Skip to main content
SpringerLink
Log in

Serum uric acid and risk of incident diabetes in middle-aged and elderly Chinese adults: prospective cohort study

  • Research Article
  • Published:
Frontiers of Medicine Aims and scope Submit manuscript

Abstract

The association between serum uric acid and the risk of incident diabetes in Chinese adults remains unknown. This study aimed to investigate this association in a community-dwelling population aged ≥ 40 years in Shanghai, China. Oral glucose tole3rance test was conducted during baseline and follow-up visits. Relative risk regression was utilized to examine the associations between baseline gender-specific serum uric acid levels and incident diabetes risk. A total of 613 (10.3%) incident diabetes cases were identified during the follow-up visit after 4.5 years. Fasting plasma glucose, postload glucose, and glycated hemoglobin A1c during the follow-up visit progressively increased across the sex-specific quartiles of serum uric acid (all Ps < 0.05). The incidence rate of diabetes increased across the quartiles of serum uric acid (7.43%, 8.77%, 11.47%, and 13.43%). Multivariate adjusted regression analysis revealed that individuals in the highest quartile had 1.36-fold increased risk of diabetes compared with those in the lowest quartile of serum uric acid (odds ratio (95% confidence interval) = 1.36 (1.06–1.73)). Stratified analysis indicated that the association was only observed in women. Accordingly, serum uric acid was associated with the increased risk of incident diabetes among middle-aged and elderly Chinese women.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bommer C, Heesemann E, Sagalova V, Manne-Goehler J, Atun R, Bärnighausen T, Vollmer S. The global economic burden of diabetes in adults aged 20–79 years: a cost-of-illness study. Lancet Diabetes Endocrinol 2017; 5(6): 423–430

    Article  PubMed  Google Scholar 

  2. Chen-Xu M, Yokose C, Rai SK, Pillinger MH, Choi HK. Contemporary prevalence of gout and hyperuricemia in the United States and decadal trends: the National Health and Nutrition Examination Survey, 2007–2016. Arthritis Rheumatol 2019; 71(6): 991–999

    Article  PubMed  PubMed Central  Google Scholar 

  3. Juraschek SP, McAdams-Demarco M, Miller ER, Gelber AC, Maynard JW, Pankow JS, Young H, Coresh J, Selvin E. Temporal relationship between uric acid concentration and risk of diabetes in a community-based study population. Am J Epidemiol 2014; 179(6): 684–691

    Article  PubMed  PubMed Central  Google Scholar 

  4. Major TJ, Dalbeth N, Stahl EA, Merriman TR. An update on the genetics of hyperuricaemia and gout. Nat Rev Rheumatol 2018; 14 (6): 341–353

    Article  CAS  PubMed  Google Scholar 

  5. White J, Sofat R, Hemani G, Shah T, Engmann J, Dale C, Shah S, Kruger FA, Giambartolomei C, Swerdlow DI, Palmer T, McLachlan S, Langenberg C, Zabaneh D, Lovering R, Cavadino A, Jefferis B, Finan C, Wong A, Amuzu A, Ong K, Gaunt TR, Warren H, Davies TL, Drenos F, Cooper J, Ebrahim S, Lawlor DA, Talmud PJ, Humphries SE, Power C, Hypponen E, Richards M, Hardy R, Kuh D, Wareham N, Ben-Shlomo Y, Day IN, Whincup P, Morris R, Strachan MWJ, Price J, Kumari M, Kivimaki M, Plagnol V, Whittaker JC, Smith GD, Dudbridge F, Casas JP, Holmes MV, Hingorani AD; UCLEB (University College London-London School of Hygiene & Tropical Medicine-Edinburgh-Bristol Consortium). Plasma urate concentration and risk of coronary heart disease: a Mendelian randomisation analysis. Lancet Diabetes Endocrinol 2016; 4(4): 327–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Bhole V, Choi JW, Kim SW, de Vera M, Choi H. Serum uric acid levels and the risk of type 2 diabetes: a prospective study. Am J Med 2010; 123(10): 957–961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Dai CY, Chuang WL, Ho CK, Ou TT, Huang JF, Hsieh MY, Yu ML. High serum uric acid as a novel risk factor for type 2 diabetes: response to Dehghan et al. Diabetes Care 2008; 31(9): e67

    Article  PubMed  Google Scholar 

  8. Dehghan A, van Hoek M, Sijbrands EJ, Hofman A, Witteman JC. High serum uric acid as a novel risk factor for type 2 diabetes. Diabetes Care 2008; 31(2): 361–362

    Article  CAS  PubMed  Google Scholar 

  9. Boner G. Uric acid and diabetes. Lancet 1982; 320(8309): 1224

    Article  Google Scholar 

  10. Han T, Meng X, Shan R, Zi T, Li Y, Ma H, Zhao Y, Shi D, Qu R, Guo X, Liu L, Na L, Li Y, Sun C. Temporal relationship between hyperuricemia and obesity, and its association with future risk of type 2 diabetes. Int J Obes 2018; 42(7): 1336–1344

    Article  CAS  Google Scholar 

  11. Liu J, Tao L, Zhao Z, Mu Y, Zou D, Zhang J, Guo X. Two-year changes in hyperuricemia and risk of diabetes: a five-year prospective cohort study. J Diabetes Res 2018; 2018: 6905720

    PubMed  PubMed Central  Google Scholar 

  12. Wang Y, Chi J, Che K, Chen Y, Sun X, Wang Y, Wang Z. Fasting plasma glucose and serum uric acid levels in a general Chinese population with normal glucose tolerance: a U-shaped curve. PLoS One 2017; 12(6): e0180111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Tuomilehto J, Zimmet P, Wolf E, Taylor R, Ram P, King H. Plasma uric acid level and its association with diabetes mellitus and some biologic parameters in a biracial population of Fiji. Am J Epidemiol 1988; 127(2): 321–336

    Article  CAS  PubMed  Google Scholar 

  14. Keenan T, Zhao W, Rasheed A, Ho WK, Malik R, Felix JF, Young R, Shah N, Samuel M, Sheikh N, Mucksavage ML, Shah O, Li J, Morley M, Laser A, Mallick NH, Zaman KS, Ishaq M, Rasheed SZ, Memon FU, Ahmed F, Hanif B, Lakhani MS, Fahim M, Ishaq M, Shardha NK, Ahmed N, Mahmood K, Iqbal W, Akhtar S, Raheel R, O’Donnell CJ, Hengstenberg C, März W, Kathiresan S, Samani N, Goel A, Hopewell JC, Chambers J, Cheng YC, Sharma P, Yang Q, Rosand J, Boncoraglio GB, Kazmi SU, Hakonarson H, Köttgen A, Kalogeropoulos A, Frossard P, Kamal A, Dichgans M, Cappola T, Reilly MP, Danesh J, Rader DJ, Voight BF, Saleheen D. Causal assessment of serum urate levels in cardiometabolic diseases through a Mendelian randomization study. J Am Coll Cardiol 2016; 67(4): 407–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kivity S, Kopel E, Steinlauf S, Segev S, Sidi Y, Olchovsky D. The association between serum uric acid and diabetes mellitus is stronger in women. J Womens Health (Larchmt) 2013; 22(9): 782–789

    Article  Google Scholar 

  16. Lu J, Zhang J, Du R, Wang T, Xu M, Xu Y, Wang W, Bi Y, Li D, Chen Y, Ning G. Age at menarche is associated with the prevalence of non-alcoholic fatty liver disease later in life. J Diabetes 2017; 9 (1): 53–60

    Article  CAS  PubMed  Google Scholar 

  17. Li M, Xu Y, Xu M, Ma L, Wang T, Liu Y, Dai M, Chen Y, Lu J, Liu J, Bi Y, Ning G. Association between nonalcoholic fatty liver disease (NAFLD) and osteoporotic fracture in middle-aged and elderly Chinese. J Clin Endocrinol Metab 2012; 97(6): 2033–2038

    Article  CAS  PubMed  Google Scholar 

  18. Chen Y, Lu J, Huang Y, Wang T, Xu Y, Xu M, Li M, Wang W, Li D, Bi Y, Ning G. Association of previous schistosome infection with diabetes and metabolic syndrome: a cross-sectional study in rural China. J Clin Endocrinol Metab 2013; 98(2): E283–E287

    Article  CAS  PubMed  Google Scholar 

  19. Lee PH, Macfarlane DJ, Lam TH, Stewart SM. Validity of the International Physical Activity Questionnaire Short Form (IPAQSF): a systematic review. Int J Behav Nutr Phys Act 2011; 8(1): 115

    Article  PubMed  PubMed Central  Google Scholar 

  20. Lloyd-Jones DM, Hong Y, Labarthe D, Mozaffarian D, Appel LJ, Van Horn L, Greenlund K, Daniels S, Nichol G, Tomaselli GF, Arnett DK, Fonarow GC, Ho PM, Lauer MS, Masoudi FA, Robertson RM, Roger V, Schwamm LH, Sorlie P, Yancy CW, Rosamond WD; American Heart Association Strategic Planning Task Force and Statistics Committee. Defining and setting national goals for cardiovascular health promotion and disease reduction: the American Heart Association’s strategic Impact Goal through 2020 and beyond. Circulation 2010; 121(4): 586–613

    Article  PubMed  Google Scholar 

  21. Pickering TG, Hall JE, Appel LJ, Falkner BE, Graves J, Hill MN, Jones DW, Kurtz T, Sheps SG, Roccella EJ; Subcommittee of Professional and Public Education of the American Heart Association Council on High Blood Pressure Research. Recommendations for blood pressure measurement in humans and experimental animals: Part 1: blood pressure measurement in humans: a statement for professionals from the Subcommittee of Professional and Public Education of the American Heart Association Council on High Blood Pressure Research. Hypertension 2005; 45(1): 142–161

    Article  CAS  PubMed  Google Scholar 

  22. Lin L, Peng K, Du R, Huang X, Lu J, Xu Y, Xu M, Chen Y, Bi Y, Wang W. Metabolically healthy obesity and incident chronic kidney disease: the role of systemic inflammation in a prospective study. Obesity (Silver Spring) 2017; 25(3): 634–641

    Article  CAS  Google Scholar 

  23. Hertz-Picciotto I, Rockhill B. Validity and efficiency of approximation methods for tied survival times in Cox regression. Biometrics 1997; 53(3): 1151–1156

    Article  CAS  PubMed  Google Scholar 

  24. McNutt LA, Wu C, Xue X, Hafner JP. Estimating the relative risk in cohort studies and clinical trials of common outcomes. Am J Epidemiol 2003; 157(10): 940–943

    Article  PubMed  Google Scholar 

  25. Zoppini G, Targher G, Negri C, Stoico V, Perrone F, Muggeo M, Bonora E. Elevated serum uric acid concentrations independently predict cardiovascular mortality in type 2 diabetic patients. Diabetes Care 2009; 32(9): 1716–1720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Meisinger C, Thorand B, Schneider A, Stieber J, Döring A, Löwel H. Sex differences in risk factors for incident type 2 diabetes mellitus: the MONICA Augsburg cohort study. Arch Intern Med 2002; 162(1): 82–89

    Article  PubMed  Google Scholar 

  27. Yamada T, Fukatsu M, Suzuki S, Wada T, Joh T. Elevated serum uric acid predicts impaired fasting glucose and type 2 diabetes only among Japanese women undergoing health checkups. Diabetes Metab 2011; 37(3): 252–258

    Article  CAS  PubMed  Google Scholar 

  28. Nakanishi N, Okamoto M, Yoshida H, Matsuo Y, Suzuki K, Tatara K. Serum uric acid and risk for development of hypertension and impaired fasting glucose or type II diabetes in Japanese male office workers. Eur J Epidemiol 2003; 18(6): 523–530

    Article  CAS  PubMed  Google Scholar 

  29. Levine W, Dyer AR, Shekelle RB, Schoenberger JA, Stamler J. Serum uric acid and 11.5-year mortality of middle-aged women: findings of the Chicago Heart Association Detection Project in Industry. J Clin Epidemiol 1989; 42(3): 257–267

    Article  CAS  PubMed  Google Scholar 

  30. Wingrove CS, Walton C, Stevenson JC. The effect of menopause on serum uric acid levels in non-obese healthy women. Metabolism 1998; 47(4): 435–438

    Article  CAS  PubMed  Google Scholar 

  31. Chou P, Lin KC, Lin HY, Tsai ST. Gender differences in the relationships of serum uric acid with fasting serum insulin and plasma glucose in patients without diabetes. J Rheumatol 2001; 28 (3): 571–576

    CAS  PubMed  Google Scholar 

  32. Johnson RJ, Nakagawa T, Sanchez-Lozada LG, Shafiu M, Sundaram S, Le M, Ishimoto T, Sautin YY, Lanaspa MA. Sugar, uric acid, and the etiology of diabetes and obesity. Diabetes 2013; 62 (10): 3307–3315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zhou Y, Fang L, Jiang L, Wen P, Cao H, He W, Dai C, Yang J. Uric acid induces renal inflammation via activating tubular NF-kB signaling pathway. PLoS One 2012; 7(6): e39738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Mazzali M, Hughes J, Kim YG, Jefferson JA, Kang DH, Gordon KL, Lan HY, Kivlighn S, Johnson RJ. Elevated uric acid increases blood pressure in the rat by a novel crystal-independent mechanism. Hypertension 2001; 38(5): 1101–1106

    Article  CAS  PubMed  Google Scholar 

  35. Nakagawa T, Tuttle KR, Short RA, Johnson RJ. Hypothesis: fructose-induced hyperuricemia as a causal mechanism for the epidemic of the metabolic syndrome. Nat Clin Pract Nephrol 2005; 1(2): 80–86

    Article  CAS  PubMed  Google Scholar 

  36. Li C, Hsieh MC, Chang SJ. Metabolic syndrome, diabetes, and hyperuricemia. Curr Opin Rheumatol 2013; 25(2): 210–216

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the field working staff for their contribution and the participants for their cooperation. This study was supported by the Ministry of Science and Technology of the People’s Republic of China (Nos. 2016YFC1305202 and 2016YFC1304904) and National Natural Science Foundation of China (Nos. 81670795 and 81870604). Yuhong Chen was supported by the Shanghai Shenkang Hospital Development Center for improving the control of type 2 diabetes in the suburbs of Shanghai (No. 16CR4020A).

Author information

Author notes

  1. Di Cheng, Chunyan Hu, Rui Du, and Hongyan Qi contributed equally to this work.

Authors and Affiliations

  1. Department of Endocrine and Metabolic Diseases, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, 200025, China

    Di Cheng, Chunyan Hu, Rui Du, Hongyan Qi, Lin Lin, Xueyan Wu, Lina Ma, Kui Peng, Mian Li, Min Xu, Yu Xu, Yufang Bi, Weiqing Wang & Jieli Lu

  2. Department of Endocrine and Metabolic Diseases, Ruijin Hospital North, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, 201821, China

    Lin Lin & Yuhong Chen

Authors
  1. Di Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chunyan Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rui Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hongyan Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lin Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xueyan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lina Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kui Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mian Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Min Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yu Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yufang Bi
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Weiqing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Yuhong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Jieli Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yuhong Chen or Jieli Lu.

Ethics declarations

Di Cheng, Chunyan Hu, Rui Du, Hongyan Qi, Lin Lin, XueyanWu, Lina Ma, Kui Peng, Mian Li, Min Xu, Yu Xu, Yufang Bi, Weiqing Wang, Yuhong Chen, and Jieli Lu declare that they have no conflict of interest. All procedures followed were in accordance with the ethical standards of the Institutional Review Board of Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine and with the Helsinki Declaration of 1975, as revised in 2000. Informed consent was obtained from all patients for being included in the study.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, D., Hu, C., Du, R. et al. Serum uric acid and risk of incident diabetes in middle-aged and elderly Chinese adults: prospective cohort study. Front. Med. 14, 802–810 (2020). https://doi.org/10.1007/s11684-019-0723-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11684-019-0723-7

Keywords

Search

Navigation