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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptHHS Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
 
J Cancer Surviv. Author manuscript; available in PMC 2013 June 17.
Published in final edited form as:
PMCID: PMC3683656
NIHMSID: NIHMS472609

Quality of life among breast cancer patients with lymphedema: a systematic review of patient-reported outcome instruments and outcomes

Abstract

Purpose

Lymphedema following breast cancer surgery remains a common and feared treatment complication. Accurate information on health-related quality of life (HRQOL) outcomes among patients with lymphedema is critically needed to inform shared medical decision making and evidence-based practice in oncologic breast surgery. Our systematic review aimed to (1) identify studies describing HRQOL outcomes in breast cancer-related lymphedema (BCRL) patients, (2) assess the quality of these studies, and (3) assess the quality and appropriateness of the patient-reported outcome (PRO) instruments used.

Methods

Using the PRISMA statement, we performed a systematic review including studies describing HRQOL outcomes among BCRL patients. Studies were classified by levels of evidence and fulfillment of the Efficace criteria. PRO instruments were assessed using the COSMIN criteria.

Results

Thirty-nine studies met inclusion criteria, including 8 level I and 14 level II studies. Sixteen of 39 studies were compliant with the Efficace criteria. Seventeen HRQOL instruments were used, two specific to lymphedema patients. Exercise and complex decongestive therapy treatment interventions were associated with improved HRQOL.

Conclusions

High-quality data on HRQOL outcomes is required to inform surgical decisions for breast cancer management and survivors. Of the lymphedema-specific PRO instruments, the Upper Limb Lymphedema 27 (ULL-27) was found to have strong psychometric properties. Future studies should strive to use high-quality condition-specific PRO instruments, follow existing guidelines for HRQOL measurement and to consider economic burdens of BCRL.

Implications for Cancer Survivors

As lymphedema may develop many years after breast cancer surgery, the ULL-27 may offer greater content validity for use in survivorship research.

Keywords: Lymphedema, Breast cancer, Quality of life

Introduction

Breast cancer is the most common cancer in women with an estimated 230,480 new cases in 2011 [1]. While treatment of breast cancer has improved, arm lymphedema following axillary lymph node dissection (ALND) remains a common complication occurring in as many as 30–50 % of patients who undergo this treatment. Affected patients develop chronic accumulation of interstitial fluid resulting in fibro-adipose deposition and swelling. This swelling can lead to pain, decreased function, body image disturbance, and anxiety [2]. Treatment for lymphedema is limited and primarily palliative in nature, aiming to prevent disease progression. Accurate information on health-related quality of life (HRQOL) outcomes among patients with breast cancer-related lymphedema (BCRL) is important since lymphedema is known to have a significant impact on the physical, psychological, and social health of patients [2, 3]. In fact, recent studies have shown that some patients develop symptoms of lymphedema without objective changes in arm circumference, indicating that clinical measurements may underestimate the incidence and impact of lymphedema [4].

Assessments of patient symptoms and HRQOL outcomes are made using patient-reported outcome (PRO) instruments, or questionnaires, that quantify significant outcome variables from the patient’s perspective [5, 6]. When developed and validated according to international guidelines, PRO instruments can facilitate reliable and valid patient assessment. While generic PRO instruments are designed to measure outcomes across diverse patient populations, condition- or disease-specific measures may provide more sensitive assessment for specific populations, such as patients with lymphedema. International standards have also now been established to evaluate HRQOL study methodology (Efficace criteria, Table 1) with a goal of improving study design and minimizing the risk of bias [7]. As researchers seek to better understand the impact of BCRL on HRQOL, high-quality studies that incorporate the best available PRO instruments and use the most rigorous study methodology are needed in order to provide the highest level of evidence to guide treatment decisions.

Table 1
The Efficace criteria [7]

To better understand the level of scientific evidence afforded by existing studies, the aims of our systematic review were threefold: (1) To identify and summarize results from studies that describe HRQOL outcomes in BCRL patients, (2) to assess the quality of these studies using established criteria for HRQOL study methodology; and (3) to assess the quality and appropriateness of the PRO instruments used in these studies.

Methods

Search Strategy

Our review was guided by the PRISMA statement and included a search strategy focused on three components (1) breast cancer; (2) lymphedema; and (3) quality of life (Fig. 1) [8]. Limitations were placed to exclude non-BCRL studies, conference abstracts, and breast cancer in men. Potentially relevant papers were examined by two reviewers (YC and CA) who worked independently, with discrepancies of opinion resolved by a third (AP). Inclusion criteria were as follows: (1) the study cohort was composed of BCRL patients and (2) the study described HRQOL outcomes among BCRL patients using a formally developed and validated PRO instruments. Studies were excluded if they were not in English, used a non-validated PRO instrument, or a modified version of standardized instrument that was itself not validated. Citations for relevant articles were examined to identify additional articles.

Fig. 1
Flow diagram for systematic review methodology in line with PRISMA guidelines [8]

Indicators of the methodological quality of each publication included study design and Efficace compliancy. Studies were classified by levels of evidence (Table 2) [9]. PRO instruments used to evaluate HRQOL in each study were assessed using the Consensus-based Standards for the Selection of Health Measurement Instruments (COSMIN) criteria [10].

Table 2
Description of scientific levels of evidence and corresponding studies as outlined by the AHRQ [9]

Results

Search results

The literature search identified 1,792 articles and of these 85 studies met some or all inclusion criteria. An additional seven articles were identified through review of citations. A total of 39 manuscripts met inclusion criteria (Table 3).

Table 3
Studies assessing HRQOL in breast cancer-related lymphedema patients

Study quality: levels of evidence and Efficace criteria

Studies were categorized by level of evidence as follows: 8 studies were level I [4, 1117], 14 studies level II [1831], 8 level III [2, 3238], and 9 studies level IV [3947]. Sixteen [4, 1113, 15, 16, 18, 2022, 26, 27, 31, 34, 38, 46] of 39 studies were compliant with the Efficace criteria (Table 1). Of the 16 compliant studies, six were level I studies, seven level II, two level III, and one level IV.

HRQOL instrument quality: COSMIN criteria

Seventeen HRQOL instruments were identified in the 39 articles. Most studies used a generic instrument with or without oncology-specific instruments. Four different generic HRQOL instruments were used including the SF-36 (used in 15 studies). Nine HRQOL instruments were oncology-specific including the EORTC-QLQ-30 (11 studies), EORTC-QLQ-BR23 (2 studies), WHOQOL-BREF (1 study), FACT-B (5 studies), and FACT-B +4 (4 studies). Table 3 also provides a summary of the HRQOL instrument and the HRQOL domains evaluated. While all these instruments have been extensively validated, they are relatively generic (with the notable exception of the FACT-B +4 which has five lymphedema-specific questions).

We identified two HRQOL instruments developed specifically for BCRL patients. These instruments were the Wesley Clinic Lymphedema Scale (WCLS) [31] and the Upper Limb Lymphedema—27 questionnaire (ULL-27) [48].

The WCLS was used in two studies and the ULL-27 in three. The WCLS was developed by adapting the Functional Living Index-Cancer (FLIC) instrument [49]. The term “lymphedema” was substituted for the words “illness” or “cancer” in the FLIC. Qualitative work to confirm the validity of the scale in patients with lymphedema was not published nor was formal psychometric analysis. The ULL-27 was developed specifically to address the need for a condition-specific instrument in assessing the unique HRQOL issues of importance to BCRL patients. Its conceptual framework and content were developed from patient interviews. The ULL-27 has a total of 27 items and measures the following domains: functional (15 items); psychological (7 items); and social (5 items) [48]. Psychometric evaluation was performed in a sample of 304 patients. Convergent and discriminant validity were evaluated against the Patient’s Arm Comfort Scale, Global Symptom Index, and the SF-36. The ULL-27 has good reliability (the extent to which scores for patients whose HRQOL has not changed are the same for repeated measurements; Cronbach’s alpha >0.9 and intra-class correlation coefficients of >0.8), validity (as measured by the degree of interrelatedness among the items in a scale; internal consistency 0.42–0.77) and responsiveness (ability to detect change over time; effect size of >0.4) [48]. Despite its careful qualitative development and strong psychometric properties, the ULL-27 has been used in only three published studies to date.

HRQOL Outcomes in BCRL patients

The focus of most studies (15 of 39 studies) was to compare HRQOL in BCRL patients to that of breast cancer patients without lymphedema. The majority of studies reported significantly poorer HRQOL outcomes in patients with BCRL resulting in decreased physical functioning, as well as psychological and social well-being. Patient age, body weight, and race were all noted to influence or confound HRQOL outcomes among patients with BCRL. Changes in social well-being were most marked among younger patients, with women under the age of 40 experiencing decreased social well-being compared to older patients [42]. Body weight also emerged as an important covariate. Interestingly, one level II study found that BCRL patients who were either under or overweight were more likely to report decreased HRQOL compared to women of normal weight with lymphedema [18]. Obese women with lymphedema reported the most significant diminution in HRQOL [18]. Racial differences were also noted; in one level III study, 99 Caucasian women with lymphedema reported significantly higher FACT-B scores and hence better HRQOL compared with a small sample of ten non-Caucasian women with lymphedema [32].

Of the 39 studies included in this review, 18 evaluated the impact of different treatment interventions on HRQOL. Exercise and its effects on HRQOL in BCRL patients were assessed in six studies (three level I and three level II). One level 1 study found that older women (>50 years) had significantly improved strength and health scores after twice weekly exercise regardless of lymphedema status [11]. Among lymphedema patients participating in an exercise physiotherapy program (level II study), physical function was not reported to improve over 5 years; however, global health was found to significantly improve from baseline [19]. Similar findings were reported in another exercise study, where general health, vitality, and physical functioning all improved in patients undergoing exercise compared to control groups [16].

The treatment modality of complex decongestive therapy (CDT) was evaluated in six studies (five level II and one level IV). Significant improvements in physical and psychological function were reported when CDT was combined with exercise regimens [12]. Several novel therapies were also assessed such as aqua lymphatic therapy, flexi-touch, and liposuction in combination with CDT. Psychological and social function improved significantly in patients having aqua lymphatic therapy (level I study) [13].

Discussion

The objective of this review was to identify and examine published studies on HRQOL outcomes among patients with BCRL. Of the 39 publications that fulfilled our inclusion criteria, 8 provided level I evidence and 14 were level II. While these level I and II studies had generally smaller sample sizes, they utilized robust study methodology and were more likely to meet guidelines for HRQOL measurement as established by the Efficace criteria. Notably, six high level studies were performed in 2010, highlighting the growing interest in HRQOL outcomes among BCRL patients and awareness of the importance of good study design. Somewhat disappointingly, only 16 studies were compliant with the Efficace criteria.

The majority of studies reported diminished HRQOL in patients with BCRL patients. Specific HRQOL domains most affected were body image, physical, psychological, and social function. Patient age, body weight, and race were all noted to be important covariates. This has important implications for clinical decision making and patient education. For women with early-stage breast cancer who are struggling with the decision whether or not to undergo axillary lymph node dissection, it is important that they understand not only their estimated risk of developing lymphedema, but also the anticipated impact on QOL should the condition develop. As an example, obese women are not only more likely to develop BCRL, but when they do the diminution in HRQOL is greater.

In terms of targeted treatments for BCRL, exercise and CDT treatment were associated with the most profound improvements in HRQOL. For years, patients at risk of lymphedema have been admonished to avoid vigorous exercise [50]. Five level I and II trials refute this contention [11, 12, 19, 22, 28]. With respect to CDT therapy, the published body of evidence clearly shows that this form of treatment is of benefit; nevertheless, in an era of cost restriction, insurance payment for this therapy may still be denied. In order to optimally allocate healthcare resources, it is important that the results of such trials be acknowledged and that payers recognize the HRQOL burden of BCRL when left untreated. Importantly, no studies evaluated new therapies such as micro-lymphatic bypass and lymph node transfer despite the growing application of these procedures.

Only one study evaluated cost or provided health utility analyses [25]. As lymphedema is a chronic disease, this topic is of vital importance. Additionally, as patients and payers consider the therapeutic benefits of ALND, the economic burden of BCRL should be further evaluated. Patients with BCRL may not be able to return to work and this may further diminish their HRQOL as well as economic productivity.

We also evaluated the quality and appropriateness of the PRO instruments used in published studies of BCRL. Seventeen PRO instruments were used overall. Most studies incorporated well-established generic or cancer-specific PRO instruments. Such generic instruments are not developed to evaluate the specific issues of importance to lymphedema patients. As an example, the SF-36 does not capture the specific symptoms suffered by BCRL patients such as heavy and swollen arms or difficulty grasping or holding objects. While it is appropriate to use generic PRO instruments to compare and contrast values across studies, trials that rely on generic PRO instruments alone cannot be expected to detect subtle but perhaps clinically important changes before and after an intervention or changes over time. For this reason, use of a condition-specific instrument alongside a generic instrument is recommended. In this review, two lymphedema-specific PRO instruments were identified [31, 48]. Based on assessment using the COSMIN criteria, only the ULL-27 can be recommended without hesitation.

An important additional consideration is the extent to which PRO instruments developed for use among patients in active cancer treatment are valid for cancer survivors. As lymphedema is a chronic condition that may develop many years after breast cancer surgery, this is a relevant concern and should be considered when researchers are selecting outcome measures for a new study or interpreting study results. As noted above, the ULL-27 was developed with qualitative input from cancer survivors with lymphedema. As such, this instrument may offer greater content validity for use in survivorship research.

In conclusion, BCRL has a significant impact on the HRQOL of breast cancer survivors and is an important consideration when contemplating elective ALND in patients with early-stage breast cancer. Although lymphedema research has gained momentum recently, additional levels I and II studies are required. These studies will help promote therapeutic innovation, provide support for newly developed treatment options such as microsurgical bypass or lymph node transfer, and shape health care policy.

Footnotes

Conflict of interest The authors declare that they have no conflict of interest

Contributor Information

Andrea L. Pusic, Memorial Sloan Kettering Cancer Center, 1275 York Ave, New York, NY 10065, USA.

Yeliz Cemal, Memorial Sloan Kettering Cancer Center, 1275 York Ave, New York, NY 10065, USA.

Claudia Albornoz, Memorial Sloan Kettering Cancer Center, 1275 York Ave, New York, NY 10065, USA.

Anne Klassen, McMaster University, Hamilton, ON, Canada.

Stefan Cano, Clinical Neurology Research Group, Peninsula College of Medicine and Dentistry, Plymouth University, Plymouth, UK.

Isabel Sulimanoff, Memorial Sloan Kettering Cancer Center, 1275 York Ave, New York, NY 10065, USA.

Marisol Hernandez, Memorial Sloan Kettering Cancer Center, 1275 York Ave, New York, NY 10065, USA.

Marga Massey, The Dr. M Massey Practice Group, Roper Office Medical Building Suite #550, Charleston, SC, USA.

Peter Cordeiro, Memorial Sloan Kettering Cancer Center, 1275 York Ave, New York, NY 10065, USA.

Monica Morrow, Memorial Sloan Kettering Cancer Center, 1275 York Ave, New York, NY 10065, USA.

Babak Mehrara, Memorial Sloan Kettering Cancer Center, 1275 York Ave, New York, NY 10065, USA.

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