Skip to main content
Top
Published in: BMC Nephrology 1/2019

Open Access 01-12-2019 | Chronic Kidney Disease | Research article

Higher serum uric acid level is inversely associated with renal function assessed by cystatin C in a Japanese general population without chronic kidney disease: the KOBE study

Authors: Sachimi Kubo, Yoko Nishida, Yoshimi Kubota, Aya Higashiyama, Daisuke Sugiyama, Takumi Hirata, Naomi Miyamatsu, Ayumi Tanabe, Aya Hirata, Yukako Tatsumi, Aya Kadota, Kazuyo Kuwabara, Tomofumi Nishikawa, Yoshihiro Miyamoto, Tomonori Okamura

Published in: BMC Nephrology | Issue 1/2019

Login to get access

Abstract

Background

Although several epidemiological studies have suggested that high serum uric acid (SUA) levels are related to a decline in kidney function, only a few studies have investigated using cystatin C to calculate estimated glomerular filtration rate (eGFR). We aimed to clarify the relationship between SUA levels and kidney function assessed by cystatin C in a Japanese general community population without chronic kidney disease (CKD).

Methods

We conducted a community-based cross-sectional study that included 1086 healthy participants, aged 40–74 years, without CKD and not undergoing treatment of hyperuricemia, who had participated in the baseline survey of the Kobe Orthopedic and Biomedical Epidemiological (KOBE) study. The preconditions for participation in this study were no past histories of cardiovascular disease or cancer, and not undergoing treatment for diabetes, hypertension, or dyslipidemia. We classified the participants into quartiles stratified by sex according to their SUA level and then examined the relationship with eGFR. The odds ratios for having a low eGFR, defined as the lowest quartile of eGFR (i.e., ≤78.4 mL/min/1. 73m2) was estimated according to SUA quartiles (men, Q1 ≤ 5.0, Q2 5.1–5.9, Q3 6.0–6.6, and Q4 ≥ 6.7; women, Q1 ≤ 3.8, Q2 3.9–4.3, Q3 4.4–4.9, and Q4 ≥ 5.0 mg/dL) after adjustment for age, body mass index, systolic blood pressure, HbA1c, high and low density lipoprotein cholesterol, and smoking and drinking habits. The adjusted mean of each quartile was also calculated.

Results

Multivariable-adjusted means of eGFR showed a graded decrease in higher SUA quartiles (men, Q1 90.5, Q2 88.0, Q3 83.5, and Q4 82.0; women, Q1 95.7, Q2 91.3, Q3 89.2, and Q4 86.7). In addition, the multivariable-adjusted odds ratios for having a lower eGFR (95% confidence interval) for each SUA quartile compared with Q1 was Q2 2.29 (0.98, 5.35), Q3 4.94 (2.04, 11.97), and Q4 8.01 (3.20, 20.04) for men, and was Q2 2.20 (1.12, 4.32), Q3 2.68 (1.39, 5.20), and Q4 4.96 (2.62, 9.41) for women.

Conclusions

There was a graded inverse relationship between mild elevations in SUA levels and eGFR assessed by cystatin C in an apparently healthy Japanese population without CKD. This association was similar in both men and women.
Literature
1.
go back to reference Iseki K, Ikemiya Y, Inoue T, Iseki C, Kinjo K, Takishita S. Significance of hyperuricemia as a risk factor for developing ESRD in a screened cohort. Am J Kidney Dis. 2004;44:642–50.CrossRef Iseki K, Ikemiya Y, Inoue T, Iseki C, Kinjo K, Takishita S. Significance of hyperuricemia as a risk factor for developing ESRD in a screened cohort. Am J Kidney Dis. 2004;44:642–50.CrossRef
2.
go back to reference Takae K, Nagata M, Hata J, Mukai N, Hirakawa Y, Yoshida D, et al. Serum uric acid as a risk factor for chronic kidney disease in a Japanese community – the Hisayama study. Circ J. 2016;80:1857–62.CrossRef Takae K, Nagata M, Hata J, Mukai N, Hirakawa Y, Yoshida D, et al. Serum uric acid as a risk factor for chronic kidney disease in a Japanese community – the Hisayama study. Circ J. 2016;80:1857–62.CrossRef
3.
go back to reference Weiner DE, Tighiouart H, Elsayed EF, Griffith JL, Salem DN, Levey AS. Uric acid and incident kidney disease in the community. J Am Soc Nephrol. 2008;19:1204–11.CrossRef Weiner DE, Tighiouart H, Elsayed EF, Griffith JL, Salem DN, Levey AS. Uric acid and incident kidney disease in the community. J Am Soc Nephrol. 2008;19:1204–11.CrossRef
4.
go back to reference Obermayr RP, Temml C, Gutjahr G, Knechtelsdorfer M, Oberbauer R, Klauser-Braun R. Elevated uric acid increases the risk for kidney disease. J Am Soc Nephrol. 2008;19:2407–13.CrossRef Obermayr RP, Temml C, Gutjahr G, Knechtelsdorfer M, Oberbauer R, Klauser-Braun R. Elevated uric acid increases the risk for kidney disease. J Am Soc Nephrol. 2008;19:2407–13.CrossRef
5.
go back to reference Domrongkitchaiporn S, Sritara P, Kitiyakara C, Stitchantrakul W, Krittaphol V, Lolekha P, et al. Risk factors for development of decreased kidney function in a southeast Asian population: a 12-year cohort study. J Am Soc Nephrol. 2005;16:791–9.CrossRef Domrongkitchaiporn S, Sritara P, Kitiyakara C, Stitchantrakul W, Krittaphol V, Lolekha P, et al. Risk factors for development of decreased kidney function in a southeast Asian population: a 12-year cohort study. J Am Soc Nephrol. 2005;16:791–9.CrossRef
6.
go back to reference Iseki K, Oshiro S, Tozawa M, Iseki C, Ikemiya Y, Takishita S. Significance of hyperuricemia on the early detection of renal failure in a cohort of screened subjects. Hypertens Res. 2001;24:691–7.CrossRef Iseki K, Oshiro S, Tozawa M, Iseki C, Ikemiya Y, Takishita S. Significance of hyperuricemia on the early detection of renal failure in a cohort of screened subjects. Hypertens Res. 2001;24:691–7.CrossRef
7.
go back to reference Ishani A, Grandits GA, Grimm RH, Svendsen KH, Collins AJ, Prineas RJ, et al. Association of single measurements of dipstick proteinuria, estimated glomerular filtration rate, and hematocrit with 25- year incidence of end-stage renal disease in the multiple risk factor intervention trial. J Am Soc Nephrol. 2006;17:1444–52.CrossRef Ishani A, Grandits GA, Grimm RH, Svendsen KH, Collins AJ, Prineas RJ, et al. Association of single measurements of dipstick proteinuria, estimated glomerular filtration rate, and hematocrit with 25- year incidence of end-stage renal disease in the multiple risk factor intervention trial. J Am Soc Nephrol. 2006;17:1444–52.CrossRef
8.
go back to reference Conchol MB, Shlipak MG, Katz R, Sarnak MJ, Newman AB, Siscovick DS, et al. Relationship of uric acid with progression of kidney disease. Am J Kidney Dis. 2007;50:239–47.CrossRef Conchol MB, Shlipak MG, Katz R, Sarnak MJ, Newman AB, Siscovick DS, et al. Relationship of uric acid with progression of kidney disease. Am J Kidney Dis. 2007;50:239–47.CrossRef
9.
go back to reference Stevens LA, Coresh J, Schmid CH, Feldman HI, Froissart M, Kusek J, Rossert J, et al. Estimating GFR using serum cystatin C alone and in combination with serum creatinine: a pooled analysis of 3,418 individuals with CKD. Am J Kidney Dis. 2008;51:395–406.CrossRef Stevens LA, Coresh J, Schmid CH, Feldman HI, Froissart M, Kusek J, Rossert J, et al. Estimating GFR using serum cystatin C alone and in combination with serum creatinine: a pooled analysis of 3,418 individuals with CKD. Am J Kidney Dis. 2008;51:395–406.CrossRef
10.
go back to reference Higashiyama A, Wakabayashi I, Kubota Y, Adachi Y, Hayashibe A, Nishimura K, et al. Does high-sensitivity C-reactive protein or low-density lipoprotein cholesterol show a stronger relationship with the cardioankle vascular index in healthy community dwellers?: the KOBE study. J Atheroscler Thromb. 2012;19:1027–34.CrossRef Higashiyama A, Wakabayashi I, Kubota Y, Adachi Y, Hayashibe A, Nishimura K, et al. Does high-sensitivity C-reactive protein or low-density lipoprotein cholesterol show a stronger relationship with the cardioankle vascular index in healthy community dwellers?: the KOBE study. J Atheroscler Thromb. 2012;19:1027–34.CrossRef
11.
go back to reference Hirata T, Higashiyama A, Kubota Y, Nishimura K, Sugiyama D, Kadota A, et al. HOMA-IR values are associated with glycemic control in Japanese subjects without diabetes or obesity: the KOBE study. J Epidemiol. 2015;25:407–14.CrossRef Hirata T, Higashiyama A, Kubota Y, Nishimura K, Sugiyama D, Kadota A, et al. HOMA-IR values are associated with glycemic control in Japanese subjects without diabetes or obesity: the KOBE study. J Epidemiol. 2015;25:407–14.CrossRef
12.
go back to reference Sugiyama D, Higashiyama A, Wakabayashi I, Kubota Y, Adachi Y, Hayashibe A, et al. The relationship between lectin-like oxidized low-density lipoprotein receptor-1 ligands containing apolipoprotein B and the cardio-ankle vascular index in healthy community inhabitants: the KOBE study. J Atheroscler Thromb. 2015;22:499–508.CrossRef Sugiyama D, Higashiyama A, Wakabayashi I, Kubota Y, Adachi Y, Hayashibe A, et al. The relationship between lectin-like oxidized low-density lipoprotein receptor-1 ligands containing apolipoprotein B and the cardio-ankle vascular index in healthy community inhabitants: the KOBE study. J Atheroscler Thromb. 2015;22:499–508.CrossRef
13.
go back to reference Kubota Y, Higashiyama A, Imano H, Sugiyama D, Kawamura K, Kadota A, et al. Serum polyunsaturated fatty acid composition and serum high-sensitivity C-reactive protein levels in healthy Japanese residents: the KOBE study. J Nutr Health Aging. 2015;19:719–28.CrossRef Kubota Y, Higashiyama A, Imano H, Sugiyama D, Kawamura K, Kadota A, et al. Serum polyunsaturated fatty acid composition and serum high-sensitivity C-reactive protein levels in healthy Japanese residents: the KOBE study. J Nutr Health Aging. 2015;19:719–28.CrossRef
14.
go back to reference Tanaka T, Okamura T, Miura K, Kadowaki T, Ueshima H, Nakagawa H, et al. A simple method to estimate populational 24-h urinary sodium and potassium excretion using a casual urine specimen. J Hum Hypertens. 2002;16:97–103.CrossRef Tanaka T, Okamura T, Miura K, Kadowaki T, Ueshima H, Nakagawa H, et al. A simple method to estimate populational 24-h urinary sodium and potassium excretion using a casual urine specimen. J Hum Hypertens. 2002;16:97–103.CrossRef
15.
go back to reference Fossati P, Prencipe L, Berti G. Use of 3, 5-dichloro- 2-hydroxybenzenesulfonic acid / 4-aminophenazone chromogenic system in direct enzymic assay of uric acid in serum and urine. Clin Chem. 1980;26:227–31.PubMed Fossati P, Prencipe L, Berti G. Use of 3, 5-dichloro- 2-hydroxybenzenesulfonic acid / 4-aminophenazone chromogenic system in direct enzymic assay of uric acid in serum and urine. Clin Chem. 1980;26:227–31.PubMed
16.
go back to reference 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.PubMed 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.PubMed
17.
go back to reference The Japanese Society of Nephrology. Clinical practice guidebook for diagnosis and treatment of chronic kidney disease 2012. Jpn J Nephrol. 2012;54:1031–189. The Japanese Society of Nephrology. Clinical practice guidebook for diagnosis and treatment of chronic kidney disease 2012. Jpn J Nephrol. 2012;54:1031–189.
18.
go back to reference Uedono H, Akihiro T, Ishimura E, Nakatani S, Kurajoh M, Mori K, et al. U-shape relationship between serum uric acid levels and internal hemodynamic parameters in healthy subjects. Am J Physiol Renal Physiol. 2017;312:F992–7.CrossRef Uedono H, Akihiro T, Ishimura E, Nakatani S, Kurajoh M, Mori K, et al. U-shape relationship between serum uric acid levels and internal hemodynamic parameters in healthy subjects. Am J Physiol Renal Physiol. 2017;312:F992–7.CrossRef
19.
go back to reference Horio M, Imai E, Yasuda Y, Watanabe T, Matsuo S. Modification of the CKD epidemiology collaboration (CKD-EPI) equation for Japanese: accuracy and use for population estimates. Am J Kidney Dis. 2010;56:32–8.CrossRef Horio M, Imai E, Yasuda Y, Watanabe T, Matsuo S. Modification of the CKD epidemiology collaboration (CKD-EPI) equation for Japanese: accuracy and use for population estimates. Am J Kidney Dis. 2010;56:32–8.CrossRef
20.
go back to reference Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation: modification of diet in renal disease study group. Ann Intern Med. 1999;130:461–70.CrossRef Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation: modification of diet in renal disease study group. Ann Intern Med. 1999;130:461–70.CrossRef
21.
go back to reference Guideline for the management of hyperuricemia and gout: Second edition. Japanese Society of Gout and Nucleic Acid Metabolism; Osaka: 2010. p. 30. [in Japanese]. Guideline for the management of hyperuricemia and gout: Second edition. Japanese Society of Gout and Nucleic Acid Metabolism; Osaka: 2010. p. 30. [in Japanese].
22.
go back to reference Hakoda M, Masunari N, Yamada M, Fujiwara S, Suzuki G, Kodama K, et al. SUA concentration as a risk factor for cardiovascular mortality: a long term cohort study of atomic bomb survivors. J Rheumatol. 2005;32:906–12.PubMed Hakoda M, Masunari N, Yamada M, Fujiwara S, Suzuki G, Kodama K, et al. SUA concentration as a risk factor for cardiovascular mortality: a long term cohort study of atomic bomb survivors. J Rheumatol. 2005;32:906–12.PubMed
23.
go back to reference Zhang W, Iso H, Murakami Y, Miura K, Nagai M, Sugiyama D, EPOCH-JAPAN GROUP, et al. Serum uric acid and mortality form cardiovascular disease: EPOCH-JAPAN study. J Atheroscler Thromb. 2016;23:692–703.CrossRef Zhang W, Iso H, Murakami Y, Miura K, Nagai M, Sugiyama D, EPOCH-JAPAN GROUP, et al. Serum uric acid and mortality form cardiovascular disease: EPOCH-JAPAN study. J Atheroscler Thromb. 2016;23:692–703.CrossRef
24.
go back to reference Guideline for the management of hyperuricemia and gout: Second edition. Japanese Society of Gout and Nucleic Acid Metabolism; Osaka: 2010. p. 30–31. [in Japanese]. Guideline for the management of hyperuricemia and gout: Second edition. Japanese Society of Gout and Nucleic Acid Metabolism; Osaka: 2010. p. 30–31. [in Japanese].
25.
go back to reference Freedman DS, Williamson DF, Gunter EW, Byers T. Relation of serum uric acid to mortality and ischemic heart disease: The NHANES I Epidemiologic Follow-up Study. Am J Epidemiol. 1995;141:637–44.CrossRef Freedman DS, Williamson DF, Gunter EW, Byers T. Relation of serum uric acid to mortality and ischemic heart disease: The NHANES I Epidemiologic Follow-up Study. Am J Epidemiol. 1995;141:637–44.CrossRef
26.
go back to reference Fang J, Alderman MH. Serum uric acid and cardiovascular mortality the NHANES I epidemiologic follow-up study, 1971–1992. National Health and nutrition examination survey. JAMA. 2000;283:2404–10.CrossRef Fang J, Alderman MH. Serum uric acid and cardiovascular mortality the NHANES I epidemiologic follow-up study, 1971–1992. National Health and nutrition examination survey. JAMA. 2000;283:2404–10.CrossRef
27.
go back to reference Bos MJ, Koudstaal PJ, Hofman A, Witteman JC, Breteler MM. Uric acid is a risk factor for myocardial infarction and stroke: the Rotterdam study. Stroke. 2006;37:1503–7.CrossRef Bos MJ, Koudstaal PJ, Hofman A, Witteman JC, Breteler MM. Uric acid is a risk factor for myocardial infarction and stroke: the Rotterdam study. Stroke. 2006;37:1503–7.CrossRef
28.
go back to reference Hozawa A, Folsom AR, Ibrahim H, Javier Nieto F, Rosamond WD, Shahar E. Serum uric acid and risk of ischemic stroke: the ARIC study. Atherosclerosis. 2006;187:401–7.CrossRef Hozawa A, Folsom AR, Ibrahim H, Javier Nieto F, Rosamond WD, Shahar E. Serum uric acid and risk of ischemic stroke: the ARIC study. Atherosclerosis. 2006;187:401–7.CrossRef
29.
go back to reference Culleton BF, Larson MG, Kannel WB, Levy D. Serum uric acid and risk for cardiovascular disease and death: the Framingham heart study. Ann Intern Med. 1999;131:7–13.CrossRef Culleton BF, Larson MG, Kannel WB, Levy D. Serum uric acid and risk for cardiovascular disease and death: the Framingham heart study. Ann Intern Med. 1999;131:7–13.CrossRef
30.
go back to reference Moriarity JT, Folsom AR, Iribarren C, Nieto FJ, Rosamond WD. Serum uric acid and risk of coronary heart disease: Atherosclerosis Risk in Communities (ARIC) Study. Ann Epidemiol. 2000;10:136–43.CrossRef Moriarity JT, Folsom AR, Iribarren C, Nieto FJ, Rosamond WD. Serum uric acid and risk of coronary heart disease: Atherosclerosis Risk in Communities (ARIC) Study. Ann Epidemiol. 2000;10:136–43.CrossRef
31.
go back to reference Price KL, Sautin YY, Long DA, Zhang L, Miyazaki H, Mu W, et al. Human vascular smooth muscle cells express a urate transporter. J Am Soc Nephrol. 2006;17:1791–5.CrossRef Price KL, Sautin YY, Long DA, Zhang L, Miyazaki H, Mu W, et al. Human vascular smooth muscle cells express a urate transporter. J Am Soc Nephrol. 2006;17:1791–5.CrossRef
32.
go back to reference Johnson RJ, Kang DH, Feig D, Kivlighn S, Kanellis J, Watanabe S, et al. Is there a pathogenetic role for uric acid in hypertension and cardiovascular and renal disease? Hypertension. 2003;41:1183–90.CrossRef Johnson RJ, Kang DH, Feig D, Kivlighn S, Kanellis J, Watanabe S, et al. Is there a pathogenetic role for uric acid in hypertension and cardiovascular and renal disease? Hypertension. 2003;41:1183–90.CrossRef
33.
go back to reference Talaat KM, El-Sheikh AR. The effect of mild hyperuricemia on urinary transforming growth factor Beta and the progression of chronic kidney disease. Am J Nephrol. 2007;27:435–40.CrossRef Talaat KM, El-Sheikh AR. The effect of mild hyperuricemia on urinary transforming growth factor Beta and the progression of chronic kidney disease. Am J Nephrol. 2007;27:435–40.CrossRef
34.
go back to reference Sanchez-Lozada LG, Tapia E, Avila-Casado C, Soto V, Franco M, Santamaria J. Et.al. Mild hyperuricemia induces glomerular hypertension in normal rats. Am J Physiol Renal Physiol. 2002;283:F1105–10.CrossRef Sanchez-Lozada LG, Tapia E, Avila-Casado C, Soto V, Franco M, Santamaria J. Et.al. Mild hyperuricemia induces glomerular hypertension in normal rats. Am J Physiol Renal Physiol. 2002;283:F1105–10.CrossRef
Metadata
Title
Higher serum uric acid level is inversely associated with renal function assessed by cystatin C in a Japanese general population without chronic kidney disease: the KOBE study
Authors
Sachimi Kubo
Yoko Nishida
Yoshimi Kubota
Aya Higashiyama
Daisuke Sugiyama
Takumi Hirata
Naomi Miyamatsu
Ayumi Tanabe
Aya Hirata
Yukako Tatsumi
Aya Kadota
Kazuyo Kuwabara
Tomofumi Nishikawa
Yoshihiro Miyamoto
Tomonori Okamura
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Nephrology / Issue 1/2019
Electronic ISSN: 1471-2369
DOI
https://doi.org/10.1186/s12882-019-1291-4

Other articles of this Issue 1/2019

BMC Nephrology 1/2019 Go to the issue