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Feasibility of eccentric overloading and neuromuscular electrical stimulation to improve muscle strength and muscle mass after treatment for head and neck cancer

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Abstract

Purpose

Treatment of head and neck cancer (HNC) results in severe weight loss, mainly due to the loss of lean body mass. Consequently, decreases in muscular strength and health-related quality of life (HRQL) occur. This study investigated the feasibility of a 12-week novel strength training (NST) and conventional strength training (CST) intervention delivered after HNC treatment.

Methods

Participants were randomized to a NST group (n = 11) involving eccentric overloaded strength training and neuromuscular electrical stimulation (NMES), or a CST group (n = 11) involving dynamic resistance exercises matched for training volume. Feasibility outcomes included recruitment, completion, adherence, and evidence of progression. A neuromuscular assessment involving maximal isometric voluntary contractions (MIVCs) in the knee extensors was evaluated prior to and during incremental cycling to volitional exhaustion at baseline and after the interventions. Anthropometrics and patient-reported outcomes (PROs) were also assessed.

Results

Although recruitment was challenging, completion was 100% in NST and 82% in CST. Adherence was 92% in NST and 81% in CST. Overall, MIVC increased by 19 ± 23%, muscle cross-sectional area improved 18 ± 22%, cycling exercise time improved by 18 ± 13%, and improvements in HRQL and fatigue were clinically relevant.

Conclusions

Both interventions were found to be feasible for HNC patients after treatment. Strength training significantly improved maximal muscle strength, muscle cross-sectional area, and PROs after HNC treatment. Future research should include fully powered trials and consider the use of eccentric overloading and NMES during HNC treatment.

Implications for Cancer Survivors

Eccentric- and NMES-emphasized strength training may be useful alternatives to conventional strength training after HNC treatment.

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References

  1. Adelstein DJ, Saxton JP, Lavertu P, Tuason L, Wood BG, Wanamaker JR, et al. A phase III randomized trial comparing concurrent chemotherapy and radiotherapy with radiotherapy alone in resectable stage III and IV squamous cell head and neck cancer: preliminary results. Head Neck J Sci Spec. 1997;19:567–75. https://doi.org/10.1002/(SICI)1097-0347(199710)19:7<567::AID-HED2>3.0.CO;2-5.

    Article  CAS  Google Scholar 

  2. Rathod S, Gupta T, Ghosh-Laskar S, Murthy V, Budrukkar A, Agarwal J. Quality-of-life (QOL) outcomes in patients with head and neck squamous cell carcinoma (HNSCC) treated with intensity-modulated radiation therapy (IMRT) compared to three-dimensional conformal radiotherapy (3D-CRT): Evidence from a prospective randomized study. Oral Oncol. 2013;49:634–42. https://doi.org/10.1016/j.oraloncology.2013.02.013.

    Article  PubMed  Google Scholar 

  3. Gulliford SL, Miah AB, Brennan S, McQuaid D, Clark CH, Partridge M, et al. Dosimetric explanations of fatigue in head and neck radiotherapy: an analysis from the PARSPORT Phase III trial. Radiother Oncol. 2012;104:205–12. https://doi.org/10.1016/j.radonc.2012.07.005.

    Article  PubMed  Google Scholar 

  4. Rosenthal DI, Chambers MS, Fuller CD, Rebueno NCS, Garcia J, Kies MS, et al. Beam path toxicities to non-target structures during intensity-modulated radiation therapy for head and neck cancer. Int J Radiat Oncol Biol Phys. 2008;72:747–55. https://doi.org/10.1016/j.ijrobp.2008.01.012.

    Article  PubMed  Google Scholar 

  5. Nutting CM, Morden JP, Harrington KJ, Sydenham MA, Emson M, Hall E, et al. Parotid-sparing intensity modulated versus conventional radiotherapy in head and neck cancer (PARSPORT): a phase 3 multicentre randomised controlled trial. www.thelancet.com/oncology. 2011;12:127–63. https://doi.org/10.1016/S1470.

  6. Nguyen NP, Frank C, Moltz CC, Vos P, Smith HJ, Karlsson U, et al. Impact of dysphagia on quality of life after treatment of head-and-neck cancer. Int J Radiat Oncol Biol Phys. 2005;61:772–8. https://doi.org/10.1016/j.ijrobp.2004.06.017.

    Article  PubMed  Google Scholar 

  7. Sandmæl JA, Bye A, Solheim TS, Stene GB, Thorsen L, Kaasa S, et al. Feasibility and preliminary effects of resistance training and nutritional supplements during versus after radiotherapy in patients with head and neck cancer: a pilot randomized trial. Cancer. 2017;123:4440–8. https://doi.org/10.1002/cncr.30901.

    Article  PubMed  Google Scholar 

  8. Silver HJ, Dietrich MS, Murphy BA. Changes in body mass, energy balance, physical function, and inflammatory state in patients with locally advanced head and neck cancer treated with concurrent chemoradiation after low-dose induction chemotherapy. Head Neck. 2007;29:893–900. https://doi.org/10.1002/hed.20607.

    Article  PubMed  Google Scholar 

  9. Chauhan NS, Samuel SR, Meenar N, Saxena PP, Keogh JWL. Sarcopenia in male patients with head and neck cancer receiving chemoradiotherapy: a longitudinal pilot study. PeerJ. 2020;8:e8617. https://doi.org/10.7717/peerj.8617.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Grisold W, Grisold A, Löscher WN. Neuromuscular complications in cancer. J Neurol Sci. 2016;367:184–202. https://doi.org/10.1016/j.jns.2016.06.002.

    Article  CAS  PubMed  Google Scholar 

  11. Kluger BM, Krupp LB, Enoka RM. Fatigue and fatigability in neurologic illnesses: proposal for a unified taxonomy. Neurology. 2013;80:409–16. https://doi.org/10.1212/WNL.0b013e31827f07be.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Samuel SR, Maiya GA, Babu AS, Vidyasagar MS. Effect of exercise training on functional capacity & quality of life in head & neck cancer patients receiving chemoradiotherapy. Indian J Med Res. 2013;137:515–20.

    PubMed  PubMed Central  Google Scholar 

  13. Samuel SR, Maiya AG, Fernandes DJ, Guddattu V, Saxena PP, Kurian JR, et al. Effectiveness of exercise-based rehabilitation on functional capacity and quality of life in head and neck cancer patients receiving chemo-radiotherapy. Support Care Cancer. 2019;27:3913–20. https://doi.org/10.1007/s00520-019-04750-z.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Lonkvist CK, Vinther A, Zerahn B, Rosenbom E, Deshmukh AS, Hojman P, et al. Progressive resistance training in head and neck cancer patients undergoing concomitant chemoradiotherapy. Laryngoscope Investig Otolaryngol. 2017;2:295–306. https://doi.org/10.1002/lio2.88.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Lønbro S, Dalgas U, Primdahl H, Overgaard J, Overgaard K. Feasibility and efficacy of progressive resistance training and dietary supplements in radiotherapy treated head and neck cancer patients-the DAHANCA 25A study. Acta Oncol. 2013;52:310–8. https://doi.org/10.3109/0284186X.2012.741325.

    Article  CAS  PubMed  Google Scholar 

  16. Lønbro S, Dalgas U, Primdahl H, Johansen J, Nielsen JL, Aagaard P, et al. Progressive resistance training rebuilds lean body mass in head and neck cancer patients after radiotherapy - results from the randomized DAHANCA 25B trial. Radiother Oncol. 2013;108:314–9. https://doi.org/10.1016/j.radonc.2013.07.002.

    Article  PubMed  Google Scholar 

  17. Capozzi LC, Boldt KR, Lau H, Shirt L, Bultz B, Culos-Reed SN. A clinic-supported group exercise program for head and neck cancer survivors: managing cancer and treatment side effects to improve quality of life. Support Care Cancer. 2015;23:1001–7. https://doi.org/10.1007/s00520-014-2436-4.

    Article  PubMed  Google Scholar 

  18. Ratamess NA, Alvar BA, Evetoch TK, Housh TJ, Ben KW, Kraemer WJ, et al. Progression models in resistance training for healthy adults. Med Sci Sport Exerc. 2009;41:687–708.

    Article  Google Scholar 

  19. Lavigne C, Lau H, Francis G, Culos-Reed SN, Millet GY, Twomey R. Neuromuscular function and fatigability in people diagnosed with head and neck cancer before versus after treatment [e-pub ahead of print April 6, 2020]. Eur J Appl Physiol. 2020. https://doi.org/10.1007/s00421-020-04362-0.

  20. Douglas J, Pearson S, Ross A, McGuigan M. Eccentric exercise: physiological characteristics and acute responses. Sports Med. 2017;47:663–75. https://doi.org/10.1007/s40279-016-0624-8.

    Article  PubMed  Google Scholar 

  21. Raj IS, Bird SR, Westfold BA, Shield AJ. Effects of eccentrically biased versus conventional weight training in older adults. Med Sci Sports Exerc. 2012;44:1167–76. https://doi.org/10.1249/MSS.0b013e3182442ecd.

    Article  PubMed  Google Scholar 

  22. Lastayo PC, Larsen S, Smith S, Dibble L, Marcus R. The feasibility and efficacy of eccentric exercise with older cancer survivors: a preliminary study. J Geriatr Phys Ther. 2010;33:135–40. https://doi.org/10.1097/JPT.0b013e3181eda45e.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Baroni B, Ronei SP, Herzog W, Vaz A. Eccentric resistance training of the knee extensor muscle: training programs and neuromuscular adaptations. Isokinet Exerc Sci. 2015;23:183–98. https://doi.org/10.3233/IES-150580.

    Article  Google Scholar 

  24. Lastayo P, Marcus R, Dibble L, Frajacomo F, Lindstedt S. Eccentric exercise in rehabilitation : safety, feasibility, and application. J Appl Physiol. 2014;116:1426–34. https://doi.org/10.1152/japplphysiol.00008.2013.

    Article  PubMed  Google Scholar 

  25. Wagle JP, Taber CB, Cunanan AJ, Bingham GE, Carroll KM, DeWeese BH, et al. Accentuated eccentric loading for training and performance: a review. Sports Med. 2017;47:2473–95. https://doi.org/10.1007/s40279-017-0755-6.

    Article  PubMed  Google Scholar 

  26. Marcus RL, Lastayo PC, Dibble LE, Hill L, McClain DA. Increased strength and physical performance with eccentric training in women with impaired glucose tolerance: a pilot study. J Women's Health. 2009;18:253–60. https://doi.org/10.1089/jwh.2007.0669.

    Article  Google Scholar 

  27. Maffiuletti NA. Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol. 2010;110:223–34. https://doi.org/10.1007/s00421-010-1502-y.

    Article  PubMed  Google Scholar 

  28. Babault N, Cometti G, Bernardin M, Pousson M, Chatard JC. Effects of electromyostimulation training on muscle strength and power of elite rugby players. J Strength Cond Res. 2007;21:431–7.

    PubMed  Google Scholar 

  29. Maffiuletti NA, Gometti C, Amiridis IG, Martin A, Pousson M, Chatard J-C. The effects of electromyostimulation training and basketball practice on muscle strength and jumping ability. Int J Sports Med. 2000;21:437–43. https://doi.org/10.1055/s-2000-3837.

    Article  CAS  PubMed  Google Scholar 

  30. Feil S, Newell J, Minogue C, Paessler HH. The effectiveness of supplementing a standard rehabilitation program with superimposed neuromuscular electrical stimulation after anterior cruciate ligament reconstruction: a prospective, randomized, single-blind study. Am J Sports Med. 2011;39:1238–47. https://doi.org/10.1177/0363546510396180.

    Article  PubMed  Google Scholar 

  31. Vaz MA, Baroni BM, Geremia JM, Lanferdini FJ, Mayer A, Arampatzis A, et al. Neuromuscular electrical stimulation (NMES) reduces structural and functional losses of quadriceps muscle and improves health status in patients with knee osteoarthritis. J Orthop Res. 2013;31:511–6. https://doi.org/10.1002/jor.22264.

    Article  PubMed  Google Scholar 

  32. Gerovasili V, Stefanidis K, Vitzilaios K, Karatzanos E, Politis P, Koroneos A, et al. Electrical muscle stimulation preserves the muscle mass of critically ill patients: a randomized study. Crit Care. 2009;13:R161. https://doi.org/10.1186/cc8123.

    Article  PubMed  PubMed Central  Google Scholar 

  33. O’Connor D, Caulfield B, Lennon O. The efficacy and prescription of neuromuscular electrical stimulation (NMES) in adult cancer survivors: a systematic review and meta-analysis. Support Care Cancer. 2018;26:3985–4000. https://doi.org/10.1007/s00520-018-4342-7.

    Article  PubMed  Google Scholar 

  34. Capozzi LC, McNeely ML, Lau HY, Reimer RA, Giese-Davis J, Fung TS, et al. Patient-reported outcomes, body composition, and nutrition status in patients with head and neck cancer: results from an exploratory randomized controlled exercise trial. Cancer. 2016;122:1185–200. https://doi.org/10.1002/cncr.29863.

    Article  PubMed  Google Scholar 

  35. Nguyen-Tan PF, Zhang Q, Ang KK, Weber RS, Rosenthal DI, Soulieres D, et al. Randomized phase III trial to test accelerated versus standard fractionation in combination with concurrent cisplatin for head and neck carcinomas in the radiation therapy oncology group 0129 trial: long-term report of efficacy and toxicity. J Clin Oncol. 2014;32:3858–67. https://doi.org/10.1200/JCO.2014.55.3925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Saghaei M, Saghaei S. Implementation of an open-source customizable minimization program for allocation of patients to parallel groups in clinical trials. J Biomed Sci Eng. 2011;04:734–9. https://doi.org/10.4236/jbise.2011.411090.

    Article  Google Scholar 

  37. Scott JM, Martin DS, Ploutz-Snyder R, Matz T, Caine T, Downs M, et al. Panoramic ultrasound: a novel and valid tool for monitoring change in muscle mass. J Cachexia Sarcopenia Muscle. 2017;8:475–81. https://doi.org/10.1002/jcsm.12172.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Millor N, Lecumberri P, Gómez M, Martínez-Ramírez A, Izquierdo M. An evaluation of the 30-s chair stand test in older adults: frailty detection based on kinematic parameters from a single inertial unit. J Neuroeng Rehabil. 2013;10:86. https://doi.org/10.1186/1743-0003-10-86.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Grgic J, Schoenfeld BJ. Are the hypertrophic adaptations to high and low-load resistance training muscle fiber type specific? Front Physiol. 2018. https://doi.org/10.3389/fphys.2018.00402.doi:10.3389/fphys.2018.00402.

  40. Schoenfeld BJ, Ogborn D, Krieger JW. Effects of resistance training frequency on measures of muscle hypertrophy: a systematic review and meta-analysis. Sports Med. 2016;46:1689–97. https://doi.org/10.1007/s40279-016-0543-8.

    Article  PubMed  Google Scholar 

  41. Micklewright D. St Clair Gibson A, Gladwell V, Al Salman A. Development and validity of the rating-of-fatigue scale. Sports Med. 2017;47:2375–93. https://doi.org/10.1007/s40279-017-0711-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Integrating electro muscle stimulation into fitness training level 1. 2016. www.compex.info.

  43. Maffiuletti NA, Gondin J, Place N, Stevens-Lapsley J, Vivodtzev I, Minetto MA. Clinical use of neuromuscular electrical stimulation for neuromuscular rehabilitation: what are we overlooking? Arch Phys Med Rehabil. 2018;99:806–12. https://doi.org/10.1016/j.apmr.2017.10.028.

    Article  PubMed  Google Scholar 

  44. Schoenfeld BJ, Ogborn D, Krieger JW. Dose-response relationship between weekly resistance training volume and increases in muscle mass: a systematic review and meta-analysis. J Sports Sci. 2017;35:1073–82. https://doi.org/10.1080/02640414.2016.1210197.

    Article  PubMed  Google Scholar 

  45. Krieger JW. Single vs. multiple sets of resistance exercise for muscle hypertrophy: a meta-analysis. J Strength Cond Res. 2010;24:1150–9. https://doi.org/10.1519/JSC.0b013e3181d4d436.

    Article  PubMed  Google Scholar 

  46. Lasevicius T, Ugrinowitsch C, Schoenfeld BJ, Roschel H, Tavares LD, De Souza EO, et al. Effects of different intensities of resistance training with equated volume load on muscle strength and hypertrophy. Eur J Sport Sci. 2018;ISSN homep:1–9. https://doi.org/10.1080/17461391.2018.1450898.

  47. Carvalho AP, Vital FM, Soares BG. Exercise interventions for shoulder dysfunction in patients treated for head and neck cancer. Cochrane Database Syst Rev. 2012;4:CD008693. https://doi.org/10.1002/14651858.CD008693.pub2.

    Article  Google Scholar 

  48. McNeely ML, Parliament M, Courneya KS, Seikaly H, Jha N, Scrimger R, et al. A pilot study of a randomized controlled trial to evaluate the effects of progressive resistance exercise training on shoulder dysfunction caused by spinal accessory neurapraxia/neurectomy in head and neck cancer survivors. Head Neck. 2004;26:518–30. https://doi.org/10.1002/hed.20010.

    Article  PubMed  Google Scholar 

  49. McNeely ML, Parliament MB, Seikaly H, Jha N, Magee DJ, Haykowsky MJ, et al. Effect of exercise on upper extremity pain and dysfunction in head and neck cancer survivors: a randomized controlled trial. Cancer. 2008;113:214–22. https://doi.org/10.1002/cncr.23536.

    Article  PubMed  Google Scholar 

  50. Schmitz KH, Courneya KS, Matthews C, Demark-Wahnefried W, Galvão DA, Pinto BM, et al. American college of sports medicine roundtable on exercise guidelines for cancer survivors. Med Sci Sports Exerc. 2010;42:1409–26. https://doi.org/10.1249/MSS.0b013e3181e0c112.

    Article  PubMed  Google Scholar 

  51. Franz F, Erdfelder E, Lang A-G, Buchner A. G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical science. Behav Res Methods. 2007;39:175–91. https://doi.org/10.3758/BF03193146.

    Article  Google Scholar 

  52. Cohen J. Statistical power analysis for the behavioral sciences. Hillsdale: Erlbaum; 1988. http://www.utstat.toronto.edu/~brunner/oldclass/378f16/readings/CohenPower.pdf. Accessed 24 Jun 2019

    Google Scholar 

  53. Maffiuletti NA, Roig M, Karatzanos E, Nanas S. Neuromuscular electrical stimulation for preventing skeletal-muscle weakness and wasting in critically ill patients: a systematic review. BMC Med. 2013;11:137. https://doi.org/10.1186/1741-7015-11-137.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Ringash J, Waldron JN, Siu LL, Martino R, Winquist E, Wright JR, et al. Quality of life and swallowing with standard chemoradiotherapy versus accelerated radiotherapy and panitumumab in locoregionally advanced carcinoma of the head and neck: a phase III randomised trial from the Canadian Cancer Trials Group (HN.6). Eur J Cancer. 2017;72:192–9. https://doi.org/10.1016/j.ejca.2016.11.008.

    Article  CAS  PubMed  Google Scholar 

  55. Oberoi S, Robinson PD, Cataudella D, Culos-Reed SN, Davis H, Duong N, et al. Physical activity reduces fatigue in patients with cancer and hematopoietic stem cell transplant recipients: a systematic review and meta-analysis of randomized trials. Crit Rev Oncol Hematol. 2018;122:52–9. https://doi.org/10.1016/j.critrevonc.2017.12.011.

    Article  PubMed  Google Scholar 

  56. Jager-Wittenaar H, Dijkstra PU, Vissink A, Van Der Laan BFAM, Van Oort RP, Roodenburg JLN. Malnutrition and quality of life in patients treated for oral or oropharyngeal cancer. Head Neck. 2011;33:490–6. https://doi.org/10.1002/hed.21473.

    Article  PubMed  Google Scholar 

  57. Henneman E, Somjen G, Carpenter DO. Functional significance of cell size in spinal motoneurons. J Neurophysiol. 1965;28:560–80. https://doi.org/10.1152/jn.1965.28.3.560.

    Article  CAS  PubMed  Google Scholar 

  58. da Silva CF, e Silva FX, Vianna KB, dos Santos Oliveira G, Vaz MA, Baroni BM. Eccentric training combined to neuromuscular electrical stimulation is not superior to eccentric training alone for quadriceps strengthening in healthy subjects: a randomized controlled trial. Braz J Phys Ther. 2018;22:502–11. https://doi.org/10.1016/j.bjpt.2018.03.006.

    Article  Google Scholar 

  59. Paillard T. Combined application of neuromuscular electrical stimulation and voluntray muscular contractions. SportMed. 2008;38:161–77. https://doi.org/10.2165/00007256-200838020-00005.

    Article  Google Scholar 

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Acknowledgments

The authors sincerely thank Erin MacDonald (Head & Neck Tumor Group Coordinator, Tom Baker Cancer Centre) for her contributions to participant recruitment and all the volunteers who participated in the study.

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Correspondence to Guillaume Y. Millet.

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Lavigne, C., Twomey, R., Lau, H. et al. Feasibility of eccentric overloading and neuromuscular electrical stimulation to improve muscle strength and muscle mass after treatment for head and neck cancer. J Cancer Surviv 14, 790–805 (2020). https://doi.org/10.1007/s11764-020-00893-9

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