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Comparison of the malnutrition–inflammation score in chronic kidney disease patients and kidney transplant recipients

  • Nephrology - Original Paper
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Abstract

Background

Protein–energy wasting (PEW) is a common condition in patients with chronic kidney disease (CKD) including dialysis and kidney transplant recipients (TX) and frequently assessed with malnutrition–inflammation score (MIS). We hypothesized that (1) the MIS and PEW parameters are correlated with kidney function and (2) the MIS and PEW parameters are more severe in TX than in non-dialysis (ND) CKD patients with similar eGFR.

Methods

In this study, we matched 203 ND-CKD and 203 TX patients from two independently assembled cohorts of patients based on estimated glomerular filtration rate (eGFR) and compared various PEW parameters between the two groups using unadjusted and case-mix adjusted linear regression and conditional logistic regression analysis models.

Results

In the combined cohort (n = 406) of patients, the mean ± SD age was 57 ± 12 years; included 55 % men and 35 % diabetics; and demonstrated a mean ± SD baseline eGFR of 29 ± 11 ml/min/1.73 m2. The eGFR correlated positively with serum albumin (ρ = 0.26, p < 0.001) and negatively (ρ = −0.33, p < 0.001) with MIS. ND-CKD and TX patients had similar MIS, PEW parameters such as waist circumference, serum CRP, albumin, and leptin levels. After case-mix adjustment, TX status was associated with higher waist circumference (standardized coefficient: 0.187, p < 0.001), lower BMI (standardized coefficient: −0.204, p < 0.001), and lower SGA score (standardized coefficient: 0.156, p = 0.006).

Conclusions

We found associations between lower eGFR and various PEW measures in both the ND-CKD and TX populations. Additionally, we did not observe significant differences in the burden of PEW parameters between the CKD and TX populations.

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References

  1. Karadag F, Kirdar S, Karul AB, Ceylan E (2008) The value of C-reactive protein as a marker of systemic inflammation in stable chronic obstructive pulmonary disease. Eur J Intern Med 19:104–108

    Article  CAS  PubMed  Google Scholar 

  2. Carriere I, Dupuy AM, Lacroux A, Cristol JP, Delcourt C (2008) Biomarkers of inflammation and malnutrition associated with early death in healthy elderly people. J Am Geriatr Soc 56:840–846

    Article  PubMed Central  PubMed  Google Scholar 

  3. Nakamura K, Moriyama Y, Kariyazono H, Hamada N, Toyohira H, Taira A, Yamada K (1999) Influence of preoperative nutritional state on inflammatory response after surgery. Nutrition 15:834–841

    Article  CAS  PubMed  Google Scholar 

  4. Amparo FC, Cordeiro AC, Carrero JJ, Cuppari L, Lindholm B, Amodeo C, Kamimura MA (2013) Malnutrition-inflammation score is associated with handgrip strength in nondialysis-dependent chronic kidney disease patients. J Ren Nutr 23:283–287

    Article  PubMed  Google Scholar 

  5. Cuppari L, Meireles MS, Ramos CI, Kamimura MA (2014) Subjective global assessment for the diagnosis of protein–energy wasting in nondialysis-dependent chronic kidney disease patients. J Ren Nutr 24(6):385–389

    Article  PubMed  Google Scholar 

  6. Ikizler TA, Cano NJ, Franch H, Fouque D, Himmelfarb J, Kalantar-Zadeh K, Kuhlmann MK, Stenvinkel P, TerWee P, Teta D, Wang AY, Wanner C (2013) International Society of Renal N, Metabolism: prevention and treatment of protein energy wasting in chronic kidney disease patients: a consensus statement by the International Society of Renal Nutrition and Metabolism. Kidney Int 84:1096–1107

    Article  CAS  PubMed  Google Scholar 

  7. Rambod M, Bross R, Zitterkoph J, Benner D, Pithia J, Colman S, Kovesdy CP, Kopple JD, Kalantar-Zadeh K (2009) Association of malnutrition-inflammation score with quality of life and mortality in hemodialysis patients: a 5-year prospective cohort study. Am J Kidney Dis 53:298–309

    Article  PubMed  Google Scholar 

  8. Gracia-Iguacel C, Gonzalez-Parra E, Perez-Gomez MV, Mahillo I, Egido J, Ortiz A, Carrero JJ (2013) Prevalence of protein–energy wasting syndrome and its association with mortality in haemodialysis patients in a centre in Spain. Nefrologia 33:495–505

    PubMed  Google Scholar 

  9. Molnar MZ, Keszei A, Czira ME, Rudas A, Ujszaszi A, Haromszeki B, Kosa JP, Lakatos P, Sarvary E, Beko G, Fornadi K, Kiss I, Remport A, Novak M, Kalantar-Zadeh K, Kovesdy CP, Mucsi I (2010) Evaluation of the malnutrition-inflammation score in kidney transplant recipients. Am J Kidney Dis 56:102–111

    Article  PubMed  Google Scholar 

  10. ter Wee PM (2013) Protein energy wasting and transplantation. J Ren Nutr 23:246–249

    Article  PubMed  Google Scholar 

  11. Tutal E, Sezer S, Uyar ME, Bal Z, Demirci BG, Acar FN (2013) Evaluation of nutritional status in renal transplant recipients in accordance with changes in graft function. Transplant Proc 45:1418–1422

    Article  CAS  PubMed  Google Scholar 

  12. Kovesdy CP, George SM, Anderson JE, Kalantar-Zadeh K (2009) Outcome predictability of biomarkers of protein–energy wasting and inflammation in moderate and advanced chronic kidney disease. Am J Clin Nutr 90:407–414

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Molnar MZ, Czira ME, Rudas A, Ujszaszi A, Lindner A, Fornadi K, Kiss I, Remport A, Novak M, Kennedy SH, Rosivall L, Kovesdy CP, Mucsi I (2011) Association of the malnutrition-inflammation score with clinical outcomes in kidney transplant recipients. Am J Kidney Dis 58:101–108

    Article  PubMed  Google Scholar 

  14. Ujszaszi A, Czira ME, Fornadi K, Novak M, Mucsi I, Molnar MZ (2012) Quality of life and protein–energy wasting in kidney transplant recipients. Int Urol Nephrol 44:1257–1268

    Article  PubMed  Google Scholar 

  15. Czira ME, Lindner AV, Szeifert L, Molnar MZ, Fornadi K, Kelemen A, Laszlo G, Mucsi I, Keszei AP, Kennedy SH, Novak M (2011) Association between the malnutrition-inflammation score and depressive symptoms in kidney transplanted patients. Gen Hosp Psychiatry 33:157–165

    Article  PubMed  Google Scholar 

  16. Molnar MZ, Czira ME, Rudas A, Ujszaszi A, Haromszeki B, Kosa JP, Lakatos P, Beko G, Sarvary E, Varga M, Fornadi K, Novak M, Rosivall L, Kiss I, Remport A, Goldsmith DJ, Kovesdy CP, Mucsi I (2011) Association between the malnutrition-inflammation score and post-transplant anaemia. Nephrol Dial Transplant 26:2000–2006

    Article  CAS  PubMed  Google Scholar 

  17. Kim JC, Kalantar-Zadeh K, Kopple JD (2013) Frailty and protein–energy wasting in elderly patients with end stage kidney disease. J Am Soc Nephrol 24:337–351

    Article  PubMed  Google Scholar 

  18. Molnar MZ, Bunnapradist S, Huang E, Krishnan M, Nissenson AR, Kovesdy CP, Kalantar-Zadeh K (2012) Association of pre-transplant erythropoiesis-stimulating agent responsiveness with post-transplant outcomes. Nephrol Dial Transplant 27:3345–3351

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Fouque D, Kalantar-Zadeh K, Kopple J, Cano N, Chauveau P, Cuppari L, Franch H, Guarnieri G, Ikizler TA, Kaysen G, Lindholm B, Massy Z, Mitch W, Pineda E, Stenvinkel P, Trevino-Becerra A, Wanner C (2008) A proposed nomenclature and diagnostic criteria for protein–energy wasting in acute and chronic kidney disease. Kidney Int 73:391–398

    Article  CAS  PubMed  Google Scholar 

  20. Kalantar-Zadeh K, Kopple JD, Block G, Humphreys MH (2001) A malnutrition-inflammation score is correlated with morbidity and mortality in maintenance hemodialysis patients. Am J Kidney Dis 38:1251–1263

    Article  CAS  PubMed  Google Scholar 

  21. Amparo FC, Kamimura MA, Molnar MZ, Cuppari L, Lindholm B, Amodeo C, Carrero JJ, Cordeiro AC (2014) Diagnostic validation and prognostic significance of the malnutrition-inflammation score in nondialyzed chronic kidney disease patients. Nephrol Dial Transplant. doi:10.1093/ndt/gfu380

    PubMed  Google Scholar 

  22. Carrero JJ, Stenvinkel P, Cuppari L, Ikizler TA, Kalantar-Zadeh K, Kaysen G, Mitch WE, Price SR, Wanner C, Wang AY, ter Wee P, Franch HA (2013) Etiology of the protein–energy wasting syndrome in chronic kidney disease: a consensus statement from the International Society of Renal Nutrition and Metabolism (ISRNM). J Ren Nutr 23:77–90

    Article  PubMed  Google Scholar 

  23. Jassal SV, Schaubel DE, Fenton SS (2005) Baseline comorbidity in kidney transplant recipients: a comparison of comorbidity indices. Am J Kidney Dis 46:136–142

    Article  PubMed  Google Scholar 

  24. Levey A, Greene T, Kusek J, Beck G, Group MS (2000) A simplified equation to predict glomerular filtration rate from serum creatinine {Abstract}. J Am Soc Nephrol 11:155A

    Google Scholar 

  25. Cordeiro AC, Qureshi AR, Lindholm B, Amparo FC, Tito-Paladino-Filho A, Perini M, Lourenco FS, Pinto IM, Amodeo C, Carrero JJ (2013) Visceral fat and coronary artery calcification in patients with chronic kidney disease. Nephrol Dial Transplant 28(Suppl 4):152–159

    Article  Google Scholar 

  26. Cordeiro AC, Lindholm B, Sousa MG, Picotti JC, Nunes GJ, Santana MR, Grimaldi W Jr, Amparo FC, Amodeo C, Carrero JJ (2014) Reliability of electrocardiographic surrogates of left ventricular mass in patients with chronic kidney disease. J Hypertens 32:439–445

    Article  CAS  PubMed  Google Scholar 

  27. Enia G, Sicuso C, Alati G, Zoccali C (1993) Subjective global assessment of nutrition in dialysis patients. Nephrol Dial Transplant 8:1094–1098

    CAS  PubMed  Google Scholar 

  28. Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40:373–383

    Article  CAS  PubMed  Google Scholar 

  29. Kovesdy CP, Czira ME, Rudas A, Ujszaszi A, Rosivall L, Novak M, Kalantar-Zadeh K, Molnar MZ, Mucsi I (2010) Body mass index, waist circumference and mortality in kidney transplant recipients. Am J Transplant 10:2644–2651

    Article  CAS  PubMed  Google Scholar 

  30. Segall L, Moscalu M, Hogas S, Mititiuc I, Nistor I, Veisa G, Covic A (2014) Protein–energy wasting, as well as overweight and obesity, is a long-term risk factor for mortality in chronic hemodialysis patients. Int Urol Nephrol 46:615–621

    Article  CAS  PubMed  Google Scholar 

  31. Carrero JJ, Chmielewski M, Axelsson J, Snaedal S, Heimburger O, Barany P, Suliman ME, Lindholm B, Stenvinkel P, Qureshi AR (2008) Muscle atrophy, inflammation and clinical outcome in incident and prevalent dialysis patients. Clin Nutr 27:557–564

    Article  PubMed  Google Scholar 

  32. Johansen KL, Kaysen GA, Young BS, Hung AM, da Silva M, Chertow GM (2003) Longitudinal study of nutritional status, body composition, and physical function in hemodialysis patients. Am J Clin Nutr 77:842–846

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

JJC acknowledges grant support from the Swedish Research Council and Stockholm County Council (ALF). MIVC cohort was supported by grants by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Process number: 2010/16593-2), Adib Jatene’s Foundation, and the Swedish Research Council.

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Division of Nephrology, Department of Medicine, University of Tennessee Health Science Center, 956 Court Ave., Room B216B, Memphis, TN, 38103, USA

    Miklos Z. Molnar & Csaba P. Kovesdy

  2. Divisions of Renal Medicine and Baxter Novum, Department of Clinical Science, Intervention and Technology, Karolinska Institutet, Stockholm, Sweden

    Juan J. Carrero

  3. Center for Molecular Medicine, Karolinska Institutet, Stockholm, Sweden

    Juan J. Carrero

  4. Department of Medicine, Division of Nephrology, University Health Network, University of Toronto, Toronto, ON, Canada

    Istvan Mucsi

  5. Department of Transplantation and Surgery, Semmelweis University, Budapest, Hungary

    Adam Remport

  6. Division of Nephrology and Hypertension, University of California Irvine Medical Center, Orange, CA, USA

    Connie M. Rhee & Kamyar Kalantar-Zadeh

  7. Nephrology Section, Memphis Veterans Affairs Medical Center, Memphis, TN, USA

    Csaba P. Kovesdy

  8. Department of Hypertension and Nephrology, Dante Pazzanese Institute of Cardiology, São Paulo, Brazil

    Antonio C. Cordeiro

Authors
  1. Miklos Z. Molnar
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Correspondence to Miklos Z. Molnar.

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Molnar, M.Z., Carrero, J.J., Mucsi, I. et al. Comparison of the malnutrition–inflammation score in chronic kidney disease patients and kidney transplant recipients. Int Urol Nephrol 47, 1025–1033 (2015). https://doi.org/10.1007/s11255-015-0984-2

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  • DOI: https://doi.org/10.1007/s11255-015-0984-2

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