Methods to improve rehabilitation of patients following breast cancer surgery: a review of systematic reviews

Figures & data

Table 1 PICOS inclusion and exclusion criteria

	Inclusion criteria	Exclusion criteria
Population	Adults aged 18 years and over Women with post-operation breast cancer	Children and adolescents Participants involving men Co-morbidity physical (such as severe cardiac disease and hypertension) and psychiatric illnesses Women with metastatic cancer
Interventions	Physical and occupational therapy (eg, complex decongestive therapy, manual lymph drainage, standard physiotherapy, occupational therapy) Exercise (eg, exercise therapy, home based exercise routine, weight training) Psychosocial (eg, CBT, psycho-education) Alternative/complementary (eg, hypnotherapy, acupuncture, homeopathy, yoga) Nutritional (eg, dietary regime) Complex (eg, combination of psycho-education and nutrition etc rehabilitation) Reviews on pharmacological therapies and alternative medicine may be included if other rehabilitation methods mentioned above were also reviewed	Pharmacological therapies Alternative medicine – eg, Chinese medicine herbal
Comparator (eg, control)	Systematic reviews of RCT interventions, cross-sectional studies, qualitative studies with or without control/comparison groups	None
Outcomes	Physical (eg, lymphedema, shoulder mobility) Psychosocial (eg, anxiety, depression, affect/mood, QoL) Occupational (eg, return to work, occupational gap, lifestyle) Cognition (eg, “chemo-brain”, cognitive functioning)	None
Study design	Systematic reviews (systematic reviews of RCTs, non-randomized studies, cross-sectional, qualitative studies, etc) English language Dated from January 2009 to October 2014	Individual studies (RCTs, non-randomized studies, cross-sectional, qualitative, etc) Meta-analysis of studies Systematic reviews dated before January 2009 Systematic reviews with too few included studies (less than four included studies) Systematic reviews with too few databases searched (less than three electronic searches)

Abbreviations: RCTs, randomized controlled trials; PICOS, Population, Intervention, Comparator, Outcomes, and Study designs; CBT, cognitive behavior therapy; QoL, quality of life.

Figure 1 Flow diagram of systematic review process.

Abbreviation: RCTs, randomized controlled trials.

Table 2 A 11-item “assessment of multiple systematic reviews” (AMSTAR) for assessing systematic reviews

The AMSTAR tool

1. Was an “a priori” design provided?

2. Was there duplicate study selection and data extraction?

3. Was a comprehensive literature search performed? At least two electronic sources, include years and databases used (eg, Central, EMBASE, and MEDLINE).

4. Was the status of publication (ie, grey literature) used as an inclusion criterion?

5. Was a list of studies (included and excluded) provided?

6. Were the characteristics of the included studies provided?

7. Was the scientific quality of the included studies assessed and documented?

8. Was the scientific quality of the included studies used appropriately in formulating conclusions?

9. Were the methods used to combine the findings of studies appropriate?

10. Was the likelihood of publication bias assessed?

11. Was the conflict of interest included?

Table 3 AMSTAR (assessment of multiple systematic reviews) checklist

The AMSTAR Tool	Chan et al^Citation37 (2010)	McNeely et al^Citation38 (2010)	Paramanandam and Roberts^Citation39 (2014)	Fors et al^Citation40 (2011)	Hoving et al^Citation41 (2009)	Juvet et al^Citation22 (2009)	Selamat et al^Citation7 (2014)
1. Was an “a priori” design provided?
Yes	√	√	√	√	√	√	√
No	–	–	–	–	–	–	–
Can’t answer	–	–	–	–	–	–	–
Not applicable	–	–	–	–	–	–	–
2. Was there duplicate study selection and data extraction?
Yes	√	√	√	√	–	√	√
No	–	–	–	–	√	–	–
Can’t answer	–	–	–	–	–	–	–
Not applicable	–	–	–	–	–	–	–
3. Was a comprehensive literature search performed?
Yes	√	√	√	√	√	√	–
No	–	–	–	–	–	–	√
Can’t answer	–	–	–	–	–	–	–
Not applicable	–	–	–	–	–	–	–
4. Was the status of publication (ie, grey literature) used as an inclusion criterion?
Yes	–	√	–	–	–	–	–
No	√	–	√	√	√	√	√
Can’t answer	–	–	–	–	–	–	–
Not applicable	–	–	–	–	–	–	–
5. Was a list of studies (included and excluded) provided?
Yes	√	√	–	–	–	√	–
No	–	–	√	√	√		√
Can’t answer	–	–	–	–	–	–	–
Not applicable	–	–	–	–	–	–	–
6. Were the characteristics of the included studies provided?
Yes	√	√	√	√	√	√	√
No	–	–	–	–	–	–	–
Can’t answer	–	–	–	–	–	–	–
Not applicable	–	–	–	–	–	–	–
7. Was the scientific quality of the included studies assessed and documented?
Yes	√	√	√	√	–	√	√
No	–	–	–	–	√	–	–
Can’t answer	–	–	–	–	–	–	–
Not applicable	–	–	–	–	–	–	–
8. Was the scientific quality of the included studies used appropriately in formulating conclusions?
Yes	–	√	–	√	–	√	–
No	√	–	√	–	√	–	√
Can’t answer	–	–	–	–	–	–	–
Not applicable	–	–	–	–	–	–	–
9. Were the methods used to combine the findings of studies appropriate?
Yes	√	√	√	√	–	√	–
No	–	–	–	–	√	–	√
Can’t answer	–	–	–	–	–	–	–
Not applicable	–	–	–	–	–	–	–
10. Was the likelihood of publication bias assessed?
Yes	–	√	√	–	–	–	–
No	√	–	–	√	√	√	√
Can’t answer	–	–	–	–	–	–	–
Not applicable	–	–	–	–	–	–	–
11. Was the conflict of interest included?
Yes	√	√	√	–	√	–	√
No	–	–	–	√	–	√	–
Can’t answer	–	–	–	–	–	–	–
Not applicable	–	–	–	–	–	–	–
Overall score	8/11	11/11	7/11	7/11	4/11	8/11	5/11
	High quality	High quality	Moderate quality	Moderate quality	Low quality	High quality	Moderate quality

Table 4 Characteristics of systematic reviews on rehabilitation methods after breast cancer surgery

No	Review, year	Type of rehabilitation method	Aim	Search strategy	Inclusion and exclusion criteria	No of studies included	Total number and age of participants	Assessed outcomes
1	Chan et al^Citation37 (2010)	Exercise	To review the efficacy of exercise programs on shoulder function and lymphedema in post-operative patients with breast cancer having ALND, as revealed by RCT.	Databases: Cumulative Index to Nursing and Allied Health Literature, Ovid MEDLINE, the British Nursing Index, Proquest, ScienceDirect, PubMED, Scopus and the Cochrane Library Published articles between 2000 and 2009 Search terms: breast cancer, exercise, lymphoedema, shoulder mobility, randomized controlled trials. Limited to English language articles	Inclusion: RCT, published in English. Intervention: various types of exercise programs – weight training, aerobic and strengthening exercises, stretching and range of motion (ROM) exercises. Outcome: range of shoulder motion, arm mobility, arm volume (at least one of these outcome variables). Exclusion: therapeutic intervention which only reported decongestive therapy involving MLD, compression garments and/or skin care, studies dealing with patients undergoing SLNB	6 RCTs	429 (range: 27–205); mean age of the participants was <60 years	Shoulder mobility and lymphedema: range of shoulder motion, shoulder mobility, arm circumference and arm volume
2	McNeely et al^Citation38 (2010)	Exercise	To examine the evidence of efficacy from RCTs involving exercise for preventing, minimizing and/or improving upper-limb dysfunction due to breast cancer treatment.	Databases: Cochrane Breast Cancer Group Specialised Register, MEDLINE, EMBASE, PEDro, LILACS No language restriction Search strategy: specified Published and unpublished up to 2008	Inclusion: adults: 17 years and older. Interventions – therapeutic exercise interventions for the upper-limb therapy program: 1) ROM exercises; 2) Passive ROM/manual stretching exercises; 3) Stretching exercises; 4) Strengthening or resistance exercises. Outcomes: upper-extremity ROM, muscular strength, lymphedema and pain, upper-extremity/shoulder function and QoL, early post-operative complications such as seroma formation, post-operative wound drainage, wound healing and effect modifiers such as adherence to exercise.	24 RCTs	2,132; mean age of participants ranged from 46.3 to 62.1 years	Primary outcomes: upper-extremity ROM, muscular strength, lymphedema and pain Secondary outcomes: upper-extremity/shoulder function (eg, reaching overhead, fastening a brassiere, doing a zipper up from behind) and QoL, early post-operative complications such as seroma formation, post-operative wound drainage, wound healing and effect modifiers such as adherence to exercise.
3	Paramanandam and Roberts^Citation39 (2014)	Weight training exercise	To investigate whether weight-training exercise intervention is harmful to women with or at risk of breast cancer related lymphedema.	Databases: PubMED, EMBASE, PsycINFO, CINAHL, AMED, Cochrane, PEDro, SPORTDiscus and Web of Science. Search terms: specified Published after 2001–2012	Inclusion: Design – RCTs, peer reviewed, published in English after 2001. Population – women at risk of developing lymphedema. Intervention – weight-training exercises outcomes – lymphedema, strength, QoL, comparison – sham exercise, no-intervention control, only lower body exercises and education	11 RCTs	1,091; age of participants ranged from 49 to 57 years	Lymphedema onset or exacerbation, limb strength, QoL, BMI
4	Fors et al^Citation40 (2011)	Psychosocial	To determine the efficacy of psycho-education, CBT and social support interventions used in rehabilitation of breast cancer patients.	Databases: Cochrane Library, The Centre for Reviews and Dissemination databases, Medline, Embase, Cinahl, PsycINFO, AMED, PEDro Published articles between 1999 and 2008 Search terms: specified in Juvet et al^Citation22 (2009)	Inclusion: RCTs investigating the effect of psychosocial rehabilitation with ≥20 female breast cancer Exclusion: low quality studies, less than 20 participants in each group, patients with metastatic cancer, data not presented separately for breast cancer and studies with other types of cancer	18 RCTs	3,272; N/A	QoL, fatigue, mood, health behavior, social functioning
5	Hoving et al^Citation41 (2009)	Occupational rehabilitation	To determine the effects of interventions on breast cancer survivors on return to work.	Databases: Ovid Medline, EMBASE, PsycInfo and the Cochrane Controlled Trials Register (The Cochrane Library, Issue 4, 2006) Published articles between 1970 and 2007 Search term: specified	Inclusion: types of studies: RCTs, cohort studies and observational studies, Interventions: all non-pharmacological interventions, types of outcome measures: work-related outcomes such as return to work, absenteeism, work disability, sick leave or employment status	4 studies (1 controlled study, 3 uncontrolled studies)	1,172; N/A	Return to work, absenteeism, work disability, sick leave or employment status
6	Juvet et al^Citation22 (2009)	Physical exercise, physiotherapy, psychosocial interventions, nutrition, complementary treatment, complex interventions	To assess the efficacy of single treatments and combination of treatments with respect to improvements in physical function and psychological wellbeing.	Databases: Cochrane Library, The Centre for Reviews and Dissemination databases, Medline, Embase, Cinahl, PsycINFO, AMED, PEDro Published articles up until 2008 Search term: specified	Inclusion: study design: RCTs. Physical exercise, therapy, psychosocial interventions, nutritional complementary or complex interventions. Outcomes: somatic, psycho-social outcomes. Exclusion: low quality studies, studies with less than 20 per arm	46 RCTs	5,645; N/A	Outcomes: somatic, psychological, and social outcomes
7	Selamat et al^Citation7 (2014)	Cognitive rehabilitation	To review qualitative studies that explored the life/daily experiences of “chemo-brain” among breast cancer survivors, with particular attention given to the impact of “chemo-brain” on daily living and quality of life.	Databases: CINAHL, Web of Knowledge, EMBASE, Proquest, OVID SP, MEDLINE, Oxford Journal, ScienceDirect, PubMED, Wiley Published from 2002 to 2014. English language text Search terms: specified	Inclusion: breast cancer and “chemo-brain”, qualitative study, studies published from 2002 to 2014, English publication. Exclusion: study design other than a qualitative design Methodology, studies with patients with cancers other than breast cancer, non-English papers	7 qualitative studies	193; N/A	Cognitive functioning or “chemo-brain”: Perception of “chemo-brain”, coping strategies towards cognitive dysfunction, self- management in being breast cancer survivor

Abbreviations: ALND, axillary lymph node dissection; BMI, body mass index; CBT, cognitive behavior therapy; CPT, mastectomy; MLD, manual lymph drainage; N/A, not assessed; QoL, quality of life; RCTs, randomized controlled trials; SLNB, sentinel lymph node biopsy.

Table 5 Results of studies on rehabilitation methods on physical outcomes

	Chan et al^Citation37 (2010)	McNeely et al^Citation38 (2010)	Paramanandam and Roberts^Citation39 (2014)	Fors et al^Citation40 (2011)	Juvet et al^Citation22 (2009)
Outcomes
Upper body symptoms	Exercise: shoulder movement – overall improvement in shoulder mobility, irrespective of time period of implementation. However, most exercise programs were implemented soon after operation. Improvement in flexion and abduction movement measurements of the shoulder joint was significantly better in treatment groups. Most studies had used a goniometer to measure range of motion.	Exercise: shoulder movement – delayed versus early – (ten studies). Early exercise was more effective than delayed in the short-term recovery of shoulder flexion ROM. Structured exercise versus usual care (14 studies) – six were post-operative, three during adjuvant treatment and five following cancer treatment. Structured exercise programs in the post-operative period improved shoulder flexion ROM in the short-term and yielded additional benefit for shoulder function post-intervention and at 6-month follow-up.	Exercise: weight training exercise – limb strength of low to moderate intensity with relatively slow progression improved the upper limb strength and lower limb strength	–	Physiotherapy: shoulder movement – of the seven RCTs examining the effect of physiotherapy, three investigated shoulder function. Shoulder mobility improved after physiotherapy, but results were influenced by type of surgery (ie, BCT or MRM). There is a lack of high quality studies to guide conclusion on the effect of physiotherapy interventions to improve shoulder function after breast cancer surgery. Complex intervention: shoulder movement – inconclusive results. Only one study (psycho-education and exercise) investigated effect on shoulder mobility (ROM) with improvements found in the intervention group. Arm movement – inconclusive results
Lymphedema	Exercise: no significant change in incidence of lymphedema in studies involving upper limb exercise. Mean change in arm circumferences in different positions ranged from 0.10 to 0.30 cm, which was not significant. There was minimal difference in arm volume. In two studies a difference of only 0.70 and 2 mL was noted between groups.	Exercise: structured exercise versus usual care – there was no evidence of increased risk of lymphedema from exercise at any time point.	Exercise: weight training exercise of low to moderate intensity with relatively slow progression does not increase arm volume or incidence of lymphedema	–	Physiotherapy: inconclusive results (lack of high quality studies). Of the seven RCTs examining physiotherapy, four studied the effects on arm lymphedema. MLD (three studies) – no significant benefit of MLD. One study showed a decrease in lymphedema with complex decongestive therapy (lymph drainage, compression bandage, evaluation, medical exercise, and skin care) compared to SLNB. Three studies showed that effect of physiotherapy is not influenced by timing. Six studies are done after ALND and not after SLNB, while one study was done in mixed ALND and SLNB population Exercise: moderate level of evidence. Three studies showed that early exercise was not associated with aggravated lymphedema
Wound healing	–	Exercise: delayed versus early – early exercise resulted in significant increase in wound drainage volume.	–	–	–
Body composition	–	–	Exercise: weight training exercise of low to moderate intensity with relatively slow progression – no significant effects for BMI	–	Exercise: inconclusive results for BMI Nutrition: two RCTs. Inconclusive results on body weight Complex: inconclusive results on body composition
Fatigue	–	–	–	Psycho-education: overall significant short-term benefit for fatigue was observed CBT – inconclusive results. Modest short-term benefit on fatigue was found in one study reviewed	Exercise: inconclusive results. Three studies showed that exercise after primary treatment may reduce fatigue. Exercise intervention during primary cancer treatment showed varied result. Psycho-education: inconclusive results. CBT: inconclusive results. Social and emotional support intervention: inconclusive results
Hot flashes	–	–	–	–	Complementary/alternative rehabilitation: inconclusive results. Incidence of hot flashes was addressed in two studies, relaxation training intervention reduced the incidence, while acupuncture also reduced but did not reach statistical significance

Abbreviations: ALND, axillary lymph node dissection; BCT, breast conservative therapy; BMI, body mass index; CBT, cognitive behavior therapy; MRM, modified radical mastectomy; MLD, manual lymph drainage; RCTs, randomized controlled trials; ROM, range of motion; SLNB, sentinel lymph node biopsy.

Table 6 Results of studies on rehabilitation methods on psychosocial, occupational, and cognitive outcomes

	Paramanandam and Roberts^Citation39 (2014)	Fors et al^Citation40 (2011)	Hoving et al^Citation41 (2009)	Juvet et al^Citation22 (2009)	Selamat et al^Citation7 (2011)
Outcomes
Psychosocial: quality of life	Exercise: weight training exercise of low to moderate intensity with relatively slow progression. Inconclusive results. Some aspects of QoL may improve with weight training.	Psycho-education: inconclusive results. No significant increase in QoL. Three RCTs on effect of the interventions during and another three on effects after primary treatment CBT: seven trials on CBT, four on after versus three during primary treatment. Overall significant short-term increase in QoL. Social and emotional support interventions: inconclusive impact (five studies).	–	Exercise: moderate level of evidence (ten studies). Four studies showed that exercise after primary treatment may improve short-term QoL. Psycho-education: six RCTs on psycho-educational. Inconclusive results. CBT: seven RCTs examined CBT. Inconclusive results. Social and emotional support – five studies. Inconclusive results. Complementary: five studies. Small effect on the QoL.	–
Psychosocial: health behaviors	–	Inconclusive results for all types of interventions	–	CBT: inconclusive results Social and emotional support intervention: inconclusive results	–
Psychosocial: social function and coping	–	Inconclusive results for all types of interventions	–	Social and emotional support intervention: inconclusive results Complementary: inconclusive results	–
Psychosocial: mood	–	Psycho-education: inconclusive results CBT: inconclusive results on mood. Social and emotional support: inconclusive results. Improvement seen on the POMS scale, but not on HADS and MAC scales	–	Exercise: inconclusive results. Psycho-education: inconclusive results. CBT: inconclusive results. Improved mood – three CBT studies measured mood (anxiety, event related distress and depression) Social and emotional support – inconclusive results Complementary rehabilitation: small effect on mood outcomes	–
Cognitive: cognitive dysfunction	–	–	–	–	Five studies on self-management rehabilitation. Psychosocial interventions and practical reminders were good coping strategies. With cultural differences in coping strategies Asians are more likely to use complementary medicine
Occupational: return to work	–	–	Inconclusive results – counseling or exercise – as three studies had no comparison group. Longer time needed to return to work was related to more extensive surgical procedures.	–	–

Abbreviations: CBT, cognitive behavior therapy; HADS, Hospital Anxiety and Depression Scale; MAC, the Mental Adjustment to Cancer; POMS, Profile of Mood States; QoL, quality of life; RCTs, randomized controlled trials.

Table S1 Screening inclusion/exclusion table

Study reference	Dated 2009–2014?	Exercise, physiotherapy, psychosocial, nutrition or alternative rehabilitation?	Published systematic review in English?	Review include adult breast cancer survivors after surgery?	Four included studies or more per systematic review?	More than two databases searched?	Non-metastatic, no physical co-morbidity?	Measure more than one component of physical, psycho-social, cognitive, or occupational outcomes?	Decision
40. Fors EA, Bertheussen GF, Thune I, et al. Psychosocial interventions as part of breast cancer rehabilitation programs? Results from a systematic review.	1	1	1	1	1	1	1	1	Yes (include)
41. Hoving JL, Broekhuizen ML, Frings-Dresen MH. Return to work of breast cancer survivors: a systematic review of intervention studies.	1	1	1	1	1	1	1	1	Yes
22. Juvet LK, Elvsaas IK, Leivseth G, et al. Rehabilitation of breast cancer patients.	1	1	1	1	1	1	1	1	Yes
38. McNeely ML, Campbell K, Ospina M, et al. Exercise interventions for upper-limb dysfunction due to breast cancer treatment.	1	1	1	1	1	1	1	1	Yes
39. Paramanandam VS, Roberts, D Weight training is not harmful for women with breast cancer-related lympho-edema: a systematic review.	1	1	1	1	1	1	1	1	Yes
7. Selamat MH, Loh SY, Mackenzie L, Vardy J. Chemobrain Experienced by Breast Cancer Survivors: A Meta-Ethnography Study Investigating Research and Care Implications. PloS one, 9(9), e108002.	1	1	1	1	1	1	1	1	Yes
37. Chan DN, Lui LY, So WK. Effectiveness of exercise programmes on shoulder mobility and lympho-edema after axillary lymph node dissection for breast cancer: systematic review.	1	1	1	1	1	1	1	1	Yes
42. E Lima MT, E Lima JG, de Andrade MF, Bergmann A. Low-level laser therapy in secondary lymphedema after breast cancer: systematic review.	1	1	1	1	1	1	1	0	No (exclude)
43. Huang TW, Tseng SH, Lin CC, et al. Effects of manual lymphatic drainage on breast cancer-related lymphedema: a systematic review and meta-analysis of randomized controlled trials.	1	1	1	1	1	1	1	0	No
44. Johannsen M, Farver I, Beck N, Zachariae R. The efficacy of psychosocial intervention for pain in breast cancer patients and survivors: a systematic review and meta-analysis.	1	1	1	1	1	1	1	0	No
45. Khan F, Amatya B, Ng L, Demetrios M, Zhang NY, Turner-Stokes L. Multidisciplinary rehabilitation for follow-up of women treated for breast cancer.	1	1	1	1	0	1	1	1	No
46. Markes M. Exercise for women receiving adjuvant therapy of breast-cancer: a systematic review.	1	1	0	1	1	1	1	1	No
47. Moseley AL, Carati CJ, Piller NB. A systematic review of common conservative therapies for arm lymphoedema secondary to breast cancer treatment.	0	1	1	1	1	1	1	0	No
48. Shamley DR, Barker K, Simonite V, Beardshaw A. Delayed versus immediate exercises following surgery for breast cancer: a systematic review.	0	1	1	1	1	1	1	1	No
8. Chung C, Lee S, Hwang S, Park E. Systematic Review of Exercise Effects on Health Outcomes in Women with Breast Cancer.	1	1	1	1	1	0	1	1	No

Notes: Excluded – if “nil/no” for any one. Included – if “yes” for all.

Table S2 Search strategy

The Cochrane Database of Systematic Reviews

01. Breast cancer

The Database of Abstracts of Reviews of Effects (2009–2014)

01. Breast cancer

02. Surgery

03. Rehabilitation

04. Therapy

05. 01 and 02

06. 03 or 04

07. 05 and 06

ScienceDirect (2009–2014)

01. Breast cancer

02. Breast carcinoma

03. Surgery

04. Mastectomy

05. MRM

06. Lumpectomy

07. Breast conservation

08. Axillary lymph node dissection

09. ALND

10. Rehabilitation

11. Treatment

12. Physiotherapy

13. Psychological

14. Psychosocial

15. Psychotherapy

16. Exercise

17. Physical activity

18. Cognitive

19. Occupational

20. Alternative

21. Complementary

22. Systematic Review

23. 1 or 2

24. 3 or 4 or 5 or 6 or 7 or 8 or 9

25. 10 or 11 or 12 or 13 or 14 or 15 or 16 or 17 or 18 or 19 or 20 or 21

26. 22

27. 23 and 24 and 25 and 26

PubMed (2009–2014)

01. Breast cancer

02. Breast carcinoma

03. Surgery

04. Mastectomy

05. MRM

06. Lumpectomy

07. Breast conservation

08. Axillary lymph node dissection

09. ALND

10. Rehabilitation

11. Treatment

12. Physiotherapy

13. Psychological

14. Psychosocial

15. Psychotherapy

16. Exercise

17. Physical activity

18. Cognitive

19. Occupational

20. Alternative

21. Complementary

22. Systematic Review

23. 1 or 2

24. 3 or 4 or 5 or 6 or 7 or 8 or 9

25. 10 or 11 or 12 or 13 or 14 or 15 or 16 or 17 or 18 or 19 or 20 or 21

26. 22

27. 23 and 24 and 25 and 26

Abbreviations: ALND, axillary lymph node dissection; MRM, modified radical mastectomy.

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