Effects of whole-body electromyostimulation combined with individualized nutritional support on body composition in patients with advanced cancer: a controlled pilot trial

Kristin Schink, Hans J Herrmann, Raphaela Schwappacher, Julia Meyer, Till Orlemann, Elisabeth Waldmann, Bernd Wullich, Andreas Kahlmeyer, Rainer Fietkau, Dorota Lubgan, Matthias W Beckmann, Carolin Hack, Wolfgang Kemmler, Jürgen Siebler, Markus F Neurath, Yurdagül Zopf, Kristin Schink, Hans J Herrmann, Raphaela Schwappacher, Julia Meyer, Till Orlemann, Elisabeth Waldmann, Bernd Wullich, Andreas Kahlmeyer, Rainer Fietkau, Dorota Lubgan, Matthias W Beckmann, Carolin Hack, Wolfgang Kemmler, Jürgen Siebler, Markus F Neurath, Yurdagül Zopf

Abstract

Background: Physical exercise and nutritional treatment are promising measures to prevent muscle wasting that is frequently observed in advanced-stage cancer patients. However, conventional exercise is not always suitable for these patients due to physical weakness and therapeutic side effects. In this pilot study, we examined the effect of a combined approach of the novel training method whole-body electromyostimulation (WB-EMS) and individualized nutritional support on body composition with primary focus on skeletal muscle mass in advanced cancer patients under oncological treatment.

Methods: In a non-randomized controlled trial design patients (56.5% male; 59.9 ± 12.7 years) with advanced solid tumors (UICC III/IV, N = 131) undergoing anti-cancer therapy were allocated to a usual care control group (n = 35) receiving individualized nutritional support or to an intervention group (n = 96) that additionally performed a supervised physical exercise program in form of 20 min WB-EMS sessions (bipolar, 85 Hz) 2×/week for 12 weeks. The primary outcome of skeletal muscle mass and secondary outcomes of body composition, body weight and hand grip strength were measured at baseline, in weeks 4, 8 and 12 by bioelectrical impedance analysis and hand dynamometer. Effects of WB-EMS were estimated by linear mixed models. Secondary outcomes of physical function, hematological and blood chemistry parameters, quality of life and fatigue were assessed at baseline and week 12. Changes were analyzed by t-tests, Wilcoxon signed-rank or Mann-Whitney-U-tests.

Results: Twenty-four patients of the control and 58 of the WB-EMS group completed the 12-week trial. Patients of the WB-EMS group had a significantly higher skeletal muscle mass (0.53 kg [0.08, 0.98]; p = 0.022) and body weight (1.02 kg [0.05, 1.98]; p = 0.039) compared to controls at the end of intervention. WB-EMS also significantly improved physical function and performance status (p < 0.05). No significant differences of changes in quality of life, fatigue and blood parameters were detected between the study groups after 12 weeks.

Conclusions: Supervised WB-EMS training is a safe strength training method and combined with nutritional support it shows promising effects against muscle wasting and on physical function in advanced-stage cancer patients undergoing treatment.

Trial registration: ClinicalTrials.gov NCT02293239 (Date: November 18, 2014).

Keywords: Advanced cancer; Cancer cachexia; Nutrition; Physical exercise; Skeletal muscle mass; WB-EMS whole-body electromyostimulation.

Conflict of interest statement

Ethics approval and consent to participate

Before study inclusion the declaration of the written informed consent to participate was obtained from every patient. The study was conducted according to the guidelines of the Helsinki Declaration and the protocol of the study was approved by the Ethics Committee of the Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU) (Reg.Nr.155_13B).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Patient flowchart. The flowchart shows the number of recruited and allocated patients, the number of patients who refused to participate before baseline assessment, the number of patients who dropped out during study course mentioning specific reasons and the number of patients that completed the whole intervention period of 12 weeks. Abbreviations: WB-EMS, whole-body electromyostimulation
Fig. 2
Fig. 2
Estimated marginal means from LMM for body composition parameters and hand grip strength. a-f Estimated marginal means from linear mixed models (error bars show SEM) for body composition and hand grip strength are illustrated of the control group and the WB-EMS group at the different measuring times during the 12-week intervention period. Abbreviations: ECW, extracellular water; ICW, intracellular water; LMM, linear mixed models; WB-EMS, whole-body electromyostimulation

References

    1. von Haehling S, Anker SD. Prevalence, incidence and clinical impact of cachexia: facts and numbers-update 2014. J Cachexia Sarcopenia Muscle. 2014; 10.1007/s13539-014-0164-8.
    1. Argiles JM, Busquets S, Stemmler B, Lopez-Soriano FJ. Cancer cachexia: understanding the molecular basis. Nat Rev Cancer. 2014;14(11):754–762. doi: 10.1038/nrc3829.
    1. Zhang LL, Wang XJ, Zhou GQ, Tang LL, Lin AH, Ma J, et al. Dose-volume relationships for moderate or severe neck muscle atrophy after intensity-modulated radiotherapy in patients with nasopharyngeal carcinoma. Sci Rep. 2015;5:18415. doi: 10.1038/srep18415.
    1. Blauwhoff-Buskermolen S, Versteeg KS, de van der Schueren MA, den Braver NR, Berkhof J, Langius JA, et al. Loss of muscle mass during chemotherapy is predictive for poor survival of patients with metastatic colorectal cancer. J Clin Oncol. 2016;34(12):1339–1344. doi: 10.1200/JCO.2015.63.6043.
    1. Choi Y, Oh DY, Kim TY, Lee KH, Han SW, Im SA, et al. Skeletal muscle depletion predicts the prognosis of patients with advanced pancreatic Cancer undergoing palliative chemotherapy, independent of body mass index. PLoS One. 2015;10(10):e0139749. doi: 10.1371/journal.pone.0139749.
    1. Miyamoto Y, Baba Y, Sakamoto Y, Ohuchi M, Tokunaga R, Kurashige J, et al. Negative impact of skeletal muscle loss after systemic chemotherapy in patients with unresectable colorectal cancer. PLoS One. 2015;10(6):e0129742. doi: 10.1371/journal.pone.0129742.
    1. Jung HW, Kim JW, Kim JY, Kim SW, Yang HK, Lee JW, et al. Effect of muscle mass on toxicity and survival in patients with colon cancer undergoing adjuvant chemotherapy. Support Care Cancer. 2015;23(3):687–694. doi: 10.1007/s00520-014-2418-6.
    1. Van Cutsem E, Arends J. The causes and consequences of cancer-associated malnutrition. Eur J Oncol Nurs. 2005;9(Suppl 2):S51–S63. doi: 10.1016/j.ejon.2005.09.007.
    1. Escamilla DM, Jarrett P. The impact of weight loss on patients with cancer. Nurs Times. 2016;112(11):20–22.
    1. Powers SK, Lynch GS, Murphy KT, Reid MB, Zijdewind I. Disease-induced skeletal muscle atrophy and fatigue. Med Sci Sports Exerc. 2016;48(11):2307–2319. doi: 10.1249/MSS.0000000000000975.
    1. Albrecht TA, Taylor AG. Physical activity in patients with advanced-stage cancer: a systematic review of the literature. Clin J Oncol Nurs. 2012;16(3):293–300. doi: 10.1188/12.CJON.293-300.
    1. Argiles JM, Busquets S, Stemmler B, Lopez-Soriano FJ. Cachexia and sarcopenia: mechanisms and potential targets for intervention. Curr Opin Pharmacol. 2015;22:100–106. doi: 10.1016/j.coph.2015.04.003.
    1. Stene GB, Helbostad JL, Balstad TR, Riphagen II, Kaasa S, Oldervoll LM. Effect of physical exercise on muscle mass and strength in cancer patients during treatment--a systematic review. Crit Rev Oncol Hematol. 2013;88(3):573–593. doi: 10.1016/j.critrevonc.2013.07.001.
    1. Johns N, Greig C, Fearon KC. Is tissue cross-talk important in cancer cachexia? Crit Rev Oncog. 2012;17(3):263–276. doi: 10.1615/CritRevOncog.v17.i3.40.
    1. Onesti JK, Guttridge DC. Inflammation based regulation of cancer cachexia. Biomed Res Int. 2014;2014:168407. doi: 10.1155/2014/168407.
    1. Mustian KM, Fisher S, Adams J, Janelsins M, Palesh O, Darling T, et al. Cytokine-mediated changes associated with improvements in cancer-related fatigue induced by exercise: results from a randomized pilot study of cancer patients receiving radiotherapy. J Clin Oncol. 2009;27(15_suppl):9632.
    1. Al-Majid S, Waters H. The biological mechanisms of cancer-related skeletal muscle wasting: the role of progressive resistance exercise. Biol Res Nurs. 2008;10(1):7–20. doi: 10.1177/1099800408317345.
    1. Filipovic A, Kleinoder H, Dormann U, Mester J. Electromyostimulation--a systematic review of the effects of different electromyostimulation methods on selected strength parameters in trained and elite athletes. J Strength Cond Res. 2012;26(9):2600–2614. doi: 10.1519/JSC.0b013e31823f2cd1.
    1. Kemmler W, Schliffka R, Mayhew JL, von Stengel S. Effects of whole-body electromyostimulation on resting metabolic rate, body composition, and maximum strength in postmenopausal women: the training and ElectroStimulation trial. J Strength Cond Res. 2010;24(7):1880–1887. doi: 10.1519/JSC.0b013e3181ddaeee.
    1. Kemmler W, von Stengel S. Whole-body electromyostimulation as a means to impact muscle mass and abdominal body fat in lean, sedentary, older female adults: subanalysis of the TEST-III trial. Clin Interv Aging. 2013;8:1353–1364. doi: 10.2147/CIA.S52337.
    1. Kemmler W, Bebenek M, Engelke K, von Stengel S. Impact of whole-body electromyostimulation on body composition in elderly women at risk for sarcopenia: the training and ElectroStimulation trial (TEST-III) Age (Dordr) 2014;36(1):395–406. doi: 10.1007/s11357-013-9575-2.
    1. van Buuren F, Mellwig KP, Prinz C, Korber B, Frund A, Fritzsche D, et al. Electrical myostimulation improves left ventricular function and peak oxygen consumption in patients with chronic heart failure: results from the exEMS study comparing different stimulation strategies. Clin Res Cardiol. 2013;102(7):523–534. doi: 10.1007/s00392-013-0562-5.
    1. van Buuren F, Mellwig KP, Frund A, Bogunovic N, Oldenburg O, Kottmann T, et al. Electrical myostimulation: improvement of quality of life, oxygen uptake and left ventricular function in chronic heart failure. Rehabilitation (Stuttg) 2014;53(5):321–326.
    1. Fritzsche D, Fruend A, Schenk S, Mellwig KP, Kleinoder H, Gummert J, et al. Electromyostimulation (EMS) in cardiac patients. Will EMS training be helpful in secondary prevention? Herz. 2010;35(1):34–40. doi: 10.1007/s00059-010-3268-8.
    1. Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, Bozzetti F, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr. 2016; 10.1016/j.clnu.2016.07.015.
    1. Arends J, Bertz H, Bischoff SC, Fietkau R, Herrmann HJ, Holm E, et al. S3-guideline of the German Society for Nutritional Medicine (DGEM) in cooperation with the DGHO, the ASORS and the AKE clinical nutrition in oncology. Aktuel Ernahrungsmed. 2015;40(05):e1–e74. doi: 10.1055/s-0035-1552741.
    1. Fearon KC. Cancer cachexia: developing multimodal therapy for a multidimensional problem. Eur J Cancer. 2008;44(8):1124–1132. doi: 10.1016/j.ejca.2008.02.033.
    1. Chevalier S, Winter A. Do patients with advanced cancer have any potential for protein anabolism in response to amino acid therapy? Curr Opin Clin Nutr Metab Care. 2014;17(3):213–218. doi: 10.1097/MCO.0000000000000047.
    1. Drummond MJ, Dreyer HC, Fry CS, Glynn EL, Rasmussen BB. Nutritional and contractile regulation of human skeletal muscle protein synthesis and mTORC1 signaling. J Appl Physiol (1985) 2009;106(4):1374–1384. doi: 10.1152/japplphysiol.91397.2008.
    1. Salomao EM, Gomes-Marcondes MC. Light aerobic physical exercise in combination with leucine and/or glutamine-rich diet can improve the body composition and muscle protein metabolism in young tumor-bearing rats. J Physiol Biochem. 2012;68(4):493–501. doi: 10.1007/s13105-012-0164-0.
    1. Schofield WN. Predicting basal metabolic rate, new standards and review of previous work. Hum Nutr Clin Nutr. 1985;39(Suppl 1):5–41.
    1. Cano N, Fiaccadori E, Tesinsky P, Toigo G, Druml W, Kuhlmann M, et al. ESPEN guidelines on enteral nutrition: adult renal failure. Clin Nutr. 2006;25(2):295–310. doi: 10.1016/j.clnu.2006.01.023.
    1. Kondrup J, Rasmussen HH, Hamberg O, Stanga Z. Nutritional risk screening (NRS 2002): a new method based on an analysis of controlled clinical trials. Clin Nutr. 2003;22(3):321–336. doi: 10.1016/S0261-5614(02)00214-5.
    1. Bosy-Westphal A, Later W, Hitze B, Sato T, Kossel E, Gluer CC, et al. Accuracy of bioelectrical impedance consumer devices for measurement of body composition in comparison to whole body magnetic resonance imaging and dual X-ray absorptiometry. Obes Facts. 2008;1(6):319–324. doi: 10.1159/000176061.
    1. Kilgour RD, Vigano A, Trutschnigg B, Lucar E, Borod M, Morais JA. Handgrip strength predicts survival and is associated with markers of clinical and functional outcomes in advanced cancer patients. Support Care Cancer. 2013;21(12):3261–3270. doi: 10.1007/s00520-013-1894-4.
    1. Schmidt K, Vogt L, Thiel C, Jager E, Banzer W. Validity of the six-minute walk test in cancer patients. Int J Sports Med. 2013;34(7):631–636. doi: 10.1055/s-0032-1323746.
    1. Karnofsky DBJ. Evaluation of chemotherapeutic agents. 1949. The clinical evaluation of chemotherapeutic agents in cancer; pp. 191–205.
    1. Aaronson NK, Ahmedzai S, Bergman B, Bullinger M, Cull A, Duez NJ, et al. The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst. 1993;85(5):365–376. doi: 10.1093/jnci/85.5.365.
    1. Lai JS, Cella D, Chang CH, Bode RK, Heinemann AW. Item banking to improve, shorten and computerize self-reported fatigue: an illustration of steps to create a core item bank from the FACIT-fatigue scale. Qual Life Res. 2003;12(5):485–501. doi: 10.1023/A:1025014509626.
    1. Clarkson PM, Kearns AK, Rouzier P, Rubin R, Thompson PD. Serum creatine kinase levels and renal function measures in exertional muscle damage. Med Sci Sports Exerc. 2006;38(4):623–627. doi: 10.1249/01.mss.0000210192.49210.fc.
    1. Kemmler W, Teschler M, Bebenek M, von Stengel S. (Very) high Creatinkinase concentration after exertional whole-body electromyostimulation application: health risks and longitudinal adaptations. Wien Med Wochenschr. 2015;165(21–22):427–435. doi: 10.1007/s10354-015-0394-1.
    1. Peters SA, Bots ML, den Ruijter HM, Palmer MK, Grobbee DE, Crouse JR, 3rd, et al. Multiple imputation of missing repeated outcome measurements did not add to linear mixed-effects models. J Clin Epidemiol. 2012;65(6):686–695. doi: 10.1016/j.jclinepi.2011.11.012.
    1. Chakraborty H, Gu H. A mixed model approach for intent-to-treat analysis in longitudinal clinical trials with missing values. Research Triangle Park: RTI Press; 2009.
    1. Gonzalez MC, Pastore CA, Orlandi SP, Heymsfield SB. Obesity paradox in cancer: new insights provided by body composition. Am J Clin Nutr. 2014;99(5):999–1005. doi: 10.3945/ajcn.113.071399.
    1. Norman K, Stobaus N, Zocher D, Bosy-Westphal A, Szramek A, Scheufele R, et al. Cutoff percentiles of bioelectrical phase angle predict functionality, quality of life, and mortality in patients with cancer. Am J Clin Nutr. 2010;92(3):612–619. doi: 10.3945/ajcn.2010.29215.
    1. Fearon K, Arends J, Baracos V. Understanding the mechanisms and treatment options in cancer cachexia. Nat Rev Clin Oncol. 2013;10(2):90–99. doi: 10.1038/nrclinonc.2012.209.
    1. Yamaoka Y, Fujitani K, Tsujinaka T, Yamamoto K, Hirao M, Sekimoto M. Skeletal muscle loss after total gastrectomy, exacerbated by adjuvant chemotherapy. Gastric Cancer. 2015;18(2):382–389. doi: 10.1007/s10120-014-0365-z.
    1. Chang D, Joseph DJ, Ebert MA, Galvao DA, Taaffe DR, Denham JW, et al. Effect of androgen deprivation therapy on muscle attenuation in men with prostate cancer. J Med Imaging Radiat Oncol. 2014;58(2):223–228. doi: 10.1111/1754-9485.12124.
    1. Aoyagi T, Terracina KP, Raza A, Matsubara H, Takabe K. Cancer cachexia, mechanism and treatment. World J Gastrointest Oncol. 2015;7(4):17–29. doi: 10.4251/wjgo.v7.i4.17.
    1. Mustian KM, Peppone L, Darling TV, Palesh O, Heckler CE, Morrow GR. A 4-week home-based aerobic and resistance exercise program during radiation therapy: a pilot randomized clinical trial. J Support Oncol. 2009;7(5):158–167.
    1. Demark-Wahnefried W, Case LD, Blackwell K, Marcom PK, Kraus W, Aziz N, et al. Results of a diet/exercise feasibility trial to prevent adverse body composition change in breast cancer patients on adjuvant chemotherapy. Clin Breast Cancer. 2008;8(1):70–79. doi: 10.3816/CBC.2008.n.005.
    1. Battaglini C, Bottaro M, Dennehy C, Rae L, Shields E, Kirk D, et al. The effects of an individualized exercise intervention on body composition in breast cancer patients undergoing treatment. Sao Paulo Med J. 2007;125(1):22–28. doi: 10.1590/S1516-31802007000100005.
    1. Coleman EA, Coon S, Hall-Barrow J, Richards K, Gaylor D, Stewart B. Feasibility of exercise during treatment for multiple myeloma. Cancer Nurs. 2003;26(5):410–419. doi: 10.1097/00002820-200310000-00012.
    1. Courneya KS, Segal RJ, Mackey JR, Gelmon K, Reid RD, Friedenreich CM, et al. Effects of aerobic and resistance exercise in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial. J Clin Oncol. 2007;25(28):4396–4404. doi: 10.1200/JCO.2006.08.2024.
    1. Jones S, Man WD, Gao W, Higginson IJ, Wilcock A, Maddocks M. Neuromuscular electrical stimulation for muscle weakness in adults with advanced disease. Cochrane Database Syst Rev. 2016;10:Cd009419.
    1. Maddocks M, Halliday V, Chauhan A, Taylor V, Nelson A, Sampson C, et al. Neuromuscular electrical stimulation of the quadriceps in patients with non-small cell lung cancer receiving palliative chemotherapy: a randomized phase II study. PLoS One. 2013;8(12):e86059. doi: 10.1371/journal.pone.0086059.
    1. Oldervoll LM, Loge JH, Lydersen S, Paltiel H, Asp MB, Nygaard UV, et al. Physical exercise for cancer patients with advanced disease: a randomized controlled trial. Oncologist. 2011;16(11):1649–1657. doi: 10.1634/theoncologist.2011-0133.
    1. Dewys WD, Begg C, Lavin PT, Band PR, Bennett JM, Bertino JR, et al. Prognostic effect of weight loss prior to chemotherapy in cancer patients. Eastern cooperative oncology group. Am J Med. 1980;69(4):491–497. doi: 10.1016/S0149-2918(05)80001-3.
    1. Andreyev HJ, Norman AR, Oates J, Cunningham D. Why do patients with weight loss have a worse outcome when undergoing chemotherapy for gastrointestinal malignancies? Eur J Cancer. 1998;34(4):503–509. doi: 10.1016/S0959-8049(97)10090-9.
    1. Paccagnella A, Morassutti I, Rosti G. Nutritional intervention for improving treatment tolerance in cancer patients. Curr Opin Oncol. 2011;23(4):322–330. doi: 10.1097/CCO.0b013e3283479c66.
    1. van Dijk DP, van de Poll MC, Moses AG, Preston T, Olde Damink SW, Rensen SS, et al. Effects of oral meal feeding on whole body protein breakdown and protein synthesis in cachectic pancreatic cancer patients. J Cachexia Sarcopenia Muscle. 2015;6(3):212–221. doi: 10.1002/jcsm.12029.
    1. Capra S, Ferguson M, Ried K. Cancer: impact of nutrition intervention outcome--nutrition issues for patients. Nutrition. 2001;17(9):769–772. doi: 10.1016/S0899-9007(01)00632-3.
    1. Ravasco P, Monteiro Grillo I, Camilo M. Cancer wasting and quality of life react to early individualized nutritional counselling! Clin Nutr. 2007;26(1):7–15. doi: 10.1016/j.clnu.2006.10.005.
    1. Bourdel-Marchasson I, Blanc-Bisson C, Doussau A, Germain C, Blanc JF, Dauba J, et al. Nutritional advice in older patients at risk of malnutrition during treatment for chemotherapy: a two-year randomized controlled trial. PLoS One. 2014;9(9):e108687. doi: 10.1371/journal.pone.0108687.
    1. McGlory C, Devries MC, Phillips SM. Skeletal muscle and resistance exercise training; the role of protein synthesis in recovery and remodelling. J Appl Physiol (1985). 2016; 10.1152/japplphysiol.00613.2016:jap.00613.02016.
    1. Norman K, Stobäus N, Gonzalez MC, Schulzke J-D, Pirlich M. Hand grip strength: outcome predictor and marker of nutritional status. Clin Nutr. 2011;30(2):135–142. doi: 10.1016/j.clnu.2010.09.010.
    1. Andrews JS, Trupin L, Schmajuk G, Barton J, Margaretten M, Yazdany J, et al. Muscle strength predicts changes in physical function in women with systemic lupus erythematosus. Arthritis Care Res. 2015;67(8):1070–1077. doi: 10.1002/acr.22560.
    1. Lis CG, Gupta D, Lammersfeld CA, Markman M, Vashi PG. Role of nutritional status in predicting quality of life outcomes in cancer--a systematic review of the epidemiological literature. Nutr J. 2012;11:27. doi: 10.1186/1475-2891-11-27.
    1. Turner K, Tookman A, Bristowe K, Maddocks M. ‘I am actually doing something to keep well. That feels really good’: experiences of exercise within hospice care. Prog Palliat Care. 2016;24(4):204–212. doi: 10.1080/09699260.2015.1123441.
    1. Leach LM, Kleski A, Spencer K, Anthony J, LaLonde M, Sweeney TJ, et al. The effectiveness of a structured exercise and education program on clinical and quality-of-life outcomes in patients with cancer who are actively undergoing therapy compared with patients not currently receiving therapy. J Clin Oncol. 2011;29(15_suppl):9140. doi: 10.1200/jco.2011.29.15_suppl.9140.
    1. Oechsle K, Jensen W, Schmidt T, Reer R, Braumann KM, de Wit M, et al. Physical activity, quality of life, and the interest in physical exercise programs in patients undergoing palliative chemotherapy. Support Care Cancer. 2011;19(5):613–619. doi: 10.1007/s00520-010-0862-5.
    1. Bosy-Westphal A, Schautz B, Later W, Kehayias JJ, Gallagher D, Muller MJ. What makes a BIA equation unique? Validity of eight-electrode multifrequency BIA to estimate body composition in a healthy adult population. Eur J Clin Nutr. 2013;67(Suppl 1):S14–S21. doi: 10.1038/ejcn.2012.160.
    1. Bosy-Westphal A, Jensen B. Quantification of whole-body and segmental skeletal muscle mass using phase-sensitive 8-electrode medical bioelectrical impedance devices. Eur J Clin Nutr. 2017;71(9):1061–1067. doi: 10.1038/ejcn.2017.27.
    1. Janssen I, Heymsfield SB, Baumgartner RN, Ross R. Estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol (1985) 2000;89(2):465–471. doi: 10.1152/jappl.2000.89.2.465.
    1. Wladysiuk MS, Mlak R, Morshed K, Surtel W, Brzozowska A, Malecka-Massalska T. Bioelectrical impedance phase angle as a prognostic indicator of survival in head-and-neck cancer. Curr Oncol. 2016;23(5):e481–e487. doi: 10.3747/co.23.3181.
    1. Sergi G, De Rui M, Stubbs B, Veronese N, Manzato E. Measurement of lean body mass using bioelectrical impedance analysis: a consideration of the pros and cons. Aging Clin Exp Res. 2016; 10.1007/s40520-016-0622-6.

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