Abstract
Purpose
This study investigated the frequency and characteristics of sarcopenia among patients after allogeneic hematopoietic stem cell transplantation (allo-HSCT) with a specific focus on the chronic graft-versus-host disease (cGVHD) population and its association with malnutrition, vitamin D and clinical characteristics.
Methods
We assessed sarcopenia, vitamin D levels, and nutritional status in 73 patients who underwent allo-HSCT, of which 45 were diagnosed with cGVHD. Sarcopenia was diagnosed according to the European Working Group on Sarcopenia in Older People (EWGSOP) criteria.
Results
Sarcopenia was diagnosed in 19.2% of patients after allo-HSCT with statistically no significant difference between cGVHD and non-cGVHD patients. The risk factor for sarcopenia was the male gender. Sarcopenia in allo-HSCT patients correlated strongly with malnutrition and with current corticosteroid treatment (p < 0.005). Among cGVHD patients sarcopenia additionally correlated strongly with the number of prior systemic immunosuppressive therapy lines (p < 0.005) and moderately with the intensity of immunosuppression, cGVHD severity global rating assessed by both the health care provider and the patient and joint and fascia cGVHD involvement (p < 0.05). Vitamin D deficiency was found in more than 54.8% of patients, but the correlation to sarcopenia was not found.
Conclusion
Sarcopenia was found to be common in long term survivors of allo-HSCT independently of the cGVHD diagnosis. Prospective longitudinal studies are needed for a better understanding of factors affecting the development of sarcopenia after allo-HSCT.
Similar content being viewed by others
References
Ando T, Fujisawa S, Sakuma T, Teshigawara H, Matsumura A, Suzuki T, Teranaka H, Negoro A, Ogusa E, Aoki J, Miyashita K, Ishii Y, Takahashi H, Nakajima Y, Miyazaki T, Hagihara M, Matsumoto K, Yamazaki E, Nakajima H (2017) Value of computed tomography-defined sarcopenia: a prognostic predictor of non-relapse mortality following allogeneic hematopoietic stem cell transplantation in patients with acute myeloid leukemia and myelodysplastic syndrome. Blood 130(1):4562
Baker JF, Long J, Ibrahim S, Leonard MB, Katz P (2015) Are men at greater risk of lean mass deficits in rheumatoid arthritis? Arthritis Care Res 67(1):112–119
Barone M, Viggiani MT, Anelli MG, Fanizzi R, Lorusso O, Lopalco G, Cantarini L, Di Leo A, Lapadula G, Iannone F (2018) Sarcopenia in patients with rheumatic diseases: prevalence and associated risk factors. J Clin Med 7(12):504
Bassim CW, Fassil H, Dobbin M, Steinberg SM, Baird K, Cole K, Joe G, Comis LE, Mitchell SA, Grkovic L, Edwards D, Mays JW, Cowen EW, Pulanic D, Williams KM, Gress RE, Pavletic SZ (2014) Malnutrition in patients with chronic GVHD. Bone Marrow Transplant 49(10):1300–1306
Bodine SC, Furlo JD (2015) Glucocorticoids and skeletal muscle. Adv Exp Med Biol 872:145–176
Cederholm T, Barazzoni R, Austin P, Ballmer P, Biolo G, Bischoff SC, Compher C, Correia I, Higashiguchi T, Holst M, Jensen GL, Malone A, Muscaritoli M, Nyulasi I, Pirlich M, Rothenberg E, Schindler K, Schneider SM, de van der Schueren MA, Sieber C, Valentini L, Yu JC, Van Gossum A, Singer P (2017) ESPEN guidelines on definitions and terminology of clinical nutrition. Clin Nutr 36:49–64
Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinková E, Vandewoude M, Zamboni M, European Working Group on Sarcopenia in Older People (2010) Sarcopenia: European consensus on definition and diagnosis: report of the european working group on sarcopenia in older people. Age Ageing 39(4):412–423
Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M, Writing group for the European Working Group on sarcopenia in older people 2 (EWGSOP2), the extended group for EWGSOP2 (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48(1):16–31
Ebadi M, Bhanji RA, Mazurak VC, Montano-Loza AJ (2019) Sarcopenia in cirrhosis: from pathogenesis to interventions. J Gastroenterol 54(10):845–859
Filipovich AH, Weisdorf D, Pavletic S, Socie G, Wingard JR, Lee SJ, Martin P, Chien J, Przepiorka D, Couriel D, Cowen EW, Dinndorf P, Farrell A, Hartzman R, Henslee-Downey J, Jacobsohn D, McDonald G, Mittleman B, Rizzo JD, Robinson M, Schubert M, Schultz K, Shulman H, Turner M, Vogelsang G, Flowers ME (2005) National institutes of health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. Diagnosis and staging working group report. Biol Blood Marrow Transplant 11(12):945–956
Fiuza-Luces C, Garatachea N, Simpson RJ, Berger NA, Ramírez M, Lucia A (2015) Understanding graft-versus-host disease. Preliminary findings regarding the effects of exercise in affected patients. Exerc Immunol Rev 21:80–112
Fraser CJ, Bhatia S, Ness K, Carter A, Francisco L, Arora M, Parker P, Forman S, Weisdorf D, Gurney JG, Baker KS (2006) Impact of chronic graft-versus-host disease on the health status of hematopoietic cell transplantation survivors: a report from the Bone Marrow Transplant Survivor Study. Blood 108(8):2867–2873
Garnett C, Apperley JF, Pavlů J (2013) Treatment and management of graft-versus-host disease: improving response and survival. Ther Adv Hematol 4(6):366–378
Glotzbecker B, Ho VT, Aldridge J, Kim HT, Horowitz G, Ritz J, Soiffer R, Avigan D, Rosenblatt J (2013) Low levels of 25-hydroxyvitamin D before allogeneic hematopoietic SCT correlate with the development of chronic GVHD. Bone Marrow Transplant 48(4):593–597
Jacobsohn DA, Margolis J, Doherty J, Anders V, Vogelsang GB (2002) Weight loss and malnutrition in patients with chronic graft-versus-host disease. Bone Marrow Transplant 29(3):231–236
Jagasia MH, Greinix HT, Arora M, Williams KM, Wolff D, Cowen EW, Palmer J, Weisdorf D, Treister NS, Cheng GS, Kerr H, Stratton P, Duarte RF, McDonald GB, Inamoto Y, Vigorito A, Arai S, Datiles MB, Jacobsohn D, Heller T, Kitko CL, Mitchell SA, Martin PJ, Shulman H, Wu RS, Cutler CS, Vogelsang GB, Lee SJ, Pavletic SZ, Flowers ME (2015) National institutes of health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. The 2014 diagnosis and staging working group report. Biol Blood Marrow Transplant 21(3):389–401
Janssen I, Heymsfield SB, Baumgartner RN, Ross R (2000) Estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol 89(2):465–471
Katić M, Pirsl F, Steinberg SM, Dobbin M, Curtis LM, Pulanić D, Desnica L, Titarenko I, Pavletic SZ (2016) Vitamin D levels and their associations with survival and major disease outcomes in a large cohort of patients with chronic graft-vs-host disease. Croat Med J 57(3):276–286
Kinney T (1997) Glucocorticoid-induced muscle atrophy. J Cardiopulm Rehabil 17:76–84
Kyle UG, Chalandon Y, Miralbell R, Karsegard VL, Hans D, Trombetti A, Rizzoli R, Helg C, Pichard C (2005) Longitudinal follow-up of body composition in hematopoietic stem cell transplant patients. Bone Marrow Transplant 35:1171–1177
Lenssen P, Sherry ME, Cheney CL, Nims JW, Sullivan KM, Stern JM, Moe G, Aker SN (1990) Prevalence of nutrition-related problems among long-term survivors of allogeneic marrow transplantation. J Am Diet Assoc 90:835–842
Lucas RM, Gorman S, Geldenhuys S, Hart PH (2014) Vitamin D and immunity. F1000Prime Rep 6:118
Mastaglia SR, Seijo M, Muzio D, Somoza J, Nuñez M, Oliveri B (2011) Effect of vitamin D nutritional status on muscle function and strength in healthy women aged over sixty-five years. J Nutr Health Aging 15(5):349–354
Mitchell SA, Leidy NK, Mooney KH, Dudley WN, Beck SL, LaStayo PC, Cowen EW, Palit P, Comis LE, Krumlauf MC, Avila DN, Atlam N, Fowler DH, Pavletic SZ (2010) Determinants of functional performance in long-term survivors of allogeneic hematopoietic stem cell transplantation with chronic graft-versus-host disease (cGVHD). Bone Marrow Transplant 45:762–769
Moctezuma-Velázquez C, Low G, Mourtzakis M, Ma M, Burak KW, Tandon P, Montano-Loza AJ (2018) Association between low testosterone levels and sarcopenia in cirrhosis: a cross-sectional study. Ann Hepatol 17(4):615–623
Moorthi RN, Avin KG (2017) Clinical relevance of sarcopenia in chronic kidney disease. Curr Opin Nephrol Hypertens 26(3):219–228
Morishita S, Kaida K, Tanaka T, Itani Y, Ikegame K, Okada M, Ishii S, Kodama N, Ogawa H, Domen K (2012) Prevalence of sarcopenia and relevance of body composition, physiological function, fatigue, and health-related quality of life in patients before allogeneic hematopoietic stem cell transplantation. Support Care Cancer 20(12):3161–3168
Muscaritoli M, Anker SD, Argilés J, Aversa Z, Bauer JM, Biolo G, Boirie Y, Bosaeus I, Cederholm T, Costelli P, Fearon KC, Laviano A, Maggio M, Rossi Fanelli F, Schneider SM, Schols A, Sieber CC (2010) Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by Special Interest Groups (SIG) “cachexia-anorexia in chronic wasting diseases” and “nutrition in geriatrics”. Clin Nutr 29:154–159
Orio F, Muscogiuri G, Palomba S, Serio B, Sessa M, Giudice V, Ferrara I, Tauchmanovà L, Colao A, Selleri C (2014) Endocrinopathies after allogeneic and autologous transplantation of hematopoietic stem cells. Sci World J 2014:282147
Ottery FD (2000) Patient-generated subjective global assessment. In: McCallum PD, Polisena CG (eds) The clinical guide to oncology nutrition. The American Dietetic Association, Chicago, pp 11–23
Pavletic SZ, Martin P, Lee SJ, Mitchell S, Jacobsohn D, Cowen EW, Turner ML, Akpek G, Gilman A, McDonald G, Schubert M, Berger A, Bross P, Chien JW, Couriel D, Dunn JP, Fall-Dickson J, Farrell A, Flowers ME, Greinix H, Hirschfeld S, Gerber L, Kim S, Knobler R, Lachenbruch PA, Miller FW, Mittleman B, Papadopoulos E, Parsons SK, Przepiorka D, Robinson M, Ward M, Reeve B, Rider LG, Shulman H, Schultz KR, Weisdorf D, Vogelsang GB, Response Criteria Working Group (2006) Measuring therapeutic response in chronic graft-versus-host disease: national institutes of health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: IV. Response criteria working group report. Biol Blood Marrow Transplant 12:252–266
Robien K, Strayer LG, Majhail N, Lazovich D, Baker KS, Smith AR, Mulrooney DA, Burns LJ (2011) Vitamin D status among long-term survivors of hematopoietic cell transplantation. Bone Marrow Transplant 46(11):1472–1479
Siegert E, March C, Otten L, Makowka A, Preis E, Buttgereit F, Riemekasten G, Müller-Werdan U, Norman K (2018) Prevalence of sarcopenia in systemic sclerosis: assessing body composition and functional disability in patients with systemic sclerosis. Nutrition 55–56:51–55
Tanaka S, Imataki O, Kitaoka A, Fujioka S, Hanabusa E, Ohbayashi Y, Uemura M, Arima N, Yamamoto T (2017) Clinical impact of sarcopenia and relevance of nutritional intake in patients before and after allogeneic hematopoietic stem cell transplantation. J Cancer Res Clin Oncol 143(6):1083–1092
Vandewoude MF, Alish CJ, Sauer AC, Hegazi RA (2012) Malnutrition-sarcopenia syndrome: is this the future of nutrition screening and assessment for older adults? J Aging Res 2012:651570
Vranesic Bender D, Giljevic Z, Kusec V, Laktasic Zerjavic N, Bosnjak Pasic M, Vrdoljak E, Ljubas Kelecic D, Reiner Z, Anic B, Krznaric Z (2016) Guidelines for the prevention, detection and therapy of vitamin D deficiency in adults. Liječ Vjesn 138:121–132
Vukić T, Robinson Smith S, Ljubas Kelečić D, Desnica L, Prenc E, Pulanić D, Vrhovac R, Nemet D, Pavletic SZ (2016) Joint and fascial chronic graft-vs-host disease: correlations with clinical and laboratory parameters. Croat Med J 57(3):266–275
Waters RL, Lunsford BR, Perry J, Byrd R (1988) Energy-speed relationship of walking: standard tables. J Orthop Res 6:215–222
Acknowledgements
This work was supported, in part, by the Unity Through Knowledge Fund project entitled “Clinical and biological factors determining severity and activity of chronic Graft-versus-Host disease after allogeneic hematopoietic stem cell transplantation”, and also, in part, by the Croatian Science Foundation project IP-2016-06-8046 entitled “New biomarkers for chronic graft-versus-host disease”. We would also like to thank the many members of the multidisciplinary team for cGVHD at the University Hospital Center Zagreb, Croatia.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of intrest
None.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ljubas Kelecic, D., Lelas, A., Karas, I. et al. Sarcopenia among patients after allogeneic hematopoietic stem cell transplantation and the impact of chronic graft-versus-host disease. J Cancer Res Clin Oncol 146, 2967–2978 (2020). https://doi.org/10.1007/s00432-020-03280-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00432-020-03280-0