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Erschienen in:

07.10.2021 | original Article

Low skeletal muscle mass by computerized tomography is associated with increased mortality risk in end-stage kidney disease patients on hemodialysis

verfasst von: Alice Sabatino, Giuseppe Regolisti, Giuseppe Benigno, Francesca Di Mario, Carla Maria Avesani, Enrico Fiaccadori

Erschienen in: Journal of Nephrology | Ausgabe 2/2022

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Abstract

Background and aims

Skeletal muscle (SM) area, as measured by abdominal CT at the level of the third lumbar vertebra (L3), has been proposed as a proxy of whole body muscle mass. However, population-specific reference values are lacking. In the present study we aimed at: (1) detecting low SM area on abdominal CT images in patients on hemodialysis by applying cut-offs derived from a group of healthy subjects, and (2) estimating the independent risk of all-cause mortality associated with low SM area.

Methods

We retrospectively enrolled 212 adult patients on hemodialysis, undergoing abdominal CT scan (study group), and 87 healthy kidney donors (reference group). We obtained the gender-specific 5th percentile values of the abdominal SM area distribution from both the whole control group and the subgroup of younger (29–60 years) subjects, which we used as reference cut-offs. Then we applied those cut-offs in the study group to identify patients with low SM area. We used survival and Cox regression analysis to evaluate the risk of all-cause mortality associated with low abdominal SM area.

Results

In the fully adjusted Cox regression analysis, the patients with low abdominal SM area had a higher risk of death than the patients with values above the reference cut-off derived in the subgroup of younger controls (adjHR = 1.79 (1.21; 2.67), P = 0.004).

Conclusions

Abdominal CT imaging can be used to detect low abdominal SM area in patients on hemodialysis by applying cut-offs derived from healthy subjects sharing a similar ethnic background. Low SM area as assessed by CT is independently associated with all-cause mortality in ESKD patients on hemodialysis.

Graphic abstract

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Sabatino A, Regolisti G, Karupaiah T, Sahathevan S, Sadu Singh BK, Khor BH, Salhab N, Karavetian M, Cupisti A, Fiaccadori E (2017) Protein-energy wasting and nutritional supplementation in patients with end-stage renal disease on hemodialysis. Clin Nutr 36(3):663–671. https://doi.org/10.1016/j.clnu.2016.06.007CrossRefPubMed

Sabatino A, Regolisti G, Delsante M, Di Motta T, Cantarelli C, Pioli S, Grassi G, Batini V, Gregorini M, Fiaccadori E (2019) Noninvasive evaluation of muscle mass by ultrasonography of quadriceps femoris muscle in End-Stage Renal Disease patients on hemodialysis. Clin Nutr 38(3):1232–1239. https://doi.org/10.1016/j.clnu.2018.05.004CrossRefPubMed

Foley RN, Wang C, Ishani A, Collins AJ, Murray AM (2007) Kidney function and sarcopenia in the United States general population: NHANES III. Am J Nephrol 27(3):279–286. https://doi.org/10.1159/000101827CrossRefPubMed

Giglio J, Kamimura M, Lamarca F, Rodrigues J, Santin F, Avesani C (2018) Association of sarcopenia with nutritional parameters, quality of life, hospitalization, and mortality rates of elderly patients on hemodialysis. J Ren Nutr 28(3):197–207. https://doi.org/10.1053/j.jrn.2017.12.003CrossRefPubMed

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(4):557–564. https://doi.org/10.1016/j.clnu.2008.04.007CrossRefPubMed

Miyamoto T, Carrero JJ, Qureshi AR, Anderstam B, Heimburger O, Barany P, Lindholm B, Stenvinkel P (2011) Circulating follistatin in patients with chronic kidney disease: implications for muscle strength, bone mineral density, inflammation, and survival. Clin J Am Soc Nephrol 6(5):1001–1008. https://doi.org/10.2215/cjn.10511110CrossRefPubMedPubMedCentral

Martinson M, Ikizler TA, Morrell G, Wei G, Almeida N, Marcus RL, Filipowicz R, Greene TH, Beddhu S (2014) Associations of body size and body composition with functional ability and quality of life in hemodialysis patients. Clin J Am Soc Nephrol 9(6):1082–1090. https://doi.org/10.2215/cjn.09200913CrossRefPubMedPubMedCentral

Beddhu S, Pappas LM, Ramkumar N, Samore M (2003) Effects of body size and body composition on survival in hemodialysis patients. J Am Soc Nephrol 14(9):2366–2372. https://doi.org/10.1097/01.asn.0000083905.72794.e6CrossRefPubMed

Noori N, Kopple JD, Kovesdy CP, Feroze U, Sim JJ, Murali SB, Luna A, Gomez M, Luna C, Bross R, Nissenson AR, Kalantar-Zadeh K (2010) Mid-arm muscle circumference and quality of life and survival in maintenance hemodialysis patients. Clin J Am Soc Nephrol 5(12):2258–2268. https://doi.org/10.2215/cjn.02080310CrossRefPubMedPubMedCentral

10.

Ikizler T, Burrowes J, Byham-Gray L, Campbell K, Carrero J, Chan W, Fouque D, Friedman A, Ghaddar S, Goldstein-Fuchs D, Kaysen G, Kopple J, Teta D, Yee-Moon WA, Cuppari L (2020) KDOQI clinical practice guideline for nutrition in CKD: 2020 update. Am J Kidney Dis 76(3 Suppl 1):S1–S10. https://doi.org/10.1053/j.ajkd.2020.05.006CrossRefPubMed

11.

Sergi G, De Rui M, Veronese N, Bolzetta F, Berton L, Carraro S, Bano G, Coin A, Manzato E, Perissinotto E (2015) Assessing appendicular skeletal muscle mass with bioelectrical impedance analysis in free-living Caucasian older adults. Clin Nutr 34(4):667–673. https://doi.org/10.1016/j.clnu.2014.07.010CrossRefPubMed

12.

Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48(1):16–31. https://doi.org/10.1093/ageing/afy169CrossRefPubMed

13.

Sabatino A, D’Alessandro C, Regolisti G, di Mario F, Guglielmi G, Bazzocchi A, Fiaccadori E (2020) Muscle mass assessment in renal disease: the role of imaging techniques. Quant Imaging Med Surg 10(8):1672–1686. https://doi.org/10.21037/qims.2020.03.05CrossRefPubMedPubMedCentral

14.

Pietrobelli A, Formica C, Wang Z, Heymsfield SB (1996) Dual-energy X-ray absorptiometry body composition model: review of physical concepts. Am J Physiol 271(6 Pt 1):E941-951. https://doi.org/10.1152/ajpendo.1996.271.6.E941CrossRefPubMed

15.

Sabatino A, Regolisti G, Bozzoli L, Fani F, Antoniotti R, Maggiore U, Fiaccadori E (2017) Reliability of bedside ultrasound for measurement of quadriceps muscle thickness in critically ill patients with acute kidney injury. Clin Nutr 36(6):1710–1715. https://doi.org/10.1016/j.clnu.2016.09.029CrossRefPubMed

16.

Fukasawa H, Kaneko M, Niwa H, Matsuyama T, Yasuda H, Kumagai H, Furuya R (2017) Lower thigh muscle mass is associated with all-cause and cardiovascular mortality in elderly hemodialysis patients. Eur J Clin Nutr. https://doi.org/10.1038/ejcn.2016.186CrossRefPubMed

17.

Ohkawa S, Odamaki M, Yoneyama T, Hibi I, Miyaji K, Kumagai H (2000) Standardized thigh muscle area measured by computed axial tomography as an alternate muscle mass index for nutritional assessment of hemodialysis patients. Am J Clin Nutr. https://doi.org/10.1093/ajcn/71.2.485CrossRefPubMed

18.

Cawthon P (2015) Assessment of lean mass and physical performance in sarcopenia. J Clin Densit. https://doi.org/10.1016/j.jocd.2015.05.063CrossRef

19.

Bichels A, Cordeiro A, Avesani CM, Amparo F, Giglio J, Souza N, Pinho N, Amodeo C, Carrero JJ, Lindholm B, Stenvinkel P, Kamimura MA (2020) Muscle mass assessed by computed tomography at the third lumbar vertebra predicts patient survival in chronic kidney disease. J Ren Nutr 31(4):342–350CrossRefPubMed

20.

Takata T, Motoe A, Tanida K, Taniguchi S, Ida A, Yamada K, Hamada S, Ogawa M, Yamamoto M, Mae Y, Iyama T, Taniguchi M, Nakaoka A, Isomoto H (2020) Feasibility of computed tomography-based assessment of skeletal muscle mass in hemodialysis patients. J Nephrol. https://doi.org/10.1007/s40620-020-00871-5CrossRefPubMed

21.

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, Treviño-Becerra A, Trevinho-Becerra A, Wanner C (2008) A proposed nomenclature and diagnostic criteria for protein-energy wasting in acute and chronic kidney disease. Kidney Int 73(4):391–398. https://doi.org/10.1038/sj.ki.5002585CrossRefPubMed

22.

Gomez-Perez S, Haus J, Sheean P, Patel B, Mar W, Chaudhry V, McKeever L, Braunschweig C (2016) Measuring abdominal circumference and skeletal muscle from a single cross-sectional computed tomography image: a step-by-step guide for clinicians using National Institutes of Health ImageJ. JPEN J Parenter Enteral Nutr 40(3):308–318. https://doi.org/10.1177/0148607115604149CrossRefPubMed

23.

Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinkova E, Vandewoude M, Zamboni M (2010) Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on sarcopenia in older people. Age Ageing 39(4):412–423. https://doi.org/10.1093/ageing/afq034CrossRefPubMedPubMedCentral

24.

van der Werf A, Langius J, de van der Schueren M, Nurmohamed S, van der Pant K, Blauwhoff-Buskermolen S, Wierdsma N (2018) Percentiles for skeletal muscle index, area and radiation attenuation based on computed tomography imaging in a healthy Caucasian population. Eur J Clin Nutr 72(2):288–296. https://doi.org/10.1038/s41430-017-0034-5CrossRefPubMed

25.

Fearon K, Strasser F, Anker S, Bosaeus I, Bruera E, Fainsinger R, Jatoi A, Loprinzi C, MacDonald N, Mantovani G, Davis M, Muscaritoli M, Ottery F, Radbruch L, Ravasco P, Walsh D, Wilcock A, Kaasa S, Baracos V (2011) Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12(5):489–495. https://doi.org/10.1016/S1470-2045(10)70218-7CrossRefPubMed

26.

Chen L, Woo J, Assantachai P, Auyeung T, Chou M, Iijima K, Jang H, Kang L, Kim M, Kim S, Kojima T, Kuzuya M, Lee J, Lee S, Lee W, Lee Y, Liang C, Lim J, Lim W, Peng L, Sugimoto K, Tanaka T, Won C, Yamada M, Zhang T, Akishita M, Arai H (2020) Asian Working Group for sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc 21(3):300–307. https://doi.org/10.1016/j.jamda.2019.12.012CrossRefPubMed

27.

Weijs PJ, Looijaard WG, Dekker IM, Stapel SN, Girbes AR, Oudemans-van Straaten HM, Beishuizen A (2014) Low skeletal muscle area is a risk factor for mortality in mechanically ventilated critically ill patients. Crit Care 18(2):R12. https://doi.org/10.1186/cc13189CrossRefPubMedPubMedCentral

28.

Prado C, Baracos V, McCargar L, Reiman T, Mourtzakis M, Tonkin K, Mackey J, Koski S, Pituskin E, Sawyer M (2009) Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving capecitabine treatment. Clin Cancer Res 15(8):2920–2926. https://doi.org/10.1158/1078-0432.CCR-08-2242CrossRefPubMed

29.

Prado C, Lieffers J, McCargar L, Reiman T, Sawyer M, Martin L, Baracos V (2008) Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol 9(7):629–635. https://doi.org/10.1016/S1470-2045(08)70153-0CrossRefPubMed

30.

van Vledder M, Levolger S, Ayez N, Verhoef C, Tran T, Ijzermans J (2012) Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg 99(4):550–557. https://doi.org/10.1002/bjs.7823CrossRefPubMed

31.

Antoun S, Lanoy E, Iacovelli R, Albiges-Sauvin L, Loriot Y, Merad-Taoufik M, Fizazi K, di Palma M, Baracos V, Escudier B (2013) Skeletal muscle density predicts prognosis in patients with metastatic renal cell carcinoma treated with targeted therapies. Cancer 119(18):3377–3384. https://doi.org/10.1002/cncr.28218CrossRefPubMed

32.

Sabel M, Lee J, Cai S, Englesbe M, Holcombe S, Wang S (2011) Sarcopenia as a prognostic factor among patients with stage III melanoma. Ann Surg Oncol 18(13):3579–3585. https://doi.org/10.1245/s10434-011-1976-9CrossRefPubMed

33.

Argiles JM, Campos N, Lopez-Pedrosa JM, Rueda R, Rodriguez-Manas L (2016) Skeletal muscle regulates metabolism via interorgan crosstalk: roles in health and disease. J Am Med Dir Assoc 17(9):789–796. https://doi.org/10.1016/j.jamda.2016.04.019CrossRefPubMed

34.

Shiozu H, Higashijima M, Koga T (2015) Association of sarcopenia with swallowing problems, related to nutrition and activities of daily living of elderly individuals. J Phys Ther Sci 27(2):393–396. https://doi.org/10.1589/jpts.27.393CrossRefPubMedPubMedCentral

35.

Wolfe RR (2006) The underappreciated role of muscle in health and disease. Am J Clin Nutr 84(3):475–482. https://doi.org/10.1093/ajcn/84.3.475CrossRefPubMed

36.

Domanski M, Ciechanowski K (2012) Sarcopenia: a major challenge in elderly patients with end-stage renal disease. J Aging Res 2012:754739. https://doi.org/10.1155/2012/754739CrossRefPubMedPubMedCentral

37.

Ozkayar N, Altun B, Halil M, Kuyumcu ME, Arik G, Yesil Y, Yildirim T, Yilmaz R, Ariogul S, Turgan C (2014) Evaluation of sarcopenia in renal transplant recipients. Nephrourol Mon 6(4):e20055. https://doi.org/10.5812/numonthly.20055CrossRefPubMedPubMedCentral

38.

Streja E, Molnar MZ, Kovesdy CP, Bunnapradist S, Jing J, Nissenson AR, Mucsi I, Danovitch GM, Kalantar-Zadeh K (2011) Associations of pretransplant weight and muscle mass with mortality in renal transplant recipients. Clin J Am Soc Nephrol 6(6):1463–1473. https://doi.org/10.2215/cjn.09131010CrossRefPubMedPubMedCentral

39.

Oterdoom LH, van Ree RM, de Vries AP, Gansevoort RT, Schouten JP, van Son WJ, Homan van der Heide JJ, Navis G, de Jong PE, Gans RO, Bakker SJ (2008) Urinary creatinine excretion reflecting muscle mass is a predictor of mortality and graft loss in renal transplant recipients. Transplantation 86(3):391–398. https://doi.org/10.1097/TP.0b013e3181788aeaCrossRefPubMed

40.

Carrero JJ, Johansen KL, Lindholm B, Stenvinkel P, Cuppari L, Avesani CM (2016) Screening for muscle wasting and dysfunction in patients with chronic kidney disease. Kidney Int 90(1):53–66. https://doi.org/10.1016/j.kint.2016.02.025CrossRefPubMed

41.

Giglio J, Kamimura M, Souza N, Bichels A, Cordeiro A, Pinho N, Avesani C (2019) Muscle mass assessment by computed tomography in chronic kidney disease patients: agreement with surrogate methods. Eur J Clin Nutr. https://doi.org/10.1038/s41430-018-0130-1CrossRefPubMed

42.

Pereira R, Cordeiro A, Avesani C, Carrero J, Lindholm B, Amparo F, Amodeo C, Cuppari L, Kamimura M (2015) Sarcopenia in chronic kidney disease on conservative therapy: prevalence and association with mortality. Nephrol Dial Transplant. https://doi.org/10.1093/ndt/gfv133CrossRefPubMed

43.

Braunschweig CA, Sheean PM, Peterson SJ, Gomez Perez S, Freels S, Troy KL, Ajanaku FC, Patel A, Sclamberg JS, Wang Z (2014) Exploitation of diagnostic computed tomography scans to assess the impact of nutrition support on body composition changes in respiratory failure patients. JPEN J Parenter Enteral Nutr 38(7):880–885. https://doi.org/10.1177/0148607113500505CrossRefPubMed

44.

Fukushima H, Koga F (2017) Impact of sarcopenia in the management of urological cancer patients. Expert Rev Anticancer Ther 17(5):455–466. https://doi.org/10.1080/14737140.2017.1301209CrossRefPubMed

45.

Shen W, Punyanitya M, Wang Z, Gallagher D, St-Onge M, Albu J, Heymsfield S, Heshka S (2004) Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image. J Appl Physiol (Bethesda, Md: 1985). https://doi.org/10.1152/japplphysiol.00744.2004CrossRef

46.

Mourtzakis M, Prado C, Lieffers J, Reiman T, McCargar L, Baracos V (2008) A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Appl Physiol Nutr Metab. https://doi.org/10.1139/H08-075CrossRefPubMed

47.

Delmonico M, Harris T, Visser M, Park S, Conroy M, Velasquez-Mieyer P, Boudreau R, Manini T, Nevitt M, Newman A, Goodpaster B (2009) Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. https://doi.org/10.3945/ajcn.2009.28047CrossRefPubMedPubMedCentral

Titel: Low skeletal muscle mass by computerized tomography is associated with increased mortality risk in end-stage kidney disease patients on hemodialysis
verfasst von: Alice Sabatino
Giuseppe Regolisti
Giuseppe Benigno
Francesca Di Mario
Carla Maria Avesani
Enrico Fiaccadori
Publikationsdatum: 07.10.2021
Verlag: Springer International Publishing
Erschienen in: Journal of Nephrology / Ausgabe 2/2022
Print ISSN: 1121-8428
Elektronische ISSN: 1724-6059
DOI: https://doi.org/10.1007/s40620-021-01167-y

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Low skeletal muscle mass by computerized tomography is associated with increased mortality risk in end-stage kidney disease patients on hemodialysis