DOI QR코드

DOI QR Code

Clinical features and molecular mechanism of muscle wasting in end stage renal disease

  • Sang Hyeon Ju (Department of Internal Medicine, Chungnam National University School of Medicine) ;
  • Hyon-Seung Yi (Department of Internal Medicine, Chungnam National University School of Medicine)
  • 투고 : 2023.06.07
  • 심사 : 2023.07.17
  • 발행 : 2023.08.31

초록

Muscle wasting in end-stage renal disease (ESRD) is an escalating issue due to the increasing global prevalence of ESRD and its significant clinical impact, including a close association with elevated mortality risk. The phenomenon of muscle wasting in ESRD, which exceeds the rate of muscle loss observed in the normal aging process, arises from multifactorial processes. This review paper aims to provide a comprehensive understanding of muscle wasting in ESRD, covering its epidemiology, underlying molecular mechanisms, and current and emerging therapeutic interventions. It delves into the assessment techniques for muscle mass and function, before exploring the intricate metabolic and molecular pathways that lead to muscle atrophy in ESRD patients. We further discuss various strategies to mitigate muscle wasting, including nutritional, pharmacological, exercise, and physical modalities intervention. This review seeks to provide a solid foundation for future research in this area, fostering a deeper understanding of muscle wasting in ESRD, and paving the way for the development of novel strategies to improve patient outcomes.

키워드

과제정보

This work was supported by a grant from the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (grant number: HR22C1734). H-SY was supported by the Basic Science Research Program, through the National Research Foundation of Korea (NRF), funded by the Ministry of Science, ICT and Future Planning, Republic of Korea (NRF-2023R1A2C3006220).

참고문헌

  1. Rossing P, Caramori ML, Chan JC et al (2022) KDIGO 2022 clinical practice guideline for diabetes management in chronic kidney disease. Kidney Int 102, S1-S127 https://doi.org/10.1016/j.kint.2022.06.008
  2. Kovesdy CP (2022) Epidemiology of chronic kidney disease: an update 2022. Kidney Int Suppl (2011) 12, 7-11 https://doi.org/10.1016/j.kisu.2021.11.003
  3. Hashmi MF, Benjamin O and Lappin SL (2022) End-stage renal disease. StatPearls, Florida, United States
  4. Hill NR, Fatoba ST, Oke JL et al (2016) Global prevalence of chronic kidney disease-a systematic review and meta-analysis. PloS one 11, e0158765
  5. Bello AK, Okpechi IG, Osman MA et al (2022) Epidemiology of peritoneal dialysis outcomes. Nat Rev Nephrol 18, 779-793 https://doi.org/10.1038/s41581-022-00623-7
  6. Hong YA, Ban TH, Kang CY et al (2021) Trends in epidemiologic characteristics of end-stage renal disease from 2019 Korean Renal Data System (KORDS). Kidney Res Clin Pract 40, 52
  7. Shu X, Lin T, Wang H et al (2022) Diagnosis, prevalence, and mortality of sarcopenia in dialysis patients: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle 13, 145-158 https://doi.org/10.1002/jcsm.12890
  8. Volpi E, Nazemi R and Fujita S (2004) Muscle tissue changes with aging. Curr Opin Clin Nutr Metab Care 7, 405
  9. Mitchell WK, Williams J, Atherton P, Larvin M, Lund J and Narici M (2012) Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol 3, 260
  10. Wilkinson DJ, Piasecki M and Atherton PJ (2018) The age-related loss of skeletal muscle mass and function: measurement and physiology of muscle fibre atrophy and muscle fibre loss in humans. Ageing Res Rev 47, 123-132 https://doi.org/10.1016/j.arr.2018.07.005
  11. Kitamura M, Takazono T, Yamaguchi K et al (2021) The impact of muscle mass loss and deteriorating physical function on prognosis in patients receiving hemodialysis. Sci Rep 11, 22290
  12. Cheng TC, Huang SH, Kao CL and Hsu PC (2022) Muscle wasting in chronic kidney disease: mechanism and clinical implications-a narrative review. Int J Mol Sci 23, 6047
  13. Wang XH and Mitch WE (2014) Mechanisms of muscle wasting in chronic kidney disease. Nat Rev Nephrol 10, 504-516 https://doi.org/10.1038/nrneph.2014.112
  14. Balafa O, Halbesma N, Struijk DG, Dekker FW and Krediet RT (2011) Peritoneal albumin and protein losses do not predict outcome in peritoneal dialysis patients. Clin J Am Soc Nephrol 6, 561-566 https://doi.org/10.2215/CJN.05540610
  15. Wathanavasin W, Banjongjit A, Avihingsanon Y et al (2022) Prevalence of sarcopenia and its impact on cardiovascular events and mortality among dialysis patients: a systematic review and meta-analysis. Nutrients 14, 4077
  16. Yang L, He Y and Li X (2023) Physical function and all-cause mortality in patients with chronic kidney disease and end-stage renal disease: a systematic review and meta-analysis. Int Urol Nephrol 55, 1219-1228 https://doi.org/10.1007/s11255-022-03397-w
  17. Rosenberg I (1989) Epidemiologic and methodologic problems in determining nutritional status of older persons (Summary comments). Am J Cli Nutr 50, 1231-1233 https://doi.org/10.1093/ajcn/50.5.1231
  18. Cruz-Jentoft AJ, Baeyens JP, Bauer JM et al (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people. Age Ageing 39, 412-423 https://doi.org/10.1093/ageing/afq034
  19. Cruz-Jentoft AJ and Sayer AA (2019) Sarcopenia. Lancet 393, 2636-2646 https://doi.org/10.1016/S0140-6736(19)31138-9
  20. Baek JY, Jung HW, Kim KM et al (2023) Korean working group on sarcopenia guideline: expert consensus on sarcopenia screening and diagnosis by the Korean society of sarcopenia, the Korean society for bone and mineral research, and the Korean geriatrics society. Ann Geriatr Med Res 27, 9-21 https://doi.org/10.4235/agmr.23.0009
  21. Sabatino A, Broers NJ, Van der Sande FM, Hemmelder MH, Fiaccadori E and Kooman JP (2021) Estimation of muscle mass in the integrated assessment of patients on hemodialysis. Front Nutr 8, 697523
  22. Chamney PW, Wabel P, Moissl UM et al (2007) A whole-body model to distinguish excess fluid from the hydration of major body tissues. Am J Clin Nutr 85, 80-89 https://doi.org/10.1093/ajcn/85.1.80
  23. Ikizler TA, Burrowes JD, Byham-Gray LD et al (2020) KDOQI clinical practice guideline for nutrition in CKD: 2020 update. Am J Kidney Dis 76, S1-S107 https://doi.org/10.1053/j.ajkd.2020.05.006
  24. Kittiskulnam P, Carrero JJ, Chertow GM, Kaysen GA, Delgado C and Johansen KL (2017) Sarcopenia among patients receiving hemodialysis: weighing the evidence. J Cachexia Sarcopenia Muscle 8, 57-68 https://doi.org/10.1002/jcsm.12130
  25. Sanchez-Tocino ML, Miranda-Serrano B, Lopez-Gonzalez A et al (2022) Sarcopenia and mortality in older hemodialysis patients. Nutrients 14, 2354
  26. Seto Y, Kimura M, Matsunaga T, Miyasita E and Kanno Y (2022) Long-term body composition changes in patients undergoing hemodialysis: a single-center retrospective study. Ren Replace Ther 8, 1-8 https://doi.org/10.1186/s41100-021-00391-3
  27. Pellicano R, Strauss BJ, Polkinghorne KR and Kerr PG (2011) Longitudinal body composition changes due to dialysis. Clin J Am Soc Nephrol 6, 1668-1675 https://doi.org/10.2215/CJN.06790810
  28. John SG, Sigrist MK, Taal MW and McIntyre CW (2013) Natural history of skeletal muscle mass changes in chronic kidney disease stage 4 and 5 patients: an observational study. PloS one 8, e65372
  29. Silva MZC, Antonio KJ, Reis JMS, Alves LS, Caramori JCT and Vogt BP (2021) Age, diabetes mellitus, and dialysis modality are associated with risk of poor muscle strength and physical function in hemodialysis and peritoneal dialysis patients. Kidney Res Clin Pract 40, 294
  30. Birajdar N, Anandh U, Premlatha S and Rajeshwari G (2019) Hand grip strength in patients on maintenance hemodialysis: an observational cohort study from India. Indian J Nephrol 29, 393
  31. Van Loon I, Hamaker ME, Boereboom FT et al (2017) A closer look at the trajectory of physical functioning in chronic hemodialysis. Age Ageing 46, 594-599 https://doi.org/10.1093/ageing/afx006
  32. Kurella Tamura M, Covinsky KE, Chertow GM, Yaffe K, Landefeld CS and McCulloch CE (2009) Functional status of elderly adults before and after initiation of dialysis. N Engl J Med 361, 1539-1547 https://doi.org/10.1056/NEJMoa0904655
  33. Delmonico MJ, Harris TB, Visser M et al (2009) Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr 90, 1579-1585 https://doi.org/10.3945/ajcn.2009.28047
  34. Goodpaster BH, Park SW, Harris TB et al (2006) The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 61, 1059-1064 https://doi.org/10.1093/gerona/61.10.1059
  35. Chen X, Han P, Zhang K et al (2023) Physical performance and muscle strength rather than muscle mass are predictor of all-cause mortality in hemodialysis patients. Front Public Health 11,1087248
  36. Wang XH, Mitch WE and Price SR (2022) Pathophysiological mechanisms leading to muscle loss in chronic kidney disease. Nat Rev Nephrol 18, 138-152 https://doi.org/10.1038/s41581-021-00498-0
  37. Mitch WE and Goldberg AL (1996) Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N Engl J Med 335, 1897-1905 https://doi.org/10.1056/NEJM199612193352507
  38. Gomes MD, Lecker SH, Jagoe RT, Navon A and Goldberg AL (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci U S A 98, 14440-14445 https://doi.org/10.1073/pnas.251541198
  39. Bodine SC, Latres E, Baumhueter S et al (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 1704-1708 https://doi.org/10.1126/science.1065874
  40. Du J, Wang X, Miereles C et al (2004) Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 113, 115-123 https://doi.org/10.1172/JCI18330
  41. Wang K, Liu Q, Tang M et al (2022) Chronic kidney disease-induced muscle atrophy: molecular mechanisms and promising therapies. Biochem Pharmacol 208, 115407
  42. Spoto B, Pisano A and Zoccali C (2016) Insulin resistance in chronic kidney disease: a systematic review. Am J Physiol Renal Physiol 311, F1087-F1108 https://doi.org/10.1152/ajprenal.00340.2016
  43. Zhang L, Wang XH, Wang H, Du J and Mitch WE (2010) Satellite cell dysfunction and impaired IGF-1 signaling cause CKD-induced muscle atrophy. J Am Soc Nephrol 21, 419-427 https://doi.org/10.1681/ASN.2009060571
  44. Ding H, Gao XL, Hirschberg R, Vadgama JV and Kopple JD (1996) Impaired actions of insulin-like growth factor 1 on protein synthesis and degradation in skeletal muscle of rats with chronic renal failure. Evidence for a postreceptor defect. J Clin Invest 97, 1064-1075 https://doi.org/10.1172/JCI118499
  45. Carrero JJ, Stenvinkel P, Cuppari L et al (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 https://doi.org/10.1053/j.jrn.2013.01.001
  46. Abrigo J, Elorza AA, Riedel CA et al (2018) Role of oxidative stress as key regulator of muscle wasting during cachexia. Oxid Med Cell Longev 2018, 2063179
  47. Hyatt H, Deminice R, Yoshihara T and Powers SK (2019) Mitochondrial dysfunction induces muscle atrophy during prolonged inactivity: a review of the causes and effects. Arch Biochem Biophys 662, 49-60 https://doi.org/10.1016/j.abb.2018.11.005
  48. Mitch WE, Medina R, Grieber S et al (1994) Metabolic acidosis stimulates muscle protein degradation by activating the adenosine triphosphate-dependent pathway involving ubiquitin and proteasomes. J Clin Invest 93, 2127-2133 https://doi.org/10.1172/JCI117208
  49. Molina P, Carrero JJ, Bover J et al (2017) Vitamin D, a modulator of musculoskeletal health in chronic kidney disease. J Cachexia Sarcopenia Muscle 8, 686-701 https://doi.org/10.1002/jcsm.12218
  50. Carrero JJ, Qureshi AR, Parini P et al (2009) Low serum testosterone increases mortality risk among male dialysis patients. J Am Soc Nephrol 20, 613-620 https://doi.org/10.1681/ASN.2008060664
  51. Hu Z, Wang H, Lee IH, Du J and Mitch WE (2009) Endogenous glucocorticoids and impaired insulin signaling are both required to stimulate muscle wasting under pathophysiological conditions in mice. J Clin Invest 119, 3059-3069 https://doi.org/10.1172/JCI38770
  52. Gungor O, Ulu S, Hasbal NB, Anker SD and Kalantar-Zadeh K (2021) Effects of hormonal changes on sarcopenia in chronic kidney disease: where are we now and what can we do? J Cachexia Sarcopenia Muscle 12, 1380-1392 https://doi.org/10.1002/jcsm.12839
  53. Gharahdaghi N, Phillips BE, Szewczyk NJ, Smith K, Wilkinson DJ and Atherton PJ (2021) Links between testosterone, oestrogen, and the growth hormone/insulin-like growth factor axis and resistance exercise muscle adaptations. Front Physiol 11, 621226
  54. Hendriks FK, Smeets JS, Broers NJ et al (2020) End-stage renal disease patients lose a substantial amount of amino acids during hemodialysis. J Nutr 150, 1160-1166 https://doi.org/10.1093/jn/nxaa010
  55. Ikizler TA, Flakoll PJ, Parker RA and Hakim RM (1994) Amino acid and albumin losses during hemodialysis. Kidney Int 46, 830-837 https://doi.org/10.1038/ki.1994.339
  56. Popkov VA, Silachev DN, Zalevsky AO, Zorov DB and Plotnikov EY (2019) Mitochondria as a source and a target for uremic toxins. Int J Mol Sci 20, 3094
  57. Pieniazek A, Bernasinska-Slomczewska J and Gwozdzinski L (2021) Uremic toxins and their relation with oxidative stress induced in patients with CKD. Int J Mol Sci 22, 6196
  58. Todoriki S, Hosoda Y, Yamamoto T et al (2022) Methylglyoxal induces inflammation, metabolic modulation and oxidative stress in myoblast cells. Toxins (Basel) 14, 263
  59. Edamatsu T, Fujieda A and Itoh Y (2018) Phenyl sulfate, indoxyl sulfate and p-cresyl sulfate decrease glutathione level to render cells vulnerable to oxidative stress in renal tubular cells. PloS one 13, e0193342
  60. Bindels LB and Delzenne NM (2013) Muscle wasting: the gut microbiota as a new therapeutic target? Int J Biochem Cell Biol 45, 2186-2190 https://doi.org/10.1016/j.biocel.2013.06.021
  61. Vaziri ND, Wong J, Pahl M et al (2013) Chronic kidney disease alters intestinal microbial flora. Kidney Int 83, 308-315 https://doi.org/10.1038/ki.2012.345
  62. Ramezani A and Raj DS (2014) The gut microbiome, kidney disease, and targeted interventions. J Am Soc Nephrol 25, 657-670 https://doi.org/10.1681/ASN.2013080905
  63. Wang XH (2013) MicroRNA in myogenesis and muscle atrophy. Curr Opin Clin Nutr Metab Care 16, 258
  64. Pupim LB, Flakoll PJ, Brouillette JR, Levenhagen DK, Hakim RM and Ikizler TA (2002) Intradialytic parenteral nutrition improves protein and energy homeostasis in chronic hemodialysis patients. J Clin Invest 110, 483-492 https://doi.org/10.1172/JCI0215449
  65. Pupim LB, Majchrzak KM, Flakoll PJ and Ikizler TA (2006) Intradialytic oral nutrition improves protein homeostasis in chronic hemodialysis patients with deranged nutritional status. J Am Soc Nephrol 17, 3149-3157 https://doi.org/10.1681/ASN.2006040413
  66. Tomayko EJ, Kistler BM, Fitschen PJ and Wilund KR (2015) Intradialytic protein supplementation reduces inflammation and improves physical function in maintenance hemodialysis patients. J Ren Nutr 25, 276-283 https://doi.org/10.1053/j.jrn.2014.10.005
  67. Matsuzawa R, Yamamoto S, Suzuki Y et al (2021) The effects of amino acid/protein supplementation in patients undergoing hemodialysis: a systematic review and meta-analysis of randomized controlled trials. Clin Nutr ESPEN 44, 114-121 https://doi.org/10.1016/j.clnesp.2021.04.027
  68. Weiner DE, Tighiouart H, Ladik V, Meyer KB, Zager PG and Johnson DS (2014) Oral intradialytic nutritional supplement use and mortality in hemodialysis patients. Am J Kidney Dis 63, 276-285 https://doi.org/10.1053/j.ajkd.2013.08.007
  69. Maruyama T, Maruyama N, Higuchi T et al (2019) Efficacy of L-carnitine supplementation for improving lean body mass and physical function in patients on hemodialysis: a randomized controlled trial. Eur J Clin Nutr 73, 293-301 https://doi.org/10.1038/s41430-018-0348-y
  70. Fitschen PJ, Biruete A, Jeong J and Wilund KR (2017) Efficacy of beta-hydroxy-beta-methylbutyrate supplementation in maintenance hemodialysis patients. Hemodial Int 21, 107-116 https://doi.org/10.1111/hdi.12440
  71. Ju SH, Lee EJ, Sim BC et al (2023) Leucine-enriched amino acid supplementation and exercise to prevent sarcopenia in patients on hemodialysis: a single-arm pilot study. Front Nutr 10, 1069651
  72. Shah AP, Kalantar-Zadeh K and Kopple JD (2015) Is there a role for ketoacid supplements in the management of CKD? Am J Kidney Dis 65, 659-673 https://doi.org/10.1053/j.ajkd.2014.09.029
  73. Garibotto G, Saio M, Aimasso F et al (2021) How to overcome anabolic resistance in dialysis-treated patients? Front Nutr 8, 701386
  74. Baker LA, March DS, Wilkinson TJ et al (2022) Clinical practice guideline exercise and lifestyle in chronic kidney disease. BMC Nephrol 23, 1-36 https://doi.org/10.1186/s12882-021-02628-z
  75. Clarkson MJ, Bennett PN, Fraser SF and Warmington SA (2019) Exercise interventions for improving objective physical function in patients with end-stage kidney disease on dialysis: a systematic review and meta-analysis. Am J Physiol Renal Physiol 316, F856-F872 https://doi.org/10.1152/ajprenal.00317.2018
  76. March DS, Wilkinson TJ, Burnell T et al (2022) The effect of non-pharmacological and pharmacological interventions on measures associated with sarcopenia in end-stage kidney disease: a systematic review and meta-analysis. Nutrients 14, 1817
  77. Sheng K, Zhang P, Chen L, Cheng J, Wu C and Chen J (2014) Intradialytic exercise in hemodialysis patients: a systematic review and meta-analysis. Am J Nephrol 40, 478-490 https://doi.org/10.1159/000368722
  78. Hendriks FK, Smeets JS, van der Sande FM, Kooman JP and van Loon LJ (2019) Dietary protein and physical activity interventions to support muscle maintenance in end-stage renal disease patients on hemodialysis. Nutrients 11, 2972
  79. Young HM, March DS, Graham-Brown MP et al (2018) Effects of intradialytic cycling exercise on exercise capacity, quality of life, physical function and cardiovascular measures in adult haemodialysis patients: a systematic review and meta-analysis. Nephrol Dial Transplant 33, 1436-1445 https://doi.org/10.1093/ndt/gfy045
  80. Zhao Q, He Y, Wu N et al (2023) Non-pharmacological interventions to improve physical function in patients with end-stage renal disease: a network meta-analysis. Am J Nephrol 54, 35-41 https://doi.org/10.1159/000530219
  81. Macdonald JH, Marcora SM, Jibani MM, Kumwenda MJ, Ahmed W and Lemmey AB (2007) Nandrolone decanoate as anabolic therapy in chronic kidney disease: a randomized phase II dose-finding study. Nephron Clin Pract 106, c125-c135 https://doi.org/10.1159/000103000
  82. Johansen KL, Mulligan K and Schambelan M (1999) Anabolic effects of nandrolone decanoate in patients receiving dialysis: a randomized controlled trial. JAMA 281, 1275-1281 https://doi.org/10.1001/jama.281.14.1275
  83. Supasyndh O, Satirapoj B, Aramwit P et al (2013) Effect of oral anabolic steroid on muscle strength and muscle growth in hemodialysis patients. Clin J Am Soc Nephrol 8, 271-279 https://doi.org/10.2215/CJN.00380112
  84. Becker C, Lord SR, Studenski SA et al (2015) Myostatin antibody (LY2495655) in older weak fallers: a proof-of-concept, randomised, phase 2 trial. Lancet Diabetes Endocrinol 3, 948-957 https://doi.org/10.1016/S2213-8587(15)00298-3
  85. Hung AM, Ellis CD, Shintani A, Booker C and Ikizler TA (2011) IL-1β receptor antagonist reduces inflammation in hemodialysis patients. J Am Soc Nephrol 22, 437-442 https://doi.org/10.1681/ASN.2010070760
  86. Kittiskulnam P, Srijaruneruang S, Chulakadabba A et al (2020) Impact of serum bicarbonate levels on muscle mass and kidney function in pre-dialysis chronic kidney disease patients. Am J Nephrol 51, 24-34 https://doi.org/10.1159/000504557
  87. Abramowitz MK, Melamed ML, Bauer C, Raff AC and Hostetter TH (2013) Effects of oral sodium bicarbonate in patients with CKD. Clin J Am Soc Nephrol 8, 714-720 https://doi.org/10.2215/CJN.08340812
  88. Garibotto G, Barreca A, Russo R et al (1997) Effects of recombinant human growth hormone on muscle protein turnover in malnourished hemodialysis patients. J Clin Invest 99, 97-105 https://doi.org/10.1172/JCI119139
  89. Hansen T, Gram J, Jensen P et al (2000) Influence of growth hormone on whole body and regional soft tissue composition in adult patients on hemodialysis. A double-blind, randomized, placebo-controlled study. Clin Nephrol 53, 99-107
  90. Pupim LB, Flakoll PJ, Yu C and Ikizler TA (2005) Recombinant human growth hormone improves muscle amino acid uptake and whole-body protein metabolism in chronic hemodialysis patients. Am J Clin Nutr 82, 1235-1243 https://doi.org/10.1093/ajcn/82.6.1235
  91. Niemczyk S, Sikorska H, Wiecek A et al (2010) A super-agonist of growth hormone-releasing hormone causes rapid improvement of nutritional status in patients with chronic kidney disease. Kidney Int 77, 450-458 https://doi.org/10.1038/ki.2009.480
  92. Bajaj M, Baig R, Suraamornkul S et al (2010) Effects of pioglitazone on intramyocellular fat metabolism in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab 95, 1916-1923 https://doi.org/10.1210/jc.2009-0911
  93. Yokota T, Kinugawa S, Hirabayashi K et al (2017) Pioglitazone improves whole-body aerobic capacity and skeletal muscle energy metabolism in patients with metabolic syndrome. J Diabetes Investig 8, 535-541 https://doi.org/10.1111/jdi.12606
  94. Yen CL, Wu CY, See LC et al (2020) Pioglitazone reduces mortality and adverse events in patients with type 2 diabetes and with advanced chronic kidney disease: national cohort study. Diabetes Care 43, e152-e153 https://doi.org/10.2337/dc20-1584
  95. Bataille S, Landrier JF, Astier J et al (2016) The "dose-effect" relationship between 25-hydroxyvitamin D and muscle strength in hemodialysis patients favors a normal threshold of 30 ng/mL for plasma 25-hydroxyvitamin D. J Ren Nutr 26, 45-52 https://doi.org/10.1053/j.jrn.2015.08.007
  96. Wang L, Luo Q, Zhu B and Zhou F (2019) Relation of serum 25-hydroxyvitamin D Status with skeletal muscle mass and grip strength in patients on peritoneal dialysis. J Nutr Sci Vitaminol (Tokyo) 65, 477-482 https://doi.org/10.3177/jnsv.65.477
  97. Gordon PL, Sakkas GK, Doyle JW, Shubert T and Johansen KL (2007) Relationship between vitamin D and muscle size and strength in patients on hemodialysis. J Ren Nutr 17, 397-407 https://doi.org/10.1053/j.jrn.2007.06.001
  98. Taskapan H, Baysal O, Karahan D, Durmus B, Altay Z and Ulutas O (2011) Vitamin D and muscle strength, functional ability and balance in peritoneal dialysis patients with vitamin D deficiency. Clin Nephrol 76, 110-116 https://doi.org/10.5414/CN107160
  99. Ashby DR, Ford HE, Wynne KJ et al (2009) Sustained appetite improvement in malnourished dialysis patients by daily ghrelin treatment. Kidney Int 76, 199-206 https://doi.org/10.1038/ki.2009.114
  100. Wynne K, Giannitsopoulou K, Small CJ et al (2005) Subcutaneous ghrelin enhances acute food intake in malnourished patients who receive maintenance peritoneal dialysis: a randomized, placebo-controlled trial. J Am Soc Nephrol 16, 2111-2118 https://doi.org/10.1681/ASN.2005010039
  101. Campbell GA, Patrie JT, Gaylinn BD, Thorner MO and Bolton WK (2018) Oral ghrelin receptor agonist MK0677 increases serum insulin-like growth factor 1 in hemodialysis patients: a randomized blinded study. Nephrol Dial Transplant 33, 523-530
  102. Monfared A, Heidarzadeh A, Ghaffari M and Akbarpour M (2009) Effect of megestrol acetate on serum albumin level in malnourished dialysis patients. J Ren Nutr 19, 167-171 https://doi.org/10.1053/j.jrn.2008.11.003
  103. Golebiewska JE, Lichodziejewska-Niemierko M, Aleksandrowicz-Wrona E, Majkowicz M, Lysiak-Szydlowska W and Rutkowski B (2012) Influence of megestrol acetate on nutrition, inflammation and quality of life in dialysis patients. Int Urol Nephrol 44, 1211-1222 https://doi.org/10.1007/s11255-011-0025-8
  104. Valenzuela PL, Morales JS, Ruilope LM, de la Villa P, Santos-Lozano A and Lucia A (2020) Intradialytic neuromuscular electrical stimulation improves functional capacity and muscle strength in people receiving haemodialysis: a systematic review. J Physiother 66, 89-96 https://doi.org/10.1016/j.jphys.2020.03.006
  105. Cho YS, Joo SY, Lee EK, Kee YK, Seo CH and Kim DH (2021) Effect of extracorporeal shock wave therapy on muscle mass and function in patients undergoing maintenance hemodialysis: a randomized controlled pilot study. Ultrasound Med Biol 47, 3202-3210 https://doi.org/10.1016/j.ultrasmedbio.2021.07.021
  106. Dompe C, Moncrieff L, Matys J et al (2020) Photobiomodulation-underlying mechanism and clinical applications. J Clin Med 9, 1724
  107. Schardong J, Falster M, Sisto IR et al (2021) Photobiomodulation therapy increases functional capacity of patients with chronic kidney failure: randomized controlled trial. Lasers Med Sci 36, 119-129 https://doi.org/10.1007/s10103-020-03020-3
  108. Macagnan FE, Baroni BM, Cristofoli EZ, Godoy M, Schardong J and Plentz RDM (2019) Acute effect of photobiomodulation therapy on handgrip strength of chronic kidney disease patients during hemodialysis. Lasers Med Sci 34, 835-840 https://doi.org/10.1007/s10103-018-2593-7
  109. Dienemann T, Ziolkowski SL, Bender S et al (2021) Changes in body composition, muscle strength, and fat distribution following kidney transplantation. Am J Kidney Dis 78, 816-825 https://doi.org/10.1053/j.ajkd.2020.11.032
  110. Kosoku A, Ishihara T, Iwai T et al (2022) The change in muscle mass among kidney transplant recipients: a prospective cohort study. Transplant Proc 54, 346-350 https://doi.org/10.1016/j.transproceed.2021.08.064
  111. Moreau K, Desseix A, Germain C et al (2021) Evolution of body composition following successful kidney transplantation is strongly influenced by physical activity: results of the CORPOS study. BMC Nephrol 22, 31
  112. Deger SM, Hewlett JR, Gamboa J et al (2018) Insulin resistance is a significant determinant of sarcopenia in advanced kidney disease. Am J Physiol Endocrinol Metab 315, E1108-E1120 https://doi.org/10.1152/ajpendo.00070.2018
  113. Dember LM, Hung A, Mehrotra R et al (2022) A randomized controlled pilot trial of anakinra for hemodialysis inflammation. Kidney Int 102, 1178-1187 https://doi.org/10.1016/j.kint.2022.06.022
  114. Zanchi A, Tappy L, Le KA et al (2014) Pioglitazone improves fat distribution, the adipokine profile and hepatic insulin sensitivity in non-diabetic end-stage renal disease subjects on maintenance dialysis: a randomized cross-over pilot study. PloS one 9, e109134
  115. Rattanasompattikul M, Molnar MZ, Lee ML et al (2013) Anti-Inflammatory and Anti-Oxidative Nutrition in Hypoalbuminemic Dialysis Patients (AIONID) study: results of the pilot-feasibility, double-blind, randomized, placebo-controlled trial. J Cachexia Sarcopenia Muscle 4, 247-257 https://doi.org/10.1007/s13539-013-0115-9
  116. Hung AM, Booker C, Ellis CD et al (2015) Omega-3 fatty acids inhibit the up-regulation of endothelial chemokines in maintenance hemodialysis patients. Nephrol Dial Transplant 30, 266-274 https://doi.org/10.1093/ndt/gfu283