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Published in: BMC Nephrology 1/2014

Open Access 01-12-2014 | Research article

Low serum calcium is associated with poor renal outcomes in chronic kidney disease stages 3–4 patients

Authors: Lee-Moay Lim, Hung-Tien Kuo, Mei-Chuan Kuo, Yi-Wen Chiu, Jia-Jung Lee, Shang-Jyh Hwang, Jer-Chia Tsai, Chi-Chih Hung, Hung-Chun Chen

Published in: BMC Nephrology | Issue 1/2014

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Abstract

Background

Mineral disorders are associated with adverse renal outcomes in chronic kidney disease (CKD) patients. Previous studies have associated hypercalcemia and hypocalcemia with mortality; however, the association between serum calcium and renal outcome is not well-described. Whether adding calcium besides phosphorus or in the form of calcium-phosphorus (Ca × P) product into the model of survival analysis could improve the prediction of renal outcomes is not known.

Methods

A prospective cohort of 2144 outpatients with CKD stages 3–4 was evaluated. Cox proportional hazard analysis was performed according to calcium quartiles.

Results

The mean calcium level was 9.2 ± 0.7 mg/dL. Low serum calcium (<9.0 mg/dL) was associated with increased risk of requiring renal replacement therapy (RRT) (hazards ratio [HR]:2.12 (95% CI: 1.49–3.02, P <0.05) and rapid renal function progression (odds ratio [OR]: 1.65 (95% CI: 1.19–2.27, P <0.05) compared with high serum calcium (>9.8 mg/dL). Adding calcium into the survival model increased the integrated discrimination improvement by 0.80% (0.12% – 1.91%) while calcium-phosphorus product did not improve risk prediction.
The combination of high serum phosphorus (>4.2 mg/dL) and low serum calcium (<9.1 mg/dL) was associated with the highest risk of RRT (HR:2.31 (95% CI: 1.45–3.67, P < 0.05).

Conclusion

Low serum calcium is associated with increased risk of RRT and rapid renal function progression in CKD stage 3–4 patients. The integration of serum calcium and phosphorus, but not calcium-phosphorus product should be considered in a predictive model of renal outcome.
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Literature
1.
go back to reference Kovesdy CP, Kalantar-Zadeh K: Bone and mineral disorders in pre-dialysis CKD. Int Urol Nephrol. 2008, 40 (2): 427-440. 10.1007/s11255-008-9346-7.CrossRefPubMed Kovesdy CP, Kalantar-Zadeh K: Bone and mineral disorders in pre-dialysis CKD. Int Urol Nephrol. 2008, 40 (2): 427-440. 10.1007/s11255-008-9346-7.CrossRefPubMed
2.
go back to reference Schwarz S, Trivedi BK, Kalantar-Zadeh K, Kovesdy CP: Association of disorders in mineral metabolism with progression of chronic kidney disease. Clin J Am Soc Nephrol. 2006, 1 (4): 825-831. 10.2215/CJN.02101205.CrossRefPubMed Schwarz S, Trivedi BK, Kalantar-Zadeh K, Kovesdy CP: Association of disorders in mineral metabolism with progression of chronic kidney disease. Clin J Am Soc Nephrol. 2006, 1 (4): 825-831. 10.2215/CJN.02101205.CrossRefPubMed
3.
go back to reference Menon V, Greene T, Pereira AA, Wang X, Beck GJ, Kusek JW, Collins AJ, Levey AS, Sarnak MJ: Relationship of phosphorus and calcium-phosphorus product with mortality in CKD. Am J Kidney Dis. 2005, 46 (3): 455-463. 10.1053/j.ajkd.2005.05.025.CrossRefPubMed Menon V, Greene T, Pereira AA, Wang X, Beck GJ, Kusek JW, Collins AJ, Levey AS, Sarnak MJ: Relationship of phosphorus and calcium-phosphorus product with mortality in CKD. Am J Kidney Dis. 2005, 46 (3): 455-463. 10.1053/j.ajkd.2005.05.025.CrossRefPubMed
4.
go back to reference Bellasi A, Mandreoli M, Baldrati L, Corradini M, Di Nicolo P, Malmusi G, Santoro A: Chronic kidney disease progression and outcome according to serum phosphorus in mild-to-moderate kidney dysfunction. Clin J Am Soc Nephrol. 2011, 6 (4): 883-891. 10.2215/CJN.07810910.CrossRefPubMedPubMedCentral Bellasi A, Mandreoli M, Baldrati L, Corradini M, Di Nicolo P, Malmusi G, Santoro A: Chronic kidney disease progression and outcome according to serum phosphorus in mild-to-moderate kidney dysfunction. Clin J Am Soc Nephrol. 2011, 6 (4): 883-891. 10.2215/CJN.07810910.CrossRefPubMedPubMedCentral
5.
go back to reference Voormolen N, Noordzij M, Grootendorst DC, Beetz I, Sijpkens YW, van Manen JG, Boeschoten EW, Huisman RM, Krediet RT, Dekker FW: High plasma phosphate as a risk factor for decline in renal function and mortality in pre-dialysis patients. Nephrol Dial Transplant. 2007, 22 (10): 2909-2916. 10.1093/ndt/gfm286.CrossRefPubMed Voormolen N, Noordzij M, Grootendorst DC, Beetz I, Sijpkens YW, van Manen JG, Boeschoten EW, Huisman RM, Krediet RT, Dekker FW: High plasma phosphate as a risk factor for decline in renal function and mortality in pre-dialysis patients. Nephrol Dial Transplant. 2007, 22 (10): 2909-2916. 10.1093/ndt/gfm286.CrossRefPubMed
6.
go back to reference Norris KC, Greene T, Kopple J, Lea J, Lewis J, Lipkowitz M, Miller P, Richardson A, Rostand S, Wang X, Appel LJ: Baseline predictors of renal disease progression in the African American Study of Hypertension and Kidney Disease. J Am Soc Nephrol. 2006, 17 (10): 2928-2936. 10.1681/ASN.2005101101.CrossRefPubMed Norris KC, Greene T, Kopple J, Lea J, Lewis J, Lipkowitz M, Miller P, Richardson A, Rostand S, Wang X, Appel LJ: Baseline predictors of renal disease progression in the African American Study of Hypertension and Kidney Disease. J Am Soc Nephrol. 2006, 17 (10): 2928-2936. 10.1681/ASN.2005101101.CrossRefPubMed
7.
go back to reference Ravani P, Malberti F, Tripepi G, Pecchini P, Cutrupi S, Pizzini P, Mallamaci F, Zoccali C: Vitamin D levels and patient outcome in chronic kidney disease. Kidney Int. 2009, 75 (1): 88-95. 10.1038/ki.2008.501.CrossRefPubMed Ravani P, Malberti F, Tripepi G, Pecchini P, Cutrupi S, Pizzini P, Mallamaci F, Zoccali C: Vitamin D levels and patient outcome in chronic kidney disease. Kidney Int. 2009, 75 (1): 88-95. 10.1038/ki.2008.501.CrossRefPubMed
8.
go back to reference Kendrick J, Cheung AK, Kaufman JS, Greene T, Roberts WL, Smits G, Chonchol M: Associations of plasma 25-hydroxyvitamin D and 1,25-dihydroxyvitamin D concentrations with death and progression to maintenance dialysis in patients with advanced kidney disease. Am J Kidney Dis. 2012, 60 (4): 567-575. 10.1053/j.ajkd.2012.04.014.CrossRefPubMedPubMedCentral Kendrick J, Cheung AK, Kaufman JS, Greene T, Roberts WL, Smits G, Chonchol M: Associations of plasma 25-hydroxyvitamin D and 1,25-dihydroxyvitamin D concentrations with death and progression to maintenance dialysis in patients with advanced kidney disease. Am J Kidney Dis. 2012, 60 (4): 567-575. 10.1053/j.ajkd.2012.04.014.CrossRefPubMedPubMedCentral
9.
go back to reference Ferro CJ, Chue CD, Steeds RP, Townend JN: Is lowering phosphate exposure the key to preventing arterial stiffening with age?. Heart. 2009, 95 (21): 1770-1772. 10.1136/hrt.2008.162594.CrossRefPubMed Ferro CJ, Chue CD, Steeds RP, Townend JN: Is lowering phosphate exposure the key to preventing arterial stiffening with age?. Heart. 2009, 95 (21): 1770-1772. 10.1136/hrt.2008.162594.CrossRefPubMed
10.
go back to reference Moe SM, Chen NX: Pathophysiology of vascular calcification in chronic kidney disease. Circ Res. 2004, 95 (6): 560-567. 10.1161/01.RES.0000141775.67189.98.CrossRefPubMed Moe SM, Chen NX: Pathophysiology of vascular calcification in chronic kidney disease. Circ Res. 2004, 95 (6): 560-567. 10.1161/01.RES.0000141775.67189.98.CrossRefPubMed
11.
go back to reference Young EW, Humes HD: Calcium and acute renal failure. Miner Electrolyte Metab. 1991, 17 (2): 106-111.PubMed Young EW, Humes HD: Calcium and acute renal failure. Miner Electrolyte Metab. 1991, 17 (2): 106-111.PubMed
12.
go back to reference Moyses-Neto M, Guimaraes FM, Ayoub FH, Vieira-Neto OM, Costa JA, Dantas M: Acute renal failure and hypercalcemia. Ren Fail. 2006, 28 (2): 153-159. 10.1080/08860220500531005.CrossRefPubMed Moyses-Neto M, Guimaraes FM, Ayoub FH, Vieira-Neto OM, Costa JA, Dantas M: Acute renal failure and hypercalcemia. Ren Fail. 2006, 28 (2): 153-159. 10.1080/08860220500531005.CrossRefPubMed
13.
go back to reference Hurley K, Baggs D: Hypocalcemic cardiac failure in the emergency department. J Emerg Med. 2005, 28 (2): 155-159. 10.1016/j.jemermed.2004.06.014.CrossRefPubMed Hurley K, Baggs D: Hypocalcemic cardiac failure in the emergency department. J Emerg Med. 2005, 28 (2): 155-159. 10.1016/j.jemermed.2004.06.014.CrossRefPubMed
14.
go back to reference Kazmi AS, Wall BM: Reversible congestive heart failure related to profound hypocalcemia secondary to hypoparathyroidism. Am J Med Sci. 2007, 333 (4): 226-229. 10.1097/MAJ.0b013e318039b9c6.CrossRefPubMed Kazmi AS, Wall BM: Reversible congestive heart failure related to profound hypocalcemia secondary to hypoparathyroidism. Am J Med Sci. 2007, 333 (4): 226-229. 10.1097/MAJ.0b013e318039b9c6.CrossRefPubMed
15.
go back to reference National Kidney Foundation: K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am J Kidney Dis. 2002, 39 (2 Suppl 1): S1-S266. National Kidney Foundation: K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am J Kidney Dis. 2002, 39 (2 Suppl 1): S1-S266.
16.
go back to reference Payne RB, Little AJ, Williams RB, Milner JR: Interpretation of serum calcium in patients with abnormal serum proteins. Br Med J. 1973, 4 (5893): 643-646. 10.1136/bmj.4.5893.643.CrossRefPubMedPubMedCentral Payne RB, Little AJ, Williams RB, Milner JR: Interpretation of serum calcium in patients with abnormal serum proteins. Br Med J. 1973, 4 (5893): 643-646. 10.1136/bmj.4.5893.643.CrossRefPubMedPubMedCentral
17.
go back to reference Devereux RB: Detection of left ventricular hypertrophy by M-mode echocardiography: anatomic validation, standardization, and comparison to other methods. Hypertension. 1987, 9 (2 Pt 2): II19-II26.PubMed Devereux RB: Detection of left ventricular hypertrophy by M-mode echocardiography: anatomic validation, standardization, and comparison to other methods. Hypertension. 1987, 9 (2 Pt 2): II19-II26.PubMed
18.
go back to reference Pencina MJ, D’Agostino RB, D’Agostino RB, Vasan RS: Evaluating the added predictive ability of a new marker: from area under the ROC curve to reclassification and beyond. Stat Med. 2008, 27 (2): 157-172. 10.1002/sim.2929. discussion 207–112CrossRefPubMed Pencina MJ, D’Agostino RB, D’Agostino RB, Vasan RS: Evaluating the added predictive ability of a new marker: from area under the ROC curve to reclassification and beyond. Stat Med. 2008, 27 (2): 157-172. 10.1002/sim.2929. discussion 207–112CrossRefPubMed
19.
go back to reference Eddington H, Kalra PA: The association of chronic kidney disease-mineral bone disorder and cardiovascular risk. J Ren Care. 2010, 36 (Suppl 1): 61-67.CrossRefPubMed Eddington H, Kalra PA: The association of chronic kidney disease-mineral bone disorder and cardiovascular risk. J Ren Care. 2010, 36 (Suppl 1): 61-67.CrossRefPubMed
20.
go back to reference Fliser D, Kollerits B, Neyer U, Ankerst DP, Lhotta K, Lingenhel A, Ritz E, Kronenberg F, Kuen E, Konig P, Kraatz G, Mann JF, Muller GA, Kohler H, Riegler P: Fibroblast growth factor 23 (FGF23) predicts progression of chronic kidney disease: the Mild to Moderate Kidney Disease (MMKD) Study. J Am Soc Nephrol. 2007, 18 (9): 2600-2608. 10.1681/ASN.2006080936.CrossRefPubMed Fliser D, Kollerits B, Neyer U, Ankerst DP, Lhotta K, Lingenhel A, Ritz E, Kronenberg F, Kuen E, Konig P, Kraatz G, Mann JF, Muller GA, Kohler H, Riegler P: Fibroblast growth factor 23 (FGF23) predicts progression of chronic kidney disease: the Mild to Moderate Kidney Disease (MMKD) Study. J Am Soc Nephrol. 2007, 18 (9): 2600-2608. 10.1681/ASN.2006080936.CrossRefPubMed
21.
go back to reference Lundberg S, Qureshi AR, Olivecrona S, Gunnarsson I, Jacobson SH, Larsson TE: FGF23, albuminuria, and disease progression in patients with chronic IgA nephropathy. Clin J Am Soc Nephrol. 2012, 7 (5): 727-734. 10.2215/CJN.10331011.CrossRefPubMedPubMedCentral Lundberg S, Qureshi AR, Olivecrona S, Gunnarsson I, Jacobson SH, Larsson TE: FGF23, albuminuria, and disease progression in patients with chronic IgA nephropathy. Clin J Am Soc Nephrol. 2012, 7 (5): 727-734. 10.2215/CJN.10331011.CrossRefPubMedPubMedCentral
22.
go back to reference Titan SM, Zatz R, Graciolli FG, dos Reis LM, Barros RT, Jorgetti V, Moyses RM: FGF-23 as a predictor of renal outcome in diabetic nephropathy. Clin J Am Soc Nephrol. 2011, 6 (2): 241-247. 10.2215/CJN.04250510.CrossRefPubMedPubMedCentral Titan SM, Zatz R, Graciolli FG, dos Reis LM, Barros RT, Jorgetti V, Moyses RM: FGF-23 as a predictor of renal outcome in diabetic nephropathy. Clin J Am Soc Nephrol. 2011, 6 (2): 241-247. 10.2215/CJN.04250510.CrossRefPubMedPubMedCentral
23.
go back to reference 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 (23): 2432-2439. 10.1001/jama.2011.826.CrossRefPubMedPubMedCentral 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 (23): 2432-2439. 10.1001/jama.2011.826.CrossRefPubMedPubMedCentral
24.
go back to reference Nakano C, Hamano T, Fujii N, Matsui I, Tomida K, Mikami S, Inoue K, Obi Y, Okada N, Tsubakihara Y, Isaka Y, Rakugi H: Combined use of vitamin D status and FGF23 for risk stratification of renal outcome. Clin J Am Soc Nephrol. 2012, 7 (5): 810-819. 10.2215/CJN.08680811.CrossRefPubMed Nakano C, Hamano T, Fujii N, Matsui I, Tomida K, Mikami S, Inoue K, Obi Y, Okada N, Tsubakihara Y, Isaka Y, Rakugi H: Combined use of vitamin D status and FGF23 for risk stratification of renal outcome. Clin J Am Soc Nephrol. 2012, 7 (5): 810-819. 10.2215/CJN.08680811.CrossRefPubMed
25.
go back to reference Mehrotra R, Kermah D, Budoff M, Salusky IB, Mao SS, Gao YL, Takasu J, Adler S, Norris K: Hypovitaminosis D in chronic kidney disease. Clin J Am Soc Nephrol. 2008, 3 (4): 1144-1151. 10.2215/CJN.05781207.CrossRefPubMedPubMedCentral Mehrotra R, Kermah D, Budoff M, Salusky IB, Mao SS, Gao YL, Takasu J, Adler S, Norris K: Hypovitaminosis D in chronic kidney disease. Clin J Am Soc Nephrol. 2008, 3 (4): 1144-1151. 10.2215/CJN.05781207.CrossRefPubMedPubMedCentral
26.
go back to reference Melamed ML, Astor B, Michos ED, Hostetter TH, Powe NR, Muntner P: 25-hydroxyvitamin D levels, race, and the progression of kidney disease. J Am Soc Nephrol. 2009, 20 (12): 2631-2639. 10.1681/ASN.2009030283.CrossRefPubMedPubMedCentral Melamed ML, Astor B, Michos ED, Hostetter TH, Powe NR, Muntner P: 25-hydroxyvitamin D levels, race, and the progression of kidney disease. J Am Soc Nephrol. 2009, 20 (12): 2631-2639. 10.1681/ASN.2009030283.CrossRefPubMedPubMedCentral
27.
go back to reference de Boer IH, Katz R, Chonchol M, Ix JH, Sarnak MJ, Shlipak MG, Siscovick DS, Kestenbaum B: Serum 25-hydroxyvitamin D and change in estimated glomerular filtration rate. Clin J Am Soc Nephrol. 2011, 6 (9): 2141-2149. 10.2215/CJN.02640311.CrossRefPubMedPubMedCentral de Boer IH, Katz R, Chonchol M, Ix JH, Sarnak MJ, Shlipak MG, Siscovick DS, Kestenbaum B: Serum 25-hydroxyvitamin D and change in estimated glomerular filtration rate. Clin J Am Soc Nephrol. 2011, 6 (9): 2141-2149. 10.2215/CJN.02640311.CrossRefPubMedPubMedCentral
28.
go back to reference Levin A, Bakris GL, Molitch M, Smulders M, Tian J, Williams LA, Andress DL: Prevalence of abnormal serum vitamin D, PTH, calcium, and phosphorus in patients with chronic kidney disease: results of the study to evaluate early kidney disease. Kidney Int. 2007, 71 (1): 31-38. 10.1038/sj.ki.5002009.CrossRefPubMed Levin A, Bakris GL, Molitch M, Smulders M, Tian J, Williams LA, Andress DL: Prevalence of abnormal serum vitamin D, PTH, calcium, and phosphorus in patients with chronic kidney disease: results of the study to evaluate early kidney disease. Kidney Int. 2007, 71 (1): 31-38. 10.1038/sj.ki.5002009.CrossRefPubMed
29.
go back to reference Block GA, Klassen PS, Lazarus JM, Ofsthun N, Lowrie EG, Chertow GM: Mineral metabolism, mortality, and morbidity in maintenance hemodialysis. J Am Soc Nephrol. 2004, 15 (8): 2208-2218. 10.1097/01.ASN.0000133041.27682.A2.CrossRefPubMed Block GA, Klassen PS, Lazarus JM, Ofsthun N, Lowrie EG, Chertow GM: Mineral metabolism, mortality, and morbidity in maintenance hemodialysis. J Am Soc Nephrol. 2004, 15 (8): 2208-2218. 10.1097/01.ASN.0000133041.27682.A2.CrossRefPubMed
30.
go back to reference Kalantar-Zadeh K, Kuwae N, Regidor DL, Kovesdy CP, Kilpatrick RD, Shinaberger CS, McAllister CJ, Budoff MJ, Salusky IB, Kopple JD: Survival predictability of time-varying indicators of bone disease in maintenance hemodialysis patients. Kidney Int. 2006, 70 (4): 771-780. 10.1038/sj.ki.5001514.CrossRefPubMed Kalantar-Zadeh K, Kuwae N, Regidor DL, Kovesdy CP, Kilpatrick RD, Shinaberger CS, McAllister CJ, Budoff MJ, Salusky IB, Kopple JD: Survival predictability of time-varying indicators of bone disease in maintenance hemodialysis patients. Kidney Int. 2006, 70 (4): 771-780. 10.1038/sj.ki.5001514.CrossRefPubMed
31.
go back to reference Kovesdy CP, Ahmadzadeh S, Anderson JE, Kalantar-Zadeh K: Secondary hyperparathyroidism is associated with higher mortality in men with moderate to severe chronic kidney disease. Kidney Int. 2008, 73 (11): 1296-1302. 10.1038/ki.2008.64.CrossRefPubMed Kovesdy CP, Ahmadzadeh S, Anderson JE, Kalantar-Zadeh K: Secondary hyperparathyroidism is associated with higher mortality in men with moderate to severe chronic kidney disease. Kidney Int. 2008, 73 (11): 1296-1302. 10.1038/ki.2008.64.CrossRefPubMed
32.
go back to reference Shigematsu T, Caverzasio J, Bonjour JP: Parathyroid removal prevents the progression of chronic renal failure induced by high protein diet. Kidney Int. 1993, 44 (1): 173-181. 10.1038/ki.1993.228.CrossRefPubMed Shigematsu T, Caverzasio J, Bonjour JP: Parathyroid removal prevents the progression of chronic renal failure induced by high protein diet. Kidney Int. 1993, 44 (1): 173-181. 10.1038/ki.1993.228.CrossRefPubMed
33.
go back to reference Schumock GT, Andress DL, Marx SE, Sterz R, Joyce AT, Kalantar-Zadeh K: Association of secondary hyperparathyroidism with CKD progression, health care costs and survival in diabetic predialysis CKD patients. Nephron Clin Pract. 2009, 113 (1): c54-c61. 10.1159/000228076.CrossRefPubMed Schumock GT, Andress DL, Marx SE, Sterz R, Joyce AT, Kalantar-Zadeh K: Association of secondary hyperparathyroidism with CKD progression, health care costs and survival in diabetic predialysis CKD patients. Nephron Clin Pract. 2009, 113 (1): c54-c61. 10.1159/000228076.CrossRefPubMed
34.
go back to reference Gromadzinski L, Januszko-Giergielewicz B, Pruszczyk P: Hypocalcemia is related to left ventricular diastolic dysfunction in patients with chronic kidney disease. J Cardiol. 2014, 63 (3): 198-204. 10.1016/j.jjcc.2013.08.003.CrossRefPubMed Gromadzinski L, Januszko-Giergielewicz B, Pruszczyk P: Hypocalcemia is related to left ventricular diastolic dysfunction in patients with chronic kidney disease. J Cardiol. 2014, 63 (3): 198-204. 10.1016/j.jjcc.2013.08.003.CrossRefPubMed
35.
go back to reference Bers DM: Cardiac excitation-contraction coupling. Nature. 2002, 415 (6868): 198-205. 10.1038/415198a.CrossRefPubMed Bers DM: Cardiac excitation-contraction coupling. Nature. 2002, 415 (6868): 198-205. 10.1038/415198a.CrossRefPubMed
36.
go back to reference Tentori F, Blayney MJ, Albert JM, Gillespie BW, Kerr PG, Bommer J, Young EW, Akizawa T, Akiba T, Pisoni RL, Robinson BM, Port FK: Mortality risk for dialysis patients with different levels of serum calcium, phosphorus, and PTH: the Dialysis Outcomes and Practice Patterns Study (DOPPS). Am J Kidney Dis. 2008, 52 (3): 519-530. 10.1053/j.ajkd.2008.03.020.CrossRefPubMed Tentori F, Blayney MJ, Albert JM, Gillespie BW, Kerr PG, Bommer J, Young EW, Akizawa T, Akiba T, Pisoni RL, Robinson BM, Port FK: Mortality risk for dialysis patients with different levels of serum calcium, phosphorus, and PTH: the Dialysis Outcomes and Practice Patterns Study (DOPPS). Am J Kidney Dis. 2008, 52 (3): 519-530. 10.1053/j.ajkd.2008.03.020.CrossRefPubMed
37.
go back to reference Kovesdy CP, Kuchmak O, Lu JL, Kalantar-Zadeh K: Outcomes associated with serum calcium level in men with non-dialysis-dependent chronic kidney disease. Clin J Am Soc Nephrol. 2010, 5 (3): 468-476. 10.2215/CJN.06040809.CrossRefPubMedPubMedCentral Kovesdy CP, Kuchmak O, Lu JL, Kalantar-Zadeh K: Outcomes associated with serum calcium level in men with non-dialysis-dependent chronic kidney disease. Clin J Am Soc Nephrol. 2010, 5 (3): 468-476. 10.2215/CJN.06040809.CrossRefPubMedPubMedCentral
38.
go back to reference Block RA, Zakay D, Hancock PA: Human aging and duration judgments: a meta-analytic review. Psychol Aging. 1998, 13 (4): 584-596.CrossRefPubMed Block RA, Zakay D, Hancock PA: Human aging and duration judgments: a meta-analytic review. Psychol Aging. 1998, 13 (4): 584-596.CrossRefPubMed
39.
go back to reference Ganesh SK, Stack AG, Levin NW, Hulbert-Shearon T, Port FK: Association of elevated serum PO(4), Ca x PO(4) product, and parathyroid hormone with cardiac mortality risk in chronic hemodialysis patients. J Am Soc Nephrol. 2001, 12 (10): 2131-2138.PubMed Ganesh SK, Stack AG, Levin NW, Hulbert-Shearon T, Port FK: Association of elevated serum PO(4), Ca x PO(4) product, and parathyroid hormone with cardiac mortality risk in chronic hemodialysis patients. J Am Soc Nephrol. 2001, 12 (10): 2131-2138.PubMed
40.
go back to reference O’Neill WC: The fallacy of the calcium-phosphorus product. Kidney Int. 2007, 72 (7): 792-796. 10.1038/sj.ki.5002412.CrossRefPubMed O’Neill WC: The fallacy of the calcium-phosphorus product. Kidney Int. 2007, 72 (7): 792-796. 10.1038/sj.ki.5002412.CrossRefPubMed
Metadata
Title
Low serum calcium is associated with poor renal outcomes in chronic kidney disease stages 3–4 patients
Authors
Lee-Moay Lim
Hung-Tien Kuo
Mei-Chuan Kuo
Yi-Wen Chiu
Jia-Jung Lee
Shang-Jyh Hwang
Jer-Chia Tsai
Chi-Chih Hung
Hung-Chun Chen
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Nephrology / Issue 1/2014
Electronic ISSN: 1471-2369
DOI
https://doi.org/10.1186/1471-2369-15-183

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