Skip to main content

Advertisement

SpringerLink
Log in

Association between albumin-to-globulin ratio and long-term mortality in patients with chronic kidney disease: a cohort study

  • Nephrology - Original Paper
  • Published:
International Urology and Nephrology Aims and scope Submit manuscript

Abstract

Purpose

To examine whether albumin-to-globulin ratio (AGR) is correlated with long-term mortality in patients with chronic kidney disease (CKD), we performed this study using data from the National Health and Nutrition Examination Survey through 1999–2006.

Methods

3302 CKD patients were included. Patients’ baseline characteristics were collected. Multivariate Cox proportional hazards models were used to investigate the association between AGR and the study outcomes, including long-term all-cause and cardiovascular mortality. Subgroup analysis using the Cox proportional hazards model was performed as a sensitivity test.

Results

During a median follow-up duration of 122.00 months, 1627 (49.27%) deaths were recorded and 440 patients died from cardiovascular disease. In adjusted model 1, AGR ≥ 1.26 group was associated with a lower risk of long-term all-cause mortality HR 0.72, 95% CI 0.65–0.81) compared with AGR < 1.26 group. A similar result was obtained in adjusted model 2. In adjusted model 1, AGR ≥ 1.08 group was associated with a lower risk of long-term cardiovascular mortality (HR 0.59, 95% CI 0.45–0.78) compared with AGR < 1.08 group. In adjusted model 2, there was no significant association between AGR ≥ 1.08 group and a decreased risk of long-term cardiovascular mortality (HR 0.82, 95% CI 0.95–1.12) compared with AGR < 1.08 group. The association of AGR with long-term all-cause mortality differed by gender and age while the association of AGR with long-term cardiovascular mortality differed by age after multivariate adjustment.

Conclusion

AGR is a potential biomarker in risk predictions for long-term mortality in CKD patients, especially in males under age 65.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Webster AC, Nagler EV, Morton RL, Masson P (2017) Chronic kidney disease. Lancet 389(10075):1238–1252. https://doi.org/10.1016/S0140-6736(16)32064-5

    Article  PubMed  Google Scholar 

  2. Control CfD, Prevention (2019) Chronic kidney disease in the United States, 2019. In: US Department of Health and Human Services, Centers for Disease Control and Prevention

  3. Fox CS, Matsushita K, Woodward M, Bilo HJ, Chalmers J, Heerspink HJ, Lee BJ, Perkins RM, Rossing P, Sairenchi T, Tonelli M, Vassalotti JA, Yamagishi K, Coresh J, de Jong PE, Wen CP, Nelson RG, Chronic Kidney Disease Prognosis C (2012) Associations of kidney disease measures with mortality and end-stage renal disease in individuals with and without diabetes: a meta-analysis. Lancet 380(9854):1662–1673. https://doi.org/10.1016/S0140-6736(12)61350-6

    Article  PubMed  PubMed Central  Google Scholar 

  4. Foster MC, Coresh J, Hsu CY, Xie D, Levey AS, Nelson RG, Eckfeldt JH, Vasan RS, Kimmel PL, Schelling J, Simonson M, Sondheimer JH, Anderson AH, Akkina S, Feldman HI, Kusek JW, Ojo AO, Inker LA, Consortium CKDB, The CSI (2016) Serum beta-trace protein and beta2-microglobulin as predictors of ESRD, mortality, and cardiovascular disease in adults with CKD in the chronic renal insufficiency cohort (CRIC) study. Am J Kidney Dis 68(1):68–76. https://doi.org/10.1053/j.ajkd.2016.01.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Park M, Hsu CY, Go AS, Feldman HI, Xie D, Zhang X, Mifflin T, Waikar SS, Sabbisetti VS, Bonventre JV, Coresh J, Nelson RG, Kimmel PL, Kusek JW, Rahman M, Schelling JR, Vasan RS, Liu KD, Chronic Renal Insufficiency Cohort Study I, Consortium CKDB (2017) Urine kidney injury biomarkers and risks of cardiovascular disease events and all-cause death: the CRIC study. Clin J Am Soc Nephrol 12(5):761–771. https://doi.org/10.2215/CJN.08560816

    Article  PubMed  PubMed Central  Google Scholar 

  6. Edmonston D, Wojdyla D, Mehta R, Cai X, Lora C, Cohen D, Townsend RR, He J, Go AS, Kusek J, Weir MR, Isakova T, Pencina M, Wolf M, Investigators CS (2019) Single measurements of carboxy-terminal fibroblast growth factor 23 and clinical risk prediction of adverse outcomes in CKD. Am J Kidney Dis 74(6):771–781. https://doi.org/10.1053/j.ajkd.2019.05.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Peev V, Nayer A, Contreras G (2014) Dyslipidemia, malnutrition, inflammation, cardiovascular disease and mortality in chronic kidney disease. Curr Opin Lipidol 25(1):54–60. https://doi.org/10.1097/MOL.0000000000000045

    Article  CAS  PubMed  Google Scholar 

  8. Zhang B, Yu W, Zhou LQ, He ZS, Shen C, He Q, Li J, Liu LB, Wang C, Chen XY, Fan Y, Hu S, Zhang L, Han WK, Jin J (2015) Prognostic significance of preoperative albumin-globulin ratio in patients with upper tract urothelial carcinoma. PLoS ONE 10(12):e0144961. https://doi.org/10.1371/journal.pone.0144961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wu PP, Hsieh YP, Kor CT, Chiu PF (2019) Association between albumin-globulin ratio and mortality in patients with chronic kidney disease. J Clin Med 8:11. https://doi.org/10.3390/jcm8111991

    Article  CAS  Google Scholar 

  10. Chen TC, Parker JD, Clark J, Shin HC, Rammon JR, Burt VL (2018) National Health and nutrition examination survey: estimation procedures, 2011–2014. Vital Health Stat 2(177):1–26

    Google Scholar 

  11. Levey AS, Stevens LA (2010) Estimating GFR using the CKD Epidemiology Collaboration (CKD-EPI) creatinine equation: more accurate GFR estimates, lower CKD prevalence estimates, and better risk predictions. Am J Kidney Dis 55(4):622–627. https://doi.org/10.1053/j.ajkd.2010.02.337

    Article  PubMed  PubMed Central  Google Scholar 

  12. Selvin E, Manzi J, Stevens LA, Van Lente F, Lacher DA, Levey AS, Coresh J (2007) Calibration of serum creatinine in the National Health and Nutrition Examination Surveys (NHANES) 1988–1994, 1999–2004. Am J Kidney Dis 50(6):918–926. https://doi.org/10.1053/j.ajkd.2007.08.020

    Article  CAS  PubMed  Google Scholar 

  13. Murphy D, McCulloch CE, Lin F, Banerjee T, Bragg-Gresham JL, Eberhardt MS, Morgenstern H, Pavkov ME, Saran R, Powe NR, Hsu CY, Centers for Disease C, Prevention Chronic Kidney Disease Surveillance T (2016) Trends in prevalence of chronic kidney disease in the United States. Ann Intern Med 165(7):473–481. https://doi.org/10.7326/M16-0273

    Article  PubMed  PubMed Central  Google Scholar 

  14. Cheung CL, Sahni S, Cheung BM, Sing CW, Wong IC (2015) Vitamin K intake and mortality in people with chronic kidney disease from NHANES III. Clin Nutr 34(2):235–240. https://doi.org/10.1016/j.clnu.2014.03.011

    Article  CAS  PubMed  Google Scholar 

  15. Suh B, Park S, Shin DW, Yun JM, Keam B, Yang HK, Ahn E, Lee H, Park JH, Cho B (2014) Low albumin-to-globulin ratio associated with cancer incidence and mortality in generally healthy adults. Ann Oncol 25(11):2260–2266. https://doi.org/10.1093/annonc/mdu274

    Article  CAS  PubMed  Google Scholar 

  16. Lv GY, An L, Sun XD, Hu YL, Sun DW (2018) Pretreatment albumin to globulin ratio can serve as a prognostic marker in human cancers: a meta-analysis. Clin Chim Acta 476:81–91. https://doi.org/10.1016/j.cca.2017.11.019

    Article  CAS  PubMed  Google Scholar 

  17. Zhang H, Zhang B, Zhu K, Wu C, Gao L, Sun X, Liu C, Wang C (2019) Preoperative albumin-to-globulin ratio predicts survival in patients with non-small-cell lung cancer after surgery. J Cell Physiol 234(3):2471–2479. https://doi.org/10.1002/jcp.26766

    Article  CAS  PubMed  Google Scholar 

  18. Li K, Fu W, Bo Y, Zhu Y (2018) Effect of albumin-globulin score and albumin to globulin ratio on survival in patients with heart failure: a retrospective cohort study in China. BMJ Open 8(7):e022960. https://doi.org/10.1136/bmjopen-2018-022960

    Article  PubMed  PubMed Central  Google Scholar 

  19. Niedziela JT, Hudzik B, Szygula-Jurkiewicz B, Nowak JU, Polonski L, Gasior M, Rozentryt P (2018) Albumin-to-globulin ratio as an independent predictor of mortality in chronic heart failure. Biomark Med 12(7):749–757. https://doi.org/10.2217/bmm-2017-0378

    Article  CAS  PubMed  Google Scholar 

  20. Bharadwaj S, Ginoya S, Tandon P, Gohel TD, Guirguis J, Vallabh H, Jevenn A, Hanouneh I (2016) Malnutrition: laboratory markers vs nutritional assessment. Gastroenterol Rep (Oxf) 4(4):272–280. https://doi.org/10.1093/gastro/gow013

    Article  Google Scholar 

  21. Gatta A, Verardo A, Bolognesi M (2012) Hypoalbuminemia. Intern Emerg Med 7(3):193–199

    Article  Google Scholar 

  22. Feinstein AR, Petersdorf RG (1956) The clinical significance of hyperglobulinemia. I. Diagnostic implications. Ann Intern Med 44(5):899–924. https://doi.org/10.7326/0003-4819-44-5-899

    Article  CAS  PubMed  Google Scholar 

  23. He J, Pan H, Liang W, Xiao D, Chen X, Guo M, He J (2017) Prognostic Effect of albumin-to-globulin ratio in patients with solid tumors: a systematic review and meta-analysis. J Cancer 8(19):4002–4010. https://doi.org/10.7150/jca.21141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mihai S, Codrici E, Popescu ID, Enciu AM, Albulescu L, Necula LG, Mambet C, Anton G, Tanase C (2018) Inflammation-related mechanisms in chronic kidney disease prediction, progression, and outcome. J Immunol Res 2018:2180373. https://doi.org/10.1155/2018/2180373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Zoccali C, Vanholder R, Massy ZA, Ortiz A, Sarafidis P, Dekker FW, Fliser D, Fouque D, Heine GH, Jager KJ, Kanbay M, Mallamaci F, Parati G, Rossignol P, Wiecek A, London G, European R, Cardiovascular Medicine Working Group of the European Renal Association—European Dialysis Transplantation A (2017) The systemic nature of CKD. Nat Rev Nephrol 13(6):344–358. https://doi.org/10.1038/nrneph.2017.52

    Article  PubMed  Google Scholar 

  26. Amdur RL, Feldman HI, Gupta J, Yang W, Kanetsky P, Shlipak M, Rahman M, Lash JP, Townsend RR, Ojo A, Roy-Chaudhury A, Go AS, Joffe M, He J, Balakrishnan VS, Kimmel PL, Kusek JW, Raj DS, Investigators CS (2016) Inflammation and progression of CKD: the CRIC study. Clin J Am Soc Nephrol 11(9):1546–1556. https://doi.org/10.2215/CJN.13121215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ritchie J, Assi LK, Burmeister A, Hoefield R, Cockwell P, Kalra PA (2015) Association of serum Ig free light chains with mortality and ESRD among patients with nondialysis-dependent CKD. Clin J Am Soc Nephrol 10(5):740–749. https://doi.org/10.2215/CJN.09660914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Tuegel C, Katz R, Alam M, Bhat Z, Bellovich K, de Boer I, Brosius F, Gadegbeku C, Gipson D, Hawkins J, Himmelfarb J, Ju W, Kestenbaum B, Kretzler M, Robinson-Cohen C, Steigerwalt S, Bansal N (2018) GDF-15, galectin 3, soluble ST2, and risk of mortality and cardiovascular events in CKD. Am J Kidney Dis 72(4):519–528. https://doi.org/10.1053/j.ajkd.2018.03.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Iorember FM (2018) Malnutrition in chronic kidney disease. Front Pediatrics 6:161. https://doi.org/10.3389/fped.2018.00161

    Article  Google Scholar 

  30. Zha Y, Qian Q (2017) Protein Nutrition and Malnutrition in CKD and ESRD. Nutrients 9:3. https://doi.org/10.3390/nu9030208

    Article  CAS  Google Scholar 

  31. Friedman AN, Fadem SZ (2010) Reassessment of albumin as a nutritional marker in kidney disease. J Am Soc Nephrol 21(2):223–230. https://doi.org/10.1681/ASN.2009020213

    Article  CAS  PubMed  Google Scholar 

  32. Sun J, Axelsson J, Machowska A, Heimburger O, Barany P, Lindholm B, Lindstrom K, Stenvinkel P, Qureshi AR (2016) Biomarkers of cardiovascular disease and mortality risk in patients with advanced CKD. Clin J Am Soc Nephrol 11(7):1163–1172. https://doi.org/10.2215/CJN.10441015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Alves FC, Sun J, Qureshi AR, Dai L, Snaedal S, Barany P, Heimburger O, Lindholm B, Stenvinkel P (2018) The higher mortality associated with low serum albumin is dependent on systemic inflammation in end-stage kidney disease. PLoS ONE 13(1):e0190410. https://doi.org/10.1371/journal.pone.0190410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank participants and staff of the NHANES.

Funding

The authors received no specific funding for this work.

Author information

Authors and Affiliations

  1. Department of Nephrology, Hunan Key Laboratory of Kidney Disease and Blood Purification, The Second Xiangya Hospital of Central South University, Changsha, Hunan, China

    Mengru Zeng, Yu Liu, Fuyou Liu, Youming Peng, Lin Sun & Li Xiao

Authors
  1. Mengru Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fuyou Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Youming Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Li Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FL and LX designed the study. MZ and YL analysed and interpreted the data. MZ drafted the manuscript. YP and LS revised the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Li Xiao.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethics approval

NHANES was approved by the NCHS Research Ethics Review Board (ERB) and all participants provided written informed consent. The data of ERB approval can found at the website, https://www.cdc.gov/nchs/nhanes/irba98.htm. The approval numbers are protocol #98–12 for NHANES 1999–2004 and protocol #2005–06 for NHANES 2005–2006. Given it was an analysis of anonymous data, the Central South University Institutional Review Board waived the need for reviewing the study.

Informed consent

All participants provided written informed consent in the NHANES.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zeng, M., Liu, Y., Liu, F. et al. Association between albumin-to-globulin ratio and long-term mortality in patients with chronic kidney disease: a cohort study. Int Urol Nephrol 52, 1103–1115 (2020). https://doi.org/10.1007/s11255-020-02453-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11255-020-02453-7

Keywords

Search

Navigation