Journal List > Korean J Adult Nurs > v.31(5) > 1135962

Park and Jung: Effects of Exercise on Breast Cancer-related Upper Extremity Lymphedema in Breast Cancer Survivors: A Systematic Review and Meta-analysis

Abstract

Purpose

This systematic review and meta-analysis was performed to confirm the effects of exercise on Breast Cancer-Related Lymphedema (BCRL) in breast cancer survivors.

Methods

Totally, 1,614 articles were retrieved from databases including PubMed, Ovid MEDLINE, Embase, Cochrane CENTRAL, CINAHL, Korea Med, Kmbase, KISS, NDSL, KiSTi, and academic journals related to nursing in Korea between June 17 and 18, 2019. Fifteen Randomized Controlled Trials (RCTs) were selected for the analysis from June 19 to July 12, 2019. Cochrane's Risk of Bias assessed the quality and risk of bias of selected articles. Review Manager version 5.3 was used for the meta-analysis.

Results

Studies were published since 2006 including a total of 1,109 participants who were diagnosed with or at risk of BCRL or had undergone surgery for breast cancer treatment. Although exercises were found ineffective for reducing upper extremity edema (Z=0.37, 95% Confidence Interval [CI]=−0.06~0.04, p=.710), they significantly improved shoulder Range of Motion (ROM), especially flexion (Z=5.88, 95% CI=3.06~6.12, p<.001) and abduction (Z=3.41, 95% CI=2.71~10.06, p<.001), upper extremity function (Z=4.02, 95% CI=−12.09~−4.17, p<.001), and Quality of Life (QoL) (Z=3.00, 95% CI=0.13~0.61, p=.003). Egger's regression test assessed publication bias (Intercept=3.75, t=1.79, df=8, p=.111).

Conclusion

Results suggest that exercise is beneficial to BCRL management, especially improvement of shoulder ROM, upper extremity function, and QoL. However, exercise must be performed carefully to prevent side effects. Therefore, nurses should continuously observe signs and symptoms related to BCRL and educate breast cancer survivors on safely performing exercise.

Figures and Tables

Figure 1

Flow diagram for study selection.

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Figure 2

The results of risk of bias.

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Table 1

Characteristics of 15 Studies Included in Systematic Review and Meta-analysis

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ALND=axillary lymph node dissection; BCRL=breast cancer-related lymphedema; BIS=bioimpedance spectroscopy; CDT=complete or complex decongestive therapy; CG=comparison group; CTx=chemotherapy; DLE=distal to the midpoint of the lateral epicondyle; Hormone Tx=hormone therapy; IG=intervention group; MCP joint=metacarpophalangeal joint; MRM=modified radical mastectomy; PLE=proximal to the midpoint of the lateral epicondyle; ROM=range of motion; RTx=radiotherapy; SLNB=sentinel lymph node biopsy; US=ulnar styloid; Studies included in meta-analysis.

Table 2

Effect Measurement of Exercise from the 15 included Studies

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AC=arm circumference; AV=arm volume; CDT=complete or complex decongestive therapy; DASH=diasabilities of arm, shoulder, and hand; ECF=extracellular fluid; FACT-B=functional assessment of cancer therapy for breast cancer; LYMQoL=lymphoedema quality of life questionnaire; PO=primary outcome; QLQ-BR23=Eucopean organization for research and treatment of cancer-breast cancer-specific QoL questionnaire; QLQ-C30=Eucopean organization for research and treatment of cancer QoL questionnaire C30; QoL=quality of life; ROM=range of motion; SF-36=short-form 36 health survey; SO=secondary outcome; Studies included in meta-analysis.

Table 3

The Effects of Exercise on Breast Cancer-related Lymphedema

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CG=comparison group; CI=confidence interval; IG=intervention group; QoL=quality of life; ROM=range of motion; The sample size of [A4] was used as the number that were participating in low-load exercise; The sample size of [A14] was used as the number that were participating in gym exercise.

ACKNOWLEDGEMENT

This work was supported by 2018 Hannam University Research Fund.

Notes

CONFLICTS OF INTEREST The authors declared no conflict of interest.

AUTHORSHIP

  • Study conception and design acquisition - PJ.

  • Data collection - PJ and JM.

  • Analysis and interpretation of the data - PJ and JM.

  • Drafting - PJ and JM.

  • Critical revision of the manuscript - PJ and JM.

  • Final approval - PJ.

Appendix

Appendix 1

Studies included in Systematic Review and Meta-analysis

A1. Kizil R, Dilek B, Şahin E, Engin O, Soylu AC, Akalin E, et al. Is continuous passive motion effective in patients with lymphedema? A randomized controlled trial. Lymphatic Research and Biology. 2018;16(3):263-9.† https://doi.org/10.1089/lrb.2017.0018
A2. Park J-H. The effects of complex exercise on shoulder range of motion and pain for women with breast cancer-related lymphedema: a single-blind, randomized controlled trial. Breast Cancer. 2017;24(4):608-14.† https://doi.org/10.1007/s12282-016-0747-7
A3. Do JH, Kim W, Cho YK, Lee J, Song EJ, Chun YM, et al. Effects of resistance exercises and complex decongestive therapy on arm function and muscular strength in breast cancer related lymphedema. Lymphology. 2015;48(4):184-96.†
A4. Cormie P, Pumpa K, Galvão DA, Turner E, Spry N, Saunders C, et al. Is it safe and efficacious for women with lymphedema secondary to breast cancer to lift heavy weights during exercise: a randomized controlled trial. Journal of Cancer Survivorship. 2013;7(3):413-24.† https://doi.org/10.1007/s11764-013-0284-8
A5. Johansson K, Hayes S, Speck RM, Schmitz KH. Water-based exercise for patients with chronic arm lymphedema: a randomized controlled pilot trial. American Journal of Physical Medicine & Rehabilitation. 2013;92(4):312-9. https://doi.org/10.1097/PHM.0b013e318278b0e8
A6. Jeffs E, Wiseman T. Randomised controlled trial to determine the benefit of daily home-based exercise in addition to selfcare in the management of breast cancer-related lymphoedema: a feasibility study. Supportive Care in Cancer. 2013;21 (4):1013-23. https://doi.org/10.1007/s00520-012-1621-6
A7. Kilbreath SL, Refshauge KM, Beith JM, Ward LC, Lee MJ, Simpson JM, et al. Upper limb progressive resistance training and stretching exercises following surgery for early breast cancer: a randomized controlled trial. Breast Cancer Research and Treatment. 2012;133(2):667-76.† https://doi.org/10.1007/s10549-012-1964-1
A8. Schmitz KH, Ahmed RL, Troxel AB, Cheville A, Lewis-Grant L, Smith R, et al. Weight lifting for women at risk for breast cancer-related lymphedema: a randomized trial. JAMA. 2010; 304(24):2699-705. https://doi.org/10.1001/jama.2010.1837
A9. Kim DS, Sim Y-J, Jeong HJ, Kim GC. Effect of active resistive exercise on breast cancer-related lymphedema: a randomized controlled trial. Archives of Physical Medicine and Rehabilitation. 2010;91(12):1844-8.† https://doi.org/10.1016/j.apmr.2010.09.008
A10. Sagen Å, Kåresen R, Risberg MA. Physical activity for the affected limb and arm lymphedema after breast cancer surgery. A prospective, randomized controlled trial with two years follow-up. Acta Oncologica. 2009;48(8):1102-10. https://doi.org/10.3109/02841860903061683
A11. Speck RM, Gross CR, Hormes JM, Ahmed RL, Lytle LA, Hwang WT, et al. Changes in the body image and relationship scale following a one-year strength training trial for breast cancer survivors with or at risk for lymphedema. Breast Cancer Research and Treatment. 2010;121(2):421-30.† https://doi.org/10.1007/s10549-009-0550-7
A12. Hayes SC, Reul-Hirche H, Turner J. Exercise and secondary lymphedema: safety, potential benefits, and research issues. Medicine & Science in Sports & Exercise. 2009;41(3):483-9.† https://doi.org/10.1249/MSS.0b013e31818b98fb
A13. Ahmed RL, Thomas W, Yee D, Schmitz KH. Randomized controlled trial of weight training and lymphedema in breast cancer survivors. Journal of Clinical Oncology. 2006;24(18): 2765-72. https://doi.org/10.1200/JCO.2005.03.6749
A14. Portela ALM, Santaella CLC, Gómez CC, Burch A. Feasibility of an exercise program for Puerto Rican women who are breast cancer survivors. Rehabilitation Oncology. 2008;26(2):20-31.†
A15. Lee SG. Effects of strengthening exercise and complex decongestive therapy on edema and quality of life for patients with upper lymphedema [master's thesis]. Seoul: Korea University; 2008.†

References

1. International Agency for Research on Cancer. Latest global cancer data: cancer burden rises to 18.1 million new cases and 9.6 million cancer deaths in 2018 [Internet]. Lyon: International Agency for Research on Cancer;2018. cited 2019 August 18. Available from: https://www.iarc.fr/wp-content/uploads/2018/09/pr263_E.pdf.
2. Korean Breast Cancer Society. Breast cancer facts & figures 2018 [Internet]. Seoul: Korean Breast Cancer Society;2018. cited 2019 May 31. Available from: http://www.kbcs.or.kr/sub02/sub04.html.
3. Lee SK, Choi JH, Lim HI, Kim WW, Kim S, Choe J-H, et al. Arm sentinel lymph node detection for preserving the arm lymphatic system. Journal of Breast Cancer. 2009; 12(4):272–277. DOI: 10.4048/jbc.2009.12.4.272.
crossref
4. Rockson SG. Lymphedema after breast cancer treatment. The New England Journal of Medicine. 2018; 379(20):1937–1944. DOI: 10.1056/NEJMcp1803290.
crossref
5. International Society of Lymphology. The diagnosis and treatment of peripheral lymphedema. 2009 Concensus Document of the International Society of Lymphology. Lymphology. 2009; 42(2):51–60.
6. Wanchai A, Armer JM, Stewart BR, Lasinski BB. Breast cancer-related lymphedema: a literature review for clinical practice. International Journal of Nursing Sciences. 2016; 3(2):202–207. DOI: 10.1016/j.ijnss.2016.04.006.
crossref
7. Stuiver MM, ten Tusscher MR, Agasi-Idenburg CS, Lucas C, Aaronson NK, Bossuyt PMM. Conservative interventions for preventing clinically detectable upper-limb lymphoedema in patients who are at risk of developing lymphoedema after breast cancer therapy. The Cochrane database of systematic reviews. 2015; 13(2):CD009765. DOI: 10.1002/14651858.CD009765.pub2.
crossref
8. DiSipio T, Rye S, Newman B, Hayes S. Incidence of unilateral arm lymphoedema after breast cancer: a systematic review and meta-analysis. The Lancet Oncology. 2013; 14(6):500–515. DOI: 10.1016/S1470-2045(13)70076-7.
crossref
9. Taghian NR, Miller CL, Jammallo LS, O'Toole J, Skolny MN. Lymphedema following breast cancer treatment and impact on quality of life: a review. Critical Reviews in Oncology/Hematology. 2014; 92(3):227–234. DOI: 10.1016/j.critrevonc.2014.06.004.
crossref
10. McLaughlin SA, Wright MJ, Morris KT, Giron GL, Sampson MR, Brockway JP, et al. Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: objective measurements. Journal of Clinical Oncology. 2008; 26(32):5213–5219. DOI: 10.1200/JCO.2008.16.3725.
crossref
11. Lee SH, Min YS, Park HY, Jung TD. Health-related quality of life in breast cancer patients with lymphedema who survived more than one year after surgery. Journal of Breast Cancer. 2012; 15(4):449–453. DOI: 10.4048/jbc.2012.15.4.449.
crossref
12. Kilbreath SL, Refshauge KM, Beith JM, Ward LC, Ung OA, Dylke ES, et al. Risk factors for lymphoedema in women with breast cancer: a large prospective cohort. The Breast. 2016; 28:29–36. DOI: 10.1016/j.breast.2016.04.011.
crossref
13. Vassard D, Olsen MH, Zinckernagel L, Vibe-Petersen J, Dalton SO, Johansen C. Psychological consequences of lymphoedema associated with breast cancer: a prospective cohort study. European Journal of Cancer. 2010; 46(18):3211–3218. DOI: 10.1016/j.ejca.2010.07.041.
crossref
14. Smoot B, Wong J, Cooper B, Wanek L, Topp K, Byl N, et al. Upper extremity impairments in women with or without lymphedema following breast cancer treatment. Journal of Cancer Survivorship. 2010; 4(2):167–178. DOI: 10.1007/s11764-010-0118-x.
crossref
15. Cidón EU, Perea C, López-Lara F. Life after breast cancer: dealing with lymphoedema. Clinical Medicine Insights: Oncology. 2011; 5:9–14. DOI: 10.4137/CMO.S6389.
crossref
16. Ridner SH, Sinclair V, Deng J, Bonner CM, Kidd N, Dietrich MS. Breast cancer survivors with lymphedema: glimpses of their daily lives. Clinical Journal of Oncology Nursing. 2012; 16(6):609–614. DOI: 10.1188/12.CJON.609-614.
17. Cook KH, Park MC, Lee IJ, Lim SY, Jung YS. Vascularized free lymph node flap transfer in advanced lymphedema patient after axillary lymph node dissection. Journal of Breast Cancer. 2016; 19(1):92–95. DOI: 10.4048/jbc.2016.19.1.92.
crossref
18. Nelson NL. Breast cancer-related lymphedema and resistance exercise: a systematic review. Journal of Strength and Conditioning Research. 2016; 30(9):2656–2665. DOI: 10.1519/JSC.0000000000001355.
crossref
19. Cheema BS, Kilbreath SL, Fahey PP, Delaney GP, Atlantis E. Safety and efficacy of progressive resistance training in breast cancer: a systematic review and meta-analysis. Breast Cancer Research and Treatment. 2014; 148(2):249–268. DOI: 10.1007/s10549-014-3162-9.
crossref
20. Baumann FT, Reike A, Reimer V, Schumann M, Hallek M, Taaffe DR, et al. Effects of physical exercise on breast cancerrelated secondary lymphedema: a systematic review. Breast Cancer Research and Treatment. 2018; 170(1):1–13. DOI: 10.1007/s10549-018-4725-y.
crossref
21. NLN Medical Advisory Committee. Position Statement of the National Lymphedema Network: exercise [Internet]. New York: National Lymphedema Network;2011. cited 2019 June 7. Available from: https://lymphnet.org/position-papers.
22. Baumann FT, Reike A, Hallek M, Wiskemann J, Reimer V. Does exercise have a preventive effect on secondary lymphedema in breast cancer patients following local treatment? - a systematic review. Breast Care. 2018; 13(5):380–385. DOI: 10.1159/000487428.
crossref
23. Wanchai A, Armer JM. Effects of weight-lifting or resistance exercise on breast cancer-related lymphedema: a systematic review. International Journal of Nursing Sciences. 2019; 6(1):92–98. DOI: 10.1016/j.ijnss.2018.12.006.
crossref
24. Rogan S, Taeymans J, Luginbuehl H, Aebi M, Mahnig S, Gebruers N. Therapy modalities to reduce lymphoedema in female breast cancer patients: a systematic review and meta-analysis. Breast Cancer Research and Treatment. 2016; 159(1):1–14. DOI: 10.1007/s10549-016-3919-4.
crossref
25. Higgins JPT, Green S. Cochrane handbook for systematic reviews of interventions version 5.1.0 [Internet]. London: The Cochrane Collaboration;2011. cited 2019 May 12. Available from: https://handbook-5-1.cochrane.org/.
26. Kim SY, Park JE, Seo HJ, Lee YJ, Son HJ, Jang BH, et al. NECA's guidance for undertaking systematic reviews and meta-analyses for intervention. Seoul: National Evidence-based Healthcare Collaborating Agency;2011. p. 1–165.
27. National Collaborating Centre for Mental Health. Appendix 9. Quality checklists for clinical studies and reviews (NICE clinical guidelines, No.51) [Internet]. Leicester: British Psychological Society;2008. cited 2019 September 11. Available from: https://www.ncbi.nlm.nih.gov/books/NBK53205/.
28. Türk G, Khorshid L. The complete decongestive therapy in lymphedema management developing in relation with mastectomy. The Journal of Breast Health. 2011; 7(2):96–100.
29. Haghighat S. Lotfi-Tokaldany M, Yunesian M, Akbari ME, Nazemi F, Weiss J. Comparing two treatment methods for post mastectomy lymphedema: complex decongestive therapy alone and in combination with intermittent pneumatic compression. Lymphology. 2010; 43(1):25–33.
30. Goddard AA, Pierce CS, McLeod KJ. Reversal of lower limb edema by calf muscle pump stimulation. Journal of Cardiopulmonary Rehabilitation and Prevention. 2008; 28(3):174–179. DOI: 10.1097/01.HCR.0000320067.58599.ac.
crossref
31. Keilani M. Hasenoehrl T, Neubauer M, Crevenna R. Resistance exercise and secondary lymphedema in breast cancer survivors - a systematic review. Supportive Care in Cancer. 2016; 24(4):1907–1916. DOI: 10.1007/s00520-015-3068-z.
32. Gummesson C, Atroshi I, Ekdahl C. The disabilities of the arm, shoulder and hand (DASH) outcome questionnaire: longitudinal construct validity and measuring self-rated health change after surgery. BMC Musculoskeletal Disorders. 2003; 4:11. DOI: 10.1186/1471-2474-4-11.
crossref
33. Buchan J, Janda M, Box R, Schmitz K, Hayes S. A randomized trial on the effect of exercise mode on breast cancer-related lymphedema. Medicine & Science in Sports & Exercise. 2016; 48(10):1866–1874. DOI: 10.1249/MSS.0000000000000988.
crossref
34. Howard-Anderson J, Ganz PA, Bower JE, Stanton AL. Quality of life, fertility concerns, and behavioral health outcomes in younger breast cancer survivors: a systematic review. Journal of the National Cancer Institute. 2012; 104(5):386–405. DOI: 10.1093/jnci/djr541.
crossref
35. 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. Journal of the American Geriatrics Society. 2018; 66(6):1115–1122. DOI: 10.1111/jgs.15340.
crossref
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ORCID iDs

Jaewon Park
https://orcid.org/0000-0002-2167-486X

Miran Jung
https://orcid.org/0000-0001-7482-8706

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