The control of muscle protein turnover in patients on peritoneal dialysis

Laura Piracci, Giacomo Garibotto, Antonella Sophia, Elena Ratto, Alice Bonanni, Emanuele Luigi Parodi, Francesca Viazzi, Barbara Bonino, Daniela Picciotto, Daniela Verzola

Abstract


Wasting is observed in a large percentage of patients receiving peritoneal dialysis (PD) and it is associated with functional impairment and worse outcome. In this article, we review the current state of our knowledge regarding the effects of PD on protein metabolism and their possible interactions with the uremia-induced and comorbidity-induced alterations in protein metabolism. Available evidence shows that glucose-based PD induces a new state in muscle protein dynamics, which is characterized by decreased turnover rates and a reduced efficiency of protein turnover, a condition which may be harmful in stress conditions, when nutrient intake is diminished or during superimposed catabolic illnesses. The effects of PD on protein turnover may overlap with the effects of aging and comorbidities to promote net catabolism. There is a need to develop more effective treatments to enhance the nutritional and functional status of PD patients. New approaches include the use of icodextrins to maintain extracellular volume, amino acids/keto acids-containing supplements combined with physical exercise, vitamin D, myostatin antagonism, and ghrelin agonism for malnourished patients refractory to standard nutritional therapy.

Keywords


nutrition, peritoneal dialysis, amino acids, ckd

Full Text:

 Subscribers Only

References


Philip Kam-Tao Li et al, Changes in the worldwide epidemiology of peritoneal dialysis, Nature Reviews Nephrology, Vol. 13, February 2017

Young GA, Kopple JD, Lindholm B, Vonesh EF, De Vecchi A, Scalamogna A, et al. Nutritional assessment of continuous ambulatory peritoneal dialysis patients: an international study. Am J Kidney Dis. 1991; 17:462-71.

Mehrotra R, Chiu YW, Kalantar-Zadeh K, Bargman J, Vonesh E. Similar outcomes with hemodialysis and peritoneal dialysis in patients with end-stage renal disease. Arch Intern Med 2011; 171:110-8.

Han SH, Han DS. Nutrition in patients on peritoneal dialysis. Nat Rev Nephrol 2012; 8:163-75.

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.

Morley JE, Vellas B, van Kan GA, Anker SD, Bauer JM, Bemabei R et al. Frailty consensus: a call to action. J Am Med Dir Assoc 2013; 14: 392–397).

Kang SH, Cho KH, Park JW, Do JY. Low appendicular muscle mass is associated with mortality in peritoneal dialysis patients: a single-center cohort study. Eur J Clin Nutr. 2017 Jun 28.

Isoyama N, Qureshi AR, Avesani CM, Lindholm B, Bàràny P, Heimbürger O, Cederholm T, Stenvinkel P, Carrero JJ. Comparative associations of muscle mass and muscle strength with mortality in dialysis patients, Clin J Am Soc Nephrol, 2014 Oct 7;9(10):1720-8

Carrero JJ, Chmielewski M, Axelsson J, Snaedal S, Heimburger O, Barany P, Suliman ME, Lindholm B, Stenvinkel P, Qureshi AR: Muscle atrophy, inflammation and clinical outcome in incident and prevalent dialysis patients. Clin Nutr 27: 557-564, 2008

Stenvinkel et al, Are there two types of malnutrition in chronic renal failure? Evidence for relationships between malnutrition, inflammation and atherosclerosis (MIA syndrome). Nephrol, Dial Tranplsant 2000; 15(7)): 953-960

Krediet RT, Zuyderhoudt FM, Boeschoten EW, Arisz L. Peritoneal permeability to proteins in diabetic and non-diabetic continuous ambulatory peritoneal dialysis patients. Nephron 1986; 42:133-40.

Westra WM, Kopple JD, Krediet RT, Appell M, Mehrotra R. Dietary protein requirements and dialysate protein losses in chronic peritoneal dialysis patients. Perit Dial Int. 2007; 27:192-5.

Morrison G. Metabolic effects of continuous ambulatory peritoneal dialysis. Annu Rev Med 1989; 40:163-72

Kathuria, P. et al Effect of dialysis modality and membrane transport characteristics on dialysate protein losses of patients on peritoneal dialysis. Perit. Dial. Int. 17, 449-454 (1997).

Chung, S. H., Heimburger, O. & Lindholm, B. Poor outcomes for fast transporters on PD: the rise and fall of a clinical concern. Semin. Dial. 21. 7-10 (2008)

Balafa O, Halbesma N, Struijk DG, Dekker FW, Krediet RT. Peritoneal albumin and protein losses do not predict outcome in peritoneal dialysis patients. Clin J Am Soc Nephrol 2011; 6:561–6.

Grodstein GP, Blumenkrantz MJ, Kopple JD, Moran JK, Coburn JW. Glucose absorption during continuous ambulatory peritoneal dialysis. Kidney Int. 1981;19(4):564-567

Davies SJ, Russell L, Bryan J, Phillips L, Russell GI. Impact of peritoneal absorption of glucose on appetite, protein catabolism and survival in CAPD patients. Clin. Nephrol. 1996;45(3): 194-198

Abbott KC, Oliver DK, Hurst FP, Das NP, Gao SW, Perkins RM. Body mass index and peritoneal dialysis: "exceptions to the exception" in reverse epidemiology? Semin Dial. 2007; 20:561-5.

Chung SH, Carrero JJ, Lindholm B. Causes of poor appetite in patients on peritoneal dialysis. J Ren Nutr 2011; 21:12-5.

Ross EA, Koo LC. Improved nutrition after the detection and treatment of occult gastroparesis in nondiabetic dialysis patients. Am J Kidney Dis. 1998 ; 31 (1): 62-66

Schoonjans R, Van Vlem B, Vandamme W, et al. Gastric emptying of solids in cirrhotic and peritoneal dialysis patients: influence of peritoneal volume load. Eur J Gastroenterol Hepatol. 2002; 14(4): 395-398

Van V, Schoonjans RS, Struijk DG, et al. Influence of dialysate on gastric emptying time in peritoneal dialysis patients. Perit. Dial. Int. 2002; 22(1): 32-38

Lee SW, Song JH, Kim GA, Yang HJ, Lee KJ, Kim MJ. Effect of dialysis modalities on gastric myoelectrical activity in end-stage renal disease patients. Am J Kidney Dis. 2000; 36(3): 566-573

Rodríguez-Carmona A, Pérez-Fontán M, Guitián A, Peteiro J, García-Falcón T, López-Muñiz A, et al. Effect of low-GDP bicarbonate-lactate-buffered peritoneal dialysis solutions on plasma levels of adipokines and gut appetite-regulatory peptides. A randomized crossover study. Nephrol Dial Transpl. 2012; 27:369-74.

Wang XH, Mitch WE, Mechanisms of muscle wasting in chronic kidney disease. Nat Rev Nephrol. 2014 Sep;10(9):504-16.

Bailey JL, Zheng B, Hu Z, Price SR, Mitch WE. Chronic kidney disease causes defects in signalling through the insulin receptor substrate/phospatidylinositol 3-kinase/Akt pathway: implications for muscle atrophy. J Am Soc Nephrol. 2006; 17:1388-94

Zhang L, Rajan V, Lin E, Hu Z, Han HQ, Zhou X et al. Pharmacological inhibition of myostatin suppresses systemic inflammation and muscle atrophy in mice with chronic kidney disease. FASEB J 2011; 25:1653-63.

Verzola D, Procopio V, Sofia A, Villaggio B, Tarroni A, Bonanni A et al. Apoptosis and myostatin mRNA are upregulated in the skeletal muscle of patients with chronic kidney disease. Kidney Int 2011; 79:773-82.

Zhang L, Pan J, Dong Y, Tweardy DJ, Dong Y, Garibotto G, Mitch WE; Stat3 activation links a C/EBPδ to myostatin pathway to stimulate loss of muscle mass. Cell Metab. 2013 Sep 3;18(3):368-79.

Ikizler TA, Wingard RL, Harvell J, Shyr Y, Hakim R. Association of morbidity with markers of nutrition and inflammation in chronic hemodialysis patients: A prospective study. Kidney Int 1999; 55:1945–51.

Foley RN, Pafrey PS, Harnett JD, Kent GM, Murray DC. Hypoalbuminemia, cardiac morbidity, and mortality in end-stage renal disease. J Am Soc Nephrol 1996; 7:728–36.

Mehrotra R, Duong U, Jiwakanon S, Kovesdy CP, Moran J, Kopple JD, et al. Serum albumin as a predictor of mortality in peritoneal dialysis: comparisons with hemodialysis. Am J Kidney Dis 2011; 58:418-28.

Prinsen BH, Rabelink TJ, Beutler JJ, Kaysen GA, De Boer J, Boer WH, et al. Increased albumin and fibrinogen synthesis rate in patients with chronic renal failure. Kidney Int. 2003; 64:1495-504.

Clinical practice guidelines for nutrition in chronic renal failure. K/DOQI, National Kidney Foundation. AM J Kid Disease 2000;35 (suppl 2): S1-140

Kang J, Holland M, Jones H, Kaysen GA. Coordinate augmentation in expression of genes encoding transcription and liver secretory proteins in hypo-oncotic states. Kidney Int 1999; 56:454–60

Tessari P. Protein metabolism in liver cirrhosis: from albumin to muscle myofibrils. Curr Opin Clin Nutr Metab Care. 2003 ;6:79-85.

Keys A, Brozek J, Henschel A, Mickelsen O, Taylor H. The Biology of Human Starvation, Minneapolis. University of Minnesota Press; Minneapolis, MN, USA: 1950.

Rigaud D, Hassid J, Meulemans A, Poupard AT, Boulier A. A paradoxical increase in resting energy expenditure in malnourished patients near death: the king penguin syndrome. Am J Clin Nutr. 2000;72:355-60.

Kaysen GA. Biological basis of hypoalbuminemia in ESRD. J Am Soc Nephrol 1998; 9:2368-76.

John B, Tan BK, Dainty S, Spanel P, Smith D, Davies SJ. Plasma volume, albumin, and fluid status in peritoneal dialysis patients. Clin J Am Soc Nephrol. 2010; 5:1463-70.

Emerson TE. Unique features of albumin: A brief review. Crit Care Med. 1989;17:690–4.

Bergstrom J. Nutrition and mortality in hemodialysis. J Am Soc Nephrol 1995; 6:1329–41.

Yeun JY, Kaysen GA. Factors influencing serum albumin in dialysis patients. Am J Kid Dis 1998;32 Suppl 4:S 118-25

A.Y. Wang, M.M. Sea, R. Ip, et al.Independent effects of residual renal function and dialysis adequacy on actual dietary protein, calorie, and other nutrient intake in patients on continuous ambulatory peritoneal dialysis, J Am Soc Nephrol, 12 (11) (2001), pp. 2450-2457

Cheng, W. Tang, T. Wang; Strong association between volume status and nutritional status in peritoneal dialysis patients; Am J Kidney Dis, 45 (5) (2005)

G. Garibotto, A. Sofia, S. Saffioti, A. Bonanni, I. Mannucci, D. Verzola Amino acid and protein metabolism in the human kidney and in patients with chronic kidney disease; Clinical Nutrition 2010 Aug;29(4): 424-433)

P. Tessari, G. Deferrari, C. Robaudo, M. Vettore, N. Pastorino, L. De Biasi, G. Garibotto: Phenylalanine hydroxylation across the kidney in humans rapid communication, Kidney Int. 1999 Dec;56(6):2168-72

G. Garibotto, A. Sofia, M. Balbi, V. Procopio, B. Villaggio, A. Tarroni, M. Di Martino, V. Cappelli , M.T. Gandolfo, A. Valli, D. Verzola D; Kidney and splanchnic handling of interleukin-6 in humans. Cytokine. 2007 Jan;37(1):51-4.

G. Garibotto, D. Verzola, M. Vettore, Tessari P. The contribution of muscle, kidney and splanchnic tissues to leucine transamination in humans, Can J Physiol Pharmacol, 2017 Sep 11.

Jager KJ, Merkus MP, Huisman RM, Boeschoten EW, Dekker FW, Korevaar JC, et al. NECOSAD Study Group.Nutritional status over time in hemodialysis and peritoneal dialysis. J Am Soc Nephrol. 2001; 12:1272-9.

Lievense H, Kalantar-Zadeh K, Lukowsky LR, Molnar MZ, Duong U, Nissenson A, et al. Relationship of body size and initial dialysis modality on subsequent transplantation, mortality and weight gain of ESRD patients. Nephrol Dial Transplant 2012; May 2.

Garibotto G, Pastorino N, Dertenois L. Protein and amino acid metabolism in renal disease and in renal failure: in Kopple JD, Massry S (eds): Nutritional management of renal diseases. Baltimore, William & Wilkins, 2003.

Roberts JJ, Bier D, Schoeller D, Wolfe R, Matthews D, Munro HN,et al. Effects of intravenous glucose in whole body leucine dynamics, studied with 1-13-Leucine, in healthy young and elderly adults. J Gerontol 1984; 39:673 -81.

Castellino P, Luzi L, Giordano M, Defronzo RA. Effects of insulin and amino acids on glucose and leucine metabolism in CAPD patients. J Am Soc Nephrol 1999; 10:1050-8.

Garibotto G, Sofia A, Canepa A, Saffioti S, Sacco P, Sala M et al. Acute effects of peritoneal dialysis with dialysates containing dextrose or dextrose and amino acids on muscle protein turnover in patients with chronic renal failure. J Am Soc Nephrol 2001; 12:557-67.

Sofia A, Russo R, Saffioti S, Sacco P, Dertenois L, Pastorino N et al. Acute effects of peritoneal dialysis on muscle protein turnover. G Ital Nefrol 2002; 19: 37-43.

Lindeman RD. Overview: Renal physiology and pathophysiology of aging. Am J Kidney Dis 1990; 16:275–82.

Van Hoeck KJ, Rusthoven E, Vermeylen L, Vandesompel A, Marescau B, Lilien M, Schroder CH; Nutritional effects of increasing dialysis dose by adding an icodextrin daytime dwell to Nocturnal Intermittent Peritoneal Dialysis (NIPD) in children. Nephrol Dial Transplant. 2003 Jul;18(7):1383-7.

Garibotto G, Paoletti E, Fiorini F, Russo R, Robaudo C, Deferrari G, et al. Peripheral metabolism of branched-chain keto acids in patients with chronic renal failure. Miner Electrolyte Metab 1993; 19:25-31

Price SR, Reaich D, Marinovic AC, England BK, Bailey JL, Caban R et al. Mechanisms contributing to muscle-wasting in acute uremia: activation of amino acid catabolism. J Am Soc Nephrol 1998; 9:439-43

Chen Y, Sood S, McIntire K, Roth R, Rabkin R. Leucine-stimulated mTOR signaling is partly attenuated in skeletal muscle of chronically uremic rats. Am J Physiol Endocrinol Metab. 2011;301:E873-81

Oren A, Wu G, Anderson GH Marliss E, Khanna R, Petitt J, et al. Effective use of amino acid dialysate over four weeks in CAPD patients. Perit Dial Bull 1983; 3: 66-73.

Jones M, Hagen T, Boyle CA Vonesh E, Hamburger R, Charytan C, et al. Treatment of malnutrition with 1.1% amino acid peritoneal dialysis solution: results of a multicenter outpatient study. Am J Kidney Dis 1998; 32:781-9.

McCormick BB, Mujais S, Poirer F Page N, Lavoie S, et al. Metabolic effects of incremental doses of intraperitoneal amino acids on automated peritoneal dialysis. Perit Dial Int 2010; 30: 201-7.

Asola M, Virtanen K, Nagren K, Helin S, Taittonen M, Kastarinen H, et al. Amino-acid based peritoneal dialysis solution improves amino acid transport into skeletal muscle. Kidney Int Suppl 2008; 108:S131-36.

Tjiong HL, van den Berg JW, Wattimena JL, Rietveld T, van Dijk LJ, van der Wiel AM et al. Dialysate as food: combined amino acid and glucose dialysate improves preotein anabolism in renal failure patients on automated peritoneal dialysis. J Am Soc Nephrol 2005; 16:1486-93.

Boirie Y, Gachon P, Cordat N, Ritz P, Beaufrère B. Differential insulin sensitivities of glucose, amino acid, and albumin metabolism in elderly men and women. J Clin Endocrinol Metab 2001; 86:638-44.

Wang AY, Sea MM, Tang N, Lam CW, Chan IH, Lui SF et al. Energy intake and expenditure profile in chronic peritoneal dialysis patients complicated with circulatory congestion. Am J Clin Nutr 2009; 90:1179-84.

Dei Cas A, Muoio A, Zavaroni I. Chronic heart failure and cachexia: role of endocrine system. Minerva Cardioangiol 2011; 59:601-12.

Sharma R, Anker SD. Cytokines, apoptosis and cachexia: the potential for TNF antagonism. Int J Cardiol 2002; 85:161-71.

Elkina Y, von Haehling S, Anker SD, Springer J. The role of myostatin in muscle wasting: an overview. J Cachexia Sarcopenia Muscle. 2011; 2:143-51.

Sartori R, Milan G, Patron M, Mammucari C, Blaauw B, Abraham R et al. Smad2 and 3 transcription factors control muscle mass in adulthood. Am J Physiol Cell Physiol 2009; 296:C1248-57.

Wong KE, Szeto FL, Zhang W, Ye H, Kong J, Zhang Z, et al. Involvement of the vitamin D receptor in energy metabolism: regulation of uncoupling proteins. Am J Physiol Endocrinol Metab 2009; 296:E820-8.

Pilz S, Iodice S, Zittermann A, Grant WB, Gandini S. Vitamin D status and mortality risk in CKD: a meta-analysis of prospective studies. Am J Kidney Dis 2011;58:374-82.

Taskapan H, Baysal O, Karahan D, Durmus B, Altay Z, Ulutas O. Vitamin D and muscle strength, functional ability and balance in peritoneal dialysis patients with vitamin D deficiency. Clin Nephrol 2011; 76:110-6.

Mirchi, E. et Al. Association between 25-Hydroxyvitamin D level and inflammatory and nutritional factors in hemodialysis and peritoneal dialysis patients in Qom, Iran, Int Jour of Kidney Diseases, 2016; 10:205-12

Kandula P, Dobre M, Schold JD, Schreiber MJ, Mehrotra JR, Navaneethan SD. Vitamin D Supplementation in Chronic Kidney Disease: A Systematic Review and Meta-Analysis of Observational Studies and Randomized Controlled Trials. Clin J Am Soc Nephrol. 2011; 6:50-62.

Kendrick J, Andrews E, You , Moreau K, Nowak KL, Farmer-Bailey H, Seals DR, Chonchol M; Cholecalciferol, Calcitriol, and Vascular Function in CKD: A Randomized, Double-Blind Trial, Clin J Am Soc Nephrol. 2017 Sep 7;12(9):1438-1446.

Zhang L, Rajan V, Lin E, Hu Z, Han HQ, Zhou X et al. Pharmacological inhibition of myostatin suppresses systemic inflammation and muscle atrophy in mice with chronic kidney disease. FASEB J 2011; 25:1653-63.

Garcia LA, King KK; Ferrini MG, Norris KC, Artaza JN (2011) 1,25 (OH)2 vitamin D3 stimulates myogenic differentiation by inhibiting cell proliferation and modulating the expression of promyogenic growth factors and myostatin in C2C12 skeletal muscle cells. Endocrinology 152: 2976-2986

Taskapan H, Baysal O, Karahan D, Durmus B, Altay Z, Ulutas O. Vitamin D and muscle strenght, functional ability and balance in peritoneal dialysis patients with vitamin D deficiency; Clin Nephrol. 2011 Aug;76(2):110-6

Girgis CM, Cha KM, Houweling PJ, Rao R, Mokbel N, Lin M, Clifton-Bligh RJ, Gunton JE (2015) Vitamin D receptor ablation and vitamin D deficiency result in reduced grip strength, altered muscle fibers, and increased myostatin in mice. Calcif Tissue Int 97:602-610

Satirapoj B, et al. Nutritional status among peritoneal dialysis patients after oral supplement with ONCE dialyze formula. International Journal of Nephrology and Renovascular disease. 2017:10 145-151

Cheng LT, Tang W, Wang T, Strong association between volume status in peritoneal dialysis patients. Am J Kidney Dis. 2005;45(5):891-902

Aguilera A, Codoceo R, Selgas RR, Selgas R et al. Anorexigenic (TNF-alpha, cholecystokinin) and orexigen (neuropeptide Y) plasma levels in peritoneal dialysis (PD) patients: Their relationship with nutitional parameters. Nephrol Dial Transplant. Jun 1998; 13(6):1476-1483.

Fantino M, Wieteska L. Evidence for a direct central anorectic effect of tumor-necrosis-factor-alpha in the rat. Physiology and Behavior, 1993 Mar; 53(3): 477-483

Kirchgessner TG, Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Tumor necrosis factor alpha contributes to obesity-related hyperleptinemia by regulating leptin release from adipocytes. The Journal of Clinical Investigation, 1997 Dec 1;100 (11); 2777-2782

Mitch WE Malnutrition: A frequent misdiagnosis for hemodialysis patients. J Clin Invest. 2002; 110(4):437-439

Mitch WE, Goldberg Al, Mechanism of muscle wasting. The role of ubiquitin-proteasome pathway. N Engl J Med 1996; 335(25): 1897-1905.

Chung SH, Heimburger O, Stenvinkel P, Wang T, Lindholm B. Influence of peritoneal transport rate, inflammation and fluid removal on nutritional status and clinical outcome in prevalent peritoneal dialysis patients. Perit. Dil. Int. 2003;23(2): 174-183

Wei Lin, Yung-Chih Chen, Mai-Szu Wu, Heng-Jung Hsu, Chiao-Yin Sun, Ying-Kuang Lin & I-Wen Wu, Icodextrin dialysate improves nutritional and inflammatory profiles in peritoneal dialysis patients, Renal Failure, 2009, 31:2, 98-105

Opatrna S, Racek J, Stehlik P et al. Effect of a dialysis solution with icodextrin on ultrafiltration and selected metabolic parameters in patients treated with peritoneal dialysis. Cas. Lek. Cesk. 200;141(9) 281-285

De Moraes TP, Andreoli MC, Canziani ME, da Silva DR, Caramori JC, Ponce D, Cassi HV, de Andrade Bastos K, Rio DR, Pinto SW, Filho SR, de Campos LG, Olandoski M, Divino-Filho JC, Pecoits-Filho R, Icodextrin reduces insulin resistance in non-diabetic patients undergoing automated peritoneal dialysis: results of a randomized controlled trial (STARCH), Nephrol Dial Transplant 2015, 30: 1905-1911

Lee SW, Park GH, Song JH, Hong KC, Kim MJ Insulin resistance and muscle wasting in non diabetic end-stage renal disease patients. Nephrol Dial Transplant. 2007, 22, 2554-2562

Cupisti A, D’Alessandro C, Finato V, Del Corso C, Catania B, Caselli GM, Egidi MF, Assessment of physical activity, capacity and nutritional status in elderly peritoneal dialysis patients, BMC Nephrology 18:180, 2017, May 30.

Cobo G, Gallar P, Gama Axelsson T, Di Gioia C, Qureshi AR, Camacho R et al, Clinical determinants of reduced physical activity in hemodialysis and peritoneal dialysis patients. J Nephrol. 2015; 28-503-510

Tennankore KK, Bergman JM. Nutrition and the kidney: recommendations for peritoneal dialysis Adv Chronic Kidney Dis. 2013;20:190-201

Manfredini F, Mallamaci F, D’Arrigo G, Baggetta R et al, Exercise in patients on dialysis: A Multicenter, Randomized Clinical Trial, J Am Soc Nephrol 28 1259-1268, 2017

Johansen KL, Chertow GM, Jin C, Kutner NG: Significance of frailty among dialysis patients. J Am Soc Nephrol 18:2960-2967,2007




DOI: http://dx.doi.org/10.18103/imr.v3i12.613

Refbacks

  • There are currently no refbacks.
Copyright 2016. All rights reserved.