Sarcopenic Obesity Versus Nonobese Sarcopenia in Hemodialysis Patients: Differences in Nutritional Status, Quality of Life, and Clinical Outcomes


      Sarcopenia and sarcopenic obesity (SO) are linked to unfavorable prognosis in maintenance hemodialysis (MHD) populations. We tested whether nonobese sarcopenia and SO, as different stages of extreme protein-energy wasting, have different prognoses.


      In this prospective observational study, 261 MHD patients were recruited from October 2010 to April 2012 and followed until October 2020. Two definitions were used to diagnose sarcopenia: the European Working Group on Sarcopenia in Older People consensus and the Foundation for the National Institutes of Health (FNIH) Biomarkers Consortium criteria. Obesity was determined as the percentage of total body fat, ≥27% for men and ≥38% for women. Data for all-cause and cardiovascular morbidity and mortality, baseline nutrition markers, inflammation and oxidative stress, adipokines, body composition parameters, handgrip strength, and quality of life (QoL) scores were measured.


      According to European Working Group on Sarcopenia in Older People, 115 (44.1%) patients were sarcopenic and 120 (46.0%) according to FNIH definitions. Of them, 28.4% and 34.5% were SO, respectively. Higher levels of albumin, creatinine, uric acid, leptin, phase angle, better nutritional scores, and lower adiponectin levels characterized SO patients compared with nonobese sarcopenic patients regardless of indexing method. Better QoL scores were noted in SO compared with nonobese sarcopenic patients using the FNIH sarcopenia criteria. The hazard of all-cause death, cardiovascular death, and first cardiovascular event for patients with SO was lower compared with the nonobese patients after multivariate adjustments. Statistical significance of these associations disappeared after including fat mass in multivariate models.


      MHD patients with SO have better nutritional status and prognosis for cardiovascular events, all-cause and cardiovascular disease mortality, and possibly better QoL compared with nonobese sarcopenic MHD patients. The better prognosis appears to be entirely due to the excess fat, which is protective in sarcopenic MHD patients similar to that described in the entire MHD population.


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        • Kittiskulnam P.
        • Chertow G.M.
        • Carrero J.J.
        • et al.
        Sarcopenia and its individual criteria are associated, in part, with mortality among patients on hemodialysis.
        Kidney Int. 2017; 92: 238-247
        • Kittiskulnam P.
        • Carrero J.J.
        • Chertow G.M.
        • Kaysen G.A.
        • Delgado C.
        • Johansen K.L.
        Sarcopenia among patients receiving hemodialysis: weighing the evidence.
        J Cachexia Sarcopenia Muscle. 2017; 8: 57-68
        • Dierkes J.
        • Dahl H.
        • LervaagWelland N.
        • et al.
        High rates of central obesity and sarcopenia in CKD irrespective of renal replacement therapy - an observational cross-sectional study.
        BMC Nephrol. 2018; 19: 259
        • Souweine J.S.
        • Pasquier G.
        • Kuster N.
        • et al.
        Dynapenia and sarcopenia in chronic haemodialysis patients: do muscle weakness and atrophy similarly influence poor outcome?.
        Nephrol Dial Transplant. 2021; 36: 1908-1918
        • Hanna R.M.
        • Ghobry L.
        • Wassef O.
        • Rhee C.M.
        • Kalantar-Zadeh K.
        A practical Approach to nutrition, protein-energy wasting, sarcopenia, and Cachexia in patients with chronic kidney disease.
        Blood Purif. 2020; 49: 202-211
        • Domański M.
        • Ciechanowski K.
        Sarcopenia: a major challenge in elderly patients with end-stage renal disease.
        J Aging Res. 2012; 2012: 754739
        • Cruz-Jentoft A.J.
        • Bahat G.
        • Bauer J.
        • et al.
        Writing group for the European Working group on sarcopenia in older People 2 (EWGSOP2), and the Extended group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis.
        Age Ageing. 2019; 481: 16-31
        • Lin Y.L.
        • Liou H.H.
        • Wang C.H.
        • et al.
        Impact of sarcopenia and its diagnostic criteria on hospitalization and mortality in chronic hemodialysis patients: a 3-year longitudinal study.
        J Formos Med Assoc. 2020; 119: 1219-1229
        • Ren H.
        • Gong D.
        • Jia F.
        • Xu B.
        • Liu Z.
        Sarcopenia in patients undergoing maintenance hemodialysis: incidence rate, risk factors and its effect on survival risk.
        Ren Fail. 2016; 38: 364-371
        • Giglio J.
        • Kamimura M.A.
        • Lamarca F.
        • Rodrigues J.
        • Santin F.
        • Avesani C.M.
        Association of sarcopenia with nutritional parameters, quality of life, hospitalization, and mortality rates of elderly patients on hemodialysis.
        J Ren Nutr. 2017; 28: 197-207
        • Kamijo Y.
        • Kanda E.
        • Ishibashi Y.
        • Yoshida M.
        Sarcopenia and Frailty in PD: impact on mortality, malnutrition, and inflammation.
        Perit Dial Int. 2018; 38: 447-454
        • Baumgartner R.N.
        Body composition in healthy aging.
        Ann N Y Acad Sci. 2000; 904: 437-448
        • Zamboni M.
        • Mazzali G.
        • Fantin F.
        • Rossi A.
        • Di Francesco V.
        Sarcopenic obesity: a new category of obesity in the elderly.
        Nutr Metab Cardiovasc Dis. 2008; 18: 388-395
        • Stenholm S.
        • Harris T.B.
        • Rantanen T.
        • Visser M.
        • Kritchevsky S.B.
        • Ferrucci L.
        Sarcopenic obesity: definition, cause and consequences.
        Curr Opin Clin Nutr Metab Care. 2008; 11: 693-700
        • Donini L.M.
        • Busetto L.
        • Bauer J.M.
        • et al.
        Critical appraisal of definitions and diagnostic criteria for sarcopenic obesity based on a systematic review.
        Clin Nutr. 2020; 39: 2368-2388
        • Guillet C.
        • Masgrau A.
        • Walrand S.
        • Boirie Y.
        Impaired protein metabolism: interlinks between obesity, insulin resistance and inflammation.
        Obes Rev. 2012; 13: 51-57
        • Honda H.
        • Qureshi A.R.
        • Axelsson J.
        • et al.
        Obese sarcopenia in patients with end-stage renal disease is associated with inflammation and increased mortality.
        Am J Clin Nutr. 2007; 86: 633-638
        • Tian S.L.
        • Zhang K.
        • Xu P.C.
        Increased prevalence of peripheral arterial disease in patients with obese sarcopenia undergoing hemodialysis.
        Exp Ther Med. 2018; 15: 5148-5152
        • Malhotra R.
        • Deger S.M.
        • Salat H.
        • et al.
        Sarcopenic obesity definitions by body composition and mortality in the hemodialysis patients.
        J Ren Nutr. 2017; 27: 84-90
        • Kalantar-Zadeh K.
        • Abbott K.C.
        • Salahudeen A.K.
        • Kilpatrick R.D.
        • Horwich T.B.
        Survival advantages of obesity in dialysis patients.
        Am J Clin Nutr. 2005; 81: 543-554
        • Park J.
        • Ahmadi S.F.
        • Streja E.
        • et al.
        Obesity paradox in end-stage kidney disease patients.
        Prog Cardiovasc Dis. 2014; 56: 415-425
        • Kalantar-Zadeh K.
        • Kuwae N.
        • Wu D.Y.
        • et al.
        Associations of body fat and its changes over time with quality of life and prospective mortality in hemodialysis patients.
        Am J Clin Nutr. 2006; 83: 202-210
        • Fouque D.
        • Vennegoor M.
        • ter Wee P.
        • et al.
        EBPG guideline on nutrition.
        Nephrol Dial Transpl. 2007; 22: ii45-ii87
        • Bouillanne O.
        • Morineau G.
        • Dupont C.
        • et al.
        Geriatric Nutritional Risk Index: a new index for evaluating at-risk elderly medical patients.
        Am J Clin Nutr. 2005; 82: 777-783
        • Rambod M.
        • Bross R.
        • Zitterkoph J.
        • et al.
        Association of Malnutrition-Inflammation Score with quality of life and mortality in hemodialysis patients: a 5-year prospective cohort study.
        Am J Kidney Dis. 2009; 53: 298-309
        • Beberashvili I.
        • Azar A.
        • Sinuani I.
        • et al.
        Comparison analysis of nutritional scores for serial monitoring of nutritional status in hemodialysis patients.
        Clin J Am Soc Nephrol. 2013; 8: 443-451
        • Beberashvili I.
        • Azar A.
        • Sinuani I.
        • et al.
        Geriatric nutritional risk index, muscle function, quality of life and clinical outcome in hemodialysis patients.
        Clin Nutr. 2016; 35: 1522-1529
        • Kalantar-Zadeh K.
        • Kopple J.D.
        • Block G.
        • Humphreys M.H.
        Association among SF36 quality of life measures and nutrition, hospitalization, and mortality in hemodialysis.
        J Am Soc Nephrol. 2001; 12: 2797-2806
        • Sexton D.J.
        • Lowney A.C.
        • O'Seaghdha C.M.
        • et al.
        Do patient-reported measures of symptoms and health status predict mortality in hemodialysis? An assessment of POS-S Renal and EQ-5D.
        Hemodial Int. 2016; 20: 618-630
        • Liu J.
        • Huang Z.
        • Gilbertson D.T.
        • Foley R.N.
        • Collins A.J.
        An improved comorbidity index for outcome analyses among dialysis patients.
        Kidney Int. 2010; 77: 141-151
        • Beberashvili I.
        • Azar A.
        • Sinuani I.
        • et al.
        Bioimpedance phase angle predicts muscle function, quality of life and clinical outcome in maintenance hemodialysis patients.
        Eur J Clin Nutr. 2014; 68: 683-689
        • Janssen I.
        • Heymsfield S.B.
        • Baumgartner R.N.
        • Ross R.
        Estimation of skeletal muscle mass by bioelectrical impedance analysis.
        J Appl Physiol. 2000; 89: 465-471
        • Sergi G.
        • De Rui M.
        • Veronese N.
        • et al.
        Assessing appendicular skeletal muscle mass with bioelectrical impedance analysis in free-living Caucasian older adults.
        Clin Nutr. 2015; 34: 667-673
        • Cruz-Jentoft A.J.
        • Baeyens J.P.
        • Bauer J.M.
        • et al.
        European Working group on sarcopenia in older People: sarcopenia. European consensus on definition and diagnosis: report of the European Working group on sarcopenia in older People.
        Age Ageing. 2010; 39: 412-423
        • Studenski S.A.
        • Peters K.W.
        • Alley D.E.
        • et al.
        The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates.
        J Gerontol A Biol Sci Med Sci. 2014; 69: 547-558
        • McGrath R.
        • Hackney K.J.
        • Ratamess N.A.
        • Vincent B.M.
        • Clark B.C.
        • Kraemer W.J.
        Absolute and body mass index normalized handgrip strength percentiles by gender, ethnicity, and hand dominance in Americans.
        Adv Geriatr Med Res. 2020; 2: e200005
        • Batsis J.A.
        • Mackenzie T.A.
        • Barre L.K.
        • Lopez-Jimenez F.
        • Bartels S.J.
        Sarcopenia, sarcopenic obesity and mortality in older adults: results from the National Health and Nutrition Examination Survey III.
        Eur J Clin Nutr. 2014; 68: 1001-1007
        • Lamarca F.
        • Carrero J.J.
        • Rodrigues J.C.
        • Bigogno F.G.
        • Fetter R.L.
        • Avesani C.M.
        Prevalence of sarcopenia in elderly maintenance hemodialysis patients: the impact of different diagnostic criteria.
        J Nutr Health Aging. 2014; 18: 710-717
        • Yoowannakul S.
        • Tangvoraphonkchai K.
        • Vongsanim S.
        • Mohamed A.
        • Davenport A.
        Differences in the prevalence of sarcopenia in haemodialysis patients: the effects of gender and ethnicity.
        J Hum Nutr Diet. 2018; 31: 689-696
        • Beberashvili I.
        • Sinuani I.
        • Azar A.
        • et al.
        Serum uric acid as a clinically useful nutritional marker and predictor of outcome in maintenance hemodialysis patients.
        Nutrition. 2015; 31: 138-147
        • Beberashvili I.
        • Sinuani I.
        • Azar A.
        • et al.
        Longitudinal study of leptin levels in chronic hemodialysis patients.
        Nutr J. 2011; 10: 68
        • Małgorzewicz S.
        • Aleksandrowicz-Wrona E.
        • Owczarzak A.
        • Debska-Slizień A.
        • Rutkowski B.
        • Łysiak-Szydłowska W.
        Adipokines and nutritional status for patients on maintenance hemodialysis.
        J Ren Nutr. 2009; 20: 303-308
        • Kalantar-Zadeh K.
        • Block G.
        • McAllister C.J.
        • Humphreys M.H.
        • Kopple J.D.
        Appetite and inflammation, nutrition, anemia, and clinical outcome in hemodialysis patients.
        Am J Clin Nutr. 2004; 80: 299-307
        • Reis J.M.S.
        • Alves L.S.
        • Vogt B.P.
        According to revised EWGSOP sarcopenia consensus cut-off points, low physical function is associated with nutritional status and quality of life in maintenance hemodialysis patients.
        J Ren Nutr. 2021; 20
        • Martinson M.
        • Ikizler T.A.
        • Morrell G.
        • et al.
        Associations of body size and body composition with functional ability and quality of life in hemodialysis patients.
        Clin J Am Soc Nephrol. 2014; 9: 1082-1090
        • Kakiya R.
        • Shoji T.
        • Tsujimoto Y.
        • et al.
        Body fat mass and lean mass as predictors of survival in hemodialysis patients.
        Kidney Int. 2006; 70: 549-556
        • Androga L.
        • Sharma D.
        • Amodu A.
        • Abramowitz M.K.
        Sarcopenia, obesity, and mortality in US adults with and without chronic kidney disease.
        Kidney Int Rep. 2017; 2: 201-211
        • Kim J.K.
        • Kim S.G.
        • Oh J.E.
        • et al.
        Impact of sarcopenia on long-term mortality and cardiovascular events in patients undergoing hemodialysis.
        Korean J Intern Med. 2019; 34: 599-607
        • Cobo G.
        • Lindholm B.
        • Stenvinkel P.
        Chronic inflammation in end-stage renal disease and dialysis.
        Nephrol Dial Transpl. 2018; 33: iii35-iii40
        • Pietiläinen K.H.
        • Kaye S.
        • Karmi A.
        • Suojanen L.
        • Rissanen A.
        • Virtanen K.A.
        Agreement of bioelectrical impedance with dual-energy X-ray absorptiometry and MRI to estimate changes in body fat, skeletal muscle and visceral fat during a 12-month weight loss intervention.
        Br J Nutr. 2013; 109: 1910-1916
        • Dent E.
        • Morley J.E.
        • Cruz-Jentoft A.J.
        • et al.
        International clinical practice Guidelines for sarcopenia (ICFSR): Screening, diagnosis and Management.
        J Nutr Health Aging. 2018; 22: 1148-1161