Abstract
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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
The data analyzed during this study are available from the corresponding author on reasonable request.
References
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.
Domanski M, Ciechanowski K. Sarcopenia: a major challenge in elderly patients with end-stage renal disease. J Aging Res. 2012;2012:754739.
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.
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.
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.
Wolfe RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr. 2006;84:475–82.
Demling RH. Nutrition, anabolism, and the wound healing process: an overview. Eplasty. 2009;9:e9.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Frisancho A. Nutritional anthropometry. J Am Diet Assoc. 1988;88:553–5.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Author contributions
AS was responsible for designing the protocol, data collection, and analysis, as well as writing the manuscript. JPK, mentorship and contribution to writing the manuscript. TDM, CC, MG, and SB, contributed by collecting data and revising the manuscript. GR was responsible for analyzing the data and writing the manuscript. EF, mentorship and revision of the manuscript.
Funding
This study was partially funded by the young investigator research fellowship by the Italian Society of Parenteral and Enteral Nutrition (SINPE, Società Italiana di Nutrizione Parenterale ed Enterale) for the project: “Valutazione nutrizionale nell’insufficienza renale mediante ecografia del muscolo quadricipite femorale” (“Nutritional assessment of patients with chronic kidney disease and acute kidney injury through ultrasound of the quadriceps femoris muscle”) received by Alice Sabatino.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethical approval
The study was approved by the local Institutional Review Board (AVEN ref. no 45737, December 12th, 2015).
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
Sabatino, A., Kooman, J.P., Di Motta, T. et al. Quadriceps muscle thickness assessed by ultrasound is independently associated with mortality in hemodialysis patients. Eur J Clin Nutr 76, 1719–1726 (2022). https://doi.org/10.1038/s41430-022-01166-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41430-022-01166-7
This article is cited by
-
Muscle ultrasound to diagnose sarcopenia in chronic kidney disease: a systematic review and bayesian bivariate meta-analysis
BMC Nephrology (2024)
-
Sarcopenia diagnosed by ultrasound-assessed quadriceps muscle thickness and handgrip strength predicts mortality in patients on hemodialysis
Journal of Nephrology (2024)
-
Ultrasound quadriceps muscle thickness is variably associated with frailty in haemodialysis recipients
BMC Nephrology (2023)