Fibroblast growth factor-23 and incident coronary heart disease, heart failure, and cardiovascular mortality: The atherosclerosis risk in communities study

Journal of the American Heart Association

Volumn 3, Issue 3, 2014, Pages

  Lutsey, Pamela L ^a   Alonso, Alvaro ^a   Selvin, Elizabeth ^c   Pankow, James S ^a   Michos, Erin D ^c   Agarwal, Sunil K ^c   Loehr, Laura R ^d   Eckfeldt, John H ^b   Coresh, Josef ^c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d IL   (United States)

Author keywords

Atherosclerosis Risk In Communities; Cardiovascular mortality; Coronary heart disease; Epidemiology; Fibroblast growth factor 23; Heart failure

Indexed keywords

FIBROBLAST GROWTH FACTOR 23; FIBROBLAST GROWTH FACTOR;

ADULT; AGE DISTRIBUTION; ARTICLE; ATHEROSCLEROSIS; CARDIOVASCULAR MORTALITY; CARDIOVASCULAR RISK; COHORT ANALYSIS; COMMUNITY ASSESSMENT; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FOLLOW UP; HEART FAILURE; HUMAN; HYPERTENSION; INCIDENCE; ISCHEMIC HEART DISEASE; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; OUTCOME ASSESSMENT; POPULATION RESEARCH; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RISK ASSESSMENT; UPREGULATION; BLOOD; CARDIOVASCULAR DISEASE; CORONARY DISEASE; MORTALITY; PROPORTIONAL HAZARDS MODEL; PROSPECTIVE STUDY; RISK FACTOR; UNITED STATES;

CARDIOVASCULAR DISEASES; CORONARY DISEASE; FEMALE; FIBROBLAST GROWTH FACTORS; HEART FAILURE; HUMANS; INCIDENCE; MALE; MIDDLE AGED; PROPORTIONAL HAZARDS MODELS; PROSPECTIVE STUDIES; RISK FACTORS; UNITED STATES;

EID: 84922286250     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.114.000936     Document Type: Article

References (51)

1. Shimada T, Hasegawa H, Yamazaki Y, Muto T, Hino R, Takeuchi Y, Fujita T, Nakahara K, Fukumoto S, Yamashita T. FGF-23 is a potent regulator of vitamin D metabolism and phosphate homeostasis. J Bone Miner Res. 2004;19:429-435.
2. Wolf M. Update on fibroblast growth factor 23 in chronic kidney disease. Kidney Int. 2012;82:737-747.
3. Heine GH, Seiler S, Fliser D. FGF-23: the rise of a novel cardiovascular risk marker in CKD. Nephrol Dial Transplant. 2012;27:3072-3081.
4. Shigematsu T, Kazama JJ, Yamashita T, Fukumoto S, Hosoya T, Gejyo F, Fukagawa M. Possible involvement of circulating fibroblast growth factor 23 in the development of secondary hyperparathyroidism associated with renal insufficiency. Am J Kidney Dis. 2004;44:250-256.
5. Gutierrez O, Isakova T, Rhee E, Shah A, Holmes J, Collerone G, Juppner H, Wolf M. Fibroblast growth factor-23 mitigates hyperphosphatemia but accentuates calcitriol deficiency in chronic kidney disease. J Am Soc Nephrol. 2005; 16:2205-2215.
6. Fliser D, Kollerits B, Neyer U, Ankerst DP, Lhotta K, Lingenhel A, Ritz E, Kronenberg F; for the MSG. Fibroblast growth factor 23 (FGF-23) predicts progression of chronic kidney disease: the Mild to Moderate Kidney Disease (MMKD) Study. J Am Soc Nephrol. 2007;18:2600-2608.
7. Gutierrez OM, Mannstadt M, Isakova T, Rauh-Hain JA, Tamez H, Shah A, Smith K, Lee H, Thadhani R, Juppner H, Wolf M. Fibroblast growth factor 23 and mortality among patients undergoing hemodialysis. N Engl J Med. 2008; 359:584-592.
8. Isakova T, Xie H, Yang W, Xie D, Anderson AH, Scialla J, Wahl P, Gutierrez OM, Steigerwalt S, He J, Schwartz S, Lo J, Ojo A, Sondheimer J, Hsu CY, Lash J, Leonard M, Kusek JW, Feldman HI, Wolf M. Fibroblast growth factor 23 and risks of mortality and end-stage renal disease in patients with chronic kidney disease. JAMA. 2011;305:2432-2439.
9. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu C-Y. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med. 2004;351:1296-1305.
10. Wang L, Song Y, Manson JE, Pilz S, März W, Michaëlsson K, Lundqvist A, Jassal SK, Barrett-Connor E, Zhang C, Eaton CB, May HT, Anderson JL, Sesso HD. Circulating 25-hydroxy-vitamin D and risk of cardiovascular disease: a metaanalysis of prospective studies. Circ Cardiovasc Qual Outcomes. 2012;5: 819-829.
11. Faul C, Amaral AP, Oskouei B, Hu M-C, Sloan A, Isakova T, Gutiérrez OM, Aguillon-Prada R, Lincoln J, Hare JM, Mundel P, Morales A, Scialla J, Fischer M, Soliman EZ, Chen J, Go AS, Rosas SE, Nessel L, Townsend RR, Feldman HI, St. John Sutton M, Ojo A, Gadegbeku C, Di Marco GS, Reuter S, Kentrup D, Tiemann K, Brand M, Hill JA, Moe OW, Kuro-o M, Kusek JW, Keane MG, Wolf M. FGF-23 induces left ventricular hypertrophy. J Clin Invest. 2011;121:4393-4408.
12. Desai CS, Ning H, Lloyd-Jones DM. Competing cardiovascular outcomes associated with electrocardiographic left ventricular hypertrophy: the Atherosclerosis Risk in Communities Study. Heart. 2012;98:330-334.
13. Scialla JJ, Xie H, Rahman M, Anderson AH, Isakova T, Ojo A, Zhang X, Nessel L, Hamano T, Grunwald JE, Raj DS, Yang W, He J, Lash JP, Go AS, Kusek JW, Feldman H, Wolf M; Investigators tCRICS. Fibroblast growth factor-23 and cardiovascular events in CKD. J Am Soc Nephrol. 2014;25:349-360.
14. Kendrick J, Cheung AK, Kaufman JS, Greene T, Roberts WL, Smits G, Chonchol M; Investigators tH. FGF-23 associates with death, cardiovascular events, and initiation of chronic dialysis. J Am Soc Nephrol. 2011;22:1913-1922.
15. Seiler S, Reichart B, Roth D, Seibert E, Fliser D, Heine GH. FGF-23 and future cardiovascular events in patients with chronic kidney disease before initiation of dialysis treatment. Nephrol Dial Transplant. 2010;25:3983-3989.
16. Nakano C, Hamano T, Fujii N, Obi Y, Matsui I, Tomida K, Mikami S, Inoue K, Shimomura A, Nagasawa Y, Okada N, Tsubakihara Y, Rakugi H, Isaka Y. Intact fibroblast growth factor 23 levels predict incident cardiovascular event before but not after the start of dialysis. Bone. 2012;50:1266-1274.
17. Parker BD, Schurgers LJ, Brandenburg VM, Christenson RH, Vermeer C, Ketteler M, Shlipak MG, Whooley MA, Ix JH. The associations of fibroblast growth factor 23 and uncarboxylated matrix Gla protein with mortality in coronary artery disease: the Heart and Soul Study. Ann Intern Med. 2010;152:640-648.
18. Ix JH, Katz R, Kestenbaum BR, de Boer IH, Chonchol M, Mukamal KJ, Rifkin D, Siscovick DS, Sarnak MJ, Shlipak MG. Fibroblast growth factor-23 and death, heart failure, and cardiovascular events in community-living individuals: CHS (Cardiovascular Health Study). J Am Coll Cardiol. 2012;60:200-207.
19. Arnlov J, Carlsson AC, Sundstrom J, Ingelsson E, Larsson A, Lind L, Larsson TE. Higher fibroblast growth factor-23 increases the risk of all-cause and cardiovascular mortality in the community. Kidney Int. 2013;83:160-166.
20. The ARIC I. The Atherosclerosis Risk in Communities (ARIC) Study: design and objectives. Am J Epidemiol. 1989;129:687-702.
21. Baecke JB, Burema J, Frijters JER. A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr. 1982 ;36:936-942.
22. Machado DB, Crow RS, Boland LL, Hannan PJ, Taylor HA Jr, Folsom AR. Electrocardiographic findings and incident coronary heart disease among participants in the Atherosclerosis Risk in Communities (ARIC) study. Am J Cardiol. 2006;97:1176-1181.e1173.
23. Siedel J, Hagele EO, Ziegenhorn J, Wahlefeld AW. Reagent for the enzymatic determination of serum total cholesterol with improved lipolytic efficiency. Clin Chem. 1983;29:1075-1080.
24. Nagele U, Hagele EO, Sauer G, Wiedemann E, Lehmann P, Wahlefeld AW, Gruber W. Reagent for the enzymatic determination of serum total triglycerides with improved lipolytic efficiency. J Clin Chem Clin Biochem. 1984;22: 165-174.
25. Warnick GR, Benderson J, Albers JJ. Dextran sulfate-Mg2+ precipitation procedure for quantitation of high-density-lipoprotein cholesterol. Clin Chem. 1982;28:1379-1388.
26. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18:499-502.
27. Inker LA, Schmid CH, Tighiouart H, Eckfeldt JH, Feldman HI, Greene T, Kusek JW, Manzi J, Van Lente F, Zhang YL, Coresh J, Levey AS. Estimating glomerular filtration rate from serum creatinine and cystatin C. N Engl J Med. 2012;367: 20-29.
28. Eriksson H, Caidaul K, Larsson B, Ohlson L-O, Welin L, Wilhelmsen L, Svardsudd K. Cardiac and pulmonary causes of dyspnoea-validation of a scoring test for clinical-epidemiological use: the Study of Men Born in 1913. Eur Heart J. 1987;8:1007-1014.
29. Loehr LR, Rosamond WD, Chang PP, Folsom AR, Chambless LE. Heart failure incidence and survival (from the Atherosclerosis Risk in Communities Study). Am J Cardiol. 2008;101:1016-1022.
30. Folsom AR, Yatsuya H, Nettleton JA, Lutsey PL, Cushman M, Rosamond WD. Community prevalence of ideal cardiovascular health, by the American Heart Association definition, and relationship with cardiovascular disease incidence. J Am Coll Cardiol. 2011;57:1690-1696.
31. Mirza MA, Larsson A, Melhus H, Lind L, Larsson TE. Serum intact FGF-23 associate with left ventricular mass, hypertrophy and geometry in an elderly population. Atherosclerosis. 2009;207:546-551.
32. Gutierrez OM, Januzzi JL, Isakova T, Laliberte K, Smith K, Collerone G, Sarwar A, Hoffmann U, Coglianese E, Christenson R, Wang TJ, deFilippi C, Wolf M. Fibroblast growth factor 23 and left ventricular hypertrophy in chronic kidney disease. Circulation. 2009;119:2545-2552.
33. Stevens K, McQuarrie E, Sands W, Hillyard D, Patel R, Mark P, Jardine A. Fibroblast growth factor 23 predicts left ventricular mass and induces cell adhesion molecule formation. Int J Nephrol. 2011;2011:297070.
34. Mirza MA, Larsson A, Lind L, Larsson TE. Circulating fibroblast growth factor-23 is associated with vascular dysfunction in the community. Atherosclerosis. 2009;205:385-390.
35. Yilmaz MI, Sonmez A, Saglam M, Yaman H, Kilic S, Demirkaya E, Eyileten T, Caglar K, Oguz Y, Vural A, Yenicesu M, Zoccali C. FGF-23 and vascular dysfunction in patients with stage 3 and 4 chronic kidney disease. Kidney Int. 2010;78:679-685.
36. Manghat P, Fraser WD, Wierzbicki AS, Fogelman I, Goldsmith DJ, Hampson G. Fibroblast growth factor-23 is associated with C-reactive protein, serum phosphate and bone mineral density in chronic kidney disease. Osteoporos Int. 2010;21:1853-1861.
37. Munoz Mendoza J, Isakova T, Ricardo AC, Xie H, Navaneethan SD, Anderson AH, Bazzano LA, Xie D, Kretzler M, Nessel L, Hamm LL, Negrea L, Leonard MB, Raj D, Wolf M; Cohort ftCRI. Fibroblast growth factor 23 and inflammation in CKD. Clin J Am Soc Nephrol. 2012;7:1155-1162.
38. Foley RN, Collins AJ, Herzog CA, Ishani A, Kalra PA. Serum phosphorus levels associate with coronary atherosclerosis in young adults. J Am Soc Nephrol. 2009;20:397-404.
39. Amann K, Tornig J, Kugel B, Gross M-L, Tyralla K, El-Shakmak A, Szabo A, Ritz E. Hyperphosphatemia aggravates cardiac fibrosis and microvascular disease in experimental uremia. Kidney Int. 2003;63:1296-1301.
40. Foley RN, Collins AJ, Herzog CA, Ishani A, Kalra PA. Serum phosphate and left ventricular hypertrophy in young adults: the coronary artery risk development in young adults study. Kidney Blood Press Res. 2009;32:37-44.
41. Foley RN, Collins AJ, Ishani A, Kalra PA. Calcium-phosphate levels and cardiovascular disease in community-dwelling adults: the Atherosclerosis Risk in Communities (ARIC) Study. Am Heart J. 2008;156:556-563.
42. Tonelli M, Sacks F, Pfeffer M, Gao Z, Curhan G. Relation between serum phosphate level and cardiovascular event rate in people with coronary disease. Circulation. 2005;112:2627-2633.
43. Dhingra R, Sullivan LM, Fox CS, Wang TJ, D'Agostino RB Sr, Gaziano JM, Vasan RS. Relations of serum phosphorus and calcium levels to the incidence of cardiovascular disease in the community. Arch Intern Med. 2007;167:879-885.
44. Dhingra R, Gona P, Benjamin EJ, Wang TJ, Aragam J, D'Agostino RB, Kannel WB, Vasan RS. Relations of serum phosphorus levels to echocardiographic left ventricular mass and incidence of heart failure in the community. Eur J Heart Fail. 2010;12:812-818.
45. Lopez FL, Agarwal SK, Grams ME, Loehr LR, Soliman EZ, Lutsey PL, Chen LY, Huxley RR, Alonso A. Relation of serum phosphorus levels to the incidence of atrial fibrillation (from the Atherosclerosis Risk in Communities [ARIC] Study). Am J Cardiol. 2013;111:857-862.
46. Isakova T, Wahl P, Vargas GS, Gutierrez OM, Scialla J, Xie H, Appleby D, Nessel L, Bellovich K, Chen J, Hamm L, Gadegbeku C, Horwitz E, Townsend RR, Anderson CAM, Lash JP, Hsu C-Y, Leonard MB, Wolf M. Fibroblast growth factor 23 is elevated before parathyroid hormone and phosphate in chronic kidney disease. Kidney Int. 2011;79:1370-1378.
47. Taylor EN, Rimm EB, Stampfer MJ, Curhan GC. Plasma fibroblast growth factor 23, parathyroid hormone, phosphorus, and risk of coronary heart disease. Am Heart J. 2011;161:956-962.
48. Koiwa F, Kazama JJ, Tokumoto A, Onoda N, Kato H, Okada T, Nii-Kono T, Fukagawa M, Shigematsu T; Group RODCR. Sevelamer hydrochloride and calcium bicarbonate reduce serum fibroblast growth factor 23 levels in dialysis patients. Ther Apher Dial. 2005;9:336-339.
49. Nagano N, Miyata S, Abe M, Kobayashi N, Wakita S, Yamashita T, Wada M. Effect of manipulating serum phosphorus with phosphate binder on circulating PTH and FGF-23 in renal failure rats. Kidney Int. 2006;69:531-537.
50. Clarke R, Shipley M, Lewington S, Youngman L, Collins R, Marmot M, Peto R. Underestimation of risk associations due to regression dilution in longterm follow-up of prospective studies. Am J Epidemiol. 1999;150:341-353.
51. Rosamond WD, Chang PP, Baggett C, Johnson A, Bertoni AG, Shahar E, Deswal A, Heiss G, Chambless LE. Classification of heart failure in the Atherosclerosis Risk in Communities (ARIC) Study: a comparison of diagnostic criteria. Circ Heart Fail. 2012;5:152-159.