Muscle-bone axis in children with chronic kidney disease: current knowledge and future perspectives.
Chronic kidney disease
Mineral and bone disorder
Muscle wasting
Muscle-bone crosstalk
Myokines
Osteokines
Journal
Pediatric nephrology (Berlin, Germany)
ISSN: 1432-198X
Titre abrégé: Pediatr Nephrol
Pays: Germany
ID NLM: 8708728
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
28
09
2020
accepted:
07
01
2021
revised:
06
12
2020
pubmed:
4
2
2021
medline:
5
2
2022
entrez:
3
2
2021
Statut:
ppublish
Résumé
Bone and muscle tissue are developed hand-in-hand during childhood and adolescence and interact through mechanical loads and biochemical pathways forming the musculoskeletal system. Chronic kidney disease (CKD) is widely considered as both a bone and muscle-weakening disease, eventually leading to frailty phenotype, with detrimental effects on overall morbidity. CKD also interferes in the biomechanical communication between two tissues. Pathogenetic mechanisms including systemic inflammation, anorexia, physical inactivity, vitamin D deficiency and secondary hyperparathyroidism, metabolic acidosis, impaired growth hormone/insulin growth factor 1 axis, insulin resistance, and activation of renin-angiotensin system are incriminated for longitudinal uncoordinated loss of bone mineral content, bone strength, muscle mass, and muscle strength, leading to mechanical impairment of the functional muscle-bone unit. At the same time, CKD may also interfere in the biochemical crosstalk between the two organs, through inhibiting or stimulating the expression of certain osteokines and myokines. This review focuses on presenting current knowledge, according to in vitro, in vivo, and clinical studies, concerning the pathogenetic pathways involved in the muscle-bone axis, and suggests approaches aimed at preventing bone loss and muscle wasting in the pediatric population. Novel therapeutic targets for preserving musculoskeletal health in the context of CKD are also discussed.
Identifiants
pubmed: 33534001
doi: 10.1007/s00467-021-04936-w
pii: 10.1007/s00467-021-04936-w
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
3813-3827Informations de copyright
© 2021. IPNA.
Références
Brotto M, Bonewald L (2005) Bone and muscle: interactions beyond mechanical. Bone 80:109–114
Maggioli C, Stagi S (2017) Bone modeling, remodeling, and skeletal health in children and adolescents: mineral accrual, assessment and treatment. Ann Pediatr Endocrinol Metab 22:1–5
pubmed: 5401817
pmcid: 5401817
Sioen I, Lust E, De Henauw S, Moreno LA, Jiménez-Pavón D (2016) Associations between body composition and bone health in children and adolescents: a systematic review. Calcif Tissue Int 99:557–577
pubmed: 27484027
pmcid: 27484027
Kristinsson JO, Valdimarsson O, Steingrimsdottir L, Sigurdsson G (1994) Relation between calcium intake, grip strength and bone mineral density in the forearms of girls aged 13 and 15. J Intern Med 236:385–390
pubmed: 7931041
pmcid: 7931041
Chan DC, Lee WT, Lo DH, Leung JC, Kwok AW, Leung PC (2008) Relationship between grip strength and bone mineral density in healthy Hong Kong adolescents. Osteoporos Int 19:1485–1495
pubmed: 18373053
pmcid: 18373053
Rauch F, Bailey DA, Baxter-Jones A, Mirwald R, Faulkner R (2004) The 'muscle-bone unit' during the pubertal growth spurt. Bone 34:771–775
pubmed: 15121007
pmcid: 15121007
Cianferotti L, Brandi ML (2014) Muscle-bone interactions: basic and clinical aspects. Endocrine 45:165–177
pubmed: 23990248
pmcid: 23990248
Frost HM, Schoenau E (2000) The "muscle-bone unit" in children and adolescents: a 2000 overview. J Pediatr Endocrinol Metab 13:571–590
pubmed: 10905381
pmcid: 10905381
Schoenau E (2005) From mechanostat theory to development of the "functional muscle-bone-unit". J Musculoskelet Neuronal Interact 5:232–238
pubmed: 16172514
pmcid: 16172514
Kaji H (2014) Interaction between muscle and bone. J Bone Metab 21:29–40
pubmed: 3970293
pmcid: 3970293
Bakkaloglu SA, Wesseling-Perry K, Pereira RC, Gales B, Wang HJ, Elashoff RM, Salusky IB (2010) Value of the new bone classification system in pediatric renal osteodystrophy. Clin J Am Soc Nephrol 5:1860–1866
pubmed: 2974387
pmcid: 2974387
Wesseling-Perry K, Pereira RC, Tseng CH, Elashoff R, Zaritsky JJ, Yadin O, Sahney S, Gales B, Jüppner H, Salusky IB (2012) Early skeletal and biochemical alterations in pediatric chronic kidney disease. Clin J Am Soc Nephrol 7:146–152
pubmed: 22052943
pmcid: 22052943
Denburg MR, Tsampalieros AK, de Boer IH, Shults J, Kalkwarf HJ, Zemel BS, Foerster D, Stokes D, Leonard MB (2013) Mineral metabolism and cortical volumetric bone mineral density in childhood chronic kidney disease. J Clin Endocrinol Metab 98:1930–1938
pubmed: 23547048
pmcid: 23547048
Wang XH, Mitch WE (2014) Mechanisms of muscle wasting in chronic kidney disease. Nat Rev Nephrol 10:504–516
pubmed: 24981816
pmcid: 24981816
Foster BJ, Kalkwarf HJ, Shults J, Zemel BS, Wetzsteon RJ, Thayu M, Foerster DL, Leonard MB (2011) Association of chronic kidney disease with muscle deficits in children. J Am Soc Nephrol 22:377–386
pubmed: 21115614
pmcid: 21115614
Hogan J, Schneider MF, Pai R, Denburg MR, Kogon A, Brooks ER, Kaskel FJ, Reidy KJ, Saland JM, Warady BA, Furth SL, Patzer RE, Greenbaum LA (2020) Grip strength in children with chronic kidney disease. Pediatr Nephrol 35:891–899
pubmed: 31932960
pmcid: 31932960
Kirk B, Al Saedi A, Duque G (2019) Osteosarcopenia: a case of geroscience. Aging Med (Milton) 2:147–156
Sgambat K, Matheson MB, Hooper SR, Warady B, Furth S, Moudgil A (2019) Prevalence and outcomes of fragility: a frailty-inflammation phenotype in children with chronic kidney disease. Pediatr Nephrol 34:2563–2569
pubmed: 31375914
pmcid: 31375914
Li G, Thabane L, Papaioannou A, Ioannidis G, Levine MA, Adachi JD (2017) An overview of osteoporosis and frailty in the elderly. BMC Musculoskelet Disord 18:46
pubmed: 28125982
pmcid: 28125982
Karava V, Dotis J, Christoforidis A, Liakopoulos V, Kondou A, Tsigaras G, Tsioni K, Kollios K, Printza N (2021) Association between insulin growth factor-1, bone mineral density and frailty phenotype in children with chronic kidney disease. Pediatr Nephrol. https://doi.org/10.1007/s00467-021-04918-y
Cheung WW, Paik KH, Mak RH (2010) Inflammation and cachexia in chronic kidney disease. Pediatr Nephrol 25:711–724
Hardy R, Cooper MS (2009) Bone loss in inflammatory disorders. J Endocrinol 201:309–320
Mazzaferro S, De Martini N, Rotondi S, Tartaglione L, Ureña-Torres P, Bover J, Pasquali M, ERA-EDTA Working Group on CKD-MBD (2020) Bone, inflammation and chronic kidney disease. Clin Chim Acta 506:236–240
Barreto FC, Barreto DV, Moyses RM, Neves CL, Jorgetti V, Draibe SA, Canziani ME, Carvalho AB (2006) Osteoporosis in hemodialysis patients revisited by bone histomorphometry: a new insight into an old problem. Kidney Int 69:1852–1857
Ferreira A, Saraiva M, Behets G, Macedo A, Galvão M, D'Haese P, Drüeke TB (2009) Evaluation of bone remodeling in hemodialysis patients: serum biochemistry, circulating cytokines and bone histomorphometry. J Nephrol 22:783–793
Evenepoel P, Opdebeeck B, David K, D’Haese PC (2019) Bone-vascular axis in chronic kidney disease. Adv Chronic Kidney Dis 26:472–483
Avesani CM, Carrero JJ, Axelsson J, Qureshi AR, Lindholm B, Stenvinkel P (2006) Inflammation and wasting in chronic kidney disease: partners in crime. Kidney Int 70:S8–S13
Mak RH, Cheung W, Cone RD, Marks DL (2005) Orexigenic and anorexigenic mechanisms in the control of nutrition in chronic kidney disease. Pediatr Nephrol 20:427–431
Cheung WW, Zhan JY, Paik KH, Mak RH (2011) The impact of inflammation on bone mass in children. Pediatr Nephrol 26:1937–1946
pubmed: 3178021
pmcid: 3178021
Karsenty G (2006) Convergence between bone and energy homeostases: leptin regulation of bone mass. Cell Metab 4:341–348
pubmed: 17084709
pmcid: 17084709
Oner-Iyidogan Y, Gurdol F, Kocak H, Oner P, Cetinalp-Demircan P, Caliskan Y, Kocak T, Turkmen A (2011) Appetite-regulating hormones in chronic kidney disease patients. J Ren Nutr 21:316–321
pubmed: 21193324
pmcid: 21193324
Daschner M, Tönshoff B, Blum WF, Englaro P, Wingen AM, Schaefer F, Wühl E, Rascher W, Mehls O (1998) Inappropriate elevation of serum leptin levels in children with chronic renal failure. European Study Group for Nutritional Treatment of Chronic Renal Failure in Childhood. J Am Soc Nephrol 9:1074–1079
pubmed: 9621291
pmcid: 9621291
Monzani A, Perrone M, Prodam F, Moia S, Genoni G, Testa S, Paglialonga F, Rapa A, Bona G, Montini G, Edefonti A (2018) Unacylated ghrelin and obestatin: promising biomarkers of protein energy wasting in children with chronic kidney disease. Pediatr Nephrol 33:661–672
pubmed: 29150712
pmcid: 29150712
Zhang J, Wang N (2014) Leptin in chronic kidney disease: a link between hematopoiesis, bone metabolism, and nutrition. Int Urol Nephrol 46:1169–1174
pubmed: 24338492
pmcid: 24338492
Molina P, Carrero JJ, Bover J, Chauveau P, Mazzaferro S, Torres PU (2017) Vitamin D, a modulator of musculoskeletal health in chronic kidney disease. J Cachexia Sarcopenia Muscle 8:686–701
pubmed: 28675610
pmcid: 28675610
Taskapan H, Baysal O, Karahan D, Durmus B, Altay Z, 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
pubmed: 21762642
pmcid: 21762642
Gordon PL, Doyle JW, Johansen KL (2012) Association of 1,25-dihydroxyvitamin D levels with physical performance and thigh muscle cross-sectional area in chronic kidney disease stage 3 and 4. J Ren Nutr 22:423–433
pubmed: 22227183
pmcid: 22227183
Garber AJ (1983) Effects of parathyroid hormone on skeletal muscle protein and amino acid metabolism in the rat. J Clin Invest 71:1806–1821
pubmed: 6306055
pmcid: 6306055
Baczynski R, Massry SG, Magott M, el-Belbessi S, Kohan R, Brautbar N (1985) Effect of parathyroid hormone on energy metabolism of skeletal muscle. Kidney Int 28:722–727
pubmed: 2935672
pmcid: 2935672
Kir S, Komaba H, Garcia AP, Economopoulos KP, Liu W, Lanske B, Hodin RA, Spiegelman BM (2016) PTH/PTHrP receptor mediates cachexia in models of kidney failure and cancer. Cell Metab 23:315–323
pubmed: 26669699
pmcid: 26669699
Kraut JA (1995) The role of metabolic acidosis in the pathogenesis of renal osteodystrophy. Adv Ren Replace Ther 2:40–51
pubmed: 7614335
pmcid: 7614335
Lu KC, Lin SH, Yu FC, Chyr SH, Shieh SD (1995) Influence of metabolic acidosis on serum 1,25(OH)2D3 levels in chronic renal failure. Miner Electrolyte Metab 21:398–402
pubmed: 8592483
pmcid: 8592483
Mehrotra R, Kopple JD, Wolfson M (2003) Metabolic acidosis in maintenance dialysis patients: clinical considerations. Kidney Int Suppl 88:S13–S25
Ordóñez FA, Santos F, Martínez V, García E, Fernández P, Rodríguez J, Fernández M, Alvarez J, Ferrando S (2000) Resistance to growth hormone and insulin-like growth factor-I in acidotic rats. Pediatr Nephrol 14:720–725
pubmed: 10955915
pmcid: 10955915
Coen G, Manni M, Addari O, Ballanti P, Pasquali M, Chicca S, Mazzaferro S, Napoletano I, Sardella D, Bonucci E (1995) Metabolic acidosis and osteodystrophic bone disease in predialysis chronic renal failure: effect of calcitriol treatment. Miner Electrolyte Metab 21:375–382
pubmed: 8592480
pmcid: 8592480
Coen G, Mazzaferro S, Ballanti P, Sardella D, Chicca S, Manni M, Bonucci E, Taggi F (1996) Renal bone disease in 76 patients with varying degrees of predialysis chronic renal failure: a cross-sectional study. Nephrol Dial Transplant 11:813–819
pubmed: 8671900
pmcid: 8671900
Domrongkitchaiporn S, Pongsakul C, Stitchantrakul W, Sirikulchayanonta V, Ongphiphadhanakul B, Radinahamed P, Karnsombut P, Kunkitti N, Ruang-raksa C, Rajatanavin R (2001) Bone mineral density and histology in distal renal tubular acidosis. Kidney Int 59:1086–1093
pubmed: 11231364
pmcid: 11231364
Bailey JL, Wang X, England BK, Price SR, Ding X, Mitch WE (1996) The acidosis of chronic renal failure activates muscle proteolysis in rats by augmenting transcription of genes encoding proteins of the ATP-dependent ubiquitin-proteasome pathway. J Clin Invest 97:1447–1453
pubmed: 8617877
pmcid: 8617877
Lim VS, Yarasheski KE, Flanigan MJ (1998) The effect of uraemia, acidosis, and dialysis treatment on protein metabolism: a longitudinal leucine kinetic study. Nephrol Dial Transplant 13:1723–1730
pubmed: 9681719
pmcid: 9681719
Boirie Y, Broyer M, Gagnadoux MF, Niaudet P, Bresson JL (2000) Alterations of protein metabolism by metabolic acidosis in children with chronic renal failure. Kidney Int 58:236–241
Bikle DD, Tahimic C, Chang W, Wang Y, Philippou A, Barton ER (2015) Role of IGF-I signaling in muscle bone interactions. Bone 80:79–88
pubmed: 4600536
pmcid: 4600536
Jia T, Gama Axelsson T, Heimbürger O, Bárány P, Lindholm B, Stenvinkel P, Qureshi AR (2014) IGF-1 and survival in ESRD. Clin J Am Soc Nephrol 9:120–127
Park SH, Jia T, Qureshi AR, Bárány P, Heimbürger O, Larsson TE, Axelsson J, Stenvinkel P, Lindholm B (2013) Determinants and survival implications of low bone mineral density in end-stage renal disease patients. J Nephrol 26:485–494
Qureshi AR, Alvestrand A, Danielsson A, Divino-Filho JC, Gutierrez A, Lindholm B, Bergström J (1998) Factors predicting malnutrition in hemodialysis patients: a cross- sectional study. Kidney Int 53:773–782
Ulinski T, Mohan S, Kiepe D, Blum WF, Wingen AM, Mehls O, Tönshoff B (2000) Serum insulin-like growth factor binding protein (IGFBP)-4 and IGFBP-5 in children with chronic renal failure: relationship to growth and glomerular filtration rate. Pediatr Nephrol 14:589–597
Spoto B, Pisano A, Zoccali C (2016) Insulin resistance in chronic kidney disease: a systematic review. Am J Physiol Ren Physiol 311:F1087–F1108
Clemmons DR (2004) The relative roles of growth hormone and IGF-1 in controlling insulin sensitivity. J Clin Invest 113:25–27
pubmed: 300772
pmcid: 300772
Conte C, Epstein S, Napoli N (2018) Insulin resistance and bone: a biological partnership. Acta Diabetol 55:305–314
pubmed: 29333578
pmcid: 29333578
Thrailkill KM, Lumpkin CK, Bunn RC, Kemp SF, Fowlkes JL (2005) Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab 289:E735–E745
Dimitriadis G, Mitron P, Lambadiari V, Maratou E, Raptis SA (2011) Insulin effects in muscle and adipose tissue. Diabetes Res Clin Pract Suppl 1:S52–S59
Wang X, Hu Z, Hu J, Du J, Mitch WE (2006) Insulin resistance accelerates muscle protein degradation: activation of the ubiquitin-proteasome pathway by defects in muscle cell signaling. Endocrinology 147:4160–4168
pubmed: 16777975
pmcid: 16777975
Siew ED, Pupim LB, Majchrzak KM, Shintani A, Flakoll PJ, Ikizler TA (2007) Insulin resistance is associated with skeletal muscle protein breakdown in non-diabetic chronic hemodialysis patients. Kidney Int 71:146–152
pubmed: 17063174
pmcid: 17063174
Karava V, Dotis J, Kondou A, Christoforidis A, Liakopoulos V, Tsioni K, Kollios K, Papachristou F, Printza N (2020) Association between relative fat mass, uric acid, and insulin resistance in children with chronic kidney disease. Pediatr Nephrol. https://doi.org/10.1007/s00467-020-04716-y
Cabello-Verrugio C, Morales MG, Rivera JC, Cabrera D, Simon F (2015) Renin-angiotensin system: an old player with novel functions in skeletal muscle. Med Res Rev 35:437–463
pubmed: 25764065
pmcid: 25764065
Powers SK, Morton AB, Hyatt H, Hinkley MJ (2018) The renin-angiotensin system and skeletal muscle. Exerc Sport Sci Rev 46:205–214
pubmed: 30001274
pmcid: 30001274
Sukhanov S, Semprun-Prieto L, Yoshida T, Michael Tabony A, Higashi Y, Galvez S, Delafontaine P (2011) Angiotensin II, oxidative stress and skeletal muscle wasting. Am J Med Sci 342:143–147
pubmed: 3217236
pmcid: 3217236
Tamargo J, Caballero R, Delpón E (2015) The renin–angiotensin system and bone. Clinic Rev Bone Miner Metab 13:125–148
Shimizu H, Nakagami H, Osako MK, Hanayama R, Kunugiza Y, Kizawa T, Tomita T, Yoshikawa H, Ogihara T, Morishita R (2008) Angiotensin II accelerates osteoporosis by activating osteoclasts. FASEB J 22:2465–24751
Schoenau E, Neu CM, Beck B, Manz F, Rauch F (2002) Bone mineral content per muscle cross-sectional area as an index of the functional muscle-bone unit. J Bone Miner Res 17:1095–1101
Ruth EM, Weber LT, Schoenau E, Wunsch R, Seibel MJ, Feneberg R, Mehls O, Tönshoff B (2004) Analysis of the functional muscle-bone unit of the forearm in pediatric renal transplant recipients. Kidney Int 66:1694–1706
Tsampalieros A, Kalkwarf HJ, Wetzsteon RJ, Shults J, Zemel BS, Foster BJ, Foerster DL, Leonard MB (2013) Changes in bone structure and the muscle-bone unit in children with chronic kidney disease. Kidney Int 83:495–502
Lee DY, Wetzsteon RJ, Zemel BS, Shults J, Organ JM, Foster BJ, Herskovitz RM, Foerster DL, Leonard MB (2015) Muscle torque relative to cross-sectional area and the functional muscle-bone unit in children and adolescents with chronic disease. J Bone Miner Res 30:563–571
Delgado-Calle J, Sato AY, Bellido T (2017) Role and mechanism of action of sclerostin in bone. Bone 96:29–37
Huang J, Romero-Suarez S, Lara N, Mo C, Kaja S, Brotto L, Dallas SL, Johnson ML, Jähn K, Bonewald LF, Brotto M (2017) Crosstalk between MLO-Y4 osteocytes and C2C12 muscle cells is mediated by the Wnt/β-catenin pathway. JBMR Plus 1:86–100
pubmed: 5667655
pmcid: 5667655
Dufresne SS, Dumont NA, Boulanger-Piette A, Fajardo VA, Gamu D, Kake-Guena SA, David RO, Bouchard P, Lavergne É, Penninger JM, Pape PC, Tupling AR, Frenette J (2016) Muscle RANK is a key regulator of Ca2+ storage, SERCA activity, and function of fast-twitch skeletal muscles. Am J Phys Cell Phys 310:C663–C672
Dufresne SS, Boulanger-Piette A, Bossé S, Argaw A, Hamoudi D, Marcadet L, Gamu D, Fajardo VA, Yagita H, Penninger JM, Russell Tupling A, Frenette J (2018) Genetic deletion of muscle RANK or selective inhibition of RANKL is not as effective as full-length OPG-fc in mitigating muscular dystrophy. Acta Neuropathol Commun 6:31
pubmed: 5922009
pmcid: 5922009
Armamento-Villareal R, Sadler C, Napoli N, Shah K, Chode S, Sinacore DR, Qualls C, Villareal DT (2012) Weight loss in obese older adults increases serum sclerostin and impairs hip geometry but both are prevented by exercise training. J Bone Miner Res 27:1215–1221
Robling AG, Niziolek PJ, Baldridge LA, Condon KW, Allen MR, Alam I, Mantila SM, Gluhak-Heinrich J, Bellido TM, Harris SE, Turner CH (2008) Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem 283:5866–5875
Pelletier S, Dubourg L, Carlier MC, Hadj-Aissa A, Fouque D (2013) The relation between renal function and serum sclerostin in adult patients with CKD. Clin J Am Soc Nephrol 8:819–823
pubmed: 23430206
pmcid: 23430206
Lerch C, Shroff R, Wan M, Rees L, Aitkenhead H, Kaplan Bulut I, Thurn D, Karabay Bayazit A, Niemirska A, Canpolat N, Duzova A, Azukaitis K, Yilmaz E, Yalcinkaya F, Harambat J, Kiyak A, Alpay H, Habbig S, Zaloszyc A, Soylemezoglu O, Candan C, Rosales A, Melk A, Querfeld U, Leifheit-Nestler M, Sander A, Schaefer F, Haffner D, 4C study consortium, ESPN CKD-MBD working group (2018) Effects of nutritional vitamin D supplementation on markers of bone and mineral metabolism in children with chronic kidney disease. Nephrol Dial Transplant 33:2208–2217
pubmed: 29481636
pmcid: 29481636
Doyon A, Fischer DC, Bayazit AK, Canpolat N, Duzova A, Sözeri B, Bacchetta J, Balat A, Büscher A, Candan C, Cakar N, Donmez O, Dusek J, Heckel M, Klaus G, Mir S, Özcelik G, Sever L, Shroff R, Vidal E, Wühl E, Gondan M, Melk A, Querfeld U, Haffner D, Schaefer F, 4C Study Consortium (2015) Markers of bone metabolism are affected by renal function and growth hormone therapy in children with chronic kidney disease. PLoS One 10:e0113482
pubmed: 25659076
pmcid: 25659076
de Oliveira RB, Graciolli FG, dos Reis LM, Cancela AL, Cuppari L, Canziani ME, Carvalho AB, Jorgetti V, Moysés RM (2013) Disturbances of Wnt/β-catenin pathway and energy metabolism in early CKD: effect of phosphate binders. Nephrol Dial Transplant 28:2510–2517
pubmed: 23975746
pmcid: 23975746
Cejka D, Herberth J, Branscum AJ, Fardo DW, Monier-Faugere MC, Diarra D, Haas M, Malluche HH (2011) Sclerostin and dickkopf-1 in renal osteodystrophy. Clin J Am Soc Nephrol 6:877–882
pubmed: 21164019
pmcid: 21164019
Ishimura E, Okuno S, Ichii M, Norimine K, Yamakawa T, Shoji S, Nishizawa Y, Inaba M (2014) Relationship between serum sclerostin, bone metabolism markers, and bone mineral density in maintenance hemodialysis patients. J Clin Endocrinol Metab 99:4315–4320
pubmed: 25093620
pmcid: 25093620
Medeiros MC, Rocha N, Bandeira E, Dantas I, Chaves C, Oliveira M, Bandeira F (2020) Serum sclerostin, body composition, and sarcopenia in hemodialysis patients with diabetes. Int J Nephrol 2020:4596920
pubmed: 32095286
pmcid: 32095286
Gomes TS, Aoike DT, Baria F, Graciolli FG, Moyses RMA, Cuppari L (2017) Effect of aerobic exercise on markers of bone metabolism of overweight and obese patients with chronic kidney disease. J Ren Nutr 27:364–371
pubmed: 28606422
pmcid: 28606422
Montañez-Barragán A, Gómez-Barrera I, Sanchez-Niño MD, Ucero AC, González-Espinoza L, Ortiz A (2014) Osteoprotegerin and kidney disease. J Nephrol 27:607–617
pubmed: 24756971
pmcid: 24756971
Hamoudi D, Bouredji Z, Marcadet L, Yagita H, Landry LB, Argaw A, Frenette J (2020) Muscle weakness and selective muscle atrophy in osteoprotegerin-deficient mice. Hum Mol Genet 29:483–494
pubmed: 31943048
pmcid: 31943048
Shroff RC, Shah V, Hiorns MP, Schoppet M, Hofbauer LC, Hawa G, Schurgers LJ, Singhal A, Merryweather I, Brogan P, Shanahan C, Deanfield J, Rees L (2008) The circulating calcification inhibitors, fetuin-A and osteoprotegerin, but not matrix Gla protein, are associated with vascular stiffness and calcification in children on dialysis. Nephrol Dial Transplant 23:3263–3271
pubmed: 18463323
pmcid: 18463323
Siomou E, Challa A, Printza N, Giapros V, Petropoulou F, Mitsioni A, Papachristou F, Stefanidis CJ (2011) Serum osteoprotegerin, RANKL and fibroblast growth factor-23 in children with chronic kidney disease. Pediatr Nephrol 26:1105–1114
Kim CS, Bae EH, Ma SK, Han SH, Choi KH, Lee J, Chae DW, Oh KH, Ahn C, Kim SW, Representatives of the KNOW-CKD Investigator Group (2016) Association of serum osteoprotegerin levels with bone loss in chronic kidney disease: insights from the KNOW-CKD study. PLoS One 11:e0166792
pubmed: 5113973
pmcid: 5113973
Jiang JQ, Lin S, Xu PC, Zheng ZF, Jia JY (2011) Serum osteoprotegerin measurement for early diagnosis of chronic kidney disease-mineral and bone disorder. Nephrology (Carlton) 16:588–594
Crisafulli A, Romeo A, Floccari F, Aloisi E, Atteritano M, Cincotta M, Aloisi C, Pizzolio M, Ruello A, Artemisia A, Valenti A, Frisina N, Teti D, Buemi M (2005) Osteoprotegerin and bone mineral density in hemodiafiltration patients. Ren Fail 27:531–539
Ford ML, Smith ER, Tomlinson LA, Chatterjee PK, Rajkumar C, Holt SG (2012) FGF-23 and osteoprotegerin are independently associated with myocardial damage in chronic kidney disease stages 3 and 4. Another link between chronic kidney disease,mineral bone disorder and the heart. Nephrol Dial Transplant 27:727–733
Kaji H (2016) Effects of myokines on bone. Bonekey Rep 5:826
pubmed: 4954587
pmcid: 4954587
Colaianni G, Faienza MF, Sanesi L, Brunetti G, Pignataro P, Lippo L, Bortolotti S, Storlino G, Piacente L, D'Amato G, Colucci S, Grano M (2019) Irisin serum levels are positively correlated with bone mineral status in a population of healthy children. Pediatr Res 85:484–488
Reza MM, Subramaniyam N, Sim CM, Ge X, Sathiakumar D, McFarlane C, Sharma M, Kambadur R (2017) Irisin is a pro-myogenic factor that induces skeletal muscle hypertrophy and rescues denervation-induced atrophy. Nat Commun 8:1104
pubmed: 5653663
pmcid: 5653663
Wen MS, Wang CY, Lin SL, Hung KC (2013) Decrease in irisin in patients with chronic kidney disease. PLoS One 8:e64025
pubmed: 3646802
pmcid: 3646802
Rodríguez-Carmona A, Pérez Fontán M, Sangiao Alvarellos S, García Falcón T, Pena Bello ML, López Muñiz A, Cordido F (2016) Serum levels of the adipomyokine irisin in patients with chronic kidney disease. Nefrologia 36:496–502
Moraes C, Leal VO, Marinho SM, Barroso SG, Rocha GS, Boaventura GT, Mafra D (2013) Resistance exercise training does not affect plasma irisin levels of hemodialysis patients. Horm Metab Res 45:900–904
Tan Z, Ye Z, Zhang J, Chen Y, Cheng C, Wang C, Liu X, Lou T, Peng H (2017) Serum irisin levels correlated to peritoneal dialysis adequacy in nondiabetic peritoneal dialysis patients. PLoS One 12:e0176137
pubmed: 5406024
pmcid: 5406024
Zhou SJ, Han QF, Zhang AH, Tang W, Sun LH (2017) Irisin and volume overload are associated with protein energy wasting in peritoneal dialysis patients. Kidney Blood Press Res 42:1216–1224
Lee MJ, Lee SA, Nam BY, Park S, Lee SH, Ryu HJ, Kwon YE, Kim YL, Park KS, Oh HJ, Park JT, Han SH, Ryu DR, Kang SW, Yoo TH (2015) Irisin, a novel myokine is an independent predictor for sarcopenia and carotid atherosclerosis in dialysis patients. Atherosclerosis 242:476–482
He WY, Wu F, Pang XX, Chen GJ, LT A, He L, Wang S, Tang CS, Zhang AH (2016) Irisin is associated with urotensin II and protein energy wasting in hemodialysis patients. Kidney Blood Press Res 41:78–85
Ebert T, Focke D, Petroff D, Wurst U, Richter J, Bachmann A, Lössner U, Kralisch S, Kratzsch J, Beige J, Bast I, Anders M, Blüher M, Stumvoll M, Fasshauer M (2014) Serum levels of the myokine irisin in relation to metabolic and renal function. Eur J Endocrinol 170:501–506
He L, He WY, LT A, Yang WL, Zhang AH (2018) Lower serum Irisin levels are associated with increased vascular calcification in hemodialysis patients. Kidney Blood Press Res 43:287–295
Palermo A, Sanesi L, Colaianni G, Tabacco G, Naciu AM, Cesareo R, Pedone C, Lelli D, Brunetti G, Mori G, Colucci S, Manfrini S, Napoli N, Grano M (2019) A novel interplay between irisin and PTH: from basic studies to clinical evidence in hyperparathyroidism. J Clin Endocrinol Metab 104:3088–3096
Elkina Y, von Haehling S, Anker SD, Springer J (2011) The role of myostatin in muscle wasting: an overview. J Cachexia Sarcopenia Muscle 2:143–151
pubmed: 3177043
pmcid: 3177043
Retamales A, Zuloaga R, Valenzuela CA, Gallardo-Escarate C, Molina A, Valdés JA (2015) Insulin-like growth factor-1 suppresses the myostatin signaling pathway during myogenic differentiation. Biochem Biophys Res Commun 464:596–602
Williams NG, Interlichia JP, Jackson MF, Hwang D, Cohen P, Rodgers BD (2011) Endocrine actions of myostatin: systemic regulation of the IGF and IGF binding protein axis. Endocrinology 152:172–180
Hennebry A, Oldham J, Shavlakadze T, Grounds MD, Sheard P, Fiorotto ML, Falconer S, Smith HK, Berry C, Jeanplong F, Bracegirdle J, Matthews K, Nicholas G, Senna-Salerno M, Watson T, McMahon CD (2017) IGF1 stimulates greater muscle hypertrophy in the absence of myostatin in male mice. J Endocrinol 234:187–200
Yano S, Nagai A, Isomura M, Yamasaki M, Kijima T, Takeda M, Hamano T, Nabika T (2015) Relationship between blood myostatin levels and kidney function:Shimane CoHRE study. PLoS One 10:e0141035
pubmed: 4621051
pmcid: 4621051
Verzola D, Procopio V, Sofia A, Villaggio B, Tarroni A, Bonanni A, Mannucci I, De Cian F, Gianetta E, Saffioti S, Garibotto G (2011) Apoptosis and myostatin mRNA are upregulated in the skeletal muscle of patients with chronic kidney disease. Kidney Int 79:773–782
Verzola D, Barisione C, Picciotto D, Garibotto G, Koppe L (2019) Emerging role of myostatin and its inhibition in the setting of chronic kidney disease. Kidney Int 95:506–517
Han DS, Chen YM, Lin SY, Chang HH, Huang TM, Chi YC, Yang WS (2011) Serum myostatin levels and grip strength in normal subjects and patients on maintenance haemodialysis. Clin Endocrinol 75:857–863
Mak RH (2011) Serum myostatin in patients on maintenance haemodialysis: a useful biomarker of muscle wasting? Clin Endocrinol 75:738–789
Zhang L, Rajan V, Lin E, Hu Z, Han HQ, Zhou X, Song Y, Min H, Wang X, Du J, Mitch WE (2011) Pharmacological inhibition of myostatin suppresses systemic inflammation and muscle atrophy in mice with chronic kidney disease. FASEB J 25:1653–1663
pubmed: 3079306
pmcid: 3079306
Sugatani T, Agapova OA, Fang Y, Berman AG, Wallace JM, Malluche HH, Faugere MC, Smith W, Sung V, Hruska KA (2017) Ligand trap of the activin receptor type IIA inhibits osteoclast stimulation of bone remodeling in diabetic mice with chronic kidney disease. Kidney Int 91:86–95
Sun DF, Chen Y, Rabkin R (2006) Work-induced changes in skeletal muscle IGF-1 and myostatin gene expression in uremia. Kidney Int 70:453–459
Shroff R, Wan M, Nagler EV, Bakkaloglu S, Fischer DC, Bishop N, Cozzolino M, Bacchetta J, Edefonti A, Stefanidis CJ, Vande Walle J, Haffner D, Klaus G, Schmitt CP, European Society for Paediatric Nephrology Chronic Kidney Disease Mineral and Bone Disorders and Dialysis Working Groups (2017) Clinical practice recommendations for native vitamin D therapy in children with chronic kidney disease stages 2-5 and on dialysis. Nephrol Dial Transplant 32:1098–1113
pubmed: 28873969
pmcid: 28873969
Tahar A, Zerdoumi F, Saidani M, Griene L, Koceir EA (2018) Effects of oral vitamin D3 supplementation in stage 3 chronic kidney disease subjects: insulin resistance syndrome and hormonal disturb interactions. Ann Biol Clin (Paris) 76:313–325
Mathur RP, Dash SC, Gupta N, Prakash S, Saxena S, Bhowmik D (2006) Effects of correction of metabolic acidosis on blood urea and bone metabolism in patients with mild to moderate chronic kidney disease: a prospective randomized single blind controlled trial. Ren Fail 28:1–5
pubmed: 16526312
pmcid: 16526312
McSherry E, Morris RC (1978) Attainment and maintenance of normal stature with alkali therapy in infants and children with classic renal tubular acidosis. J Clin Invest 61:509–527
pubmed: 621287
pmcid: 621287
Domrongkitchaiporn S, Pongskul C, Sirikulchayanonta V, Stitchantrakul W, Leeprasert V, Ongphiphadhanakul B, Radinahamed P, Rajatanavin R (2002) Bone histology and bone mineral density after correction of acidosis in distal renal tubular acidosis. Kidney Int 62:2160–2166
pubmed: 12427141
pmcid: 12427141
Williams AJ, Dittmer ID, McArley A, Clarke J (1997) High bicarbonate dialysate in haemodialysis patients: effects on acidosis and nutritional status. Nephrol Dial Transplant 12:2633–2637
pubmed: 9430864
pmcid: 9430864
Abramowitz MK, Melamed ML, Bauer C, Raff AC, Hostetter TH (2013) Effects of oral sodium bicarbonate in patients with CKD. Clin J Am Soc Nephrol 8:714–720
pubmed: 23393105
pmcid: 23393105
De Brito-Ashurst I, Varagunam M, Raftery MJ, Yaqoob MM (2009) Bicarbonate supplementation slows progression of CKD and improves nutritional status. J Am Soc Nephrol 20:2075–2084
pubmed: 19608703
pmcid: 19608703
Hokken-Koelega A, Mulder P, De Jong R, Lilien M, Donckerwolcke R, Groothof J (2000) Long-term effects of growth hormone treatment on growth and puberty in patients with chronic renal insufficiency. Pediatr Nephrol 14:701–706
pubmed: 10912546
pmcid: 10912546
Boot AM, Nauta J, de Jong MC, Groothoff JW, Lilien MR, van Wijk JA, Kist-van Holthe JE, Hokken-Koelega AC, Pols HA, de Muinck Keizer-Schrama SM (1998) Bone mineral density, bone metabolism and body composition of children with chronic renal failure, with and without growth hormone treatment. Clin Endocrinol 49:665–672
van der Sluis IM, Boot AM, Nauta J, Hop WC, de Jong MC, Lilien MR, Groothoff JW, van Wijk AE, Pols HA, Hokken-Koelega AC, de Muinck Keizer-Schrama SM (2000) Bone density and body composition in chronic renal failure: effects of growth hormone treatment. Pediatr Nephrol 15:221–228
pubmed: 11149115
pmcid: 11149115
Lanes R, Gunczler P, Orta N, Bosquez M, Scovino R, Dominguez L, Esaa S, Weisinger JR (1996) Changes in bone mineral density, growth velocity and renal function of prepubertal uremic children during growth hormone treatment. Horm Res Paediatr 46:263–268
Johnson VL, Wang J, Kaskel FJ, Pierson RN (2000) Changes in body composition of children with chronic renal failure on growth hormone. Pediatr Nephrol 14:695–700
Santos F, Moreno ML, Neto A, Ariceta G, Vara J, Alonso A, Bueno A, Afonso AC, Correia AJ, Muley R, Barrios V, Gómez C, Argente J (2010) Improvement in growth after 1 year of growth hormone therapy in well-nourished infants with growth retardation secondary to chronic renal failure: results of a multicenter, controlled, randomized, open clinical trial. Clin J Am Soc Nephrol 5:1190–1197
pubmed: 20522533
pmcid: 20522533
Bacchetta J, Wesseling-Perry K, Kuizon B, Pereira RC, Gales B, Wang HJ, Elashoff R, Salusky IB (2013) The skeletal consequences of growth hormone therapy in dialyzed children: a randomized trial. Clin J Am Soc Nephrol 8:824–832
pubmed: 3641609
pmcid: 3641609
Nawrot-Wawrzyniak K, Misof BM, Roschger P, Pańczyk-Tomaszewska M, Ziółkowska H, Klaushofer K, Fratzl-Zelman N (2013) Changes in bone matrix mineralization after growth hormone treatment in children and adolescents with chronic kidney failure treated by dialysis: a paired biopsy study. Am J Kidney Dis 61:767–777
pubmed: 23465957
pmcid: 23465957
Lau KK, Obeid J, Breithaupt P, Belostotsky V, Arora S, Nguyen T, Timmons BW (2015) Effects of acute exercise on markers of inflammation in pediatric chronic kidney disease: a pilot study. Pediatr Nephrol 30:615–621
pubmed: 25301024
pmcid: 25301024
Paglialonga F, Lopopolo A, Scarfia RV, Consolo S, Galli MA, Salera S, Grassi MR, Brivio A, Edefonti A (2014) Intradialytic cycling in children and young adults on chronic hemodialysis. Pediatr Nephrol 29:431–438
pubmed: 24253591
pmcid: 24253591
Goldstein SL, Montgomery LR (2009) A pilot study of twice-weekly exercise during hemodialysis in children. Pediatr Nephrol 24:833–839
pubmed: 19093138
pmcid: 19093138
van Bergen M, Takken T, Engelbert R, Groothoff J, Nauta J, van Hoeck K, Helders P, Lilien M (2009) Exercise training in pediatric patients with end-stage renal disease. Pediatr Nephrol 24:619–622
pubmed: 18839217
pmcid: 18839217
Marinho SM, Moraes C, Barbosa JE, Carraro Eduardo JC, Fouque D, Pelletier S, Mafra D (2016) Exercise training alters the bone mineral density of hemodialysis patients. J Strength Cond Res 30:2918–2923
pubmed: 26863587
pmcid: 26863587
Molina P, Vizcaíno B, Molina MD, Beltrán S, González-Moya M, Mora A, Castro-Alonso C, Kanter J, Ávila AI, Górriz JL, Estañ N, Pallardó LM, Fouque D, Carrero JJ (2018) The effect of high-volume online haemodiafiltration on nutritional status and body composition: the ProtEin Stores prEservaTion (PESET) study. Nephrol Dial Transplant 33:1223–1235
Małyszko J, Małyszko JS, Koźminski P, Pawlak K, Wołczynski S, Myśliwiec M (2007) Markers of bone metabolism in hemodialyses and hemodiafiltration. Ren Fail 29:595–601
pubmed: 17654323
pmcid: 17654323
Fischbach M, Terzic J, Laugel V, Dheu C, Menouer S, Helms P, Livolsi A (2004) Daily on-line haemodiafiltration: a pilot trial in children. Nephrol Dial Transplant 19:2360–2367
pubmed: 15266034
pmcid: 15266034
Hoppe A, von Puttkamer C, Linke U, Kahler C, Booss M, Braunauer-Kolberg R, Hofmann K, Joachimsky P, Hirte I, Schley S, Utsch B, Thumfart J, Briese S, Gellermann J, Zimmering M, Querfeld U, Müller D (2011) A hospital-based intermittent nocturnal hemodialysis program for children and adolescents. J Pediatr 158:95–99
pubmed: 20691454
pmcid: 20691454
Fischbach M, Terzic J, Menouer S, Dheu C, Seuge L, Zalosczic A (2010) Daily on line haemodiafiltration promotes catch-up growth in children on chronic dialysis. Nephrol Dial Transplant 25:867–887
pubmed: 19889872
pmcid: 19889872
Shroff R, Smith C, Ranchin B, Bayazit AK, Stefanidis CJ, Askiti V, Azukaitis K, Canpolat N, Ağbaş A, Aitkenhead H, Anarat A, Aoun B, Aofolaju D, Bakkaloglu SA, Bhowruth D, Borzych-Dużałka D, Bulut IK, Büscher R, Deanfield J, Dempster C, Duzova A, Habbig S, Hayes W, Hegde S, Krid S, Licht C, Litwin M, Mayes M, Mir S, Nemec R, Obrycki L, Paglialonga F, Picca S, Samaille C, Shenoy M, Sinha MD, Spasojevic B, Stronach L, Vidal E, Vondrák K, Yilmaz A, Zaloszyc A, Fischbach M, Schmitt CP, Schaefer F (2019) Effects of hemodiafiltration versus conventional hemodialysis in children with ESKD: the HDF, heart and height study. J Am Soc Nephrol 30:678–691
pubmed: 30846560
pmcid: 30846560
Rees L, Jones H (2013) Nutritional management and growth in children with chronic kidney disease. Pediatr Nephrol 28:527–536
pubmed: 22825360
pmcid: 22825360
Yamamoto S, Kido R, Onishi Y, Fukuma S, Akizawa T, Fukagawa M, Kazama JJ, Narita I, Fukuhara S (2015) Use of renin-angiotensin system inhibitors is associated with reduction of fracture risk in hemodialysis patients. PLoS One 10:e0122691
pubmed: 4395204
pmcid: 4395204
Lin YL, Chen SY, Lai YH, Wang CH, Kuo CH, Liou HH, Hsu BG (2019) Angiotensin II receptor blockade is associated with preserved muscle strength in chronic hemodialysis patients. BMC Nephrol 20:54
pubmed: 30764799
pmcid: 30764799
Bonnet N, Bourgoin L, Biver E, Douni E, Ferrari S (2019) RANKL inhibition improves muscle strength and insulin sensitivity and restores bone mass. J Clin Invest 129:3214–3223
pubmed: 6668701
pmcid: 6668701
Khairallah P, Nickolas TL (2018) Management of osteoporosis in CKD. Clin J Am Soc Nephrol 13:962–969
pubmed: 5989687
pmcid: 5989687
Tang L, Gao X, Yang X, Zhang D, Zhang X, Du H, Han Y, Sun L (2016) Combination of weight-bearing training and anti-MSTN polyclonal antibody improve bone quality in rats. Int J Sport Nutr Exerc Metab 26:516–524
Grimberg A, Di Vall SA, Polychronakos C, Allen DB, Cohen LE, Quintos JB, Rossi WC, Feudtner C, Murad MH, Drug and Therapeutics Committee and Ethics Committee of the Pediatric Endocrine Society (2016) Guidelines for growth hormone and insulin-like growth factor-I treatment in children and adolescents: growth hormone deficiency, idiopathic short stature, and primary insulin-like growth factor-I deficiency. Horm Res Paediatr 86:361–397
pubmed: 27884013
pmcid: 27884013
Kovács GT, Oh J, Kovács J, Tönshoff B, Hunziker EB, Zapf J, Mehls O (1996) Growth promoting effects of growth hormone and IGF-I are additive in experimental uremia. Kidney Int 49:1413–1421
pubmed: 8731108
pmcid: 8731108
Drube J, Wan M, Bonthuis M, Wühl E, Bacchetta J, Santos F, Grenda R, Edefonti A, Harambat J, Shroff R, Tönshoff B, Haffner D, European Society for Paediatric Nephrology Chronic Kidney Disease Mineral and Bone Disorders, Dialysis, and Transplantation Working Groups (2019) Clinical practice recommendations for growth hormone treatment in children with chronic kidney disease. Nat Rev Nephrol 15:577–589
pubmed: 31197263
pmcid: 31197263