Quadriceps muscle thickness assessed by ultrasound is independently associated with mortality in hemodialysis patients.
Journal
European journal of clinical nutrition
ISSN: 1476-5640
Titre abrégé: Eur J Clin Nutr
Pays: England
ID NLM: 8804070
Informations de publication
Date de publication:
12 2022
12 2022
Historique:
received:
20
12
2021
accepted:
16
05
2022
revised:
12
05
2022
pubmed:
1
6
2022
medline:
2
12
2022
entrez:
31
5
2022
Statut:
ppublish
Résumé
Estimation of muscle mass is an integral part of nutritional assessment in End-Stage Kidney Disease (ESKD) patients on chronic hemodialysis (HD). In this respect, muscle ultrasound (US) is a valid and reliable tool but has not been previously related to outcomes in this population. Aims of this study were to assess the relationship between quadriceps muscle thickness as assessed by US and outcomes in ESKD patients on HD; we also compared US with anthropometry and malnutrition inflammation score (MIS). In this prospective study, 181 prevalent patients on HD were included. Thickness of the quadriceps rectus femoris and vastus intermedius (VIT) were assessed separately using ultrasonography, and were indexed for height squared. Mid-arm muscle circumference (MAMC) and area (MAMA) were assessed by anthropometry. MIS was evaluated. In the absence of predetermined cut-offs, values below the median of the distribution of VIT index were considered low. Instead, cut-off for anthropometric values such as MAMC and MAMA were set at ≥90% of agreement with the 50th percentile of the sex- and age-specific normal distribution. Cox-regression analysis was used to assess the association of US, MIS, and anthropometric parameters with mortality. Patients were followed for a median of 35 months. During this period 36% of patients died. Multivariable Cox-regression analysis (adjusted for demographic, biochemical and clinical variables), demonstrated that higher VIT distal index values were independently associated with lower mortality risk (HR: 0.76 (0.59-0.99); P = 0.040), whilst higher MIS values were independently associated with higher (HR 1.22 (1.10-1.35); P < 0.001) mortality risk. When assessing muscle parameters as categorical variables, both low VIT distal index (HR: 1.71 (1.01-2.89); 0.045) and MAMC (HR: 1.74 (1.02-2.96); 0.042) were independently associated with increased risk of death. Indexed distal VIT was independently associated with mortality both as continuous and as a categorical variable. Muscle US is a simple practical tool that adds prognostic information to the bedside nutritional assessment in ESKD patients on maintenance HD.
Sections du résumé
BACKGROUND/OBJECTIVES
Estimation of muscle mass is an integral part of nutritional assessment in End-Stage Kidney Disease (ESKD) patients on chronic hemodialysis (HD). In this respect, muscle ultrasound (US) is a valid and reliable tool but has not been previously related to outcomes in this population. Aims of this study were to assess the relationship between quadriceps muscle thickness as assessed by US and outcomes in ESKD patients on HD; we also compared US with anthropometry and malnutrition inflammation score (MIS).
SUBJECTS/METHODS
In this prospective study, 181 prevalent patients on HD were included. Thickness of the quadriceps rectus femoris and vastus intermedius (VIT) were assessed separately using ultrasonography, and were indexed for height squared. Mid-arm muscle circumference (MAMC) and area (MAMA) were assessed by anthropometry. MIS was evaluated. In the absence of predetermined cut-offs, values below the median of the distribution of VIT index were considered low. Instead, cut-off for anthropometric values such as MAMC and MAMA were set at ≥90% of agreement with the 50th percentile of the sex- and age-specific normal distribution. Cox-regression analysis was used to assess the association of US, MIS, and anthropometric parameters with mortality.
RESULTS
Patients were followed for a median of 35 months. During this period 36% of patients died. Multivariable Cox-regression analysis (adjusted for demographic, biochemical and clinical variables), demonstrated that higher VIT distal index values were independently associated with lower mortality risk (HR: 0.76 (0.59-0.99); P = 0.040), whilst higher MIS values were independently associated with higher (HR 1.22 (1.10-1.35); P < 0.001) mortality risk. When assessing muscle parameters as categorical variables, both low VIT distal index (HR: 1.71 (1.01-2.89); 0.045) and MAMC (HR: 1.74 (1.02-2.96); 0.042) were independently associated with increased risk of death.
CONCLUSION
Indexed distal VIT was independently associated with mortality both as continuous and as a categorical variable. Muscle US is a simple practical tool that adds prognostic information to the bedside nutritional assessment in ESKD patients on maintenance HD.
Identifiants
pubmed: 35641665
doi: 10.1038/s41430-022-01166-7
pii: 10.1038/s41430-022-01166-7
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1719-1726Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Sabatino A, Regolisti G, Karupaiah T, Sahathevan S, Sadu Singh BK, Khor BH, et al. Protein-energy wasting and nutritional supplementation in patients with end-stage renal disease on hemodialysis. Clin Nutr. 2017;36:663–71.
doi: 10.1016/j.clnu.2016.06.007
pubmed: 27371993
Domanski M, Ciechanowski K. Sarcopenia: a major challenge in elderly patients with end-stage renal disease. J Aging Res. 2012;2012:754739.
doi: 10.1155/2012/754739
pubmed: 22536505
pmcid: 3321443
Ozkayar N, Altun B, Halil M, Kuyumcu ME, Arik G, Yesil Y, et al. Evaluation of sarcopenia in renal transplant recipients. Nephrourol Mon. 2014;6:e20055.
doi: 10.5812/numonthly.20055
pubmed: 25695027
pmcid: 4317720
Shiozu H, Higashijima M, Koga T. Association of sarcopenia with swallowing problems, related to nutrition and activities of daily living of elderly individuals. J Phys Ther Sci. 2015;27:393–6.
doi: 10.1589/jpts.27.393
pubmed: 25729176
pmcid: 4339146
Argiles JM, Campos N, Lopez-Pedrosa JM, Rueda R, Rodriguez-Manas L. Skeletal muscle regulates metabolism via interorgan crosstalk: roles in health and disease. J Am Med Dir Assoc. 2016;17:789–96.
doi: 10.1016/j.jamda.2016.04.019
pubmed: 27324808
Wolfe RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr. 2006;84:475–82.
doi: 10.1093/ajcn/84.3.475
pubmed: 16960159
Demling RH. Nutrition, anabolism, and the wound healing process: an overview. Eplasty. 2009;9:e9.
pubmed: 19274069
pmcid: 2642618
Fouque D, Kalantar-Zadeh K, Kopple J, Cano N, Chauveau P, Cuppari L, et al. A proposed nomenclature and diagnostic criteria for protein-energy wasting in acute and chronic kidney disease. Kidney Int. 2008;73:391–8.
doi: 10.1038/sj.ki.5002585
pubmed: 18094682
El-Kateb S, Davenport A. Changes in intracellular water following hemodialysis treatment lead to changes in estimates of lean tissue using bioimpedance spectroscopy. Nutr Clin Pract. 2016;31:375–7.
Abrahamsen B, Hansen T, Høgsberg I, Pedersen F, Beck-Nielsen H. Impact of hemodialysis on dual X-ray absorptiometry, bioelectrical impedance measurements, and anthropometry. Am J Clin Nutr. 1996;63:80–6.
Connolly B, MacBean V, Crowley C, Lunt A, Moxham J, Rafferty GF, et al. Ultrasound for the assessment of peripheral skeletal muscle architecture in critical illness: a systematic review. Crit Care Med. 2015;43:897–905.
doi: 10.1097/CCM.0000000000000821
pubmed: 25559437
Sabatino A, Regolisti G, Bozzoli L, Fani F, Antoniotti R, Maggiore U, et al. Reliability of bedside ultrasound for measurement of quadriceps muscle thickness in critically ill patients with acute kidney injury. Clin Nutr. 2017;36:1710–5.
doi: 10.1016/j.clnu.2016.09.029
pubmed: 27743614
Sabatino A, Regolisti G, Delsante M, Di Motta T, Cantarelli C, Pioli S, et al. Noninvasive evaluation of muscle mass by ultrasonography of quadriceps femoris muscle in End-Stage Renal Disease patients on hemodialysis. Clin Nutr. 2019;38:1232–9.
doi: 10.1016/j.clnu.2018.05.004
pubmed: 29866494
Sabatino A, Regolisti G, di Mario F, Ciuni A, Palumbo A, Peyronel F, et al. Validation by CT scan of quadriceps muscle thickness measurement by ultrasound in acute kidney injury. J Nephrol. 2020;33:109–17.
doi: 10.1007/s40620-019-00659-2
pubmed: 31729699
Sabatino A, D’Alessandro C, Regolisti G, di Mario F, Guglielmi G, Bazzocchi A, et al. Muscle mass assessment in renal disease: the role of imaging techniques. Quant Imaging Med Surg. 2020;10:1672–86.
doi: 10.21037/qims.2020.03.05
pubmed: 32742960
pmcid: 7378093
Carrero JJ, Thomas F, Nagy K, Arogundade F, Avesani CM, Chan M, et al. Global prevalence of protein-energy wasting in kidney disease: a meta-analysis of contemporary observational studies from the International Society of Renal Nutrition and Metabolism. J Ren Nutr. 2018;28:380–92.
doi: 10.1053/j.jrn.2018.08.006
pubmed: 30348259
Rodrigues J, Santin F, Brito FDSB, Lindholm B, Stenvinkel P, Avesani CM. Nutritional status of older patients on hemodialysis: which nutritional markers can best predict clinical outcomes? Nutrition. 2019;65:113–9.
doi: 10.1016/j.nut.2019.03.002
pubmed: 31082788
Avesani C, Sabatino A, Guerra A, Rodrigues J, Carrero J, Rossi G, et al. A comparative analysis of nutritional assessment using global leadership initiative on malnutrition versus subjective global assessment and malnutrition inflammation score in maintenance hemodialysis patients. J Ren Nutr. 2021, (online ahead of print), https://doi.org/10.1053/j.jrn.2021.06.008 .
Sabatino ARG, di Mario F, Ciuni A, Palumbo A, Peyronel F, Maggiore U, et al. Validation by CT scan of quadriceps muscle ultrasound in acute kidney injury. J Nephrol. 2020;33:9–17.
Tillquist M, Kutsogiannis DJ, Wischmeyer PE, Kummerlen C, Leung R, Stollery D, et al. Bedside ultrasound is a practical and reliable measurement tool for assessing quadriceps muscle layer thickness. J Parenter Enter Nutr. 2014;38:886–90.
doi: 10.1177/0148607113501327
Frisancho A. Nutritional anthropometry. J Am Diet Assoc. 1988;88:553–5.
doi: 10.1016/S0002-8223(21)02006-X
pubmed: 3367011
Steiber AL, Kalantar-Zadeh K, Secker D, McCarthy M, Sehgal A, McCann L. Subjective Global Assessment in chronic kidney disease: a review. J Ren Nutr. 2004;14:191–200.
doi: 10.1016/S1051-2276(04)00139-6
pubmed: 15483778
Ikizler T, Burrowes J, Byham-Gray L, Campbell K, Carrero J, Chan W, et al. KDOQI clinical practice guideline for nutrition in CKD: 2020 update. Am J Kidney Dis. 2020;76:S1–S107.
doi: 10.1053/j.ajkd.2020.05.006
pubmed: 32829751
Kalantar-Zadeh K, Kleiner M, Dunne E, Lee GH, Luft FC. A modified quantitative subjective global assessment of nutrition for dialysis patients. Nephrol Dial Transpl. 1999;14:1732–8.
doi: 10.1093/ndt/14.7.1732
Carrero JJ, Chmielewski M, Axelsson J, Snaedal S, Heimburger O, Barany P, et al. Muscle atrophy, inflammation and clinical outcome in incident and prevalent dialysis patients. Clin Nutr. 2008;27:557–64.
doi: 10.1016/j.clnu.2008.04.007
pubmed: 18538898
Miyamoto T, Carrero JJ, Qureshi AR, Anderstam B, Heimburger O, Barany P, et al. Circulating follistatin in patients with chronic kidney disease: implications for muscle strength, bone mineral density, inflammation, and survival. Clin J Am Soc Nephrol. 2011;6:1001–8.
doi: 10.2215/CJN.10511110
pubmed: 21350111
pmcid: 3087764
Beddhu S, Pappas LM, Ramkumar N, Samore M. Effects of body size and body composition on survival in hemodialysis patients. J Am Soc Nephrol. 2003;14:2366–72.
doi: 10.1097/01.ASN.0000083905.72794.E6
pubmed: 12937315
Noori N, Kopple JD, Kovesdy CP, Feroze U, Sim JJ, Murali SB, et al. Mid-arm muscle circumference and quality of life and survival in maintenance hemodialysis patients. Clin J Am Soc Nephrol. 2010;5:2258–68.
doi: 10.2215/CJN.02080310
pubmed: 20947789
pmcid: 2994088
Streja E, Molnar MZ, Kovesdy CP, Bunnapradist S, Jing J, Nissenson AR, et al. Associations of pretransplant weight and muscle mass with mortality in renal transplant recipients. Clin J Am Soc Nephrol. 2011;6:1463–73.
doi: 10.2215/CJN.09131010
pubmed: 21415312
pmcid: 3109945
Oterdoom LH, van Ree RM, de Vries AP, Gansevoort RT, Schouten JP, van Son WJ, et al. Urinary creatinine excretion reflecting muscle mass is a predictor of mortality and graft loss in renal transplant recipients. Transplantation. 2008;86:391–8.
doi: 10.1097/TP.0b013e3181788aea
pubmed: 18698241
Foley RN, Wang C, Ishani A, Collins AJ, Murray AM. Kidney function and sarcopenia in the United States general population: NHANES III. Am J Nephrol. 2007;27:279–86.
doi: 10.1159/000101827
pubmed: 17440263
Giglio J, Kamimura M, Lamarca F, Rodrigues J, Santin F, Avesani C. Association of sarcopenia with nutritional parameters, quality of life, hospitalization, and mortality rates of elderly patients on hemodialysis. J Ren Nutr. 2018;28:197–207.
Carrero JJ, Johansen KL, Lindholm B, Stenvinkel P, Cuppari L, Avesani CM. Screening for muscle wasting and dysfunction in patients with chronic kidney disease. Kidney Int. 2016;90:53–66.
doi: 10.1016/j.kint.2016.02.025
pubmed: 27157695
Giglio J, Kamimura M, Souza N, Bichels A, Cordeiro A, Pinho N, et al. Muscle mass assessment by computed tomography in chronic kidney disease patients: agreement with surrogate methods. Eur J Clin Nutr. 2019;73:46–53.
Pereira R, Cordeiro A, Avesani C, Carrero J, Lindholm B, Amparo F, et al. Sarcopenia in chronic kidney disease on conservative therapy: prevalence and association with mortality. Nephrol Dial Transplant. 2015;30:1718–25.
Araújo I, Kamimura M, Draibe S, Canziani M, Manfredi S, Avesani C, et al. Nutritional parameters and mortality in incident hemodialysis patients. J Ren Nutr. 2006;16:27–35.
doi: 10.1053/j.jrn.2005.10.003
pubmed: 16414438
Tsukasaki K, Matsui Y, Arai H, Harada A, Tomida M, Takemura M, et al. Association of muscle strength and gait speed with cross-sectional muscle area determined by mid-thigh computed tomography - a comparison with skeletal muscle mass measured by dual-energy X-ray absorptiometry. J Frailty Aging. 2020;9:82–89.
pubmed: 32259181
Fukasawa H, Kaneko M, Niwa H, Matsuyama T, Yasuda H, Kumagai H, et al. Lower thigh muscle mass is associated with all-cause and cardiovascular mortality in elderly hemodialysis patients. Eur J Clin Nutr. 2017;71:64–9.
Souza VA, Oliveira D, Cupolilo EN, Miranda CS, Colugnati FAB, Mansur HN, et al. Rectus femoris muscle mass evaluation by ultrasound: facilitating sarcopenia diagnosis in pre-dialysis chronic kidney disease stages. Clinics. 2018;73:e392.
doi: 10.6061/clinics/2018/e392
pubmed: 30379225
pmcid: 6201140
Sahathevan S, Khor B, Singh B, Sabatino A, Fiaccadori E, Daud Z, et al. Association of ultrasound-derived metrics of the quadriceps muscle with protein energy wasting in hemodialysis patients: a multicenter cross-sectional study. Nutrients. 2020;12:3597.
Sabatino A, Maggiore U, Regolisti G, Rossi G, Di Mario F, Gentile M, et al. Ultrasound for non-invasive assessment and monitoring of quadriceps muscle thickness in critically Ill patients with acute kidney injury. Front Nutr. 2021;8:622823.
doi: 10.3389/fnut.2021.622823
pubmed: 33937303
pmcid: 8081900
de Roij van Zuijdewijn C, ter Wee P, Chapdelaine I, Bots M, Blankestijn P, van den Dorpel M, et al. A comparison of 8 nutrition-related tests to predict mortality in hemodialysis patients. J Ren Nutr. 2015;25:412–9.
Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39:412–23.
doi: 10.1093/ageing/afq034
pubmed: 20392703
pmcid: 2886201
Yamamoto S, Matsuzawa R, Hoshi K, Suzuki Y, Harada M, Watanabe T, et al. Modified creatinine index and clinical outcomes of hemodialysis patients: an indicator of sarcopenia? J Ren Nutr. 2021;31:370–9.
doi: 10.1053/j.jrn.2020.08.006
pubmed: 32952008
Bichels A, Cordeiro A, Avesani C, Amparo F, Giglio J, Souza N, et al. Muscle mass assessed by computed tomography at the third lumbar vertebra predicts patient survival in chronic kidney disease. J Ren Nutr. 2021;31:342–50.
doi: 10.1053/j.jrn.2020.05.007
pubmed: 33257228
Yajima T, Arao M, Yajima K, Takahashi H, Yasuda K. The associations of fat tissue and muscle mass indices with all-cause mortality in patients undergoing hemodialysis. PLoS ONE. 2019;14:e0211988.
doi: 10.1371/journal.pone.0211988
pubmed: 30759133
pmcid: 6373951
Tabibi H, As’habi A, Najafi I, Hedayati M. Associations of body composition, muscle function, and physical activity with mortality in peritoneal dialysis patients. Iran J Kidney Dis. 2020;14:224–30.
Souweine J, Pasquier G, Kuster N, Rodriguez A, Patrier L, Morena M, et al. Dynapaenia and sarcopaenia in chronic haemodialysis patients: do muscle weakness and atrophy similarly influence poor outcome? Nephrol Dial Transplant. 2021;36:1908–18.
doi: 10.1093/ndt/gfaa353
pubmed: 33306128