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Clinical Practice Guidelines for Breast Cancer Rehabilitation
Syntheses of Guideline Recommendations and Qualitative Appraisals*
Susan R. Harris, PhD, PT1; Kathryn H. Schmitz, PhD, MPH2; Kristin L. Campbell, PhD, PT1;
and Margaret L. McNeely, PhD, PT3
BACKGROUND: Despite strides in early detection and management of breast cancer, the primary treatments for this disease continue
to result in physical impairments for some of the nearly 3 million people diagnosed annually. Over the past decade, evidence-based
clinical practice guidelines (CPGs) have been developed with goals of preventing and ameliorating these impairments. However,
translation of these guidelines into clinical practice needs to be accelerated. METHODS: Relevant health science databases (2001-
2011) were searched to identify CPGs on breast cancer rehabilitation for the following impairments: upper extremity restrictions, lym-
phedema, pain, fatigue, chemotherapy-induced peripheral neuropathy, treatment-related cardiotoxicity, bone health, and weight man-
agement. RESULTS: Recommendations from 19 relevant CPGs were first summarized by impairment within tables; commonalities
across guidelines, within each impairment, were then synthesized within the article. The CPGs were rated using the Appraisal of
Guidelines for Research and Evaluation II (AGREE II); wide variability was noted in rigor of development, clarity of presentation, and
stakeholder involvement. The most rigorous and comprehensive of those rated was the adult cancer pain guideline from the Scottish
Intercollegiate Guidelines Network. CONCLUSIONS: Based on a large body of evidence published in recent years, including random-
ized trials and systematic reviews, there is an urgent need for updating the guidelines on upper extremity musculoskeletal impair-
ments and lymphedema. Furthermore, additional research is needed to provide an evidence base for developing rehabilitation
guidelines on management of other impairments identified in the prospective surveillance model, eg, arthralgia. Cancer
2012;118(8 suppl):2312–24.VC 2012 American Cancer Society.
KEYWORDS: clinical practice guidelines, breast cancer, rehabilitation, qualitative appraisal.
Despite important strides in recent years in early detection1,2 and management of breast cancer,3-5 the primary treatmentsfor this disease (surgery, radiation, and chemotherapy) continue to lead to significant morbidity for some of the nearly 3million women (and men) around the world who are diagnosed annually.6 In addition to the profound psychosocialimpact of receiving a breast cancer diagnosis, a number of physical impairments commonly result from the treatmentsdesigned to save or prolong the lives of those affected. These include impairments of upper extremity range of motion andstrength, upper extremity and/or breast lymphedema, pain, fatigue, loss of sensation, and reduction in levels of physicalactivity and health-related quality of life.7-10
Despite the wide array of physical impairments that can occur after breast cancer treatments, there is little informa-tion in the peer-reviewed literature about how best to manage these impairments. Particularly lacking in the literature arerecent, evidence-based, clinical practice guidelines (CPGs) on upper extremity impairments and arthralgia. CPGs aredefined as ‘‘statements that include recommendations intended to optimize patient care that are informed by a systematicreview of evidence and an assessment of the benefits and harms of alternative care options.’’11(p29) Critical reviews of prac-tice guidelines have shown them to vary considerably in the strength of evidence used in their development, the search
DOI: 10.1002/cncr.27461, Received: October 19, 2011; Accepted: November 7, 2011, Published online April 6, 2012 in Wiley Online Library
(wileyonlinelibrary.com)
Corresponding author: Susan R. Harris, PhD, PT, PT, Department of Physical Therapy, Faculty of Medicine, 212-2177 Wesbrook Mall, Vancouver, British Columbia,
V6T 1Z3, Canada. Telephone: 604-264-0249. Fax: (604) 822-1870; [email protected]
1Department of Physical Therapy, Faculty of Medicine, University of British Columbia, Vancouver, Canada; 2Department of Biostatistics and Epidemiology, Univer-
sity of Pennsylvania, Philadelphia, Pennsylvania; 3Departments of Physical Therapy and Oncology, University of Alberta, Edmonton, Canada
The articles in this supplement were commissioned based on presentations and deliberations at a Roundtable Meeting on a Prospective Model of Care for Breast
Cancer Rehabilitation, held February 24-25, 2011, at the American Cancer Society National Home Office, in Atlanta, Georgia.
The opinions or views expressed in this supplement are those of the authors, and do not necessarily reflect the opinions or recommendations of the editors or
the American Cancer Society.
The authors thank Ms. Charlotte Beck, health sciences reference librarian at the University of British Columbia, for her assistance in searching the literature for rel-
evant clinical practice guidelines and Dr. Jane M. Armer of the Sinclair School of Nursing at the University of Missouri for her clarification of the evidence-based
recommendations emanating from the Putting Evidence into Practice (PEP) card. And, finally, we are indebted to Ms. Kimberly S. Andrews, Research Associate in
Cancer Control Science at the American Cancer Society, for her superb and patient editing of earlier drafts of this manuscript.
*A Prospective Surveillance Model for Rehabilitation for Women with Breast Cancer, Supplement to Cancer
2312 Cancer April 15, 2012
Original Article
methods employed to gather the evidence, and the dem-onstration of links between the evidence gleaned and theresulting practice recommendations.12-14
With publication of the Appraisal of Guidelines forResearch and Evaluation (AGREE) instrument in 200315
and recent expansion and improvement of the tool as theAGREE II,16,17 it is now possible to address this variabili-ty in guideline quality by systematically evaluating keyfactors in guideline development. The AGREE II com-prises 23 items within 6 domains: 1) scope and purpose;2) stakeholder involvement; 3) rigor of development; 4)clarity of presentation; 5) applicability; and 6) editorial in-dependence.18 Each item is rated on a 7-point scale fromstrongly disagree to strongly agree; 2 overall appraisalitems assess the overall quality of the guideline andwhether it should be recommended for practice.
Each guideline is rated by at least 2 appraisers, withother raters added if there is major discordance in 1 do-main or medium-level discordance in more than 2domains.18 Aggregate scoring across domains is not rec-ommended; instead, the 2 global appraisal items are usedto rate overall quality. Table 1 provides an example ofhow to calculate the score for Domain 1: Scope andPurpose.
Cited in more than 200 publications, the AGREEhas been used by the National Institute for Health andClinical Excellence19,20 and other policy organizations inreviewing CPGs.21 According to a recent Lancet commen-tary, updating of the AGREE to the AGREE II ‘‘will con-tinue to make an important contribution to improvingthe quality of clinical care.’’22
The overall goal of this article was to identify andreview CPGs related to the assessment and managementof physical impairment outcomes of having had breastcancer and/or from the interventions used to treat the dis-ease. Specific objectives were 1) to summarize and synthe-size recommendations from recent practice guidelines(2001-2011) in order to provide guidance to consumers,rehabilitation clinicians, and health care funding agencieson evidence-based rehabilitation for persons living withbreast cancer; 2) to rate the methodological quality of cur-rent practice guidelines using the AGREE II; and 3) toprovide recommendations for updating current guidelinesand for developing additional, evidence-based practiceguidelines related to breast cancer rehabilitation.
We focused on impairments included in the Pro-spective Surveillance Model for Physical Rehabilitationfor Women with Breast Cancer23: upper extremity restric-tions, lymphedema, pain, fatigue, chemotherapy-inducedperipheral neuropathy (CIPN), treatment-related cardio-toxicity, and bone health. Although there were no CPGson weight management, per se, we located some evidence-based recommendations on weight control that appearedin other guidelines or published reports.
METHODS
Search Strategies
We performed an initial search of MEDLINE, Google,Google Scholar, and the Physiotherapy Evidence Data-base (PEDro) from 2001 through April 2, 2011. This wasfollowed by a more extensive search by a University ofBritish Columbia health sciences reference librarian forgray literature, using Grey Matters and Intuit, and of Cu-mulative Index to Nursing and Allied Health Literature(CINAHL), and Embase (OvidSP) from 2001 to May 5,2011. Search terms were used for the concepts of breastcancer, rehabilitation, and guidelines. Based on bothsets of searches, 17 organizations that publish breastcancer guidelines were identified and are listed inTable 2.19,20,24-39
Practice guidelines were included if they focused onbreast cancer–related upper extremity physical impair-ments, upper extremity and/or breast lymphedema, pain,fatigue, CIPN, cardiotoxicity, or bone health. Because ofthe limited number of guidelines related solely to breastcancer in the latter categories, CPGs related to genericcancer pain, fatigue, CIPN, cardiotoxicity, or bone healthwere included also. In addition, we retrieved several, evi-dence-based recommendations related to weight manage-ment in breast cancer. Other inclusion criteria forguidelines were publication between 2001 and 2011,
Table 1. Scoring the AGREE II: Calculating Domain Scores18a
Item 1 Item 2 Item 3 Total
Appraiser 1 5 6 6 17
Appraiser 2 6 6 7 19
Appraiser 3 2 4 2 9
Appraiser 4 3 3 2 8
Total 16 19 18 53
a AGREE II indicates Appraisal of Guidelines for Research and Evaluation II.
Domain scores are calculated by summing up all the scores of the individ-
ual items in a domain and by scaling the total as a percentage of the maxi-
mum possible score for that domain. Example: If 4 appraisers give the
above scores for Domain 1 (scope and purpose)
Maximum possible score ¼ 7 (strongly agree) � 3 items � 4 appraisers ¼84
Minimum possible score ¼ 1 (strongly disagree) � 3 (items) � 4 (appraisers)
¼ 12
The scaled domain score will be:
Obtained score � Minimum possible score
Maximum possible score �Minimum possible score
53� 12 � 100
84� 12¼ 41
72� 100 ¼ 0:5694� 100 ¼ 57%
Breast Cancer Rehabilitation Guidelines/Harris et al
Cancer April 15, 2012 2313
Table
2.Org
anizationsSearched
forRelevantGuidelines,CountryofOrigin,and
YearofMostRecentUpdate
foranyBreastCancerGuideline
GuidelinePublisher
(ReferenceNumber)
CountryofOrigin
AdditionalInform
ationorReferralto
AnotherCPG
Database
LastUpdate
AgencyforHealthcare
ResearchandQuality
(AHRQ)24
UnitedStatesofAmerica
Refers
readers
toNationalGuidelineClearingHouse29
1994
AmericanSociety
ofClinicalOncology
(ASCO)25
UnitedStatesofAmerica
Includes9breastcancerCPGs(2001-2011)butnonerelatedto
rehabilitation
2011
BritishColumbia
CancerAgency(BCCA)26
Canada
Refers
readers
toCMAJbreastcancerCPGs26
2011
CanadianBreastCancerNetw
ork
(CBCN)27
Canada
Includesonly
theBreastCancer,Pregnancy,
andBreastfeedingCPG
from
Society
ofObstetriciansandGynecologists
ofCanada
2002
CancerCare
NovaScotia28
Canada
Refers
readers
toCMAJbreastcancerguidelines26andCancerCare
Ontarioguidelines24
2005
CancerCare
Ontario29
Canada
PDFforTheTreatm
entofLymphedemarelatedto
BreastCancer
2003
CanadianMedicalAssociation(CMA)
Infobase30
Canada
Includes22breastcancerCPGs(butnonerelatedto
rehabilitation)
2008
CanadianMedicalAssociationJournal
(CMAJ)BreastCancerPractice
Guidelines31
Canada
SixteenbreastcancerCPGs,includingno.11:Lymphedema
2005
EuropeanSociety
forMedicalOncology
(ESMO)32
Europe
Includes3breastcancerCPGs,1withreferenceto
lymphedema
2010
NationalComprehensiveCancerNetw
ork
(NCCN)33
UnitedStatesofAmerica
EightbreastcancerCPGs,butnothingrelatedto
rehabilitation.CPGs
oncancer-relatedfatigueandadultcancerpain
willbereviewed.
2011
NationalGuidelineClearingHouse34
UnitedStatesofAmerica
Includes215breastcancerCPGs;allrehabilitation-relatedCPGs
capturedvia
otherWebsites
2011
NationalHealthandMedicalResearch
Council(NHMRC)35
Australia
Rehabilitation-relatedinform
ationincludedin
theCPGsonmanagement
ofearlyandadvancedbreastcancer
2001
NationalHealthService(NHS)Evidence–
NationalLibrary
ofGuidelines36
UnitedKingdom
IncludesbreastcancerCPGsfrom
NICE32,33andSIG
N35
2011
NationalInstitute
forHealthandClinical
Excellence(NICE)19,20
UnitedKingdom
Rehabilitation-relevantinform
ationin
2CPGs:breastcancer(earlyand
locally
advanced)andbreastcancer(advanced)
2009
New
ZealandGuidelinesGroup37
New
Zealand
CPG
onmanagementofearlybreastcancer
2009
Public
HealthAgencyofCanada38
Canada
Refers
toCMA,25CMAJ,26andBCCA20breastcancerCPGs
2011
ScottishIntercollegiate
GuidelinesNetw
ork
39
UnitedKingdom
Relevantinform
ationin
CPG
106:Controlofpain
inadultswithcancer
2007
CPG
indicatesclinicalpracticeguideline.
Original Article
2314 Cancer April 15, 2012
either in a peer-reviewed journal and/or endorsed by anational/multinational government agency or health pro-fessional provider group, and available in English. We didnot include guidelines pertaining specifically to metastaticbreast cancer.
Titles were screened by the first author (S.R. Harris)and, if there was uncertainty based on the title, abstractsor quick reference guides were then screened. For themore generic cancer guidelines, tables of contents weresearched for relevant headings or subheadings, eg, upperextremity impairment, lymphedema, pain, fatigue, andrehabilitation.
Summaries and Syntheses of GuidelineRecommendations
To summarize guideline recommendations across the var-ious CPGs included in this review (Objective 1), the rec-ommendations as written in the original guidelines weregrouped for each of the major categories of interest andpresented in tables: upper extremity impairments, lym-phedema, pain, and fatigue. An additional table summa-rizes recommendations for CIPN, cardiotoxicity, bonehealth, and weight management; the weight managementrecommendations were based on 2 breast cancer follow-up CPGs and an evidence-based guide on nutrition andphysical activity during and after cancer treatment.
Evaluation of Published Guidelines
To address the second objective of this article, each CPGincluded for review in the major impairment areas wasevaluated using the AGREE II.18 Ten of the cancer-related practice guidelines had been reviewed previouslywith the AGREE II by the Cancer Guidelines ResourceCentre, an initiative of the Cancer Guidelines AdvisoryGroup of the Canadian Partnership Against Cancer,40
and are available on their Web site; those scores were usedfor this article. For the 9 guidelines not previouslyreviewed by the guidelines resource center, the recom-mendations from the AGREE II manual were followedwith at least 2 authors independently rating each. TheAGREE II concordance calculator was used to examinerater concordance.
Prior to using the AGREE II to appraise the guide-lines included in this article, its reliability was assessed. All4 author-appraisers first undertook the online AGREE IItraining. To establish inter-rater agreement, 2 breast can-cer guidelines unrelated to physical impairments41,42 werethen independently rated by each of the 4 reviewers.According to the decision rules accompanying the con-cordance calculator, no further action is required if overallscores (across raters) are <1.5 standard deviation (SD) in
all domains. However, if there is discordance of�2 SD in1 domain (major discordance) or �1.5 SD in 3 domains(medium discordance), further action is needed. For thefirst guideline evaluated to test inter-rater agreement,41
only 1 domain was found to be discordant among the 4with�2 SD from the mean; discrepancies within that do-main were resolved through consensus. For the second ar-ticle,42 only 1 domain was found to differ by 1.58 SD,thus requiring no action.
To calibrate that agreement against a gold standardcomparator, we compared our own domain appraisals forthe 2 guidelines to those on the Cancer GuidelinesResource Centre Web site40 (http://www.cancerview.ca/portal/server.pt/community/sage/521/search_sage/5751).Our goal was to obtain�70% agreement. The AGREE IIconcordance calculator was used to derive domain scoresacross the 4 raters’ scores. For the 12 domains rated acrossthe 2 articles (6 domains for each article), we agreed withthe published appraisals (within�10%) on 9 of 12, for anoverall percent agreement of 75%. Consequently, wedetermined that we had sufficient agreement to justifypooling our ratings for the 9 guidelines with the already-established ratings from the Cancer Guidelines ResourceCentreWeb site for the other 10 guidelines.
Recommendations for Updating CurrentGuidelines and for Future Guidelines
The third objective of this article, to provide recommen-dations for updating current guidelines and developingfuture practice guidelines in breast cancer rehabilitation,was based on the results stemming from the first 2 objec-tives: the syntheses of recommendations from currentCPGs and the quality appraisal of those guidelines. Rec-ommendations based on this third objective appear in theDiscussion section.
RESULTS
Summary of Guideline Recommendations
To address the first objective of this article, to summarizeand synthesize recommendations from guidelines pub-lished between 2001 and 2011, Tables 3 through 7 pro-vide recommendations from the CPGs reviewed.Recommendations are categorized by impairment, withcorresponding guideline documents referenced. Wemaintained the original text from the published guidelinesrather than inserting changes based on more recentevidence.
Recommendations from the sole CPG43 (withupdate)44 on upper extremity impairment appear in Table3. For lymphedema, we located 2 CPGs,45,46 1 evidence
Breast Cancer Rehabilitation Guidelines/Harris et al
Cancer April 15, 2012 2315
summary,29,47 and 1 Putting Evidence into Practice(PEP) resource (Table 4).48 According to the authors ofthe evidence summary, such summaries are developedwhen high-quality evidence is insufficient to make clinicalrecommendations in the form of guidelines.29,47 Becausethe PEP resource on lymphedema47 did not include spe-cific, highlighted, guideline-type recommendations (orkey opinions), we extracted several statements fromthe section labeled ‘‘Recommended for Practice,’’ aweight-of evidence category described by the authors as‘‘effectiveness is demonstrated by strong evidence fromrigorously designed studies, meta-analyses, or systematicreviews.’’48(p953)
In the area of cancer-related pain, only 1 CPG spe-cifically related to breast cancer pain49 (and a publishedsummary of it50) were located, unfortunately the oldest(2001) of the pain CPGs. An additional 5 pain CPGs thatrelated to cancer pain in general were also appraised.51-55
Guideline recommendations relating to nonpharmaco-logic management of pain are included in Table 5. Forcancer-related fatigue, 2 recent CPGs were included56,57;only nonpharmacologic recommendations from theseguidelines were listed (Table 6).
Of the 2 CIPN guidelines,58,59 the more recent(2009) included more specific rehabilitation recom-mendations.59 For the 2 CPGs on treatment-relatedcardiotoxicity,60,61 only 1 included an exercise recom-mendation60 (Table 7). Of the 2 guidelines on bonehealth,62,63 only the more recent one (National Compre-hensive Cancer Network [NCCN]) included rehabi-litation-related suggestions.62 Recommendations onweight management from 2 breast cancer follow-upCPGs64,65 and an evidence-based guide66 are alsoincluded in Table 7.
Methodological Quality of Guidelines
Tables 8 through 13 summarize the methodologicalquality ratings of the CPGs reviewed across the 6 AGREEII domains. For the 9 guidelines rated by theauthors,29,43-47,49,50,52,57,59,62 there were 22 items (of atotal of 207) in which 1 appraiser’s rating was an impor-tant outlier, ie, 1 rater gave the item a score of 1, and theother appraiser rated it significantly higher. The appraiserwho had initially given a score of 1 was asked to re-reviewthe guideline and change her score, if she deemed it neces-sary. Eleven initial scores (50% of the 22 discrepant rat-ings or 5.3% of the total ratings) were changed as a resultof these second reviews. For those ratings that remainedunchanged, the original scores were entered into theAGREE II concordance calculator to determine the over-all domain ratings across appraisers.
DISCUSSIONResults will next be discussed based on each of the 3 objec-tives for this article. Syntheses of the guideline recommen-dations summarized in Tables 3 through 7 will beprovided (Objective 1), followed by syntheses of the qual-ity appraisal results presented in Tables 8 through12 (Objective 2). Finally, recommendations for futureevidence-based practice guidelines are presented (Objec-tive 3).
Table 3. Upper Extremity Rehabilitation GuidelineRecommendations43,44
Upper Extremity RehabilitationPreoperative, bilateral upper extremity function should be
assessed to provide a baseline before treatments.
Postoperative physical therapy should begin the first day
following surgery. Gentle range of motion exercises should
be encouraged the first week after surgery.
Active stretching exercises can begin week 1 after surgery, or
when the drain is removed, and should be continued for 6 to
8 weeks or until full range of motion is achieved in the
affected upper extremity. Women should be instructed also
in scar tissue massage.
Postoperative assessments should occur regularly up to 1 year
after surgery.
Progressive resistive exercises, that is strengthening, can begin
with light weights (1-2 pounds) within 4 to 6 weeks after
surgery.
Hand and Arm CareCareful hand and arm care—for example, proper hygiene and
avoiding trauma to the arm—is important to minimize risks of
infection and lymphedema.
Specific treatment-related and host-related factors contribute
to the increased risks of complications. Minimizing the extent
of axillary dissection, preventing infection, and avoiding
obesity, for example, may help prevent the development of
lymphedema.
Generally, injections, vaccinations, venipuncture, and
intravenous access in the axillary-dissected upper extremity
have been contraindicated. There is some evidence (Level V)
that these restrictions can be relaxed.
Many suggestions regarding proper hygiene and trauma
avoidance for the axillary-dissected upper extremity are
sensible, but there is little scientific literature to support
these restrictions.
Electrotherapy ModalitiesLaser treatment, electrical stimulation, microwave, and thermal
therapy are not recommended at this time due to insufficient
evidence to support their use, and there are published
precautions and contraindications for their use in persons
with neoplasms.
Therapeutic ultrasound is contraindicated over sites of possible
metastasis in women with histories of breast cancer.
Original Article
2316 Cancer April 15, 2012
Syntheses of Guideline Recommendations
Of the articles pertaining to lymphedema,29,45-48 only 2were true practice guidelines.45,46 The older guideline45
differs from the prospective surveillance model (see Stoutet al23) in recommending circumferential measurementsfor assessment and/or diagnosis of lymphedema in womenat risk (Table 4); in the prospective surveillance model,volume measures are derived from circumferential meas-ures taken every 5 mm. This latter recommendation isbased on research published subsequent to the 2001CPG, in which it was shown that volume measurementsusing an opto-electric volumeter were especially sensitiveto subtle changes in upper limb volume.67 If an opto-elec-
tric volumeter (perometer) is available, albeit not com-mon in clinical practice, it should be used in place of armcircumference measures. Another measure that showspromise in measuring early, fluid-based changes is bioim-pedance spectroscopy, which is described in the Australianlymphedema guideline.46
As for interventions for lymphedema, there wereconsistent recommendations for the use of compressiongarments in the management of lymphedema,29,45,47
but only limited evidence to support compressionbandaging in conjunction with manual lymph drain-age (MLD) at the time these guidelines werepublished.45,47,48
Table 4. Lymphedema Guideline Recommendations,45,46 Evidence Report Key Opinions,29,47 and Putting Evidence into Practice(PEP) Recommendations48
Assessment and Diagnosis of LymphedemaEvidence supports early lymphedema diagnosis and referral for therapies to reduce patient burden.46,48
Pre- and postoperative measurements of both arms are useful in the assessment and diagnosis of lymphedema. Circumferential
measurements should be taken at 4 points: the metacarpal-phalangeal joints, the wrists, 10 cm distal to the lateral epicondyles, and
12 cm proximal to the lateral epicondyles.45
Clinicians should elicit symptoms of heaviness, tightness, or swelling in the affected arm. A difference of more than 2.0 cm at any
of the 4 measurement points may warrant treatment of the lymphedema, provided that tumor involvement of the axilla or brachial
plexus, infection, and axillary vein thrombosis have been ruled out.45
Additional efforts to define relevant clinical outcomes for the assessment or patients with lymphedema would be valuable.29,47
Interventions for LymphedemaPractitioners may want to encourage long-term and consistent use of compression garments by women with lymphedema.45
Compression garments should be worn from morning to night and be removed at bedtime. Patients should be informed that
lymphedema is a lifelong condition and that compression garments must be worn on a daily basis. Patients can expect stabilization
and/or modest improvement of lymphedema with the use of the garment in the prescribed fashion.29,47
The Supportive Care Guidelines Group endorses the recommendations from the Steering Committee for Clinical Practice Guidelines
for the care and treatment of breast cancer. The use of compression garments is consistent with what is commonly practiced clinically.29,47
Compression bandaging, a systematic application of short-stretch bandages with various types of padding, is recommended
for practice.48
Complex physical therapy, manual lymph drainage, compression and massage therapy are associated with volume reductions.46
One randomized trial has demonstrated a trend in favor of pneumatic compression pumps compared with no treatment. Further
randomized trials are required to determine whether pneumatic compression provides additional benefits over compression garments
alone.45
Complete decongestive therapy, also known as complex decongestive physiotherapy and complex physical therapy, is the
recommended treatment for lymphedema.48
There is some evidence that compression therapy and manual lymph drainage may improve established lymphedema, but further
studies are needed.29,47
There is no current evidence to support the use of medical therapies, including diuretics,29,47,48 benzopyrones, and selenium
compounds.48
Other Considerations for Lymphedema ManagementClinical experience supports encouraging patients to consider some practical advice regarding skin care, exercise, and body
weight.45,48
Evidence exists that a body mass index >30 is a risk factor for lymphedema.48
Although there is no clear relationship between high body mass index and development of secondary lymphedema following treatment
for cancer, maintenance of a healthy body weight in cancer survivors should be encouraged because of the other associated health
benefits.48
The opinions are appropriate for patients with more than mild lymphedema, where the signs and symptoms are considered important
from the patients’ perspective.29,47
Immediate attention to signs of infection and prompt initiation of antibiotic therapy are critical to preventing sepsis.48
Infection risk is essential to reduce the risk of developing or exacerbating lymphedema.46
Conservative surgical and radiation treatment for cancer should be used to reduce the risk of secondary lymphedema.46
Surgical techniques may be useful for a small subset of secondary lymphedema sufferers who have failed to obtain relief from
less invasive measures.46
Breast Cancer Rehabilitation Guidelines/Harris et al
Cancer April 15, 2012 2317
Fortunately, there are a number of CPGs availableon cancer-related pain, 6 of which were included in thisreview.49,51-55 With regard to evaluation of pain, therewas consistency across most of the guidelines that thepatient’s own report of pain intensity should be the
Table 5. Relevant Guideline Recommendations for Cancer-Related Pain49-55
Evaluation of PainThere are many reasons why a patient with breast cancer may
experience pain. Identifying the cause and understanding the
pathophysiology can lead to more effective management.49-51
The nature and severity of pain should be carefully evaluated
using the history and physical, psychosocial, and emotional
assessments. Adequacy of pain relief should be evaluated
regularly.49,50-52
The patient’s self-report of pain intensity is the primary source
of assessment data in all initial and subsequent
evaluations.49,50-54
Patients with cancer pain should have treatment outcomes
monitored regularly49-54 using visual analogue scales,
numerical rating scales, or verbal rating scales.52-54
Physicians, and other health care professionals, should
frequently reassess pain relief, side effects, and adverse
events, as well as the impact of pain and treatment on
patient function and quality of life.52,55
Management of PainGeneral Principles of Pain Management
The first objective in the management of pain is to identify the
cause and treat it whenever feasible.49,50
The first priority of treatment is to control pain rapidly and
completely, as judged by the patient; the second priority is
to prevent recurrence of pain.49-50
Patients should be given information and instruction about pain
and pain management and be encouraged to take an active
role in their pain management.52,55
Pain treatment and goals should be tailored to the needs,
desires, and circumstances of individual patients.55
Patient and Family Education
Development of a comprehensive, effective pain management
plan includes the education and involvement of the patient and
family, together with an interdisciplinary team approach.49-51,54
Patients and families should receive written information
regarding pain management options51 and education about
the range of pain control interventions available to them.52
Brief educational interventions and pain management diaries
are useful strategies that improve adherence and reduce pain
intensity.55
Nonpharmacologic Interventions for PainConsider nonpharmacologic interventions in conjunction with
pharmacologic interventions as needed. Pain is likely to be
relieved or function improved with physical modalities such
as: bed, bath, and walking supports; positioning instruction;
PT; energy conservation; pacing of activities; TENS,
acupuncture or acupressure.49-52,54
Specialty consultations for improved pain management include
physical/occupational therapy, rehabilitation/mobility spe-
cialty consultation.51
PT indicates physical therapist/physical therapy; TENS, transcutaneous
electrical nerve stimulation.
Table 6. Relevant Guideline Recommendations for Cancer-Related Fatigue56,57
Screening and Evaluation for FatigueScreen every patient for fatigue as vital sign at regular intervals
(using a 10-point scale in which a score ‡4 5 moderate
fatigue). Patients with moderate to severe fatigue should be
queried about their activity level, including changes in
exercise or activity patterns and the influence of
deconditioning.56
There is expert consensus that patients with fatigue be
screened for potentially detectable factors contributing to
fatigue.57
Before recommending an exercise program, health care
providers or exercise experts (eg, physiatrist, physical thera-
pist) should assess the conditioning level of patients.56
Interventions for Patients on Active TreatmentEducation and Counseling of Patient
Education about fatigue and its natural history should be
offered to all cancer patients but is particularly essential for
patients beginning potentially fatigue-inducing treatments
(eg, radiation, chemotherapy, or biotherapy).56
In addition to education, the National Comprehensive Cancer
Network panel recommends counseling for patients about
general strategies (energy concentration and distraction)
useful in coping with fatigue.56
Educational interventions (including teaching, counseling,
support, anticipatory guidance about fatigue patterns, coping
skills training, and coaching) are ‘‘likely to be effective’’ in
supporting positive coping in patients with fatigue and in
reducing fatigue levels.57
Physical Activity/Exercise
It is reasonable to encourage all patients to engage in a
moderate level of physical activity during and after cancer treat-
ment, eg, 30minutes ofmoderate activity most days of theweek.56
Exercising several times per week (including walking, cycling,
resistance exercise, or a combination of aerobic and
resistance exercise) can be effective in reducing fatigue
during and following cancer treatment.57
Some patients may require referrals to exercise specialists in
fields such as physical therapy, physical medicine, or
rehabilitation for assessment and an exercise prescription.56
Interventions for Patients After TreatmentMaintain optimal level of activity.56
Consider initiation of exercise program of both endurance and
resistance exercise. It is reasonable to encourage all patients
to engage in a moderate level of physical activity during and
after cancer treatment,56 eg, 30 minutes of moderate activity
most days of the week.
Consider referral to rehabilitation: physical therapy,
occupational therapy, physical medicine.56
The exercise program should be individualized based on the
patient’s age, sex, type of cancer, and physical fitness
level.56 The program should begin at a low level of intensity
and duration, progress slowly, and be modified as the
patient’s condition changes.56
Other Considerations for Cancer-Related FatigueThe guidelines for fatigue are best implemented by an
interdisciplinary institutional committee, including
representatives from the fields of medicine, nursing, social
work, physical therapy, and nutrition.56
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2318 Cancer April 15, 2012
primary source of assessment throughout initial and sub-sequent evaluations, that pain should be monitored regu-larly, and that visual analogue scales or other numericalrating scales should be used. Ongoing monitoring of painis reflected also in the prospective surveillance model.There was also consistency across the guidelines that
patients and their families should receive information andinstruction about pain and take an active role in their ownpain management, in conjunction with an interdiscipli-nary team approach. Nonpharmacologic interventionsrecommended for pain management included physical/occupational therapy, energy conservation strategies,transcutaneous electrical nerve stimulation, and acupunc-ture/acupressure.
Of the 2 cancer-related fatigue CPGs,56,57 only theNCCN guideline56 included screening and evaluationrecommendations, both of which are congruent with theprospective surveillance model. Both guidelines includedrecommendations for educating the patient about fatigueand the importance of activity enhancement or exercise asinterventions to help manage fatigue,56,57 elements thatare also supported in the prospective surveillance model.As with the recommendations for pain management, aninterdisciplinary team approach was encouraged in theNCCN guideline.56
The role of exercise and physical activity in helpingto manage treatment-related peripheral neuropathy, car-diotoxicity, bone loss and/or fractures, and weight gainare just beginning to be recognized in some of the morerecent CPGs (Table 8); additional, evidence-based recom-mendations should be incorporated into future guidelinesin these areas as this evidence base continues to grow.
Methodological Quality of Guidelines
The upper extremity rehabilitation CPG and update43,44
received strong appraisal scores (�80%) in 3 of the 6domains (Table 8). With regard to the lymphedemaguidelines (Table 9), the Canadian Medical Associationguideline45 received strong appraisal scores in 2 domains,as did the Ontario evidence summary.29,47 The AustralianCPG46 scored >80% in scope and purpose, whereas thehighest domain score for the lymphedema PEP review48
was 63.9%.
Table 7. Nonpharmacologic Guideline Recommendations forChemotherapy-Induced Peripheral Neuropathy,Treatment-Related Cardiotoxicity, Bone Health,and Weight Management
Chemotherapy-Induced Peripheral NeuropathyNational Comprehensive Cancer Network panelists generally
agreed that transcutaneous electrical nerve stimulation can
be a helpful adjuvant therapy for CIPN in those with contrain-
dications to or for whom pain medication is ineffective.59
Acupuncture is noninvasive and relatively inexpensive and may
be considered as an adjunct option in treating patients with
medication-resistant CIPN.58,59
Panelists strongly recommended referring patients with CIPN
that interferes with functioning to a physical or occupational
therapist. Therapeutic intervention, education, and practical
advice provided by these rehabilitation specialists can prove
invaluable in helping patients to both correct CIPN-induced
functional deficits and to cope with the difficulties and
challenges these deficits cause in their everyday life.59
Treatment-Related CardiotoxicityPatients should be encouraged to adopt a healthy lifestyle in
order to protect the myocardium, including a balanced diet,
moderate exercise, and smoking cessation.60
Bone HealthWeight-bearing exercise has been associated with a decreased
risk of hip fractures, probably due to a reduction in fall risk and
also through modest effects on preservation of bone density.62
Tai chi, physical therapy, and dancing are considered good
options to improve balance and prevent falls.62
Adults should aim for at least 30 minutes of moderate physical
activity daily (either in 1 continuous session or in a number of
shorter bursts). This activity can include a mix of weight-
bearing, strength training, and balance training exercises.62
Wearing hip protectors may prevent hip fracture in the event of
a fall and can be considered for patients with a high risk for
falling.62
Weight ManagementWeight management should be discussed with all breast
cancer survivors.64
Weight gain affects prognosis adversely and should be
discouraged; if necessary, nutritional counseling is recom-
mended. Regular long-term moderate to strenuous physical
activity is associated with a favorable prognosis; aerobic
training and weight lifting does not negatively affect the de-
velopment of lymphedema.65
Maintain a healthy body weight throughout life.66
� Balance caloric intake with physical activity
� Avoid excessive weight gain throughout the life cycle
� Achieve and maintain a healthy weight if currently overweight or
obese
CIPN indicates chemotherapy-induced peripheral neuropathy.
Table 8. AGREE II Quality Assessment for Upper ExtremityRehabilitation Guidelines
AGREE IIDomain
Upper ExtremityRehabilitation(BCCA)43,44a
Scope and purpose 88.9%
Stakeholder involvement 80.6%
Rigor of development 75.0%
Clarity of presentation 91.7%
Applicability 56.3%
Editorial independence 12.5%
AGREE II indicates Appraisal of Guidelines for Research and Evaluation II;
BCCA, British Columbia Cancer Agency.aGuideline rated by K.L. Campbell and M.L. McNeely.
Breast Cancer Rehabilitation Guidelines/Harris et al
Cancer April 15, 2012 2319
Table 10 displays the AGREE II domain scores forguidelines on cancer-related pain.49-55 The CanadianMedical Association breast cancer pain guideline,49,50 andthe NCCN pain guideline51 received strong ratings onlyin clarity of presentation; all other ratings for the NCCNguideline were <50%. The Scottish IntercollegiateGuidelines Network (SIGN) pain guideline52 had thestrongest ratings across all domains (all >80%), whereasthe European Society of Medical Oncology53 guidelinereceived the lowest overall domain ratings. The guidelineby Cancer Care Ontario54 received strong scores in 3domains. And, finally, the American Pain Society guide-line55 scored�80% in just 1 domain: scope and purpose.
In Table 11, domain ratings for the 2 CPGs on can-cer-related fatigue are provided.56,57 Both guidelines wererated quite similarly for scope and purpose, stakeholderinvolvement, clarity of presentation, and editorial inde-pendence. Although the CPG from the Oncology Nurs-ing Society (ONS) was rated more favorably in the thirddomain—rigor of development—the NCCN guidelinewas stronger in applicability (Domain 5).
Table 12 provides AGREE II ratings for theCIPN58,59 and cardiotoxicity60,61 guidelines. Of the 2CIPN guidelines, only the NCCN guideline was rated
�80%, and only in 1 domain. For the cardiotoxicityguidelines, all domain ratings were <60%. For the bonehealth guidelines62,63 (Table 13), no domain was rated�80%.
Across the 9 guidelines rated by the authors, therewas medium-level discordance in 4 domain appraisals(11.1% of all domains): stakeholder involvement (Do-main 2) for the Cancer Care Ontario lymphedema evi-dence summary29,46 and the Australian lymphedemaguideline;48 and scope and purpose (Domain 1) and
Table 9. AGREE II Quality Assessment for Lymphedema Guidelines
AGREE IIDomain
Lymphedema(CMA)45b
Lymphedema(CCO)29,47c
Lymphedema(ONS)48a
Lymphedema(NBOCC)46c
Scope and purpose 75.0% 83.3% 55.6% 83.3%
Stakeholder involvement 83.3% 47.2% 55.6% 50.0%
Rigor of development 66.7% 58.0% 42.7% 59.4%
Clarity of presentation 94.4% 80.6% 63.9% 75.5%
Applicability 16.7% 14.6% 29.2% 16.7%
Editorial independence 75.0% 16.7% 16.7% 20.8%
AGREE II indicates Appraisal of Guidelines for Research and Evaluation II; CMA, Canadian Medical Association; CCO, Cancer Care Ontario (Canada); NBOCC,
National Breast and Ovarian Cancer Centre (Australia); ONS, Oncology Nursing Society.a Guideline rated by Cancer Guidelines Resource Centre.40
bGuidelines rated by K.H. Schmitz and M.L. McNeely.c Guidelines rated by M.L. McNeely and S.R. Harris.
Table 10. AGREE II Quality Assessment for Cancer-Related Pain Guidelines49-55
AGREE IIDomain
CMA49,50b
(Canada)NCCN51a
(USA)SIGN52b
(Scotland)ESMO53a
(Europe)CCO54a
(Canada)APS55a
(USA)
Scope and purpose 72.2% 41.7% 88.9% 22.2% 86.1% 80.6%
Stakeholder involvement 50.0% 38.9% 100.0% 11.1% 55.6% 58.3%
Rigor of development 45.8% 38.5% 89.6% 16.7% 75.0% 67.7%
Clarity of presentation 88.9% 91.7% 100.0% 52.8% 88.9% 77.8%
Applicability 18.8% 33.3% 83.3% 6.3% 33.3% 47.9%
Editorial independence 41.7% 45.8% 83.3% 16.7% 91.7% 45.8%
APS indicates American Pain Society; CCO, Cancer Care Ontario; CMA, Canadian Medical Association; ESMO, European Society of Medical Oncology;
NCCN, National Comprehensive Cancer Network; SIGN, Scottish Intercollegiate Guidelines Network.a Guidelines rated by Cancer Guidelines Resource Centre.40
bGuidelines rated by M.L. McNeely and S.R. Harris.
Table 11. AGREE II Quality Assessment for Cancer-RelatedFatigue Guidelines
AGREE IIDomain
NationalComprehensiveCancerNetwork (USA)56a
OncologyNursingSociety(USA)57b
Scope and purpose 66.7% 77.8%
Stakeholder involvement 53.7% 47.2%
Rigor of development 28.5% 58.3%
Clarity of presentation 87.0% 77.8%
Applicability 40.3% 6.3%
Editorial independence 61.1% 58.3%
AGREE II indicates Appraisal of Guidelines for Research and Evaluation II.aGuidelines rated by Cancer Guidelines Resource Centre.40
bGuideline rated by S.R. Harris and K.H. Schmitz.
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2320 Cancer April 15, 2012
clarity of presentation (Domain 4) for the ONS fatigueguideline.57 Discrepant ratings in 2 domains in the ONSfatigue guideline57 likely arose because the informationwas not consolidated within the guideline chapter butappeared in a number of different places on the ONSWeb site and various associated links, thus making it diffi-cult to find.
For all 19 guidelines included in this review,Domains 3, 5, and 6 most frequently had the lowestratings (eg, <30%): rigor of development (n ¼ 6),applicability (n ¼ 9), and editorial independence (n ¼8). In contrast, ratings exceeded 80% for clarity of pre-sentation (Domain 4) for nearly half (47.4%) of theguidelines.
Limitations of the AGREE II
In rating the CPGs not previously appraised, we struggledespecially with assigning scores between 2 and 6, becausethere are no definitions for these scores.22 Another area ofdifficulty was Domain 6: Editorial Independence. Unlessthe criteria outlined in items 22 and 23 were explicitlystated in the guideline (or on the Web site), eg, a state-ment that the funding body did not influence the contentof the guideline, description of any competing interests,
and how they influenced the guideline process and recom-mendations, the item had to be scored as 1 (strongly dis-agree), even if the appraisers assumed that editorialindependence existed based on the organization that hadauthored the guideline.
Another limitation of the AGREE II is that the focuson methodological issues related to guideline develop-ment and reporting is not sufficient to ensure that the rec-ommendations themselves are ‘‘appropriate and valid.’’22
In other words, as with most other guideline appraisalinstruments, the greatest shortcoming of the AGREE(and subsequently the AGREE II) is their failure to assess‘‘the quality of evidence’’ supporting the guideline’s rec-ommendations.21(p239) Whereas some guideline develop-ment organizations include expert opinion as an evidencesource, others rely exclusively on randomized controlledtrials (RCTs) and systematic reviews. The AGREE andAGREE II, similar to other guideline appraisal instru-ments, assess ‘‘the process of guideline development andhow well it is reported’’11(p69) but not the quality of evi-dence underlying the recommendations.
Recommendations for Updates and FutureEvidence-Based Practice Guidelines
Although there are some excellent and recent CPGs in theareas of cancer-related pain and fatigue, most notably theSIGN guideline on pain,52 and regular updating of theguidelines is being done by both SIGN and NCCN, thereis an urgent need for updated guidelines on the assessmentand management of upper extremity musculoskeletalimpairments and lymphedema. Since the development ofthese latter guidelines (between 2001 and 2008), a largebody of published evidence, including RCTs and system-atic reviews, has become available that would be critical inupdating these guidelines.
For example, a 2007 systematic review68 and a morerecent RCT69 have shown that resistance training is both
Table 12. AGREE II Quality Assessment for Chemotherapy-Induced Peripheral Neuropathy and Cardiotoxicity Guidelines
AGREE IIDomain
CIPN(ONS)58a
CIPN(NCCN)59b
Cardiotoxicity60a Cardiotoxicity(ESMO)61a
Scope and purpose 61.1% 61.1% 52.8% 33.3%
Stakeholder involvement 41.7% 58.3% 52.8% 16.7%
Rigor of development 46.9% 27.1% 29.2% 16.7%
Clarity of presentation 75.0% 86.1% 52.8% 55.6%
Applicability 20.8% 41.7% 12.5% 12.5%
Editorial independence 20.8% 79.2% 25.0% 12.5%
AGREE II indicates Appraisal of Guidelines for Research and Evaluation II; CIPN, chemotherapy-induced peripheral neuropathy; ESMO, European Society for
Medical Oncology; NCCN, National Comprehensive Cancer Network; ONS, Oncology Nursing Society.a Guidelines rated by Cancer Guidelines Resource Centre.40
bGuidelines rated by M.L. McNeely and S.R. Harris.
Table 13. AGREE II Quality Assessment for Bone HealthGuidelines
AGREE II Domain NCCN62a ASCO63b
Scope and purpose 72.2% 54.2%
Stakeholder involvement 55.6% 44.8%
Rigor of development 26.0% 42.3%
Clarity of presentation 72.2% 68.8%
Applicability 37.5% 70.8%
Editorial independence 79.2% 33.3%
AGREE II indicates Appraisal of Guidelines for Research and Evaluation II;
ASCO, American Society of Clinical Oncology; NCCN, National Compre-
hensive Cancer Network.a Guidelines rated by 2 authors (M.L. McNeely and S.R. Harris).bGuidelines rated by Cancer Guidelines Resource Centre.40
Breast Cancer Rehabilitation Guidelines/Harris et al
Cancer April 15, 2012 2321
safe and effective for women who have been treated forbreast cancer. Another recent RCT has shown that earlyphysical therapy (manual lymph drainage, scar tissue mas-sage, active and active-assisted shoulder range of motionexercises) was effective in preventing lymphedema duringthe first year after surgery,70 and a 2011 meta-analysisreported a significant benefit of manual lymph drainagewhen added to compression therapy in treatment of breastcancer–related lymphedema.71 A 2010 Cochrane reviewreported that structured exercise during the postoperativeperiod had significant short-term benefits in improvingshoulder flexion range of motion, with physical therapyresulting in additional benefits for shoulder function.72
Certainly, the breadth and quality of research availablesince the upper extremity rehabilitation and lymphedemaguidelines were published underscore the need for themto be updated and revised to incorporate this evidence.
Furthermore, additional research is needed to pro-vide an evidence base for developing CPGs on the effectsof exercise and/or physical therapy in the management ofother impairments identified in the breast cancer prospec-tive surveillance model, eg, arthralgia. The effects of phys-ical rehabilitation interventions on patients’ activity andlife participation, as well as on their quality of life, alsoneed to be studied so that CPGs can be developed in theseimportant areas.
Conclusions
This review has summarized and synthesized recommen-dations from 19 CPGs relevant to breast cancer physicalrehabilitation, published during the preceding decade. Inaddition, the guidelines were appraised using the AGREEII. Because of the scarcity of contemporary guidelines in 2key areas—upper extremity impairment and lymphe-dema—as well as the availability of new and rigorousresearch in those areas, updated guidelines are urgentlyneeded. The prospective surveillance model described inthis supplement will provide an excellent frameworkwithin which to guide development of updatedguidelines.
Fortunately, the recent and extremely comprehen-sive Institute of Medicine report, titled ‘‘Clinical PracticeGuidelines We Can Trust,’’ includes specific steps forestablishing evidence foundations for and ratingthe strength of guideline recommendations.11(pp124,125)
The standards proposed within this report could assistgreatly in ensuring that new guidelines are based oncontemporary, rigorously designed empiric studies andindependent processes for evidence retrieval, appraisal,and synthesis.11(pp75-144)
FUNDING SOURCESSupport for this meeting and supplement were provided by theAmerican Cancer Society through The Longaberger CompanyVR ,a direct selling company offering home products including hand-crafted baskets made in Ohio, and the Longaberger Horizon ofHopeVR Campaign, which provided a grant to the AmericanCancer Society for breast cancer research and education.
CONFLICT OF INTEREST DISCLOSUREThe authors made no disclosure.
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Original Article
2324 Cancer April 15, 2012