Hyperphosphatemia is associated with anemia in adults without chronic kidney disease: results from the National Health and Nutrition Examination Survey (NHANES): 2005–2010

BMC Nephrology

Janet M Wojcicki¹ 

[1] Department of Pediatrics, University of California, San Francisco, CA 94134-0136, USA

关键词: Obesity;    Anemia;    Lower socioeconomic status;    Hypophosphatemia;    Hyperphosphatemia;   

Others  :  1082861
DOI  :  10.1186/1471-2369-14-178

 received in 2013-02-12, accepted in 2013-08-15,  发布年份 2013

【 摘 要 】

Background

Hyperphosphatemia, serum phosphorus ≥ 4.4 mg/dL, is associated with increased risk for chronic kidney disease and cardiovascular disease. Previous studies have shown a weak association between dietary phosphorus intake and serum phosphorus concentrations. While much less common in the general population, hypophosphatemia (< 2.5 mg/dL) may be associated with metabolic syndrome and obesity.

Methods

Using three cycles from the National Health and Nutrition Examination Survey (NHANES) (2005–2010), this study evaluated independent risk factors for hyperphosphatemia and hypophosphatemia.

Results

Risk factors for hyperphosphatemia included higher adjusted calcium (OR 2.90, 95% CI 2.43-3.45), increasing cholesterol (OR 1.003, 95% CI 1.001-1.005), female gender (OR 1.61, 95% CI 1.39-1.87) and low hemoglobin (OR 1.52, 95% CI 1.17-1.98). Advanced age was protective (OR 0.98, 95% CI 0.977-0.987). Models that included fasting serum glucose found lower body mass index (BMI) to be protective (OR 0.97, 95% CI 0.96-0.99) and adjusting for serum vitamin D and parathyroid hormone removed the association with low hemoglobin and BMI. Risk factors for hypophosphatemia included the following protective factors: higher albumin (OR 0.56, 95% CI 0.35-0.93), higher BUN (OR 0.90, 95% CI 0.86, 0.95), corrected calcium (OR 0.38, 95% CI 0.23-0.63) and female gender (OR 0.47, 95% 0.24-0.94). In men, higher fasting glucose levels increased risk (OR 1.01, 95% CI 1.0004-1.01).

Conclusion

This study is the first to show an association between low hemoglobin levels and increased risk for hyperphosphatemia among individuals without chronic kidney disease. We did not find any association between diabetes mellitus, increasing BMI or fasting glucose levels and hypophosphatemia.

【 授权许可】

   
2013 Wojcicki; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Levi M, Popovtzer M: Disorders of phosphate balance. In Chapter 7 in Atlases of Diseases of the Kidney (volume 1) Edited by Schrier RW, Berl T, Bonventre JV. 1999, 7.1-7.14.
• [2]Gutierrez OM, Isakova T, Enfield G, Wolf M: Impact of poverty on serum phosphate concentrations in third national health and nutrition examination survey. J Ren Nutr 2011, 21(2):140-148.
• [3]O’Seaghdha CM, Hwang SJ, Muntner P, Melamed ML, Fox CS: Serum phosphorus predicts incident chronic kidney disease and end-stage renal disease. Nephrol Dial Transplant 2011, 26:2885-2890.
• [4]Moe SM, Chen NX: Mechanisms of vascular calcification in chronic kidney disease. J Am Soc Nephrol 2008, 19:213-216.
• [5]You L, Zhu X, Shrubsole MJ, Fan H, Chen J, Dong J, Hao CM, Dai Q: Renal function, bisphenol A and alkylphenols: results from the National Health and Nutrition Examination Survey (NHNAES 2003–6). Environ Health Perspect 2011, 119(4):527-533.
• [6]Kovesdy CP, Mucsi I, Czira ME, Rudas A, Ujszaszi R, Rosivall L, Kim SJ, Wolf M, Molnar MZ: Association of serum phosphorus level with anemia in kidney transplant recipients. Transplantation 2011, 91(8):875-882.
• [7]Yoshida K, Yoneda T, Kimura S, et al.: Polyamines as an inhibitor on erythropoisesis of hemodialysis patients by in vitro bioassay using the fetal mouse liver assay. Ther Apher Dial 2006, 10:267.
• [8]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.
• [9]Uemura H, Irahara M, Yoneda N, Yasui T, Genjida K, Miyamoto KI, Aono T, Takeda E: Close correlation between estrogen treatment and renal phosphate reabsorption capacity. J Clin Endocrinol Metabol 2000, 85(3):1215-1219.
• [10]O’Connor LR, Wheeler WS, Bethune JE: Efect of hypophosphatemia on myocardial performance in man. New Engl J Med 1977, 297:901-903.
• [11]Haglin L: Hypophosphataemia: cause of the disturbed metabolism in the metabolic syndrome. Med Hypotheses 2001, 56(6):657-663.
• [12]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2005–6 Data Documentation, Codebook and Frequencies: Standard Biochemistry Profile (BIOPRO_D). 2008a. http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/BIOPRO_D.htm#Analytic_Notes webcite, accessed June 3, 2013
• [13]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2007–8 Data Documentation, Codebook and Frequencies: Standard Biochemistry Profile (BIOPRO_E). 2010a. http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/BIOPRO_E.htm#Description_of_Laboratory_Methodology webcite, accessed June 3, 2013
• [14]Center for Disease Control (CDC): National Health and Nutrition Examination Survey. 2009–2010 Data Documentation, Codebook, and Frequencies: Standard Biochemistry Profile (BIOPRO_F). 2011a. http://www.cdc.gov/nchs/nhanes/nhanes2009-2010/BIOPRO_F.htm#Description_of_Laboratory_Methodology webcite, accessed June 3, 2013
• [15]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2009–2010 Data Documentation, Codebook and Frequencies. Glycohemoglobin (GHB_D). 2012c. http://www.cdc.gov/nchs/nhanes/nhanes2009-2010/GHB_F.htm webcite, accessed June 3, 2013
• [16]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2005–6 Data Documentation, Codebook and Frequencies: Glycohemoglobin (GHB_D). 2012a. http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/GHB_D.htm webcite, accessed June 3, 2013
• [17]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2007–8 Data Documentation, Codebook and Frequencies. Glycohemoglobin (GHB_D). 2012b. http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/GHB_E.htm webcite, accessed June 3, 2013
• [18]Center for Disease Control (CDC): National Health and Nutrition Examination Survey. Center for Disease Control (CDC), National Health and Nutrition Examination Survey. 2009–2010 Data Documentation, Codebook and Frequencies. C-Reactive Protein (CRP_F). 2009a. http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/CRP_E.htm webcite, accessed June 3, 2013
• [19]Center for Disease Control (CDC): September 2009b. National Health and Nutrition Examination Survey. 2007–8 Data Documentation, Codebook, and Frequencies: C-Reactive Protein (CRP_F). 2009b. http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/CRP_E.htm webcite, accessed June 3, 2013
• [20]Center for Disease Control (CDC): National Health and Nutrition Examination Survey. Center for Disease Control (CDC), National Health and Nutrition Examination Survey 2005–6 Data Documentation, Codebook, and Frequencies. C-Reactive Protein (CRP_D). 2007. http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/CRP_D.htm webcite, accessed June 3, 2013
• [21]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2005–6 Data Documentation, Codebook and Frequencies: Ferritin (FERTIN_D). 2008b. http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/FERTIN_D.htm webcite, accessed June 3, 2013
• [22]Center for Disease Control (CDC): National Health and Nutrition Examination Survey. 2007–8 Data Documentation, Codebook, and Frequencies (FERITIN_E). 2009e. http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/FERTIN_E.htm webcite, accessed June 3, 2013
• [23]Center for Disease Control (CDC): National Health and Nutrition Examination Survey. 2009–2010 Data Documentation, Codebook and Frequencies. Ferritin. (FERITIN_F). 2012d. http://www.cdc.gov/nchs/nhanes/nhanes2009-2010/FERTIN_F.htm webcite, accessed June 3, 2013
• [24]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2005–6 Data Documentation, Codebook, and Frequencies: Transferrin Receptor (TFR_D). 2008d. http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/TFR_D.htm webcite, accessed June 3, 2013
• [25]Center for Disease Control (CDC): National Health and Nutrition Examination Survey. 2007–8 Data Documentation, Codebook, and Frequencies. Transferrin Receptor (TRF_E). 2009f. http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/TFR_E.htm webcite, accessed June 3, 2013
• [26]Center for Disease Control (CDC): National Health and Nutrition Examination Survey. 2009–2010 Data Documentation, Codebook and Frequencies. Transferrin Receptor (TRF_F). 2012e. http://www.cdc.gov/nchs/nhanes/nhanes2009-2010/TFR_F.htm webcite, accessed June 3, 2013
• [27]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2005–6 Data Documentation, Codebook and Frequencies: Plasma Fasting Glucose and Insulin (GLU_D). 2008c. http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/GLU_D.htm webcite, accessed June 3, 2013
• [28]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2007–8 Data Documentation, Codebook, and Frequencies. Glucose and Insulin. 2010c. http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/GLU_E.htm webcite, access June 3, 2013
• [29]Center for Disease Control (CDC): National Health and Nutrition Examination Survey. 2009–2010 Data Documentation, Codebook and Frequencies. Plasma Fasting Glucose and Insulin (GLU_F). 2012f. http://www.cdc.gov/nchs/nhanes/nhanes2009-2010/GLU_F.htm webcite, accessed June 3, 2013
• [30]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2005–6 Data Documentation, Codebook, and Frequencies: Parathyroid Hormone (PTH_D). 2008e. http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/PTH_D.htm webcite, accessed June 3, 2013
• [31]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2005–6 Data Documentation, Codebook, and Frequencies: Vitamin D. 2010b. http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/VID_D.htm webcite, accessed June 3, 2013
• [32]Center for Disease Control (CDC): National Health and Nutrition Examination Survey (NHANES). 2005–6 Data Documentation, Codebook, and Frequencies: Environmental Phenols and Parabens (EPH_D). 2009d. http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/EPH_D.htm webcite, accessed June 3, 2013
• [33]Center for Disease Control (CDC): National Health and Nutrition Examination Survey. (NHANES) 2007–8 Data Documentation, Codebook, and Frequencies. Environmental Phenols. 2010d. http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/EPH_E.htm webcite, access June 3, 2013
• [34]Center for Disease Control (CDC): National Health and Nutrition Examination Survey 2009–10 data Documentation, Codebook, and Frequencies: Environmental Phenol (EPH_E). 2011c. http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/EPH_E.htm webcite, accessed June 3, 2013
• [35]Center for Disease Control (CDC): MEC In-Person Dietary Interviewers Procedures Manual. Atlanta: CDC; 2009c. [National Health and Nutrition Examination Survey (NHANES)]
• [36]National Kidney Foundation: K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification and stratification. Am J Kidney Dis 2002, 29:SI-S266.
• [37]Levey AS, Stevens LA, Schmid CH, Zhang Y, Castro AF, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, Coresh J: A new equation to estimate glomerular filtration rate. Ann Intern Med 2009, 105(9):604-612.
• [38]National Health and Nutrition Examination Survey Data. Hyattsville, MD: United States Department of Health and Human Services. Centers for Disease Control and Prevention; 2004–2010. Available from: http://www.cdc.gov/nchs/nhanes/nhanes_questionnaires.htm webcite, accessed November 28, 2012
• [39]De Boer IH, Rue TC, Kestenbaum B: Serum phosphorus concentrations in the Third National Health and Nutrition Examination Survey (NHANES III). Am J Kidney Dis 2009, 53(3):399-407.
• [40]Leon JB, Sullivan CM, Sehgal AR: The prevalence of phosphorus-containing food additives in top-selling foods in grocery stores. J Renal Nutr 2013, 23(4):265-270.
• [41]Benini O, Alessandro C, Gianfaldoni D, Cupisti A: Extra-phosphate load from food additives in commonly eaten foods: a real and insidious danger for renal patients. J Ren Nutr 2011, 21(4):303-308.
• [42]Astor BC, Munter P, Levin A, Eustace JA, Coresh J: Association of kidney function with anemia: the Third National Health and Nutrition Examination Survey (1988–1994). Arch Intern Med 2002, 162(12):1401-1408.
• [43]Chonchol M, Lippi G, Montagnana M, Mugeo M, Targher G: Association of inflammation with anemia in patients with chronic kidney disease not requiring dialysis. Nephrol Dial Transplant 2008, 23(9):2879-2883.
• [44]Kendrick J, Targher G, Smits G, Chonchol M: 25-Hydroxyvitamin D deficiency and inflammation and their association with hemoglobin level in chronic kidney disease. Am J Nephroogy 2009, 30:64-72.
• [45]Uribarri J: Phosphorus homeostasis in normal health and in chronic kidney disease patients with special emphasis on dietary phosphorus intake. Semin Dial 2007, 20:295-301.
• [46]Tenenhouse HS: Regulation of phosphorus homeostasis by the type IIA Na/Phosphate cotransporter. Annu Rev Nutr 2005, 25:197-214.
• [47]Favus MJ, Bushinsky DA, Lemon J: Regulation of calcium, magnesium and phosphate metabolism. In Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism. 6th edition. Edited by Favus E. Washington, DC: American Society for Bone and Mineral Research; 2006:115.
• [48]Larsson TE, Clauson H, Hagstrom E, Ingelsson E, Amlov J, Lind L, Sundstrom J: Conjoint effects of serum calcium and phosphate on risk of total cardiovascular, and noncardiovasclar mortality in the community. Arterioscler Thromb Vasc Biol 2010, 30(2):333-339.
• [49]Haglin L, Lindblad A, Bygren LO: Hypophosphataemia in the metabolic syndrome. Gender differences in body weight and blood glucose. Eur J Clin 2001, 55(6):493-498.
• [50]Suzuki S, Egi M, Schneider AG, Bellomo R, Hart GK, Hegarty C: Hypophosphatemia in crticially ill patients. J Crit Care 2012, 28(4):536.e9.
• [51]Hoffmann M, Zemlin AE, Meyer WP, Erasmus RT: Hypophosphataemia at a large academic hospital in South Africa. J Clin Pathol 2008, 61(10):1104-1107.
• [52]Davis JL, Lewis SB, Schultz TA, Kaplan RA, Wallin JD: Acute and chronic phosphate depletion as a modulator of glucose uptake in rat skeletal muscle. Life Sci 1979, 24(7):629-632.
• [53]De Fronzo RA, Lang R: Hypophosphatemia and glucose intolerance: evidence for tissue insensitivity to insulin. New England J Med 1980, 303:1259-1263.
• [54]Skverksy AL, Kumar J, Abramowitz MK, Kaskel FJ, Melamed ML: Association of glucocorticoid use and low 25-hydroxyvitamin D levels: results from the National Health and Nutrition Examination Survey (NHANES): 2001–2006. J Clin Endocrinol Metab 2011, 96:3838-3845.