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‘This is the peer reviewed version of the following article: Nielsen, Gordon, & Selby. (2008). Breast cancer-related lymphoedema risk reduction advice: A challenge for health professionals. Cancer Treatment Reviews, 34(7), 621-628.
which has been published in final form at http://dx.doi.org/10.1016/j.ctrv.2007.11.002
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Breast cancer-related lymphoedema risk reduction advice: A challenge for health professionals 1
Cancer Treatment Reviews (2008) 34, 621– 628
Breast cancer-related lymphoedema risk reduction advice: A challenge for health
professionals
Ilsa Nielsen *, Susan Gordon a, Anita Selby
a
Discipline of Physiotherapy, James Cook University, Townsville, QLD 4811, Australia
Summary
Breast cancer-related lymphoedema (BCRL) is a debilitating, distressing condition affecting approximately one in
five breast cancer survivors (Clark B, Sitzia J, Harlow W. Incidence and risk of arm oedema following treatment
for breast cancer: a three-year follow-up study. QJM 2005;98:343–8). The evidence-base for breast cancer-related
lymphoedema risk reduction advice is scant and contradictory, with most studies in the area limited by small
numbers, retrospective design and other methodological inadequacies. Current advice has the capacity to
profoundly alter quality of life following treatment for breast cancer. Health professionals should review the risk
reduction advice they provide to reflect the current understanding of aetiology and risk factors. Further research is
required to provide more evidence for the content, to identify optimal methods of precautionary education delivery
and to determine the effect of the advice on the patient’s quality of life and perception of recovery.
KEYWORDS
Lymphoedema; Lymphedema; Breast cancer; Risk; Risk reduction
* Corresponding author. Tel.: +61 (0) 439 371209; fax: +61 (0) 74781 6868.
E-mail addresses: [email protected] (I. Nielsen), [email protected] (S. Gordon),
[email protected] (A. Selby).a
2 I. Nielsen et al.
Introduction
Breast cancer is the most common cancer affecting women worldwide and the leading cause of cancer death globally
in women.1 Improved detection and treatment procedures have reduced breast cancer mortality rates in many western
countries.1 Increased survival rates have highlighted the importance of preventing and managing morbidity resulting
from treatment effects in order to maximise the quality of life of breast cancer survivors.
Breast cancer-related lymphoedema
Breast cancer-related lymphoedema (BCRL), a distressing adverse effect of breast cancer treatment, presents as a
chronic swelling of the arm which can be accompanied by pain, skin changes, decreased joint range of motion
and recurrent infections.2,3 It can present as generalised oedema or be localised to a specific region of the arm.
4 It is
associated with significant functional, psychological and social morbidity and adversely impacts on individuals’
quality of life.5–12
Incidence and prevalence
Estimates of BCRL incidence and prevalence vary consider- ably in the literature due to a lack of standardised
diagnostic criteria and measurement procedures,13,14 limitations imposed by study designs along with variations in
study populations and follow-up duration.14,15 Studies have variously reported evaluation methods including self-
report of symptoms (e.g. heaviness, aching, swelling, loss of function),16,17 objective measurement (using an array of
measurement tools and protocols)18–20 and a combination of the self-re- port and objective measures.
21–24
The
evaluation method- ology is likely to affect incidence findings as recent studies using multiple methods have
indicated greater subjective reporting of symptoms compared with objective measurement classification of
BCRL.22,25 The multifaceted nature of morbidity resulting from BCRL, across physical, functional, social and
psychological domains, indicates that a multi-dimensional assessment methodology including subjective and
objective findings is likely to provide optimal validity. Subjective assessments which concentrate singularly on
physical symptoms may lack specificity, as numbness for example can be a consequence of breast cancer treatment
Breast cancer-related lymphoedema risk reduction advice: A challenge for health professionals 3
in the absence of measurable BCRL.26 Similarly, objective measures do not consider the variation in functional and
psychosocial impacts that can be present in women with similar objective levels of swelling.26 Lymphoscintigraphy,
a nuclear medicine imaging technique, along with other imaging technologies, have been used to investigate the
pre- and post-operative risk of lymphoedema development in patients with breast cancer.27–29 The uptake of this
imaging modality in the clinical diagnostic process is not universal30
and is the topic of continuing experimental
evaluation.31 New technologies such as bioimpedance may aid diagnosis and provide a level of accuracy in clinical
examination not previously possible through traditional measurement techniques such as circumferential
measures.32 The absence of agreed cut-off values defining BCRL may negate the advantages of technical advances
and affects comparisons across studies. Edwards22 demonstrated a more than doubling of BCRL incidence if the
criteria used to positively establish the condition was a 5% rather than 10% change in ipsilateral upper limb volume
as evaluated with circumferential measurements. Standardisation of the evaluation methodology and diagnostic
criteria used to positively identify BCRL is required. Further research is necessary as currently inter-study
comparison of assessment or management programs are confounded by the absence of a universally agreed
definition.33
An historical review of BCRL literature suggested that advances in management and detection may have created
temporal variations in breast cancer populations with respect to BCRL incidence.15 The population of breast cancer
survivors currently alive includes those treated with radical, and later, modified radical mastectomy, breast
conserving surgery, various levels of axillary dissection, radiotherapy using a multitude of protocols, as well as
numerous chemo- therapy and hormone therapy regimens.34 This creates a heterogenous population and may
account for part of the variation of reported BCRL between sample populations.
Studies have variously reported BCRL prevalence of 6– 30%14 and more recently, 26% in breast cancer
survivors.35 A prospective single-site study of breast cancer patients treated with axillary node sampling, excision
or biopsy found that by three years post-operatively 20.7% of study participants had developed BCRL.18 In contrast,
a retrospective study of women twenty years after either modified or radical mastectomy plus axillary dissection
found that lymphoedema was at least subjectively reported by 49% of participants, as evaluated by questionnaire
4 I. Nielsen et al.
and arm circumferential self-measurements.23 BCRL onset is most likely to occur during the initial two to three
years post-operatively however much later onset has been recorded.23
Clark and associates18 found that of the individuals assessed as having lymphoedema on objective evaluation
only half had previously been diagnosed and received treatment. This may occur due to the lack of agreeance
regarding parameters for diagnosis of BCRL, poor sensitivity of subjective questions used to identify BCRL or
lack of clarity regarding BCRL information provided to patients.
Costs
The health costs of management of BCRL are not available in the literature, however Moffatt et al.30 reported that
in South West London 29% of people identified with lymphoedema experienced an acute infection in the affected
area over the previous year with 27% being admitted for intravenous antibiotics. Mean length of stay for this
condition was 12 days, and the estimated mean cost was £2300. They also reported that lymphoedema caused time
off work in greater than 80% of cases, and affected employment status in 9%. The Australian Institute of Health
and Welfare36
(AIHW 2003) records show that 677 Australians were admitted to a public or private hospital with
a primary diagnosis of lymphoedema between July 1999 and June 2000. It is considered that most of these
admissions were due to infection of the affected limb and that many admissions may not have been identified due
to the coding procedures used. There also appears to be no estimates of the individuals’ lifetime cost for
compression garments and bandages, access to complex physical therapy or manual lymphatic drainage treatment
and the cost of altered and appropriate clothing. In summary there appears to be a significant cost associated with
BCRL to the individual, the health system and society which is yet to be quantified.
The ‘‘at-risk’’ population
The aetiology of BCRL remains incompletely defined, with the initial treatment-related trauma to the axillary
lymphatic system (surgery and/or radiation) generally agreed to constitute the catalyst for the condition.37,38
Incompetence of the lymphatic system within the ipsilateral upper limb and torso can then promote the chronic
accumulation of lymphatic fluid with associated skin, soft tissue and micro- vascular changes,39 including chronic
Breast cancer-related lymphoedema risk reduction advice: A challenge for health professionals 5
inflammation and fibrosis.4 A variety of characteristics of the individual’s lymphatic and microvascular
functioning along with suggested compensatory responses may be responsible for the apparently selective nature
of BCRL in the population of breast cancer survivors.28,40,41 Moreover, in the last decade examination of the
potential genetic susceptibility of individuals to lymphatic problems has commenced. A number of molecular
signatures unique to the lymphatic system have been identified. This has redefined diseases associated with
lymphatics at the molecular level. It is likely that current modes of treatment for diseases such as lymphoedema
will be augmented in the future with molecular therapies. Ani- mal models are currently being tested.42
Recent advances in the surgical management of the axilla through sentinel lymph node biopsy (SLNB) has
improved upper limb morbidity and reduced lymphoedema prevalence at least in the short-term.43,44 Findings from
a large multi- center trial showed a significantly reduced risk of developing BCRL in the first year post-operatively
following SLNB compared with Axillary Lymph Node Dissection (ALND) (5% vs 13%, respectively).43 Long-
term differences in lymphoedema occurrence with SLNB have yet to be reported. The continuing trend towards
less radical and invasive treatment such as SLNB may reduce but not eliminate the risk of upper limb symptoms43
and the increased risk remains for patients currently or previously managed with ALND or those with positive nodes
who proceed to axillary dissection techniques following SLNB. Indeed patients in their 30s currently undergoing
axillary treatment (ALND, SLNB and/or axillary radiation) will retain their lymphoedema risk for the remainder
of their lives, conceivably six or seven decades or more. For the health professional, this highlights the importance
of understanding BCRL as a chronic condition, or at least chronic threat, impacting upon the lives of each individual
diagnosed with breast cancer.
Age
Studies have shown a significant association16 or trend towards association
26 between younger age and subjective
reporting of upper limb symptoms. A study using objective arm circumferential measures found the incidence of
BCRL in older patients (>55 years old) was significantly higher than younger patients.45 It has been reported that
this may be related to a greater likelihood amongst older breast cancer survivors to attribute their symptoms to the
aging process or comorbidities26,46 and may also reflect greater awareness of functional limitations caused by BCRL
6 I. Nielsen et al.
symptoms in younger women who are more active in work, recreational and parenting roles.26
Handedness
Studies with cross-sectional design have produced variable results related to the association between BCRL and
the dominant arm including a significant association,47 a significant association with forearm oedema only
48 and no
association.49 In a recent prospective study surgery to the dominant side was shown to not be significantly
associated with BCRL risk.18
Work
An association between work outside the home and in- creased limb volume in lymphoedematous patients has been
suggested.50 Women employed outside the home may have less time to implement swelling control measures.
51
Larger limbs result in greater physical problems and the impact is particularly distressing if financial security is
threatened because employment ceases51 or alters. It has been reported that BCRL reduces a woman’s ability to
participate in the paid workforce52
and that jobs involving repeated use of the affected arm, such as lifting, gripping,
holding and other fine and gross motor tasks are difficult to per- form. Some women cease paid employment
because they are no longer able to perform their duties.7
Methodology
A literature search was conducted using Medline and CI- NAHL databases and search terms ‘‘lymphoedema’’ or
‘‘lymphedema’’ and ‘‘breast’’ and ‘‘cancer’’ or ‘‘neo- plasm’’ or ‘‘carcinoma’’ for articles published in English
between 1995 and February 2007 with 489 and 156 resultant citations respectively. This search was combined
with ‘‘risk’’ or ‘‘advice’’ or ‘‘precaution’’ or ‘‘aetiology’’ producing 134 and 74 articles which formed the basis
of the review. The resultant abstracts were reviewed by the authors AS and IN independently for relevance to the
topic of BCRL modifiable risk factors and risk reduction advice. Due to the small number of articles (30)
examining the topic, all those related to modifiable (lifestyle-related) risk factors and risk reduction advice which
had been identified by both authors were reviewed by IN. Where discrepancy arose in the inclusion of literature,
Breast cancer-related lymphoedema risk reduction advice: A challenge for health professionals 7
IN retained final determination in consultation with SG. Literature was also obtained regarding BCRL incidence
and prevalence, diagnostic methodology and clinical characteristics, however was not reviewed systematically as
this was beyond the purpose and scope of the review.
Current risk reduction advice
Advice regarding precautions and lifestyle modification aimed at reducing the life-long risk of BCRL
development is regarded as an important aspect of the care of breast cancer survivors. This advice largely lacks a
sound evidence-base, being derived primarily from anecdotal information and reasoning based on an incomplete
understanding of the condition’s aetiology.
There are a multitude of BCRL risk reduction advice information sources currently available for breast cancer
survivors. Prominent lymphoedema, cancer and health organizations publish recommendations on the World
Wide Web. The format of these ranges from very prescriptive (a list of specific do’s and don’ts) to a discussion
of broader principles. Commonly BCRL precautions include avoiding accidental and non-accidental skin trauma
and infection,53–55
limb constriction, 53,54
weight gain53–56 and exposure to extreme temperatures
, 53–55
in addition
to promoting early diagnosis and management through self-surveillance.54–56 Precautions regarding exercise and
air travel vary between organizations. Most advocate limiting strenuous exercise56 or advise the use of a
compression garment if doing resistance training54 and recommend avoiding or limiting activities such as heavy
gardening activities and lifting heavy shopping.55,56 Use of a compression garment when flying is stated as a
requirement by some organizations54,55 but is less stringently mandated by another.
56 Some also advocate for the
prophylactic use of benzopyrones55 and adherence to a nutritious, balanced diet.
53,55
Results
Flight
Evidence for the potential of air travel to exacerbate or initiate BCRL is scant and contradictory. A retrospective
questionnaire-based survey of Lymphoedema Association of Australia members indicated that a small number of
respondents (12 of the 163 identifying themselves as having arm oedema) identified air travel as having triggered
8 I. Nielsen et al.
or aggravated their lymphoedema.57 The findings should be viewed as largely anecdotal considering the
methodological limitations of unconfirmed lymphoedema diagnosis, response rate considerations (70%) and non-
representative sampling (national lymphoedema association membership). Graham58 failed to find a significant
association between flying and permanent development or exacerbation of arm oedema, however, an association
between temporary swelling and overseas flights was noted. In this study, 24% of those who flew had used
precautions, with compression garments (used by 17% of fliers) the most common strategy. Those who used
precautions were more likely to have a clinical diagnosis of BCRL, indicating potentially better knowledge, greater
contact with health professional and/or greater motivation. Graham58 noted an incidental finding among patients
experiencing increased oedema following air travel to holidays in hot regions. Larger prospective studies are
required to clarify the degree of risk posed by flight.
Temperature
BCRL risk reduction advice can include avoiding higher temperatures such as submersion of the ‘‘at-risk’’ arm in
hot tubs or saunas for greater than 15 min or submerging the limb in water above 102 °F (~38 °C).54 Temperature
precautions suggest that climate may have an impact on lymphoedema development, aggravation and therefore
management. There have been no studies which have investigated the relationship between development of BCRL
and hot or tropical climates. Moreover, the needs of breast cancer survivors in relation to risk reduction and
management of lymphoedema in hot and tropical regions remains undistinguished from those in more temperate
areas.
Exercise and activity
Bendz and Fagevik Olsen59 demonstrated early post-operative upper limb exercises produced no significant
difference in BCRL incidence in the first two years post-operatively compared to delayed commencement of
exercise at two weeks post-operatively. Following the immediate post- operative period, a review by Bicego and
associates60
indicated that the trend in the literature did not support the advice that upper limb exercise was
contraindicated in breast cancer survivors although further, more rigorous study was required. A further randomised
Breast cancer-related lymphoedema risk reduction advice: A challenge for health professionals 9
controlled trial of breast cancer survivors (with and without BCRL) found that participation in a six-month resistance
training program did not significantly elevate the risk of BCRL onset or progression.61 Lane and associates
62
suggested that exercise could in the longer-term lead to adaptive changes which would act to protect or reduce the
oedema of an ‘‘at-risk’’ limb. This suggestion requires empirical testing.
The need to use compression garments while exercising lacks consensus in the literature. Studies have included
protocols requiring the use of compression garments63,64 or leaving their use to the discretion of individual
participants.65 Johansson and associates
66 randomly assigned compression garment use to either day 1 or 4 of the
training program. Results indicated no significant difference in BCRL exacerbation dependent upon use of garments.
Further investigation of the longer-term requirements regarding garment use when exercising would assist health
professionals when providing advice and reassurance to breast cancer survivors wishing to exercise.
Venapuncture, other non-accidental trauma and infection
Intentional skin puncture to the ipsilateral arm while in hospital was found to be associated with a significantly
increased risk of developing BCRL within the first three years post-operatively.18 The findings of this prospective
study support largely anecdotal findings from previous authors.67,68 Indications from this small evidence-base
prompted Cole69
to advise against blood pressure measurement, subcutaneous and intramuscular injection and
other clinically occur- ring non-accidental skin puncture wherever possible.
A retrospective study by Petrek and associates23
identified a significant association between self-reported history
of arm infections requiring antibiotics or arm injuries and BCRL occurrence. However, the study design and
potential for recall bias limits the use of this finding in discussions of causation. Post-operative infection was found
to be associated with BCRL development in one study70 but not in another.
48 There is a lack of evidence clearly
identifying infection as a causative factor in BCRL development, how- ever the concept has a plausible
pathophysiological basis. Further, the potential for variables such as warm, tropical climates to affect infection,
skin care and compliance with current advice has not been examined in the literature.
10 I. Nielsen et al.
Limb constriction
The proposed causative role of limb constriction such as through blood pressure monitoring or wearing tight
clothing on the at-risk arm has not been studied systematically.29 Advice to avoid constriction is based on the
physiological rationale that constriction may impede lymphatic flow which is already impaired.
Obesity (high BMI)
Numerous studies have reported a statistically significant association between obesity and lymphoedema.18,22,66,70–
74 A 20-year retrospective study showed that weight gain since treatment for breast cancer was a stronger predictor
of BCRL than being overweight at diagnosis,23 however determining causation was precluded by the study design.
Findings from Johansson and associates66 suggest that individuals with BCRL have lower physical activity
participation levels than matched breast cancer survivors without lymphoedema. BCRL may promote weight gain
through reduced activity levels. The findings highlight the importance of counselling women of the importance
of returning to optimal physical activity levels as soon as possible following treatment for breast cancer in an effort
to limit weight gain and providing reassurance and opportunities for women to exercise. Addressing physical
activity levels in individuals with BCRL is also indicated in order to limit weight gain and the associated physical
and psychosocial morbidity.
Delayed diagnosis/treatment
Although not strictly a risk factor for developing BCRL, delayed diagnosis and management is likely to lead to a
more advanced clinical presentation at diagnosis, a longer and more difficult treatment program and a poorer
outcome from treatment.75–78
Early diagnosis would be facilitated by more sensitive evaluation tools and diagnostic
criteria, with new technologies such as bioimpedance offering a route for further study.
Breast cancer-related lymphoedema risk reduction advice: A challenge for health professionals 11
Discussion
Supported current advice
Clearly larger, methodologically rigorous studies are required to provide an evidence-base for health professionals’
advice for breast cancer survivors. At the current time, it is reasonable to continue to advise individuals at-risk of
developing BCRL to avoid non-accidental skin trauma to the ‘‘at-risk’’ limb (such as cannulation) and weight gain,
to try to prevent infection through taking reasonable care and treating any skin breaks promptly and to monitor their
upper limb and report changes to their treating health professional. The use of compression garments as prophylaxis
when flying or on long car journeys and when exercising has less to support it and may, with appropriate education
provided on the rationale and risks, be left to the discretion of the individual. Similarly, precautions related to
temperature should be discussed with the individual with clear indication of the lack of evidence-base but
appropriate rationale based on lymphatic physiology provided. Recent findings indicate that women should be
encouraged to participate in exercise and activity that involves the upper limb. It may be prudent, in light of limited
evidence and for consistency with other recommendations, to counsel against exercise likely to cause trauma to the
arm (either through excessive resistance or soft tissue injury). Numerous studies have indicated that exercise can
positively affect breast cancer survivors’ psychological and physical well-being65,79 Which further supports this
recommendation.
Advice delivery
Optimal methods for providing BCRL advice to breast cancer survivors have received only minimal coverage in the
literature. Collins and associates’80
qualitative study found that there was variation in women’s experience of BCRL
risk reduction education. Some women recalled receiving information on BCRL risk from health professionals
(nurses and physiotherapists) in the post-operative period. Most women in the study felt that they had not been
provided with adequate information generally on possible complications of their treatment by the doctor/oncologist.
In contrast, Coward17 found that the majority of breast cancer survivors within the study could recall being told of
the risk of BCRL. Women were selective in the risk reduction strategies they had adopted, with protecting the arm
from overuse and trying to prevent infections secondary to accidental skin trauma the most commonly adopted.
12 I. Nielsen et al.
Coward’s17 results showed that there was no difference between women with BCRL and without BCRL in terms of
their knowledge of lymphoedema. These results, based on a questionnaire, must be viewed in the context of potential
selection bias based a low response rate (45%). Ridner81 found that individuals with BCRL were significantly less
likely to recall receiving risk reduction advice.
The timing of the provision of risk reduction advice has also attracted minimal investigation. Passik and
McDonald82 suggested that some discussion of BCRL is required pre- operatively as part of informed consent
processes. Collins and associates80 suggested that the period of diagnosis and surgery is not the optimal time to
discuss BCRL precautions because of the emotional and physical intensity of the situations. Instead, they suggested
providing written and verbal educational materials and utilising opportunistic screening at follow-up appointments
to provide education, monitoring and support.
Passik and McDonald82 suggested that BCRL precautions should be stated in such a way as to educate and
empower breast cancer survivors, rather than as a list of restrictions. This would imply that precautionary advice
should therefore be linked to an appropriate level of foreground knowledge of the pathophysiology and presentation
of the condition where this is feasible and acceptable for the individual patient. However, clinical judgement is
required by the health professional in assessing the informational needs of the patient and professional training may
be required to facilitate this process. Hack and associates83 reported that with respect to discussion of their early
stage breast cancer, women have varying preferences for the volume, format and complexity of information provided
to them. A small proportion, generally those adopting a more passive treatment decision-making role, preferred to
receive limited information. Ridner’s81 recent study indicating a trend towards patients preferentially accessing
information from internet sources highlights the need for all members of the care team to be informed and provide
consistent information related to BCRL risk. Further research is needed to provide health professionals with a clearer
indication of breast cancer survivors information needs regarding BCRL, particularly considering the array of
information sources, of various quality, available through the World Wide Web and mass media.
Creating an opportunity for potentially lengthy discussion of BCRL will impact upon the management of
patient recovery from breast cancer treatment as education, particularly if reviewed over several follow-up
appointments, is more time-consuming than presenting a list of restrictions during patients’ inpatient care. Care
Breast cancer-related lymphoedema risk reduction advice: A challenge for health professionals 13
protocols vary between health systems and facilities. The United Kingdom’s National Institute for Clinical
Excellence recommends follow-up with particular focus on detecting adverse consequences of treatment,
especially BCRL, for 2–3 years post-operatively.84 Findings by Box and associates
75 support the surveillance of
breast cancer survivors for the first two years post-operatively in order to apply BCRL interventions as early as
possible. Their study found reduced incidence of BCRL in patients who received risk minimisation education and,
where an acute episode of oedema was detected, early physiotherapy intervention.
Effect of BCRL risk reduction advice
There has been minimal investigation of the effect of BCRL precautionary advice on the breast cancer survivor.
Psychological morbidity resulting from advice that is excessive and causes fear and anxiety regarding the
development of the condition, has not been studied systematically. Graham58 found that a minority of study
participants expressed fear of developing BCRL due to air travel. This fear did not significantly differ between those
who had flown and those who had not. A qualitative study by Collins and associates80 revealed that some study
participants expressed fear of developing BCRL along with frustration and confusion regarding the risk posed and
perceived risk reduction advice contradictions. Findings by Polinsky85 indicate that only 5% of study participants
reported changing their social activities (travel and flying) due to their experience with breast cancer. More than
half (54%) reported using caution with use of their arm. The psychosocial sequelae of risk reduction advice in terms
of impact on the perception of recovery and quality of life in the post-treatment period requires more specific
investigation.
Conclusion
High quality research is required across the spectrum of BCRL investigation; aetiology, epidemiology and risk
reduction, education and management. BCRL risk reduction advice for which the literature currently provides some
support includes avoiding non-accidental skin puncture of the upper limb and limiting weight gain. Avoiding
infection and trauma to the upper limb is a reasonable precaution. Early diagnosis and management should be
promoted through patient education and self-surveillance and vigilance of health professionals in clinical encounters
14 I. Nielsen et al.
in order to provide opportunistic screening. Avoidance of resistance exercise and the prophylactic use of
compression garments when exercising or travelling by air have less support but should form part of patient education
such that individuals are equipped and empowered to make decisions on their course of action.
Investigation of emerging objective tools for identification of early BCRL and increased sensitivity of subjective
measurement tools is required to improve the early diagnosis and identification of the ‘‘at-risk’’ arm in breast cancer
patients. Further, research to identify evidence for or against current risk reduction advice must be undertaken to
decrease the potential morbidity associated with lifestyle alteration in response to current largely anecdotally derived
advice.
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