Electronic Supplementary Material

Electronic Supplementary Material, Appendix S1. PubMed and Scopus search syntax

“Breast Neoplasms” [MeSH Terms] OR Breast Neoplasms [Text Word] OR Breast

Carcinoma [Text Word] OR Breast Tumo* [Text Word] OR Mammary Carcinoma [Text

Word] OR Breast Cancer [Text Word] OR Cancer, Breast [Text Word] OR Cancer of the

Breast [Text Word] OR “Carcinoma, Ductal, Breast” [MeSH Terms] OR Mammary Ductal

Carcinoma [Text Word] AND "Resistance Training" [MeSH Terms] OR Resistance Training

[Text Word] OR Strength Training [Text Word] OR Resistance exercise [Text Word] OR

"weight lifting"[MeSH Terms] OR weight training [Text Word] OR Weight-lifting [Text

Word] OR "weight-bearing"[MeSH Terms] OR weight-bearing [Text Word] OR weight

bearing [Text Word] OR Resistance exercise program*[text Word]

((TITLE-ABS-KEY("breast cancer" OR "Breast Neoplasms" OR " Breast Carcinoma")) OR

(TITLE-ABS-KEY("Ductal Breast Carcinoma" OR "Mammary Ductal Carcinoma")) OR

(TITLE-ABS-KEY("Breast Tumo*" OR "Mammary Carcinoma" OR "Cancer w/3 Breast")))

AND (TITLE-ABS-KEY("Resistance Training" OR "Strength Training" OR "Resistance

exercise" OR "weight lifting" OR "weight training" OR "weight bearing" OR "Resistance

exercise program*"))

1

Electronic Supplementary Material, Appendix S2. Excluded citations (reason)

1. Basen-Engquist K, Perkins H, Carmack C, et al. Test of a weight gain prevention

intervention in stage II and III breast cancer patients receiving neoadjuvant

chemotherapy. Cancer Epidemiology Biomarkers and Prevention. March 2010;19

(3):895-896. (abstract)

2. Battaglini C, Bottaro M, Dennehy C, et al. The effects of resistance training on

muscular strength and fatigue levels in breast cancer patients. Efeitos do treinamento

de resistência na força muscular e níveis de fadiga em pacientes com câncer de

mama. // 2006;12(3):153-158. (mixed training)

3. Battaglini C, Bottaro M, Dennehy C, et al. The effects of an individualized exercise

intervention on body composition in breast cancer patients undergoing treatment. Sao

Paulo Medical Journal. // 2007;125(1):22-28. (mixed training)

4. Baumann FT, Drosselmeyer N, Knicker A, et al. Effects of a 3-month resistance

training intervention on the cognitive abilities of breast cancer patients during

chemotherapy. Auswirkungen einer 3-monatigen krafttrainings-intervention auf die

kognitiven fähigkeiten von mammakarzinompatientinnen während der chemotherapie.

2009;41(2):70-75. (non-English)

5. Baumann FT, Drosselmeyer N, Leskaroski A, et al. 12-week resistance training with

breast cancer patients during chemotherapy: Effects on Cognitive Abilities. Breast

Care. 2011;6(2):142-143. (non-randomized)

6. Baumann FT, Müller S, Krakowski-Roosen H, Knicker A, Schneider J. Effects of

resistance training during the chemotherapy of breast cancer patients. Isokinetics &

Exercise Science. 2008;16(3):173-173. (abstract)

2

7. Benton MJ, Schlairet MC, Gibson DR. Change in quality of life among breast cancer

survivors after resistance training: is there an effect of age? Journal of aging and

physical activity. Apr 9 2013. (non-randomized, no control group)

8. Brown JC, Troxel AB, Schmitz KH. Safety of weightlifting among women with or at

risk for breast cancer-related lymphedema: musculoskeletal injuries and health care

use in a weightlifting rehabilitation trial. The oncologist. 2012;17(8):1120-1128.

(redundant citation)

9. Brown JC, Troxel AB, Schmitz KH. Musculoskeletal injuries and Healthcare needs

among women with or at-risk for breast-cancer-related lymphedema in a weight lifting

exercise trial. Medicine and Science in Sports and Exercise. May 2012;44:524-524.

(abstract)

10. Brown JC, Troxel AB, Schmitz KH. Musculoskeletal injuries in weight lifting among

women with or at-risk for breast-cancer-related lymphedema. Annals of Behavioral

Medicine. Apr 2012;43:S219-S219. (abstract)

11. Courneya KS, Segal RJ, Gelmon K, et al. Six-month follow-up of patient-rated

outcomes in a randomized controlled trial of exercise training during breast cancer

chemotherapy. Cancer epidemiology, biomarkers & prevention. Dec

2007;16(12):2572-2578. (redundant citation)

12. Crowley SA. The effect of a structured exercise program on fatigue, strength,

endurance, physical self-efficacy, and functional wellness in women with early stage

breast cancer, University of Michigan; 2003. (doctoral thesis)

13. Demark-Wahnefried W, Case LD, Blackwell K, et al. Results of a diet/exercise

feasibility trial to prevent adverse body composition change in breast cancer patients

on adjuvant chemotherapy. Clinical breast cancer. Feb 2008;8(1):70-79. (mixed

training)

3

14. Fernández-Lao C, Cantarero-Villanueva I, Ariza-Garcia A, Courtney C, Fernández-

De-Las-Peñas C, Arroyo-Morales M. Water versus land-based multimodal exercise

program effects on body composition in breast cancer survivors: A controlled clinical

trial. Supportive Care in Cancer. 2013;21(2):521-530. (mixed training)

15. Garner D, Erck EG. Effects of aerobic exercise and resistance training on stage I and

II breast cancer survivors: a pilot study. American Journal of Health Education.

2008;39(4):200-205. (mixed training)

16. Gibbs ZG, Galvao DA, Newton RU. High vs low intensity resistance exercise in late

stage breast cancer patients with lymphedema: A randomised controlled trial. Asia-

Pacific Journal of Clinical Oncology. November 2011;7:118. (abstract)

17. Hayes SC, Speck RM, Reimet E, Stark A, Schmitz KH. Does the effect of weight

lifting on lymphedema following breast cancer differ by diagnostic method: results

from a randomized controlled trial. Breast cancer research and treatment. Nov

2011;130(1):227-234. (redundant citation)

18. Herold J, Leskaroski A, Bloch W, et al. Results of a three months strength training of

breast cancer patients during chemo therapy on the symptom of fatigue. Archives of

Gynecology and Obstetrics. October 2010;282:S115. (abstract)

19. Karen BE, Murray JL, Baum G, Angelica MGB, Arun B. Randomized pilot study of a

weight gain prevention intervention for breast cancer patients receiving neoadjuvant

chemotherapy. Journal of Clinical Oncology. 20 May 2012;1). (abstract)

20. Kilbreah SL, Refshauge KM, Beith JM, Ward LC, Simpson JM, Lee MJ. Post-

operative resistance training for early breast cancer survivors is not associated with

increased prevalence of lymphedema. Cancer Research. Dec 2009;69(24):556S-557S.

(abstract)

4

21. Kilbreath S. Weight training does not promote lymphoedema in breast cancer

survivors. The Australian journal of physiotherapy. 2006;52(4):301. (abstract)

22. Kilbreath S, Refshauge K, Beith J, Lee M. Resistance and stretching shoulder

exercises early following axillary surgery for breast cancer. Rehabilitation Oncology.

2006;24(2):9-14. (redundant citation)

23. Kilbreath S, Refshauge KM, Beith JM, et al. Efficacy of a one-year exercise program

to prevent bone loss in postmenopausal women prescribed aromatase inhibitor

therapy: An RCT. Journal of Clinical Oncology. 20 May 2013;1). (abstract)

24. Kilbreath SL, Refshauge KM, Beith JM, Ward LC, Simpson JM, Lee M. Does a

weekly-supervised, 8-week exercise program improve health-related quality of life for

women treated for breast cancer? Asia-Pacific Journal of Clinical Oncology.

November 2009;5:A157. (abstract)

25. Knobf MT, Insogna K, DiPietro L, Fennie K, Thompson AS. An aerobic weight-

loaded pilot exercise intervention for breast cancer survivors: Bone remodeling and

body composition outcomes. Biological research for nursing. July 2008;10(1):34-43.

(aerobic training)

26. Lite RS, Mejia S. Resistance training for breast cancer survivors. Strength and

Conditioning Journal. Oct 2010;32(5):60-62. (not empirical study)

27. Madzima TA, Simonavice E, Liu PY, et al. Effects of resistance training on muscular

strength, body composition and functionality in breast cancer survivors. Medicine and

science in sports and exercise. May 2012;44:750-750. (abstract)

28. Martin E, Battaglini C, Groff D, Naumann F. Improving muscular endurance with the

MVe Fitness Chair™ in breast cancer survivors: A feasibility and efficacy study.

Journal of Science & Medicine in Sport. 2013;16(4):372-376. (insufficient data)

5

29. Mejia S, Lite RS. Breast cancer and exercise. Strength and Conditioning Journal.

2010;32(5):57-59. (not empirical study)

30. Ott CD, Lindsey AM, Waltman NL, et al. Facilitative strategies, psychological factors,

and strength/weight training behaviors in breast cancer survivors who are at risk for

osteoporosis. Orthopaedic nursing / National Association of Orthopaedic Nurses. Jan-

Feb 2004;23(1):45-52. (no control group)

31. Sander AP. A safe and effective upper extremity resistive exercise program for

women post breast cancer treatment. Rehabilitation Oncology. 2008;26(3):3-10. (non-

randomized)

32. Schmidt T, Weisser B, Jonat W, Baumann FT, Mundhenke C. Gentle strength training

in rehabilitation of breast cancer patients compared to conventional therapy.

Anticancer research. Aug 2012;32(8):3229-3233. (insufficient data)

33. 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 epidemiology, biomarkers & prevention. Jul

2005;14(7):1672-1680. (insufficient data)

34. Schmitz KH, Ahmed RL, Yee D. Effects of a 9-month strength training intervention

on insulin, insulin-like growth factor (IGF)-I, IGF-binding protein (IGFBP)-1, and

IGFBP-3 in 30-50-year-old women. Cancer epidemiology, biomarkers & prevention.

Dec 2002;11(12):1597-1604. (non-breast cancer cohort)

35. Schwartz AL, Cunningham K, King ME, Fow L, Gralow JR. A randomized trial to

examine effects of exercise on bone density and body composition in breast cancer

patients receiving adjuvant chemotherapy. Breast cancer research and treatment.

2001;69(3):305. (abstract)

6

36. Waltman NL, Twiss JJ, Ott CD, et al. The effect of weight training on bone mineral

density and bone turnover in postmenopausal breast cancer survivors with bone loss: a

24-month randomized controlled trial. Osteoporosis international. Aug

2010;21(8):1361-1369. (redundant citation)

37. Winters-Stone KM, Bennett JA, Reiner A, Dobek J, Schwartz A, Nail L. Strength

Training Prevents Bone Loss at the Spine in Older Breast Cancer Survivors:

Preliminary Findings from an RCT. Journal of Bone and Mineral Research. Sep

2008;23:S185-S185. (abstract)

38. Winters-Stone KM, Dobek J, Nail L, Bennett J, Naik A. One Year of Strength

Training Improves Bone Density at the Spine in Older Breast Cancer Survivors.

Medicine and science in sports and exercise. May 2010;42(5):344-344. (abstract)

39. Winters-Stone KM, Dobek J, Nail L, et al. Strength training stops bone loss and builds

muscle in postmenopausal breast cancer survivors: a randomized, controlled trial.

Breast cancer research and treatment. Jun 2011;127(2):447-456. (redundant citation)

40. Winters-Stone KM, Leo MC, Schwartz A. Exercise effects on hip bone mineral

density in older, post-menopausal breast cancer survivors are age dependent. Archives

of osteoporosis. Dec 2012;7(1-2):301-306. (redundant citation)

7

Electronic Supplementary Material, Table S1. Quality items checklist for randomized controlled trials

Study identification

Treatment Allocation (each worth 0.5 points): (1) evidence of randomization method; (2) evidence of concealment of treatment allocation

Were groups similar at baseline regarding the most important prognostic indicators?

Were the eligibility criteria specified?

Were outcomes assessors blinded? (0.5 for partial blinded assessment of outcomes)

Was compliance to the intervention reported?

Ahmed et al, 2006 1.0 1.0 1.0 0.5 1.0

Ohira et al, 2006 1.0 1.0 1.0 0.5 1.0

Courneya et al, 2007 1.0 1.0 1.0 0.0 1.0

Schwartz et al, 2007 0.0 1.0 1.0 0.0 0.0

Twiss et al, 2009 0.5 1.0 1.0 0.0 1.0

Schmitz et al, 2009 1.0 1.0 1.0 1.0 1.0

Schmitz et al, 2010 1.0 1.0 1.0 1.0 1.0

Speck et al, 2010 1.0 1.0 1.0 1.0 1.0

Kim et al, 2010 0.0 1.0 1.0 0.5 0.0

Winters-Stone et al, 2012 1.0 1.0 1.0 1.0 1.0

Musanti, 2012 1.0 1.0 1.0 1.0 1.0

Kilbreath et al, 2012 1.0 1.0 1.0 1.0 1.0

Winters-Stone et al, 2013 1.0 1.0 1.0 1.0 1.0

Cormie et al, 2013 1.0 1.0 1.0 0.0 1.0

Courneya et al, 2013 1.0 1.0 1.0 0.5 1.0

(continued>>>)

8

Were exercise sessions supervised (0.5 for partial supervision)

Were dropouts reported?

Were data presented for primary and secondary outcome measures?

Did the analysis include an intention to treat analysis?

Were adverse events reported?

Total quality score (out of 10)

0.5 1.0 1.0 1.0 1.0 9.0

0.5 1.0 1.0 1.0 1.0 9.0

1.0 1.0 1.0 1.0 1.0 9.0

0.0 1.0 1.0 1.0 0.0 5.0

0.5 1.0 1.0 1.0 1.0 8.0

0.5 1.0 1.0 1.0 1.0 9.5

0.5 1.0 1.0 1.0 1.0 9.5

0.5 1.0 1.0 1.0 1.0 9.5

0.5 0.0 1.0 1.0 1.0 6.0

0.5 1.0 1.0 1.0 1.0 9.5

0.0 1.0 1.0 0.0 1.0 8.0

0.5 1.0 1.0 1.0 0.0 8.5

0.5 1.0 1.0 1.0 1.0 9.5

1.0 1.0 1.0 1.0 1.0 9.0

1.0 1.0 1.0 1.0 1.0 9.5

(<<<continued)

9

Electronic Supplementary Material, Figure S1. Funnel plot assessing the symmetry of the standardized mean difference in arm volume

outcomes between the treatment and control groups

0.1

.2.3

se(S

MD

)

-1 -.5 0 .5SMD

Funnel plot with pseudo 95% confidence limits

10

Electronic Supplementary Material, Figure S2. Funnel plot assessing the symmetry of the standardized mean difference in breast

cancer-related lymphedema symptom severity between the treatment and control groups

0.1

.2.3

se(S

MD

)

-1 -.5 0 .5SMD

Funnel plot with pseudo 95% confidence limits

11

Electronic Supplementary Material, Table S2. Sensitivity analysis of randomized controlled trials investigating upper body muscular

strength

Sensitivity analysis Studies (n) Sample (n) SMD LCL UCL P-value I2 I2 P-value

Fixed effects model 11 1143 0.55 0.43 0.67 <0.001 58.40% 0.008

Exclusion of 2 studies where BCRL was an entry criterion 9 983 0.49 0.29 0.68 <0.001 53.20% 0.029

Exclusion of 4 studies outside the USA 7 618 0.55 0.28 0.82 <0.001 57.50% 0.028

Exclusion of 5 studies that did not include a no-treatment control group 6 626 0.68 0.37 0.99 <0.001 70.60% 0.004

Exclusion of 3 studies that did not prescribe isolated PRT 8 612 0.67 0.44 0.91 <0.001 46.80% 0.068

Exclusion of 1 study in an older cohort (≥60 years) 10 1076 0.60 0.40 0.8 <0.001 57.10% 0.013

Exclusion of 3 studies of shorter duration (≤12 weeks) 8 931 0.58 0.38 0.78 <0.001 53.90% 0.034

Exclusion of 1 study with baseline difference between groups 10 993 0.62 0.43 0.81 <0.001 48.20% 0.043

Exclusion of 3 studies where PRT prescribed during chemotherapy treatment phase 8 765 0.56 0.29 0.83 <0.001 67.10% 0.003

Exclusion of 1 study of lower quality (quality score ≤6.0) 10 1099 0.59 0.38 0.79 <0.001 61.20% 0.006

SMD=standardized mean difference, LCL=lower confidence interval, UCL=upper confidence interval; I2=I-squared statistic

12

Electronic Supplementary Material, Table S3. Sensitivity analysis of randomized controlled trials investigating lower body muscular

strength

Sensitivity analysis Studies (n) Sample (n) SMD LCL UCL P-value I2 I2 P-value

Fixed effects model 9 979 0.48 0.35 0.61 <0.001 46.70% 0.059

Exclusion of 3 studies outside the USA 6 604 0.48 0.21 0.75 <0.001 59.60% 0.03

Exclusion of 4 studies that did not include a no-treatment control group 5 481 0.59 0.26 0.92 <0.001 65.10% 0.022

Exclusion of 2 studies that did not prescribe isolated PRT 7 596 0.51 0.25 0.78 <0.001 57.00% 0.03

Exclusion of 1 study in an older cohort (≥60 years) 8 912 0.51 0.32 0.71 <0.001 48.10% 0.061

Exclusion of 1 study of shorter duration (≤12 weeks) 8 938 0.46 0.27 0.64 <0.001 47.30% 0.066

Exclusion of 1 study with baseline difference between groups 8 857 0.40 0.27 0.54 <0.001 0% 0.763

Exclusion of 3 studies where PRT prescribed during chemotherapy treatment phase 6 601 0.57 0.3 0.84 <0.001 58.50% 0.034

Exclusion of 1 study of lower quality (quality score ≤6.0) 8 935 0.51 0.32 0.7 <0.001 49.20% 0.055

SMD=standardized mean difference, LCL=lower confidence interval, UCL=upper confidence interval; I2=I-squared statistic

13

Electronic Supplementary Material, Table S4. Sensitivity analysis of randomized controlled trials investigating health-related quality of

life

Sensitivity Analysis Studies (n) Sample (n) SMD LCL UCL P-value I2 P-value

Fixed effects model 7 806 0.13 -0.01 0.27 0.06 47.0% 0.079

Exclusion of 2 studies of shorter duration (≤12 weeks) where BCRL was an entry criterion 5 725 0.11 -0.11 0.32 0.33 49.0% 0.097

Exclusion of 4 studies outside the USA 3 378 0.23 -0.11 0.56 0.186 55.7% 0.105

Exclusion of 3 studies that did not include a no-treatment control group 4 501 0.24 0.01 0.46 0.038 29.2% 0.237

Exclusion of 2 studies that did not prescribe isolated PRT 5 568 0.19 -0.02 0.4 0.078 29.5% 0.225

Exclusion of 1 study in an older cohort (≥60 years) 6 739 0.21 -0.01 0.44 0.067 51.7% 0.066

Exclusion of 2 studies where PRT prescribed during chemotherapy treatment phase 5 459 0.3 0.04 0.55 0.023 37.0% 0.174

Exclusion of 1 study of lower quality (quality score ≤6.0) 6 766 0.12 -0.07 0.32 0.213 40.9% 0.132

SMD=standardized mean difference; LCL=lower confidence interval; UCL=upper confidence interval; I2=I-squared statistic

14

Electronic Supplementary Material, Figure S3. Funnel plot assessing the symmetry of the standardized mean difference in upper body

muscular strength between the treatment and control groups

0.1

.2.3

.4.5

se(S

MD

)

-.5 0 .5 1 1.5SMD

Funnel plot with pseudo 95% confidence limits

15

Electronic Supplementary Material, Figure S4. Funnel plot assessing the symmetry of the standardized mean difference in lower body

muscular strength between the treatment and control groups

0.1

.2.3

.4se

(SM

D)

-.5 0 .5 1SMD

Funnel plot with pseudo 95% confidence limits

16

Electronic Supplementary Material, Figure S5. Funnel plot assessing the symmetry of the standardized mean difference in quality of life

between the treatment and control groups

0.1

.2.3

.4se

(SM

D)

-.5 0 .5 1SMD

Funnel plot with pseudo 95% confidence limits

17