Skip to main content
Download PDF
Download ePub

The associations of muscle-strengthening exercise with recurrence and mortality among breast cancer survivors: a systematic review

International Journal of Behavioral Nutrition and Physical Activity volume 21, Article number: 100 (2024) Cite this article

Abstract

Background

Our systematic review aimed to critically evaluate empirical literature describing the association of muscle-strengthening exercise (MSE) with recurrence and/or mortality among breast cancer survivors.

Methods

We included English-language empirical research studies examining the association between MSE and recurrence and/or mortality among females diagnosed with breast cancer. Seven databases (MEDLINE, PsycINFO, Embase, Scopus, Web of Science, Cochrane CENTRAL, and CINAHL) were searched in September 2023. Quality was appraised using the Mixed Methods Appraisal Tool. Results are summarized descriptively.

Results

Five sources were identified. MSE measurement differed in relation to the description of the MSE (i.e., muscle-strengthening vs. strength training), examples of activities (e.g., sit-ups or push-ups vs. calisthenics vs. circuit training), and exercise frequency (i.e., days vs. times/week). Findings offer provisional evidence that some MSE may lower the hazards of recurrence and mortality. This association may vary by race, weight status, and menopausal status.

Conclusions

In summary, limited available evidence suggests that MSE may lower the hazards of recurrence and mortality. More consistent measurement and analyses would help generate findings that are more readily comparable and applicable to inform clinical practice. Further research is needed to improve understanding of the strength and differences of these associations among underserved and underrepresented women.

Background

Breast cancer is the most commonly diagnosed cancer among women, [1] and among the most costly types of cancer to treat [2]. For instance, one in eight women in the U.S. are diagnosed with breast cancer every year, and there are currently over four million breast cancer survivors in the U.S. [3] The incidence of breast cancer is projected to increase by more than 50% by the year 2050 [4]. However, due to prolonged treatment, breast cancer survivors may experience reduced muscular strength, mobility, and daily activity [5, 6].

Muscle-strengthening exercise (MSE; i.e., resistance / strength / weight training or exercise) can improve short-term outcomes such as anxiety, depression, fatigue, health-related quality of life, lymphedema, and physical function among breast cancer survivors [7,8,9,10]. Therefore, the long-term benefits of MSE on events such as recurrence and mortality may be influenced by improvements in short-term outcomes associated with MSE. Moreover, MSE may also offer benefits relating to recurrence and mortality via the regulation of hormones and cytokines (myokines), as well as changes in body composition resulting in improvements in metabolic regulation and immunity among breast cancer survivors [11,12,13]. As a result, guidelines endorsed by the American Cancer Society (ACS), American College of Sports Medicine (ACSM), and Centers for Disease Control recommend that cancer survivors engage in MSE at least two times per week in addition to aerobic exercise [7]. It is also worth noting that these guidelines are largely based on evidence from trials involving early-stage breast cancer survivors, and that the guidelines do not yet refer to benefits of MSE in relation to recurrence or mortality.

MSE was introduced to U.S. [14] and international [15] guidelines approximately 15–25 years ago. For breast cancer survivors specifically, fewer studies have been designed or published relating to the long-term benefits of MSE in comparison to aerobic exercise, with no review, let alone a meta-analysis, to date. In contrast, over the past five years alone, the association of aerobic exercise with hazards of recurrence and mortality among breast cancer survivors has been the focus of five systematic reviews/meta-analyses encompassing more than 40 articles [16,17,18,19,20]. Thus, compared to aerobic exercise research, research on the association of MSE with recurrence and/or mortality among breast cancer survivors is in its infancy.

In summary, MSE promotion tends to be overlooked in clinical settings, [21] with only 16.5% of breast cancer survivors in the U.S. currently meeting national MSE guidelines compared to 35.7% meeting aerobic guidelines [22]. Thus, the overarching goal of this systematic review was to collate and critically evaluate empirical literature describing the association of MSE with recurrence and/or mortality to support the promotion of MSE among breast cancer survivors in clinical settings.

Methods

We conducted a systematic review following the established Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) guidelines (See Supplement 1 for the PRISMA Checklist) [23, 24]. Synthesis and presentation of findings was based on Cochrane methods [25]. The study was registered in Open Science Framework (doi: https://doi.org/10.17605/OSF.IO/NQRY8).

Eligibility criteria

Our review included English-language empirical research studies examining the independent association between MSE and recurrence and/or mortality among females diagnosed with breast cancer. Inclusion and exclusion criteria are detailed in Table 1 below. In the absence of a prior review, we extended our search back two decades to include the period before and after the introduction of MSE into exercise guidelines in the late 2000s and early 2010s [14, 15].

Table 1 Inclusion and exclusion criteria
Full size table

Information sources

The search strategy was developed by a trained librarian (GB) and included a combination of terms relating to breast cancer, survivorship, exercise (physical activity), recurrence, and mortality. The current review reports on studies that focused on MSE, which were separated from those that focused exclusively on participation in aerobic physical activity. The search strategy was developed using an iterative approach with three rounds by a trained librarian (GB). Each preliminary search was performed in the PubMed/MEDLINE database constrained to research published from January 2003 until September 2023 with English-only language restrictions. The search strategy included a combination of keywords, synonyms, Medical Subject Headings (MeSH) terms, and Emtree terms. The search was performed across the following seven widely used scientific databases: MEDLINE via PubMed (National Library of Medicine), PsycINFO (American Psychological Association), Embase (Elsevier), Scopus (Elsevier), Web of Science Core Collection (Clarivate Analytics), Cochrane CENTRAL (Wiley & Sons), and CINAHL (EBSCO). The date of our search was September 18, 2023. OW and KW performed a pilot test of the preliminary PubMed/MEDLINE search strategy results using Covidence [26]. A sub-sample of those included after full text screening were used to pilot the data extraction tool by OW and KW. Search strategies for each information source are reported in Supplement 2.

Selection process

Database records were imported into EndNote x20 (Clarivate) reference manager software where duplicates were removed. Covidence screening software (Veritas Health Innovation, Melbourne, Australia) was used to further identify duplicates and perform screening eligibility of records [26]. Three co-authors (OW, DK, KW) independently screened both title/abstracts and discrepancies were resolved via discussion.

Data collection process

Data were extracted into Excel to ensure consistency and inter-reviewer reliability. Two authors (KW, OW) extracted information on the study location, study purpose, research design, target population and setting, start and end date, number of participants, data source, statistical analysis technique, demographic information, breast cancer treatment and tumor characteristics, exercise measurement methods, social determinants of health, measure(s) of association, main results, study limitations, funding source, and conflicts of interest. Authors were contacted to attempt to acquire missing information.

Quality appraisal

Article quality was appraised using the Mixed Methods Appraisal Tool (MMAT) [27]. The MMAT includes two screening questions and five items to appraise the quality of quantitative non-randomized research. Items pertain to sample representativeness, measure appropriateness, data completeness, whether confounders are accounted for in design or analysis, and whether changes in the exposure were considered. Each item is appraised as either “yes”, “no”, or “can not tell”. We set the threshold for data completeness at 80% [28]. We used only items 3.1–3.4 from the quantitative non-randomized criteria; additionally, for items 3.2 and 3.4, we focused on the methodology used to assess the association of MSE with recurrence and/or mortality (Table 3).

Effect measures

Where possible, hazard ratios were extracted regarding the association of MSE with recurrence and/or mortality.

Synthesis methods

Due to the heterogeneity in MSE measurement and analytical methods used in published studies, we were unable to summarize the results in a meta-analysis. Therefore, we summarized the study findings using a narrative approach as outlined by Cochrane [25]. Accordingly, we summarized the study characteristics, quality appraisal, muscle-strengthening exercise measurements, guidelines, and MSE effect estimates in a narrative synthesis with accompanying tables offering extra details. This review included a review of published articles and study-level results, and therefore did not require submission for institutional review board approval or exemption.

Certainty

According to Cochrane, narrative approaches to synthesizing results based on statistical significance are severely limited [25]. Our approach to interpreting data is based on an evaluation of the magnitude, direction, and precision of the effect estimates rather than binary significance testing [29]. This approach allowed us to evaluate the clinical relevance of the results in the absence of established minimally clinically important differences for MSE or the reporting of absolute differences in the published studies. Since evidence falls on a continuum, dichotomization into significant vs. non-significant would devalue the information available in the data reported [30, 31].

Results

Study selection

Initial searches retrieved 5,146 sources after removing duplicates. These were screened at the title and abstract levels, followed by a full-text review of the 1,240 remaining sources. We were unable to retrieve full-text copies of three sources via Inter Library Loans or by contacting authors directly. Five articles were identified and proceeded to extraction (Fig. 1). Two studies that included MSE as a part of exercise interventions were excluded, as neither reported on the independent effects of MSE on recurrence and/or mortality [32, 33].

Fig. 1
figure 1

Article identification process using PRISMA research framework [24]

Full size image

Study characteristics

Characteristics describing each article are reported in Table 2. The articles analyzed data collected in the U.S. (N (no. of articles) = 4), [34,35,36,37] and Canada (N = 1) [38]. The review included cross-sectional (N = 2) [34, 38], prospective (N = 2), [35, 37] and retrospective cohort (N = 1) analyses [36]. All articles focused on female breast cancer survivors, and all samples were predominantly White apart from one that focused exclusively on African American women [34]. Most participants also had a favorable socioeconomic status (See Table 2).

Table 2 Study characteristics
Full size table

Quality appraisal

All articles had a clear research question, collected appropriate data to answer research questions, included participants that were representative of the target population, and had complete data. All but one article [34] measured MSE in a way that the proportion of participants meeting MSE guidelines could be determined, and three articles [35,36,37] accounted for confounders in the design and/or analysis (Table 3).

Table 3 Quality appraisal
Full size table

Muscle-strengthening exercise measurement and guidelines

The stated or implied wording of MSE measures differed across articles, where three used muscle-strengthening, [34, 36, 38] and two used strength training [35, 37]. All four articles that included an example of activities mentioned weightlifting or lifting weights, [35,36,37,38] with other exercise examples including sit-ups or push-ups, [38] calisthenics, [36] and circuit training [37]. Four articles measured participation frequency, [34, 36,37,38] two measured duration, [35, 38] and one measured exercise type [38]. Various guidelines (e.g., American College of Sports Medicine) [14, 39,40,41] were stated or implied in three articles [36,37,38]. All studies also examined aerobic exercise. However, only one article reported analyses regarding the association between MSE and mortality while adjusting for aerobic exercise participation (Table 4).

Table 4 Muscle-strengthening exercise measurement and guidelines
Full size table

Association of muscle-strengthening exercise with recurrence and mortality (Table 5)

Recurrence (N = 3)

Troeschel et al. [37] suggest that some MSE (1–2 times/wk) was associated with lower hazards of recurrence compared to none (Hazard Ratio [HR] = 0.81 (95% Confidence Interval [CI]: 0.50, 1.29)), and that more MSE (> 2 times/wk) was associated with higher hazards of recurrence compared to none (HR = 1.26 (0.84, 1.90)). However, in both instances, the data were consistent with parameter values ranging from considerably lower to considerably to considerably higher hazards of recurrence. A small (n = 248) descriptive cross-sectional study found that a higher proportion of women who were recurrence free (24%, n = 57) met MSE guidelines compared to those with recurrence (9%, n = 1) [38], whereas another small (n = 191) cross-sectional study of African American women found no apparent association between MSE and recurrence [34].

Breast cancer-specific mortality (N = 3)

Fortner et al. [35] suggest that some MSE (> 0–1 MET-hrs/wk) was associated with lower hazards of breast cancer-specific mortality compared to none (HR = 0.59 (0.33, 1.05)), and that more MSE (≥ 1 MET-hrs/wk) may be associated with even lower hazards (HR = 0.51 (0.25, 1.02)). These associations were evident even after adjusting for pre-diagnosis MSE. Troeschel et al. [37] reported that some MSE (1–2 times/wk) was associated with lower hazards of breast cancer-specific mortality compared to none (HR = 0.26 (0.08, 0.86)). Unlike Fortner et al., Troeschel et al. [37] reported that more MSE (> 2 times/wk) does not offer appear to offer additional benefits (HR = 0.84 (0.40, 1.76)), with data consistent with parameter values ranging from considerably lower to considerably high hazards of breast cancer-specific mortality. Tarasenko et al. [36] reported no association between meeting MSE guidelines and breast cancer-specific mortality (HR = 0.94 (0.59, 1.49)), but data were consistent with parameter values ranging from considerably lower to considerably higher hazards of breast cancer-specific mortality.

Cardiovascular disease specific mortality (N = 1)

Tarasenko et al. [36] reported that those who met MSE guidelines (HR = 0.69 (0.36, 1.33)) had lower cardiovascular disease specific mortality compared to those who did not. Parameter values ranged from considerably lower to higher hazards of cardiovascular disease specific mortality.

All-cause mortality (N = 3)

Fortner et al. [35] reported that some MSE (> 0–1 MET-hrs/wk) was associated with lower hazards of all-cause mortality (HR = 0.89 (0.64, 1.25)), though data were consistent with parameter values ranging from lower to higher hazards of all-cause mortality. Fortner et al. [35] also reported that more MSE (≥ 1 0 MET-hrs/wk) may offer additional benefits compared to none (HR = 0.61 (0.39, 0.97)). These associations were evident even after adjusting for pre-diagnosis MSE. Troeschel et al. [37] reported that some MSE (1–2 times/wk) was associated with lower hazards of all-cause mortality compared to none (HR = 0.63 (0.41, 0.98)). However, Troeschel et al. also reported that more MSE (> 2 times/wk) may not offer any additional benefits (HR = 0.99 (0.69, 1.42)). Data were consistent with parameter values ranging from lower to higher hazards of all-specific mortality. Tarasenko et al. [36] reported no association between meeting MSE guidelines and all-specific mortality (HR = 0.91 (0.66, 1.26)), but data were consistent with parameter values ranging from lower to higher hazards of all-cause mortality.

Variation based on individual and clinical characteristics

Only Ansa et al., [34] who focused on African American women, examined a sample that was not predominantly White [34]. Sub-group analyses based on BMI reported by Fortner et al. [35] suggest that those with a BMI < 25 kg/m2 only see a reduction in all-cause mortality when participating in high-levels of MSE, whereas some MSE may benefit those with a BMI ≥ 25 kg/m2 and additional MSE offers further benefits. Fortner et al. also reported slightly higher benefits regarding reduced hazards of breast cancer-specific mortality in postmenopausal women compared to the overall sample.

Table 5 Findings on the association of muscle-strengthening exercise with recurrence and mortality among breast cancer survivors
Full size table

Discussion

Findings of our review of the relatively limited available literature (N = 5 studies) tentatively suggest that MSE may lower the hazards of recurrence and mortality among breast cancer survivors [35,36,37,38]. This aligns with the findings regarding MSE in prospective research involving survivors of other cancers in relation to mortality [43]. However, evidence is mixed as to whether additional MSE offered benefits in reducing the hazards of mortality [35, 37]. MSE measurement differed across articles in relation to the description of the MSE (i.e., muscle-strengthening vs. strength training), examples of activities (e.g., sit-ups or push-ups vs. calisthenics vs. circuit training) and exercise frequency (i.e., days vs. times per week). These differences, combined with differences in the categorization of MSE participation and therefore comparison groups within analyses, presented challenges comparing results across articles and prevented formal meta-analysis in the current review.

Our review has several limitations. Our exclusion criteria required articles that examined associations broadly among cancer survivors, and any articles that combined MSE with aerobic exercise into a single exercise variable were excluded. We found no studies on clinical trials evaluating the independent effects of MSE on recurrence and/or mortality among breast cancer survivors. This finding is consistent with a recent systematic review of MSE trials among breast cancer survivors that included 41 articles that reported more than 30 potential benefits of MSE, however, none of these benefits included changes in the risk or hazards of recurrence or mortality [10]. The lack of trial data on the long-term effects of MSE may be explained by the lack of adequate long-term follow up, sample size, and/or power in clinical trials. Over the last two decades, the prognosis of early-stage breast cancer has improved remarkably due to recent advances in breast cancer treatment [1]. For instance, studies report that up to 99% of women diagnosed with early-stage breast cancer could remain event-free up to 5-years following diagnosis [44]. Low event rates and longer event-free intervals among early-stage breast cancer survivors would require a significant investment in large sample sizes and long-term follow-up to quantify the effects of MSE interventions on recurrence and/or mortality in a clinical trial.

With one exception, [35] the isolated association of MSE with recurrence and/or mortality independent of aerobic exercise was not examined. Two articles were cross-sectional, and only three accounted for confounders in analyses [35,36,37]. There was limited information on variations in the association of MSE with recurrence and/or mortality across various individual demographic (e.g., age, race) or clinical characteristics (e.g., stage at diagnosis). All but one article [34] included samples comprised of predominantly White women. As such, it remains unclear how the association of MSE with recurrence/mortality differs across various subgroups of the population, [45,46,47,48] as has been shown when examining the association between aerobic exercise and recurrence/mortality among breast cancer survivors [16, 20, 49,50,51].

The findings of this study may have several implications for future research and clinical practice. Our review of the measures and methods in the existing literature indicates that future research must measure, categorize, and analyze MSE consistently in a transparent manner to facilitate comparison and synthesis of results across studies. Health care providers may find absolute effects (vs. relative) more useful in informing clinical practice [52]. However, in this review, we found no studies that reported absolute benefits of MSE among breast cancer survivors. Therefore, future research should also consider including estimates of absolute (adjusted) differences in addition to the relative differences (e.g., hazard ratios) in the association of MSE with recurrence/mortality. We also found limited data on the possible variations in the association of MSE with recurrence/mortality based on individual demographic, clinical, and contextual characteristics. This data may be necessary in informing personalized exercise prescriptions as recommended by cancer exercise guidelines [7]. For example, it may be necessary to consider a woman’s stage at diagnosis, surgery, treatment, time since treatment completion, and comorbidities when recommending MSE during survivorship care. There was also limited data on the dose-response relationship of MSE with recurrence/mortality which has been reported for aerobic exercise [18]. Therefore, future research should consider providing data on variations in the association of MSE with recurrence/mortality, and the dose-response relationship between MSE and recurrence/mortality. Current cancer survivorship care guidelines recommend that clinicians discuss exercise as a part of the patient’s survivorship care plan [53, 54]. Our findings may offer clinicians with the necessary evidence to help communicate the long-term benefits (e.g., mortality reductions) of MSE in addition to the short-term benefits (e.g., fatigue, physical function, mental health) [7,8,9,10] to breast cancer survivors in clinical settings.

Conclusions

In summary, limited evidence suggests that MSE may reduce the hazards of recurrence and mortality among breast cancer survivors. However, additional research is warranted to understand the magnitude and variation of these associations. Greater consistency in measurement and analyses within MSE research could help generate findings more readily to inform clinical practice.

Data availability

Data sharing is not applicable to this article as no datasets were analyzed or generated during the current review. All the studies summarized in this systematic review are clearly identified within the article.

Abbreviations

MSE:

Muscle-strengthening exercise

References

  1. World Cancer Research Fund. Breast cancer statistics. https://www.wcrf.org/cancer-trends/breast-cancer-statistics/. Accessed February 14, 2024.

  2. Chen S, Cao Z, Prettner K, et al. Estimates and projections of the global economic cost of 29 cancers in 204 countries and territories from 2020 to 2050. JAMA Oncol. 2023;9(4):465–72. https://doi.org/10.1001/jamaoncol.2022.7826.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Giaquinto AN, Sung H, Miller KD, Kramer JL, Newman LA, Minihan A, et al. Breast cancer stat, 2022. CA Cancer J Clin. 2022;72(6):524–41. https://doi.org/10.3322/caac.21754.

    Article  Google Scholar 

  4. Weir HK, Thompson TD, Stewart SL, White MC. Cancer incidence projections in the United States between 2015 and 2050. Prev Chronic Dis. 2021;10:18:E59. https://doi.org/10.5888/pcd18.210006.

    Article  Google Scholar 

  5. Owusu C, Antognoli E, Nock N, Hergenroeder P, Austin K, Bennet E, et al. Perspective of older African-American and non-hispanic white breast cancer survivors from diverse socioeconomic backgrounds toward physical activity: a qualitative study. J Geriatr Oncol. 2018;9(3):235–42. https://doi.org/10.1016/j.jgo.2017.12.003.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kim J, Choi WJ, Jeong SH. The effects of physical activity on breast cancer survivors after diagnosis. J Cancer Prev. 2013;18(3):193–200. https://doi.org/10.15430/jcp.2013.18.3.193.

    Article  Google Scholar 

  7. Campbell KL, Winters-Stone KM, Wiskemann J, et al. Exercise guidelines for cancer survivors: Consensus statement from international multidisciplinary roundtable. Med Sci Sports Exerc. 2019;51(11):2375–90. https://doi.org/10.1249/mss.0000000000002116.

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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 Res Treat. 2014;148(2):249–68. https://doi.org/10.1007/s10549-014-3162-9.

    Article  CAS  Google Scholar 

  9. Gerland L, Baumann Freerk T, Niels T. Resistance exercise for breast cancer patients? Evidence from the last decade. Breast Care. 2021;16(6):657–63. https://doi.org/10.1159/000513129.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Montaño-Rojas LS, Romero-Pérez EM, Medina-Pérez C, Reguera-García MM, de Paz JA. Resistance training in breast Cancer survivors: a systematic review of Exercise Programs. Int J Environ Res Public Health. 2020;7(18). https://doi.org/10.3390/ijerph17186511.

  11. de Boer MC, Wörner EA, Verlaan D, van Leeuwen PAM. The mechanisms and effects of physical activity on breast cancer. Clin Breast Cancer. 2017;17(4):272–278. https://doi.org/10.1016/j.clbc.2017.01.006.

  12. Hong BS, Lee KP. A systematic review of the biological mechanisms linking physical activity and breast cancer. Phys Act Nutr Sep. 2020;24(3):25–31. https://doi.org/10.20463/pan.2020.0018.

    Article  Google Scholar 

  13. Nascimento W, Ferrari G, Martins CB, et al. Muscle-strengthening activities and cancer incidence and mortality: a systematic review and meta-analysis of observational studies. Int J Behav Nutr Phys Act. 2021;249:268. https://doi.org/10.1186/s12966-021-01142-7.

    Article  Google Scholar 

  14. Physical Activity Guidelines Advisory Committee. Physical Activity Guidelines Advisory Committee report. 2008. US Department of Health and Human Services. https://health.gov/sites/default/files/2019-10/CommitteeReport_7.pdf

  15. World Health Organization. Global recommendations on physical activity for health. 2010. https://iris.who.int/bitstream/handle/10665/44399/9789241599979_eng.pdf?sequence=1. Accessed December 10, 2023.

  16. Miyamoto T, Nagao A, Okumura N, Hosaka M. Effect of post-diagnosis physical activity on breast cancer recurrence: a systematic review and meta-analysis. Curr Oncol Rep. 2022;24(11):1645–59. https://doi.org/10.1007/s11912-022-01287-z.

    Article  Google Scholar 

  17. Zagalaz-Anula N, Mora-Rubio MJ, Obrero-Gaitán E, Del-Pino-Casado R. Recreational physical activity reduces breast cancer recurrence in female survivors of breast cancer: a meta-analysis. Eur J Oncol Nurs. 2022;59:102162. https://doi.org/10.1016/j.ejon.2022.102162.

    Article  PubMed  Google Scholar 

  18. Cariolou M, Abar L, Aune D, et al. Postdiagnosis recreational physical activity and breast cancer prognosis: Global Cancer Update Programme (CUP Global) systematic literature review and meta-analysis. Int J Cancer Feb. 2023;15(4):600–15. https://doi.org/10.1002/ijc.34324.

    Article  CAS  Google Scholar 

  19. Lee J. A meta-analysis of the association between physical activity and breast cancer mortality. Cancer Nurs. 2019;42(4):271–85. https://doi.org/10.1097/ncc.0000000000000580.

    Article  Google Scholar 

  20. Spei ME, Samoli E, Bravi F, La Vecchia C, Bamia C, Benetou V. Physical activity in breast cancer survivors: a systematic review and meta-analysis on overall and breast cancer survival. Breast. 2019;44:144–52. https://doi.org/10.1016/j.breast.2019.02.001.

    Article  Google Scholar 

  21. Fairman CM, Zourdos MC, Helms ER, Focht BC. A scientific rationale to improve resistance training prescription in exercise oncology. Sports Med. 2017;47(8):1457–65. https://doi.org/10.1007/s40279-017-0673-7.

    Article  PubMed  Google Scholar 

  22. Cao C, Patel AV, Liu R, Cao Y, Friedenreich CM, Yang L. Trends and cancer-specific patterns of physical activity, sleep duration, and daily sitting time among US cancer survivors, 1997–2018. JNCI. 2023;115(12):1563–75. https://doi.org/10.1093/jnci/djad146.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Moher D, Liberati A, Tetzlaff J, Altman D. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097. https://doi.org/10.1371/journal.pmed.1000097.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. https://doi.org/10.1136/bmj.n71.

    Article  PubMed  PubMed Central  Google Scholar 

  25. McKenzie JE, Brennan SE. Chapter 12: Synthesizing and presenting findings using other methods. In: Higgins J, Thomas J, Chandler J, Cumpston M, Li T, Page M, Welch V, eds. Cochrane Handbook for Systematic Reviews of Interventions. 2024.

  26. Veritas Health Innovation. Covidence systematic review software. www.covidence.org. Accessed August 28, 2023

  27. Hong QN, Pluye P, Fàbregues S et al. Mixed methods appraisal tool (MMAT). 2018. http://mixedmethodsappraisaltoolpublic.pbworks.com/w/file/fetch/127916259/MMAT_2018_criteria-manual_2018-08-01_ENG.pdf. Accessed January 1, 2024.

  28. Zaza S, Wright-De Agüero LK, Briss PA, Truman BI, Hopkins DP. Data collection instrument and procedure for systematic reviews in the guide to community preventive services. Am J Prev Med. 2000;188(Suppl 1):44–74.

    Article  Google Scholar 

  29. Savitz DA, Wise LA, Bond JC, Hatch EE, Ncube CN, Wesselink AK, et al. Responding to reviewers and editors about statistical significance testing. Ann Intern Med. 2024;177(3):385–6. https://doi.org/10.7326/m23-2430

    Article  PubMed  Google Scholar 

  30. Farland LV, Correia KF, Wise LA, Williams PL, Ginsburg ES, Missmer SA. P-values and reproductive health: what can clinical researchers learn from the American Statistical Association? Hum Reprod. 2016;31(11):2406–10. https://doi.org/10.1093/humrep/dew192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Rothman KJ. Random error and the role of statistics. Epidemiology: an introduction. 2nd ed. Oxford Univ; 2012. pp. 148–63.

  32. Hayes SC, Steele ML, Spence RR, Gordon L, Battistutta D, Bashford J, et al. Exercise following breast cancer: exploratory survival analyses of two randomised, controlled trials. Breast Cancer Res Treat. 2018;167(2):505–514. https://doi.org/10.1007/s10549-017-4541-9

  33. Courneya KS, Segal RJ, McKenzie DC et al. Effects of exercise during adjuvant chemotherapy on breast cancer outcomes. Med Sci Sports Exerc. 2014;46(9).

  34. Ansa B, Yoo W, Whitehead M, Coughlin S, Smith S. Beliefs and behaviors about breast cancer recurrence risk reduction among African American breast cancer survivors. Int J Environ Res Public Health. 2015;13(1):ijerph13010046. https://doi.org/10.3390/ijerph13010046.

    Article  CAS  PubMed  Google Scholar 

  35. Fortner RT, Brantley KD, Tworoger SS, et al. Physical activity and breast cancer survival: Results from the Nurses’ Health Studies. JNCI Cancer Spectr. 2023;7(1). https://doi.org/10.1093/jncics/pkac085.

  36. Tarasenko YN, Linder DF, Miller EA. Muscle-strengthening and aerobic activities and mortality among 3 + year cancer survivors in the U.S. Cancer Causes Control. 2018;29(4–5):475–84. https://doi.org/10.1007/s10552-018-1017-0.

    Article  PubMed  Google Scholar 

  37. Troeschel AN, Hartman TJ, McCullough LE, et al. Associations of post-diagnosis lifestyle with prognosis in women with invasive breast cancer. Cancer Epidemiol Biomarkers Prev. 2023;32(7):963–75. https://doi.org/10.1158/1055-9965.Epi-22-1274.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Forbes CC, Blanchard CM, Mummery WK, Courneya K. Prevalence and correlates of strength exercise among breast, prostate, and colorectal cancer survivors. Oncol Nurs Forum. 2015;42(2):118–27. https://doi.org/10.1188/15.Onf.42-02ap.

    Article  PubMed  Google Scholar 

  39. Rock CL, Doyle C, Demark-Wahnefried W, et al. Nutrition and physical activity guidelines for cancer survivors. CA Cancer J Clin. 2012;62(4):242–74. https://doi.org/10.3322/caac.21142.

    Article  Google Scholar 

  40. Schmitz KH, Courneya KS, Matthews C, et al. American College of Sports Medicine roundtable on exercise guidelines for cancer survivors. Med Sci Sports Exerc. 2010;42(7):1409–26. https://doi.org/10.1249/MSS.0b013e3181e0c112.

    Article  PubMed  Google Scholar 

  41. Runowicz CD, Leach CR, Henry NL, Henry KS, Mackey HT, Cowens-Alvarado RL, et al. American cancer society/American society of clinical oncology breast cancer survivorship care guideline. CA Cancer J Clin. 2016;66(1):43–73. https://doi.org/10.3322/caac.21319.

    Article  PubMed  Google Scholar 

  42. Speed-Andrews AE, McGowan EL, Rhodes RE, Blanchard CM, Culos-Reed SN, Friedenreich CM, Courneya KS. Correlates of strength exercise in colorectal cancer survivors. Am J Health Behav. 2013;37(2):162–70. https://doi.org/10.5993/ajhb.37.2.3.

    Article  PubMed  Google Scholar 

  43. Gorzelitz J, Trabert B, Katki HA, Moore SC, Watts E, Matthews CE. Independent and joint associations of weightlifting and aerobic activity with all-cause, cardiovascular disease and cancer mortality in the prostate, lung, colorectal and ovarian Cancer Screening Trial. Br J Sports Med. 2022;56(22):1277–83. https://doi.org/10.1136/bjsports-2021-105315.

    Article  PubMed  Google Scholar 

  44. American Cancer Society. Survival rates for breast cancer. https://www.cancer.org/cancer/types/breast-cancer/understanding-a-breast-cancer-diagnosis/breast-cancer-survival-rates.html. Accessed May 31, 2024.

  45. Sallis JF, Owen N, Fisher EB. Ecological models of health behavior. In: Glanz K, Rimer BK, Viswanath K, editors. Health behavior and health education: Theory, research, and practice. 5th ed. John Wiley & Sons, Inc.; 2015.

  46. National Institute on Minority Health and Health Disparities. NIMHD Research Framework. 2017. https://www.nimhd.nih.gov/docs/research_framework/nimhdResearchFramework.pdf. Accessed August 13, 2023

  47. Centers for Disease Control and Prevention. Physical activity: Data & statistics. https://www.cdc.gov/physicalactivity/data/index.html. Accessed January 31, 2024.

  48. National Physical Activity Plan. NPAP Sectors. https://paamovewithus.org/npap-sectors/. Accessed December 11, 2023.

  49. Ibrahim EM, Al-Homaidh A. Physical activity and survival after breast cancer diagnosis: meta-analysis of published studies. Med Oncol. 2011;28(3):753–65. https://doi.org/10.1007/s12032-010-9536-x.

    Article  Google Scholar 

  50. Schmid D, Leitzmann MF. Association between physical activity and mortality among breast cancer and colorectal cancer survivors: a systematic review and meta-analysis. Ann Oncol. 2014;25(7):1293–311. https://doi.org/10.1093/annonc/mdu012.

    Article  CAS  PubMed  Google Scholar 

  51. Lahart IM, Metsios GS, Nevill AM, Carmichael AR. Physical activity, risk of death and recurrence in breast cancer survivors: a systematic review and meta-analysis of epidemiological studies. Acta Oncol. 2015;54(5):635–54. https://doi.org/10.3109/0284186x.2014.998275.

    Article  Google Scholar 

  52. Irwig L, Irwig J, Trevena L, Sweet M. Chapter 18, relative risk, relative and absolute risk reduction, number needed to treat and confidence intervals. In: Irwig L, Irwig J, Trevena L, Sweet M, editors. Smart Health choices: making sense of Health advice. Hammersmith; 2008.

  53. American Cancer Society. ASCO Cancer Treatment and Survivorship Care Plans. https://www.cancer.org/cancer/survivorship/long-term-health-concerns/survivorship-care-plans.html. Accessed July 1, 2024

  54. American College of Surgeons. Optimal Resources for Breast Cancer: 2024 Standards. 2023. https://accreditation.facs.org/accreditationdocuments/NAPBC/Standards/Optimal_Resources_for_Breast_Care_2024.pdf. Accessed December 30, 2023

  55. National Breast Cancer Foundation. Stages. https://www.nationalbreastcancer.org/breast-cancer-staging/. Accessed October 27, 2023

  56. Canadian Society for Exercise P. Canadian 24-Hour Movement Guidelines for Children and Youth: An integration of physical activity, sedentary behaviour and sleep. https://csep.ca/2016/07/18/canadian-24-hour-movement-guidelines-for-children-and-youth-an-integration-of-physical-activity-sedentary-behaviour-and-sleep/

  57. American College of Sports Medicine. ACSM’s guidelines for exercising testing and prescription. 10th ed. American College of Sports Medicine; 2018.

Download references

Acknowledgements

The authors would like to acknowledge Kaylee Sanger and Lauren Cooper who assisted with screening.

Funding

Oliver W.A. Wilson, Kaitlyn Wojcik, and Dalya Kamil were supported by the Division of Intramural Research at the National Institute on Minority Health and Health Disparities of the National Institutes of Health. Jinani Jayasekera was supported by the Division of Intramural Research at the National Institute on Minority Health and Health Disparities of the National Institutes of Health and the National Institutes of Health Distinguished Scholars program (MD000022, Jayasekera). Charles Matthews was supported by the Division of Cancer Epidemiology and Genetics at the National Cancer Institute. Jess Gorzelitz is supported by an NCI Diversity supplement (3R01CA254628-03S1).

Author information

Authors and Affiliations

  1. Health Equity and Decision Sciences Research Laboratory, Division of Intramural Research, National Institute of on Minority Health and Health Disparities, National Institutes of Health, Bethesda, MD, 20892, USA

    Oliver W.A. Wilson, Kaitlyn M. Wojcik, Dalya Kamil & Jinani Jayasekera

  2. Department of Health and Human Physiology, University of Iowa, Iowa City, IA, USA

    Jessica Gorzelitz

  3. Office of Research Services, National Institutes of Health Library, Bethesda, MD, USA

    Gisela Butera

  4. Metabolic Epidemiology Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA

    Charles E. Matthews

Authors
  1. Oliver W.A. Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kaitlyn M. Wojcik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dalya Kamil
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jessica Gorzelitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gisela Butera
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Charles E. Matthews
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jinani Jayasekera
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the conception and design of this review. OW, KW, and DK completed screening and data extraction of articles. All authors contributed to the acquisition, analysis, and interpretation of data, drafting the work, or revising it critically for important intellectual content, and final approval of the version to be published. All authors agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Jinani Jayasekera.

Ethics declarations

Disclaimer

The contents and views in this manuscript are those of the authors and should not be construed to represent the views of the National Institutes of Health. Opinions and comments expressed in this paper belong to the authors and do not necessarily reflect those of the U.S. Government, Department of Health and Human Services, National Institutes of Health, the National Institute on Minority Health and Health Disparities, or National Cancer Institute. The review funders had no role in the design of the review, the collection, analysis, or interpretation of the data, the writing of the manuscript, or the decision to submit the manuscript for publication.

Ethical approval

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wilson, O.W., Wojcik, K.M., Kamil, D. et al. The associations of muscle-strengthening exercise with recurrence and mortality among breast cancer survivors: a systematic review. Int J Behav Nutr Phys Act 21, 100 (2024). https://doi.org/10.1186/s12966-024-01644-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12966-024-01644-0

Keywords

International Journal of Behavioral Nutrition and Physical Activity

ISSN: 1479-5868

Contact us