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The associations of malnutrition and aging with fluid volume imbalance between intra- and extracellular water in patients with chronic kidney disease

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The journal of nutrition, health & aging

Abstract

Objectives

Fluid imbalance due to sodium retention and malnutrition can be characterized by the ratio of extracellular water (ECW) to intracellular water (ICW). We investigated whether the ECW/ICW ratio is a risk factor for adverse outcomes.

Design

Retrospective cohort study.

Setting and Participants

149 patients with chronic kidney disease from 2005 to 2009, who were followed until August 2013.

Measurements

Body fluid composition was measured by bioelectrical impedance analysis. Patients were categorized according to the ECW/ICW ratio tertile. Daily nutrient intake was estimated from 24-h dietary recall and analyzed using standard food composition tables. The main outcomes were adverse renal outcomes, as defined by a decline of 50% or more from the baseline glomerular filtration rate or initiation of renal replacement therapy, cardiovascular events, and all-cause mortality.

Results

The ECW/ICW ratio increased with downward ICW slope with age and renal dysfunction besides ECW excess with massive proteinuria. Sodium intake, protein intake, and calorie intake were negatively correlated with the ECW/ICW ratios due to the steeper decreasing ICW content with the decreased dietary intake than the decreasing ECW content. During a median 4.9-year follow up, patients in the highest tertile had the worst adverse renal outcomes (15.9 vs. 5.1 per 100 patient-years, P <0.001), cardiovascular events (4.1 vs. 0.3 per 100 patient-years, P = 0.002), and mortality (11.2 vs. 1.3 per 100 patient-years, P <0.001). The adjusted hazard ratio (95% confidence intervals) for adverse renal outcomes, cardiovascular events, and mortality were 1.15 (1.03–1.26), 1.12 (0.93–1.31), and 1.29 (1.11–1.50), respectively.

Conclusion

Fluid imbalance between ICW and ECW occurring in malnourished and elderly patients with chronic kidney disease may explain the reserve capacity for volume overload and is associated with adverse renal outcomes and all-cause mortality.

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References

  1. KDIGO 2012 clinical practice guideline for the evaluation and management of chronic kidney disease. Kidney Int Suppl. 2013:S1–150.

    Google Scholar 

  2. Alvarez-Lara MA, Martin-Malo A, Espinosa M, Rodriguez-Benot A, Aljama P. Blood pressure and body water distribution in chronic renal failure patients. Nephrol Dial Transplant. 2001;16 Suppl 1:94–97. doi: 10.1093/ndt/16.suppl_1.94

    Article  PubMed  Google Scholar 

  3. Ledingham JM. Sodium retention and volume expansion as mechanisms. Am J Hypertens. 1991;4(10 Pt 2):534S–540S. doi: 10.1093/ajh/4.10.534S

    PubMed  CAS  Google Scholar 

  4. Campbell KL, Ash S, Bauer JD, Davies PS. Evaluation of nutrition assessment tools compared with body cell mass for the assessment of malnutrition in chronic kidney disease. J Ren Nutr. 2007;17:189–195. doi: 10.1053/j.jrn.2006.12.005

    Article  PubMed  Google Scholar 

  5. Bortner CD, Cidlowski JA. Cell shrinkage and monovalent cation fluxes: role in apoptosis. Arch Biochem Biophys. 2007;462:176–188. doi: 10.1016/j. abb.2007.01.020

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  6. Lang F, Ritter M, Gamper N, Huber S, Fillon S, Tanneur V, Lepple-Wienhues A, Szabo I, Gulbins E. Cell volume in the regulation of cell proliferation and apoptotic cell death. Cell Physiol Biochem. 2000;10:417–428. doi:10.1159/000016367

    Article  PubMed  CAS  Google Scholar 

  7. Franco R, Bortner CD, Cidlowski JA. Potential roles of electrogenic ion transport and plasma membrane depolarization in apoptosis. J Membr Biol. 2006;209:43–58. doi: 10.1007/s00232-005-0837-5

    Article  PubMed  CAS  Google Scholar 

  8. Maeno E, Ishizaki Y, Kanaseki T, Hazama A, Okada Y. Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci U S A. 2000;97:9487–9492. doi: 10.1073/pnas.140216197

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  9. Wehner F, Olsen H, Tinel H, Kinne-Saffran E, Kinne RK. Cell volume regulation: osmolytes, osmolyte transport, and signal transduction. Rev Physiol Biochem Pharmacol. 2003;148:1–80. doi: 10.1007/s10254-003-0009-x

    PubMed  CAS  Google Scholar 

  10. Bonanni A, Mannucci I, Verzola D, Sofia A, Saffioti S, Gianetta E, Garibotto G. Protein-energy wasting and mortality in chronic kidney disease. Int J Environ Res Public Health. 2011;8:1631–1654. doi: 10.3390/ijerph8051631

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kovesdy CP, Kalantar-Zadeh K. Why is protein-energy wasting associated with mortality in chronic kidney disease? Semin Nephrol. 2009;29:3–14. doi: 10.1016/j. semnephrol.2008.10.002

  12. Agarwal R. Body mass index-mortality paradox in hemodialysis: can it be explained by blood pressure? Hypertension. 2011;58:1014–1020. doi: 10.1161/ HYPERTENSIONAHA.111.180091

  13. Cha K, Brown EF, Wilmore DW. A new bioelectrical impedance method for measurement of the erythrocyte sedimentation rate. Physiol Meas. 1994;15:499–508. doi:10.1088/0967-3334/15/4/011

    Article  PubMed  CAS  Google Scholar 

  14. Zhu Y, Pandya BJ, Choi HK. Prevalence of gout and hyperuricemia in the US general population: the National Health and Nutrition Examination Survey 2007-2008. Arthritis Rheum. 2011;63:3136–3141. doi: 10.1002/art.30520

    Article  PubMed  Google Scholar 

  15. Matsuo S, Imai E, Horio M, Yasuda Y, Tomita K, Nitta K, Yamagata K, Tomino Y, Yokoyama H, Hishida A; Collaborators developing the Japanese equation for estimated GFR. Revised equations for estimated GFR from serum creatinine in Japan. Am J Kidney Dis. 2009;53:982–992. doi: 10.1053/j.ajkd.2008.12.034

    Article  PubMed  CAS  Google Scholar 

  16. Calhoun DA, Jones D, Textor S, Goff DC, Murphy TP, Toto RD, White A, Cushman WC, White W, Sica D, Ferdinand K, Giles TD, Falkner B, Carey RM. Resistant hypertension: diagnosis, evaluation, and treatment. A scientific statement from the American Heart Association Professional Education Committee of the Council for High Blood Pressure Research. Hypertension. 2008;51:1403–1419. doi: 10.1161/HYPERTENSIONAHA.108.189141

    PubMed  CAS  Google Scholar 

  17. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL, Jones DW, Materson BJ, Oparil S, Wright JT, Roccella EJ; National Heart, Lung, and Blood Institute Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure; National High Blood Pressure Education Program Coordinating Committee. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA. 2003;289:2560–2572. doi:10.1001/jama.289.19.2560

    Article  PubMed  CAS  Google Scholar 

  18. Amraoui F, Bos S, Vogt L, van den Born BJ. Long-term renal outcome in patients with malignant hypertension: a retrospective cohort study. BMC Nephrol. 2012;13:71. doi: 10.1186/1471-2369-13-71

    Article  PubMed  PubMed Central  Google Scholar 

  19. Parsa A, Kao WH, Xie D, Astor BC, Li M, Hsu CY, Feldman HI, Parekh RS, Kusek JW, Greene TH, Fink JC, Anderson AH, Choi MJ, Wright JT Jr, Lash JP, Freedman BI, Ojo A, Winkler CA, Raj DS, Kopp JB, He J, Jensvold NG, Tao K, Lipkowitz MS, Appel LJ; AASK Study Investigators; CRIC Study Investigators. APOL1 risk variants, race, and progression of chronic kidney disease. N Engl J Med. 2013;369:2183–2196. doi: 10.1056/NEJMoa1310345

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  20. Tsuruya K, Yoshida H, Nagata M, Kitazono T, Hirakata H, Iseki K, Moriyama T, Yamagata K, Yoshida H, Fujimoto S, Asahi K, Kurahashi I, Ohashi Y, Watanabe T. Association of the triglycerides to high-density lipoprotein cholesterol ratio with the risk of chronic kidney disease: analysis in a large Japanese population. Atherosclerosis. 2014;233:260–267. doi: 10.1016/j.atherosclerosis.2013.12.037

    Article  PubMed  CAS  Google Scholar 

  21. Furstenberg A, Davenport A. Comparison of multifrequency bioelectrical impedance analysis and dual-energy X-ray absorptiometry assessments in outpatient hemodialysis patients. Am J Kidney Dis. 2011;57:123–129. doi: 10.1053/j. ajkd.2010.05.022

    Article  PubMed  Google Scholar 

  22. Fan S, Sayed RH, Davenport A. Extracellular volume expansion in peritoneal dialysis patients. Int J Artif Organs. 2012;35:338–345. doi: 10.5301/ijao.5000080

    Article  PubMed  CAS  Google Scholar 

  23. Guo Q, Yi C, Li J, Wu X, Yang X, Yu X. Prevalence and risk factors of fluid overload in Southern Chinese continuous ambulatory peritoneal dialysis patients. PLoS One. 2013;8:e53294. doi: 10.1371/journal.pone.0053294

    Article  CAS  Google Scholar 

  24. Hung SC, Lin YP, Huang HL, Pu HF, Tarng DC. Aldosterone and mortality in hemodialysis patients: role of volume overload. PLoS One. 2013;8:e57511. doi: 10.1371/journal.pone.0057511

    Article  CAS  Google Scholar 

  25. Jacobs LH, van de Kerkhof JJ, Mingels AM, Passos VL, Kleijnen VW, Mazairac AH, van der Sande FM, Wodzig WK, Konings CJ, Leunissen KM, van Dieijen-Visser MP, Kooman JP. Inflammation, overhydration and cardiac biomarkers in haemodialysis patients: a longitudinal study. Nephrol Dial Transplant. 2010;25:243–248. doi: 10.1093/ndt/gfp417

    Article  PubMed  CAS  Google Scholar 

  26. Kumar S, Khosravi M, Massart A, Davenport A. Is there a role for N-terminal probrain-type natriuretic peptide in determining volume status in haemodialysis patients? Nephron Clin Pract. 2012;122:33–37. doi: 10.1159/000348510

    Article  PubMed  CAS  Google Scholar 

  27. Susantitaphong P, Laowaloet S, Tiranathanagul K, Chulakadabba A, Katavetin P, Praditpornsilpa K, Tungsanga K, Eiam-Ong S. Reliability of blood pressure parameters for dry weight estimation in hemodialysis patients. Ther Apher Dial. 2013;17:9–15. doi: 10.1111/j.1744-9987.2012.01136.x

    Article  PubMed  CAS  Google Scholar 

  28. Ohashi Y, Otani T, Tai R, Tanaka Y, Sakai K, Aikawa A. Assessment of body composition using dry mass index and ratio of total body water to estimated volume based on bioelectrical impedance analysis in chronic kidney disease patients. J Ren Nutr. 2013;23:28–36. doi: 10.1053/j.jrn.2011.12.006

    Article  PubMed  Google Scholar 

  29. Weir MR. Body mass index-mortality paradox in hemodialysis patients: blood pressure, blood volume, and nutritional status. Hypertension. 2011;58:989–990. doi: 10.1161/HYPERTENSIONAHA.111.181818

    Article  PubMed  CAS  Google Scholar 

  30. Ekinci EI, Clarke S, Thomas MC, Moran JL, Cheong K, Mac Isaac RJ, Jerums G.. Dietary salt intake and mortality in patients with type 2 diabetes. Diabetes Care. 2011;34:703–709. doi: 10.2337/dc10-1723

    Article  PubMed  PubMed Central  Google Scholar 

  31. 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;17:2928–2936. doi: 10.1681/ASN.2005101101

    Article  PubMed  Google Scholar 

  32. Thomas MC, Moran J, Forsblom C, Harjutsalo V, Thorn L, Ahola A, Wadén J, Tolonen N, Saraheimo M, Gordin D, Groop PH; FinnDiane Study Group. The association between dietary sodium intake, ESRD, and all-cause mortality in patients with type 1 diabetes. Diabetes Care. 2011;34:861–866. doi: 10.2337/dc10-1722

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  33. Clarys JP, Martin AD, Marfell-Jones MJ, Janssens V, Caboor D, Drinkwater DT. Human body composition: A review of adult dissection data. Am J Hum Biol. 1999;11:167–174. doi: 10.1002/(SICI)1520-6300(1999)11:2

    Article  PubMed  Google Scholar 

  34. Kyle UG, Genton L, Hans D, Karsegard VL, Michel JP, Slosman DO, Pichard C. Total body mass, fat mass, fat-free mass, and skeletal muscle in older people: crosssectional differences in 60-year-old persons. J Am Geriatr Soc. 2001;49:1633–1640. doi: 10.1111/j.1532-5415.2001.49272.x

    Article  PubMed  CAS  Google Scholar 

  35. Van Pottelbergh G, Matheï C, Vaes B, Adriaensen W, Gruson D, Degryse JM. The influence of renal function on vitamin D metabolism in the very elderly. J Nutr Health Aging. 2013;17:107–111. doi: 10.1007/s12603-012-0094-0.

    Article  PubMed  CAS  Google Scholar 

  36. Lang E, Qadri SM, Lang F. Killing me softly - suicidal erythrocyte death. Int J Biochem Cell Biol. 2012;44:1236–1243. doi: 10.1016/j.biocel.2012.04.019

    Article  PubMed  CAS  Google Scholar 

  37. Lang F, Gulbins E, Szabo I, Lepple-Wienhues A, Huber SM, Duranton C, Lang KS, Lang PA, Wieder T. Cell volume and the regulation of apoptotic cell death. J Mol Recognit. 2004;17:473–480. doi: 10.1002/jmr.705

    Article  PubMed  CAS  Google Scholar 

  38. Ahmed MS, Abed M, Voelkl J, Lang F. Triggering of suicidal erythrocyte death by uremic toxin indoxyl sulfate. BMC Nephrol. 2013;14:244. doi: 10.1186/1471-2369-14-244

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  39. Ahmed MS, Langer H, Abed M, Voelkl J, Lang F. The uremic toxin acrolein promotes suicidal erythrocyte death. Kidney Blood Press Res. 2013;37:158–167. doi: 10.1159/000350141

    Article  PubMed  Google Scholar 

  40. Lin YP, Yu WC, Hsu TL, Ding PY, Yang WC, Chen CH. The extracellular fluid-tointracellular fluid volume ratio is associated with large-artery structure and function in hemodialysis patients. Am J Kidney Dis. 2003;42:990–999. doi: 10.1016/j. ajkd.2003.07.002

    Article  PubMed  Google Scholar 

  41. Humphreys MH. Mechanisms and management of nephrotic edema. Kidney Int. 1994;45:266–81. doi:10.1038/ki.1994.33

    Article  PubMed  CAS  Google Scholar 

  42. Chen W, Guo LJ, Wang T. Extracellular water/intracellular water is a strong predictor of patient survival in incident peritoneal dialysis patients. Blood Purif. 2007;25(3):260–266. doi:10.1159/000101699.

    Article  PubMed  Google Scholar 

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Correspondence to Yasushi Ohashi.

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Ohashi, Y., Tai, R., Aoki, T. et al. The associations of malnutrition and aging with fluid volume imbalance between intra- and extracellular water in patients with chronic kidney disease. J Nutr Health Aging 19, 986–993 (2015). https://doi.org/10.1007/s12603-015-0658-x

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  • DOI: https://doi.org/10.1007/s12603-015-0658-x

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