Ultrasound use in metastatic breast cancer to measure body composition changes following an exercise intervention

Adrian Escriche-Escuder, Manuel Trinidad-Fernández, Bella Pajares, Marcos Iglesias-Campos, Emilio Alba, Antonio I Cuesta-Vargas, Cristina Roldán-Jiménez, Adrian Escriche-Escuder, Manuel Trinidad-Fernández, Bella Pajares, Marcos Iglesias-Campos, Emilio Alba, Antonio I Cuesta-Vargas, Cristina Roldán-Jiménez

Abstract

Changes in body composition and muscle dysfunction are common in metastatic breast cancer (MBC). Ultrasound imaging (US) offers reliable information about muscle and fat tissue architecture (thickness) and quality (echo-intensity). This study aimed to analyze the responsiveness of thickness and echo-intensity and its possible relationship with functional and patient reported-outcomes (PRO) in MBC patients after an exercise intervention. A prospective study was conducted in 2019. A 12-week exercise program was performed, including aerobic exercise and strength training. Measurements were made at baseline and after intervention. Thickness and echo-intensity were obtained from the quadriceps and biceps brachii and brachialis (BB). Mean differences were calculated using the T-Student parametric test for dependent samples of the differences in the means before and after the intervention (p = 0.05; 95% CI). Data from 13 MBC patients showed that some US muscle variables had significant differences after intervention. Best correlations were found between the quality of life questionnaire (QLQ-BR23) PRO and variables from BB muscle thickness in contraction (r = 0.61, p < 0.01), and Non-contraction (r = 0.55, p < 0.01). BB Muscle Non-contraction Thickness also explained 70% of QLQ-BR23 variance. In conclusion, muscle architecture biomarkers showed great responsiveness and are correlated with PRO after an exercise intervention in MBC patients.

Conflict of interest statement

There is no other relationship with Novartis as partial funder apart from defraying the expenses of employment, and there are no patents, products in development or marketed products relationship to declare according to the definition of financial competing interest given by Scientific Reports.

Figures

Figure 1
Figure 1
Position of the patient and the ultrasound device for ultrasound assessment of the quadriceps (a) and the biceps brachii and brachialis (b).
Figure 2
Figure 2
Range of interest (white rectangle) and areas selection of sample images (A: quadriceps; B: biceps/brachialis).

References

    1. Fitzmaurice C, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2016. JAMA Oncol. 2018;4:1553–1568. doi: 10.1001/jamaoncol.2018.2706.
    1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA. Cancer J. Clin. 2019;69:7–34. doi: 10.3322/caac.21551.
    1. Hanrahan EO, et al. Combined-modality treatment for isolated recurrences of breast carcinoma: Update on 30 years of experience at the University of Texas M.D. Anderson Cancer Center and assessment of prognostic factors. Cancer. 2005;104:1158–1171. doi: 10.1002/cncr.21305.
    1. Greenberg PA, et al. Long-term follow-up of patients with complete remission following combination chemotherapy for metastatic breast cancer. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 1996;14:2197–2205. doi: 10.1200/JCO.1996.14.8.2197.
    1. O’Shaughnessy J. Extending survival with chemotherapy in metastatic breast cancer. Oncologist. 2005;10(Suppl 3):20–29. doi: 10.1634/theoncologist.10-90003-20.
    1. Chia SK, et al. The impact of new chemotherapeutic and hormone agents on survival in a population-based cohort of women with metastatic breast cancer. Cancer. 2007;110:973–979. doi: 10.1002/cncr.22867.
    1. Luu T, Chung C, Somlo G. Combining emerging agents in advanced breast cancer. Oncologist. 2011;16:760–771. doi: 10.1634/theoncologist.2010-0345.
    1. Scully OJ, Bay B-H, Yip G, Yu Y. Breast cancer metastasis. Cancer Genomics Proteomics. 2012;9:311–320.
    1. Hidding JT, Beurskens CH, van der Wees PJ, van Laarhoven HW, Nijhuis-van der Sanden MW. Treatment related impairments in arm and shoulder in patients with breast cancer: A systematic review. PLoS ONE. 2014;9:e96748. doi: 10.1371/journal.pone.0096748.
    1. Penha TRL, et al. Quality of life in patients with breast cancer-related lymphedema and reconstructive breast surgery. J. Reconstr. Microsurg. 2016;32:484–490. doi: 10.1055/s-0036-1572538.
    1. Glare PA, et al. Pain in cancer survivors. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2014;32:1739–1747. doi: 10.1200/JCO.2013.52.4629.
    1. Napoli N, et al. Genetic polymorphism at Val80 (rs700518) of the CYP19A1 gene is associated with body composition changes in women on aromatase inhibitors for ER (+) breast cancer. Pharmacogenet. Genomics. 2015;25:377–381. doi: 10.1097/FPC.0000000000000146.
    1. Gianoudis J, Bailey CA, Daly RM. Associations between sedentary behaviour and body composition, muscle function and sarcopenia in community-dwelling older adults. Osteoporos. Int. J. Establ. Result Coop. Eur. Found. Osteoporos. Natl. Osteoporos. Found. USA. 2015;26:571–579. doi: 10.1007/s00198-014-2895-y.
    1. Benavides-Rodríguez L, et al. Relationship between handgrip strength and muscle mass in female survivors of breast cancer: A mediation analysis. Nutrients. 2017;9:695. doi: 10.3390/nu9070695.
    1. Zhang X-M, et al. Sarcopenia as a predictor of mortality in women with breast cancer: A meta-analysis and systematic review. BMC Cancer. 2020;20:172. doi: 10.1186/s12885-020-6645-6.
    1. Klassen O, et al. Muscle strength in breast cancer patients receiving different treatment regimes. J. Cachexia Sarcopenia Muscle. 2017;8:305–316. doi: 10.1002/jcsm.12165.
    1. Williams GR, et al. Assessment of sarcopenia measures, survival, and disability in older adults before and after diagnosis with cancer. JAMA Netw. Open. 2020;3:e204783. doi: 10.1001/jamanetworkopen.2020.4783.
    1. Gerritsen JKW, Vincent AJPE. Exercise improves quality of life in patients with cancer: A systematic review and meta-analysis of randomised controlled trials. Br. J. Sports Med. 2016;50:796–803. doi: 10.1136/bjsports-2015-094787.
    1. Segal R, et al. Exercise for people with cancer: A clinical practice guideline. Curr. Oncol. 2017;24:40–46. doi: 10.3747/co.24.3376.
    1. Dennett AM, Peiris CL, Shields N, Prendergast LA, Taylor NF. Moderate-intensity exercise reduces fatigue and improves mobility in cancer survivors: A systematic review and meta-regression. J. Physiother. 2016;62:68–82. doi: 10.1016/j.jphys.2016.02.012.
    1. Bleakney R, Maffulli N. Ultrasound changes to intramuscular architecture of the quadriceps following intramedullary nailing. J. Sports Med. Phys. Fitness. 2002;42:120–125.
    1. Scanlon TC, et al. Muscle architecture and strength: Adaptations to short-term resistance training in older adults. Muscle Nerve. 2014;49:584–592. doi: 10.1002/mus.23969.
    1. Cešeiko R, et al. The impact of maximal strength training on quality of life among women with breast cancer undergoing treatment. Exp. Oncol. 2019;41:166–172.
    1. Galvão DA, et al. Exercise preserves physical function in prostate cancer patients with bone metastases. Med. Sci. Sports Exerc. 2018;50:393–399. doi: 10.1249/MSS.0000000000001454.
    1. Kawai H, et al. Morphological and qualitative characteristics of the quadriceps muscle of community-dwelling older adults based on ultrasound imaging: Classification using latent class analysis. Aging Clin. Exp. Res. 2018;30:283–291. doi: 10.1007/s40520-017-0781-0.
    1. Martínez-Payá JJ, et al. Muscular echovariation: A new biomarker in amyotrophic lateral sclerosis. Ultrasound Med. Biol. 2017;43:1153–1162. doi: 10.1016/j.ultrasmedbio.2017.02.002.
    1. Martínez-Payá JJ, et al. Quantitative muscle ultrasonography using textural analysis in amyotrophic lateral sclerosis. Ultrason. Imaging. 2017;39:357–368. doi: 10.1177/0161734617711370.
    1. Fukumoto Y, et al. Skeletal muscle quality assessed from echo intensity is associated with muscle strength of middle-aged and elderly persons. Eur. J. Appl. Physiol. 2012;112:1519–1525. doi: 10.1007/s00421-011-2099-5.
    1. Wilhelm EN, et al. Relationship between quadriceps femoris echo intensity, muscle power, and functional capacity of older men. Age Dordr. Neth. 2014;36:9625. doi: 10.1007/s11357-014-9625-4.
    1. Ticinesi A, Meschi T, Narici MV, Lauretani F, Maggio M. Muscle ultrasound and sarcopenia in older individuals: A clinical perspective. J. Am. Med. Dir. Assoc. 2017;18:290–300. doi: 10.1016/j.jamda.2016.11.013.
    1. Jones LW, Eves ND, Peppercorn J. Pre-exercise screening and prescription guidelines for cancer patients. Lancet Oncol. 2010;11:914–916. doi: 10.1016/S1470-2045(10)70184-4.
    1. Stichling K, et al. Factors influencing GPs’ perception of specialised palliative homecare (SPHC) importance—results of a cross-sectional study. BMC Palliat. Care. 2020;19:117. doi: 10.1186/s12904-020-00603-3.
    1. Sprangers MA, et al. The European Organization for Research and Treatment of Cancer breast cancer-specific quality-of-life questionnaire module: First results from a three-country field study. J. Clin. Oncol. 1996;14:2756–2768. doi: 10.1200/JCO.1996.14.10.2756.
    1. Mock V. Clinical excellence through evidence-based practice: Fatigue management as a model. Oncol. Nurs. Forum. 2003;30:787–796. doi: 10.1188/03.ONF.787-795.
    1. Piper BF, et al. The revised Piper Fatigue Scale: Psychometric evaluation in women with breast cancer. Oncol. Nurs. Forum. 1998;25:677–684.
    1. Gabel CP, Michener LA, Burkett B, Neller A. The Upper Limb Functional Index: Development and determination of reliability, validity, and responsiveness. J. Hand Ther. Off. J. Am. Soc. Hand Ther. 2006;19:328–348. doi: 10.1197/j.jht.2006.04.001.
    1. Cuesta-Vargas AI, Gabel PC. Cross-cultural adaptation, reliability and validity of the Spanish version of the upper limb functional index. Health Qual. Life Outcomes. 2013;11:126. doi: 10.1186/1477-7525-11-126.
    1. Gabel CP, Melloh M, Burkett B, Michener LA. Lower limb functional index: Development and clinimetric properties. Phys. Ther. 2012;92:98–110. doi: 10.2522/ptj.20100199.
    1. Cuesta-Vargas AI, Gabel CP, Bennett P. Cross cultural adaptation and validation of a Spanish version of the Lower Limb Functional Index. Health Qual. Life Outcomes. 2014;12:75. doi: 10.1186/1477-7525-12-75.
    1. Nielsen PK, Jensen BR, Darvann T, Jørgensen K, Bakke M. Quantitative ultrasound image analysis of the supraspinatus muscle. Clin. Biomech. Bristol Avon. 2000;15(Suppl 1):S13–16. doi: 10.1016/S0268-0033(00)00053-X.
    1. Bradley M, O’Donnell P. Atlas of Musculoskeletal Ultrasound Anatomy. Cambridge University Press; 2010.
    1. Shrout PE, Fleiss JL. Intraclass correlations: Uses in assessing rater reliability. Psychol. Bull. 1979;86:420–428. doi: 10.1037/0033-2909.86.2.420.
    1. Hayes SC, Newton RU, Spence RR, Galvão DA. The Exercise and Sports Science Australia position statement: Exercise medicine in cancer management. J. Sci. Med. Sport. 2019;22:1175–1199. doi: 10.1016/j.jsams.2019.05.003.
    1. Runowicz CD, et al. American Cancer Society/American Society of Clinical Oncology Breast Cancer Survivorship Care Guideline. CA. Cancer J. Clin. 2016;66:43–73. doi: 10.3322/caac.21319.
    1. Pollán M, et al. Exercise and cancer: A position statement from the Spanish Society of Medical Oncology. Clin. Transl. Oncol. Off. Publ. Fed. Span. Oncol. Soc. Natl. Cancer Inst. Mex. 2020;22:1710–1729.
    1. Schmitz KH, et al. Exercise is medicine in oncology: Engaging clinicians to help patients move through cancer. CA. Cancer J. Clin. 2019;69:468–484. doi: 10.3322/caac.21579.
    1. Kokkonen K, et al. The functional capacity and quality of life of women with advanced breast cancer. Breast Cancer Tokyo Jpn. 2017;24:128–136. doi: 10.1007/s12282-016-0687-2.
    1. Heywood R, McCarthy AL, Skinner TL. Efficacy of exercise interventions in patients with advanced cancer: A systematic review. Arch. Phys. Med. Rehabil. 2018;99:2595–2620. doi: 10.1016/j.apmr.2018.04.008.
    1. Scott JM, et al. Feasibility, safety, and efficacy of aerobic training in pretreated patients with metastatic breast cancer: A randomized controlled trial. Cancer. 2018;124:2552–2560. doi: 10.1002/cncr.31368.
    1. Rief H, et al. Feasibility of isometric spinal muscle training in patients with bone metastases under radiation therapy—first results of a randomized pilot trial. BMC Cancer. 2014;14:67. doi: 10.1186/1471-2407-14-67.
    1. Yee J, et al. Physical activity and fitness in women with metastatic breast cancer. J. Cancer Surviv. Res. Pract. 2014;8:647–656. doi: 10.1007/s11764-014-0378-y.
    1. Hughes DC, Ellefsen S, Baar K. Adaptations to endurance and strength training. Cold Spring Harb. Perspect. Med. 2018;8:a029769. doi: 10.1101/cshperspect.a029769.
    1. Dos Santos, W. D. N. et al. Chronic effects of resistance training in breast cancer survivors. BioMed Res. Int.2017, 8367803. 10.1155/2017/8367803 (2017).
    1. Schmitz KH, Ahmed RL, Hannan PJ, Yee D. Safety and efficacy of weight training in recent breast cancer survivors to alter body composition, insulin, and insulin-like growth factor axis proteins. Cancer Epidemiol. Biomark. Prev. Publ. Am. Assoc. Cancer Res. Cosponsored Am. Soc. Prev. Oncol. 2005;14:1672–1680. doi: 10.1158/1055-9965.EPI-04-0736.
    1. Fry AC. The role of resistance exercise intensity on muscle fibre adaptations. Sports Med. 2004;34:663–679. doi: 10.2165/00007256-200434100-00004.
    1. Sheill G, Guinan EM, Peat N, Hussey J. Considerations for exercise prescription in patients with bone metastases: A comprehensive narrative review. PMR. 2018;10:843–864. doi: 10.1016/j.pmrj.2018.02.006.
    1. Møller AB, et al. Molecular and cellular adaptations to exercise training in skeletal muscle from cancer patients treated with chemotherapy. J. Cancer Res. Clin. Oncol. 2019;145:1449–1460. doi: 10.1007/s00432-019-02911-5.
    1. Padilha CS, et al. Evaluation of resistance training to improve muscular strength and body composition in cancer patients undergoing neoadjuvant and adjuvant therapy: A meta-analysis. J. Cancer Surviv. Res. Pract. 2017;11:339–349. doi: 10.1007/s11764-016-0592-x.
    1. LeVasseur N, et al. Perceptions of vascular access for intravenous systemic therapy and risk factors for lymphedema in early-stage breast cancer-a patient survey. Curr. Oncol. Tor. Ont. 2018;25:e305–e310. doi: 10.3747/co.25.3911.
    1. Gencay Can A, Can SS, Ekşioğlu E, Çakcı FA. Is kinesiophobia associated with lymphedema, upper extremity function, and psychological morbidity in breast cancer survivors? Turk. J. Phys. Med. Rehabil. 2019;65:139–146. doi: 10.5606/tftrd.2019.2585.
    1. Velthuis MJ, et al. Role of fear of movement in cancer survivors participating in a rehabilitation program: A longitudinal cohort study. Arch. Phys. Med. Rehabil. 2012;93:332–338. doi: 10.1016/j.apmr.2011.08.014.
    1. Sweegers MG, et al. Effects and moderators of exercise on muscle strength, muscle function and aerobic fitness in patients with cancer: A meta-analysis of individual patient data. Br. J. Sports Med. 2019;53:812. doi: 10.1136/bjsports-2018-099191.
    1. DuMontier C, Clough-Gorr KM, Silliman RA, Stuck AE, Moser A. Health-related quality of life in a predictive model for mortality in older breast cancer survivors. J. Am. Geriatr. Soc. 2018;66:1115–1122. doi: 10.1111/jgs.15340.
    1. Otten L, et al. Impact of sarcopenia on 1-year mortality in older patients with cancer. Age Ageing. 2019;48:413–418. doi: 10.1093/ageing/afy212.
    1. Pin F, Couch ME, Bonetto A. Preservation of muscle mass as a strategy to reduce the toxic effects of cancer chemotherapy on body composition. Curr. Opin. Support. Palliat. Care. 2018;12:420–426. doi: 10.1097/SPC.0000000000000382.
    1. Bozzetti F. Forcing the vicious circle: Sarcopenia increases toxicity, decreases response to chemotherapy and worsens with chemotherapy. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. 2017;28:2107–2118. doi: 10.1093/annonc/mdx271.
    1. Mcleod JC, Stokes T, Phillips SM. Resistance exercise training as a primary countermeasure to age-related chronic disease. Front. Physiol. 2019;10:645. doi: 10.3389/fphys.2019.00645.
    1. Campbell KL, et al. Exercise guidelines for cancer survivors: Consensus statement from international multidisciplinary roundtable. Med. Sci. Sports Exerc. 2019;51:2375–2390. doi: 10.1249/MSS.0000000000002116.
    1. Brown KA, et al. Menopause is a determinant of breast aromatase expression and its associations with BMI, inflammation, and systemic markers. J. Clin. Endocrinol. Metab. 2017;102:1692–1701. doi: 10.1210/jc.2016-3606.
    1. Dieli-Conwright CM, et al. Adipose tissue inflammation in breast cancer survivors: Effects of a 16-week combined aerobic and resistance exercise training intervention. Breast Cancer Res. Treat. 2018;168:147–157. doi: 10.1007/s10549-017-4576-y.

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