Wener MH, et al. Cholesterol feeding increases C-reactive protein and serum amyloid A levels in lean insulin-sensitive subjects. Circulation. 2005;111:3058-3062
17. Poitou C, Viguerie N, Cancello R, De Matteis R, Cinti S, Stich V, et al. Serum amyloid A: production by human white adipocyte and regulation by obesity and nutrition. Diabetologia. 2005;48:519-528
18. Verdaet D, Dendale P, De Bacquer D, Delanghe J, Block P, De Backer G. Association between leisure time physical activity and markers of chronic inflammation related to coronary heart disease. Atherosclerosis. 2004;176:303-310
19. Connelly PW, Hanley AJ, Harris SB, Hegele RA, Zinman B. Relation of waist circumference and glycemic status to C-reactive protein in the Sandy Lake Oji-Cree. Int J Obes Relat Metab Disord. 2003;27:347-354
20. van Dielen FM, van't Veer C, Schols AM, Soeters PB, Buurman WA, Greve JW. Increased leptin concentrations correlate with increased concentrations of inflammatory markers in morbidly obese individuals. Int J Obes Relat Metab Disord. 2001;25:1759-1766
21. Gomez-Ambrosi J, Azcona C, Patino-Garcia A, Fruhbeck G. Serum amyloid A concentration is increased in obese children and adolescents. J Pediatr. 2008;153:71-75
22. Leinonen E, Hurt-Camejo E, Wiklund O, Hulten LM, Hiukka A, Taskinen M-R. Insulin resistance and adiposity correlate with acute-phase reaction and soluble cell adhesion molecules in type 2 diabetes. Atherosclerosis. 2003;166:387-394
23. Catalan V, Gomez-Ambrosi J, Ramirez B, Rotellar F, Pastor C, Silva C, et al. Proinflammatory cytokines in obesity: impact of type 2 diabetes mellitus and gastric bypass. Obes Surg. 2007;17:1464-1474
24. Poitou C, Coupaye M, Laaban J-P, Coussieu C, Bedel JF, Bouillot J-L, et al. Serum amyloid A and obstructive sleep apnea syndrome before and after surgically-induced weight loss in morbidly obese subjects. Obes Surg. 2006;16:1475-1481
25. Poitou C, Coussieu C, Rouault C, Coupaye M, Cancello R, Bedel J-F, et al. Serum amyloid A: a marker of adiposity-induced low-grade inflammation but not of metabolic status. Obesity (Silver Spring). 2006;14:309-318
26. Gomez-Ambrosi J, Salvador J, Rotellar F, Silva C, Catalan V, Rodriguez A, et al. Increased serum amyloid A concentrations in morbid obesity decrease after gastric bypass. Obes Surg. 2006;16:262-269
27. Holdstock C, Lind L, Engstrom BE, Ohrvall M, Sundbom M, Larsson A, et al. CRP reduction following gastric bypass surgery is most pronounced in insulin-sensitive subjects. Int J Obes (Lond). 2005;29:1275-1280
28. Campbell PT, Campbell KL, Wener MH, Wood BL, Potter JD, McTiernan A, et al. A yearlong exercise intervention decreases CRP among obese postmenopausal women. Med Sci Sports Exerc. 2009;41:1533-1539
29. Lappalainen T, Kolehmainen M, Schwab U, Pulkkinen L, Laaksonen DE, Rauramaa R, et al. Serum concentrations and expressions of serum amyloid A and leptin in adipose tissue are interrelated: the Genobin Study. Eur J Endocrinol. 2008;158:333-341
30. Salas-Salvado J, Bullo M, Garcia-Lorda P, Figueredo R, Del Castillo D, Bonada A, et al. Subcutaneous adipose tissue cytokine production is not responsible for the restoration of systemic inflammation markers during weight loss. Int J Obes (Lond). 2006;30:1714-1720
31. O'Brien KD, Brehm BJ, Seeley RJ, Bean J, Wener MH, Daniels S, et al. Diet-induced weight loss is associated with decreases in plasma serum amyloid A and C-reactive protein independent of dietary macronutrient composition in obese subjects. J Clin Endocrinol Metab. 2005;90:2244-2249
32. Danesh J, Muir J, Wong YK, Ward M, Gallimore JR, Pepys MB. Risk factors for coronary heart disease and acute-phase proteins. A population-based study. Eur Heart J. 1999;20:954-959
33. Carter KW, Hung J, Powell BL, Wiltshire S, Foo BTX, Leow YC, et al. Association of interleukin-1 gene polymorphisms with central obesity and metabolic syndrome in a coronary heart disease population. Hum Genet. 2008;124:199-206.
34. Roytblat L, Rachinsky M, Fisher A, Greemberg L, Shapira Y, Doudevani A, et al. Raised interleukin-6 levels in obese patients. Obes Res. 2000;8:673-675
35. Jiao P, Chen Q, Shah S, Du J, Tao B, Tzameli I, et al. Obesity-related upregulation of monocyte chemotactic factors in adipo-cytes involvement of nuclear factor-kappa B and c-Jun NH2-terminal kinase pathways. Diabetes. 2009;58:104-115
36. Chacon MR, Fernandez-Real JM, Richart C, Megia A, Gomez JM, Miranda M, et al. Monocyte chemoattractant protein-1 in obesity and type 2 diabetes. Insulin sensitivity study. Obesity. 2007;15:664-672
37. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa KI, Kitazawa R, et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest. 2006;116:1494-1505
38. Sola E, Vaya A, Espana F, Castello R, Ramon LA, Hernandez-Mijares A, et al. Plasminogen activator inhibitor-1 levels in severe and morbid obesity. Effect of weight loss and influence of 4G/5G polymorphism. Thromb Res. 2008;122:320-327
39. Pou KM, Massaro JM, Hoffmann U, Vasan RS, Maurovich-Horvat P, Larson MG, et al. Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress\the Framingham Heart Study. Circulation. 2007;116:1234-1241
40. Greenfield JR, Samaras K, Jenkins AB, Kelly PJ, Spector TD, Gallimore JR, et al. Obesity is an important determinant of baseline serum C-reactive protein concentration in monozygotic twins, independent of genetic influences. Circulation. 2004;109:3022-3028
41. Madsen EL, Rissanen A, Bruun JM, Skogstrand K, Tonstad S, Hougaard DM, et al. Weight loss larger than 10% is needed for general improvement of levels of circulating adiponectin and markers of inflammation in obese subjects: a 3-year weight loss study. Eur J Endocrinol. 2008;158:179-187
42. Esposito K, Pontillo A, Di Palo C, Giugliano G, Masella M, Marfella R, et al. Effect of weight loss and lifestyle changes on vascular inflammatory markers in obese women\a randomized trial. JAMA. 2003;289:1799-1804
43. Cancello R, Henegar C, Viguerie N, Taleb S, Poitou C, Rouault C, et al. Reduction of macrophage infiltration and chemoattrac-tant gene expression changes in white adipose tissue of morbidly obese subjects after surgery induced weight loss. Diabetes. 2005;54:2277-2286
44. Lee CG, Carr MC, Murdoch SJ, Mitchell E, Woods NF, Wener MH, et al. Adipokines, inflammation, and visceral adiposity across the menopausal transition: a prospective study. J Clin Endocrinol Metab. 2009;94:1104-1110
45. Libby P, Ridker PM. Novel inflammatory markers of coronary risk\theory versus practice. Circulation. 1999;100:1148-1150
46. Ridker PM, Brown NJ, Vaughan DE, Harrison DG, Mehta JL. Established and emerging plasma biomarkers in the prediction of first atherothrombotic events. Circulation. 2004;109:IV6-19.
47. Koh KK, Han SH, Quon MJ. Inflammatory markers and the metabolic syndrome\insights from therapeutic interventions. J Am Coll Cardiol. 2005;46:1978-1985
48. Yang R-Z, Lee M-J, Hu H, Pollin TI, Ryan AS, Nicklas BJ, et al. Acute-phase serum amyloid A: an inflammatory adipokine, potential link between obesity, its metabolic complications. PLoS Med. 2006;3:e287.
49. Liuzzo G, Biasucci LM, Gallimore JR, Grillo RL, Rebuzzi AG, Pepys MB, et al. The prognostic value of C-reactive protein and serum amyloid-A protein in severe unstable angina. N Engl J Med. 1994;331:417-424
50. Meek RL, Urielishoval S, Benditt EP. Expression of apolipo-protein serum amyloid-A messenger-RNA in human atherosclerotic lesions and cultured vascular cells\implications for serum amyloid-A function. Proc Natl Acad Sci USA. 1994;91:3186-3190
51. Kinlay S, Schwartz GG, Olsson AG, Rifai N, Szarek M, Waters DD, et al. Inflammation, statin therapy, and risk of stroke after an acute coronary syndrome in the MIRACL study. Arterioscler Thromb Vasc Biol. 2008;28:142-147
52. Helmersson J, Vessby B, Larsson A, Basu S. Association of type 2 diabetes with cyclooxygenase-mediated inflammation and oxidative stress in an elderly population. Circulation. 2004; 109:1729-1734
53. Scheja L, Heese B, Zitzer H, Michael MD, Siesky AM, Pospisil H, et al. Acute-phase serum amyloid A as a marker of insulin resistance in mice. Exp Diabetes Res. 2008;2008:230837.
54. Jacobs M, van Greevenbroek MMJ, van der Kallen CJH, Ferreira I, Blaak EE, Feskens EJM, et al. Low-grade inflammation can partly explain the association between the metabolic syndrome and either coronary artery disease or severity of peripheral arterial disease: the CODAM study. Eur J Clin Invest. 2009;39:437-444
55. Ridker PM, Hennekens CH, Buring JE, Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med. 2000;342:836-843 (Pubitemid 30165206)
56. Johnson BD, Kip KE, Marroquin OC, Ridker PM, Kelsey SF, Shaw LJ, et al. Serum amyloid A as a predictor of coronary artery disease and cardiovascular outcome in women: the National Heart, Lung, and Blood Institute-Sponsored Women's Ischemia Syndrome Evaluation (WISE). Circulation. 2004;109:726-732
57. Lee KWJ, Hill JS, Walley KR, Frohlich JJ. Relative value of multiple plasma biomarkers as risk factors for coronary artery disease and death in an angiography cohort. CMAJ. 2006;174:461-466
58. Brea D, Sobrino T, Blanco M, Fraga M, Agulla J, Rodriguez-Yanez M, et al. Usefulness of haptoglobin and serum amyloid A proteins as biomarkers for atherothrombotic ischemic stroke diagnosis confirmation. Atherosclerosis. 2009;205:561-567
59. Rallidis LS, Vikelis M, Panagiotakos DB, Rizos I, Zolindaki MG, Kaliva K, et al. Inflammatory markers and in-hospital mortality in acute ischaemic stroke. Atherosclerosis. 2006;189:193-197
60. Wohlin M, Helmersson J, Sundstrom J, Arnlov J, Vessby B, Larsson A, et al. Both cyclooxygenase-and cytokine-mediated inflammation are associated with carotid intima-media thickness. Cytokine. 2007;38:130-136
61. Uurtuya S, Kotani K, Koibuchi H, Taniguchi N, Yamada T. Serum amyloid A protein and carotid intima-media thickness in healthy young subjects. J Atheroscler Thromb. 2009;16:299-300.
62. Maier W, Altwegg LA, Corti R, Gay S, Hersberger M, Maly FE, et al. Inflammatory markers at the site of ruptured plaque in acute myocardial infarction: locally increased interleukin-6 and serum amyloid A but decreased C-reactive protein. Circulation. 2005;111:1355-1361
63. Ley SH, Harris SB, Connelly PW, Mamakeesick M, Gittelsohn J, Hegele RA, et al. Adipokines and incident type 2 diabetes in an aboriginal Canadian corrected population: the Sandy Lake Health and Diabetes Project. Diabetes Care. 2008;31:1410-1415
64. Pitsavos C, Tampourlou M, Panagiotakos DB, Skoumas Y, Chrysohoou C, Nomikos T, et al. Association between low-grade systemic inflammation and type 2 diabetes mellitus among men and women from the ATTICA study. Rev Diabet Stud. 2007;4:98-104.
65. Herder C, Peltonen M, Koenig W, Kraft I, Muller-Scholze S, Martin S, et al. Systemic immune mediators and lifestyle changes in the prevention of type 2 diabetes: results from the Finnish Diabetes Prevention Study. Diabetes. 2006;55:2340-2346 (Pubitemid 44743633)
66. Ebeling P, Teppo AM, Koistinen HA, Viikari J, Ronnemaa T, Nissen M, et al. Troglitazone reduces hyperglycaemia and selectively acute-phase serum proteins in patients with Type II diabetes. Diabetologia. 1999;42:1433-1438
67. Ghanim H, Dhindsa S, Aljada A, Chaudhuri A, Viswanathan P, Dandona P. Low-dose rosiglitazone exerts an antiinflammatory effect with an increase in adiponectin independently of free fatty acid fall and insulin sensitization in obese type 2 diabetics. J Clin Endocrinol Metab. 2006;91:3553-3558
68. Lago F, Dieguez C, Gomez-Reino J, Gualillo O. Adipokines as emerging mediators of immune response and inflammation. Nat Clin Pract Rheumatol. 2007;3:716-724 (Pubitemid 350187017)
69. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol. 2006;6:772-783
70. Berg AH, Scherer PE. Adipose tissue, inflammation, and cardiovascular disease. Circ Res. 2005;96:939-949
71. Lin Y, Rajala MW, Berger JP, Moller DE, Barzilai N, Scherer PE. Hyperglycemia-induced production of acute phase reactants in adipose tissue. J Biol Chem. 2001;276:42077-42083
72. Subramanian S, Han CY, Chiba T, McMillen TS, Wang SA, Haw A III et al. Dietary cholesterol worsens adipose tissue macrophage accumulation and atherosclerosis in obese LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2008; 28:685-691
73. Chiba T, Han CY, Vaisar T, Shimokado K, Kargi A, Chen M-H, et al. Serum amyloid A3 does not contribute to circulating SAA levels. J Lipid Res. 2009;50:1353-1362
74. Lewis KE, Kirk EA, McDonald TO, Wang S, Wight TN, O'Brien KD, et al. Increase in serum amyloid A evoked by dietary cholesterol is associated with increased atherosclerosis in mice. Circulation. 2004;110:540-545
75. Kim F, Pham M, Maloney E, Rizzo NO, Morton GJ, Wisse BE, et al. Vascular inflammation, insulin resistance, and reduced nitric oxide production precede the onset of peripheral insulin resistance. Arterioscler Thromb Vasc Biol. 2008;28:1982-1988
76. Ye XY, Xue YM, Sha JP, Li CZ, Zhen ZJ. Serum amyloid A attenuates cellular insulin sensitivity by increasing JNK activity in 3T3-L1 adipocytes. J Endocrinol Invest. 2009;32:568-575
77. Arner P. Control of lipolysis and its relevance to development of obesity in man. Diabetes Metab Rev. 1988;4:507-515
78. Chen CH, Wang PH, Liu BH, Hsu HH, Mersmann HJ, Ding ST. Serum amyloid A protein regulates the expression of porcine genes related to lipid metabolism. J Nutr. 2008;138:674-679
79. Marx N, Froehlich J, Siam L, Ittner J, Wierse G, Schmidt A, et al. Antidiabetic PPAR gamma-activator rosiglitazone reduces MMP-9 serum levels in type 2 diabetic patients with coronary artery disease. Arterioscler Thromb Vasc Biol. 2003;23:283-288
80. Hetzel J, Balletshofer B, Rittig K, Walcher D, Kratzer W, Hombach V, et al. Rapid effects of rosiglitazone treatment on endothelial function and inflammatory biomarkers. Arterioscler Thromb Vasc Biol. 2005;25:1804-1809
81. Mohanty P, Aljada A, Ghanim H, Hofmeyer D, Tripathy D, Syed T, et al. Evidence for a potent antiinflammatory effect of rosig-litazone. J Clin Endocrinol Metab. 2004;89:2728-2735
82. Chaudhuri A, Janicke D, Wilson MF, Tripathy D, Garg R, Ban-dyopadhyay A et al. Anti-inflammatory and profibrinolytic effect of insulin in acute ST-segment-elevation myocardial infarction. Circulation. 2004;109:849-854
83. Zadelaar ASM, Boesten LSM, Jukema JW, van Vlijmen BJM, Kooistra T, Emeis JJ, et al. Dual PPARalpha/gamma agonist te-saglitazar reduces atherosclerosis in insulin-resistant and hypercholesterolemic ApoE*3Leiden mice. Arterioscler Thromb Vasc Biol. 2006;26:2560-2566
84. Kinlay S, Schwartz GG, Olsson AG, Rifai N, Leslie SJ, Sasiela WJ, et al. High-dose atorvastatin enhances the decline in inflammatory markers in patients with acute coronary syndromes in the MIRACL study. Circulation. 2003;108:1560-1566
85. Schillinger M, Exner M, Mlekusch W, Amighi J, Sabeti S, Muellner M, et al. Statin therapy improves cardiovascular outcome of patients with peripheral artery disease. Eur Heart J. 2004; 25:742-748
86. Kleemann R, Princen HMG, Emeis JJ, Jukema JW, Fontijn RD, Horrevoets AJG, et al. Rosuvastatin reduces atherosclerosis development beyond and independent of its plasma cholesterol-lowering effect in APOE*3-Leiden transgenic mice: evidence for antiinflammatory effects of rosuvastatin. Circulation. 2003;108: 1368-1374
87. Verschuren L, Kleemann R, Offerman EH, Szalai AJ, Emeis SJ, Princen HMG, et al. Effect of low dose atorvastatin versus diet-induced cholesterol lowering on atherosclerotic lesion progression and inflammation in apolipoprotein E*3-Leiden transgenic mice. Arterioscler Thromb Vasc Biol. 2005;25:161-167
88. Derosa G, Tinelli C, Maffioli P. Effects of pioglitazone and rosiglitazone combined with metformin on body weight in people with diabetes. Diabetes Obes Metab. 2009;11:1091-1099