Physical Therapist Management of Lymphedema Following Treatment for Breast Cancer: A Critical Review of Its Effectiveness.

One out of every 8 women in the United States is expected to develop breast cancer,[1] and 15% to 20% of the women who have axillary lymph nodes removed in the treatment for breast cancer will develop lymphedema in the ipsilateral upper extremity.[2] Lymphedema is a condition in which there is an accumulation of proteins in the affected tissues, causing edema and inflammation within an extremity.[3] Primary lymphedema results from congenital defects in the lymphatic system. Secondary lymphedema is acquired due to obstruction or interruption of the lymphatic flow at the site of the lymph nodes.[4] In women with breast cancer, lymphedema may arise due to damaged lymphatic vessels and obstruction in lymphatic flow caused by axillary node dissection surgery or radiation therapy.[5]

Lymphedema can lead to a feeling of heaviness and discomfort in the involved upper extremity, impairments in function, and unsatisfactory appearance.[4] Large amounts of fluid in an extremity may cause restrictions in range of motion. Chronic lymphedema can compromise the health of subcutaneous tissues, increasing the risk of developing infection. Lymphangiosarcoma, although rare, is an extremely malignant condition that has been associated with chronic lymphedema.[4] Delaying intervention to reduce lymphedema may result in poor functional outcomes, as well as increasing emotional distress.

People with lymphedema can be treated with medications or surgery, but these treatments have been largely unsuccessful.[6] Physical therapists, however, can offer less invasive treatments for lymphedema. Although a cure is not yet available, conservative treatment aims to reduce and control the amount of swelling in an affected limb, as well as to restore the function and cosmesis. Physical therapy interventions for lymphedema have included the use of elastic compression garments; the use of compression pumps; upper-extremity elevation; massage; active, isometric, and resistance exercises[7]; and ultrasound.[8]

Compression garments may be prefabricated or custom-made and are of varying degrees of elasticity. They presumably act to lessen the amount of excess fluid that can enter an affected extremity by increasing interstitial hydrostatic pressure within the limb. External compression by pneumatic pump can be either single chamber or multichamber. Multiple-chamber pumps are sequential in nature, and chambers inflate beginning distally, then inflate proximally. This action serves to move the fluid proximally and out of the affected limb.[4] Elevation reduces intravascular hydrostatic pressure, thus reducing formation of edema. Manual lymph drainage and the Foldi massage technique[9] are used to stimulate residual lymphatic vessels to carry excess fluid from the affected extremity. "Complex physical therapy" (CPT) incorporates the Foldi massage technique but also includes exercises, compression garments, and skin hygiene in an attempt to maintain the reduction in limb size gained by the massage technique.[10,11] Exercise is thought to be beneficial due to skeletal muscle activity aiding the extrinsic pumping mechanism of the lymphatic system. Ultrasound and microwave treatments heat the limb tissues; it is hypothesized that the heated tissues improve lymphatic circulation and thus restore lymphatic flow.[8,12]

Studies using modalities that generate heat, such as ultrasound[8] and microwave,[12] were conducted in Italy and China, respectively. North American experts in physical medicine and rehabilitation have long advised that any modality that generates heat (eg, shortwave diathermy, microwave diathermy, superficial heat) should be used with caution in people with active cancer due to the possibility of increasing tumor growth and metastasis.[13] A recent, well-controlled, randomized trial involving mice that had received subcutaneous injections of tumor cells demonstrated that therapeutic ultrasound enhanced tumor growth, although it did not enhance metastasis.[14] Because it is often not known whether breast cancer is truly in remission, the possibility of a recurrence (ie, active cancer) should always be considered.

There have been numerous descriptive reports and literature reviews regarding conservative treatments for people with lymphedema. Due to the many different treatment options available to practitioners, a diversity of management approaches in various care centers has resulted. The purpose of this review is not only to explore the existing research literature on the management of lymphedema following treatment for breast cancer, but to classify the literature in order to determine the strength of the available evidence. Sackett's rules of evidence[15] categorize studies according to the strength of the research design and the amount of control for possible threats to internal validity. Based on 5 hierarchical levels of evidence (I-V), 3 grades of recommendation (A, B, and C) were created to guide practitioners in treatment options.[15]

Sackett's[15] levels have previously been used to evaluate the literature regarding the physical therapist management of children with cerebral palsy,[16] physical therapy intervention for the management of children with cystic fibrosis,[17] and the efficacy of adaptive seating for children with cerebral palsy.[18] The purpose of this review is to critically analyze the recent research involving physical therapist management of lymphedema secondary to breast cancer treatments. Sackett's rules of evidence were incorporated to develop evidence-based recommendations for physical therapist management of this condition.

Method

Because we are fluent in English only, the literature search was restricted to English publications from 1966 through 1997. Index Medicus, the Cumulative Index to Nursing and Allied Health Literature (CINAHL), and Health Planning and Administration/Health Services, Technology, Administration, and Research (HEALTHSTAR) were searched using the text words "lymphedema," "physical therapy," and "occupational therapy" and specific modality names such as "compression garments," "pneumatic pump," "elevation," and "ultrasound." Reference lists from previously identified research articles were also scanned to locate additional references.

Study Selection Criteria

Studies were required to meet the following 4 criteria before they were included in our review: (1) all subjects had been treated for breast cancer, (2) subjects had secondary lymphedema in at least one upper extremity, (3) conservative or noninvasive treatment for lymphedema was the independent variable, (4) the size of the extremity being treated was a dependent variable.

Review Criteria

Studies were evaluated according to Sackett's rules of evidence.[15] Sackett's 5 hierarchical levels of evidence are as follows: (1) level I--large randomized controlled trial with low false-positive or false-negative errors (high power), (2) level II--small randomized controlled trial with high false-positive or false-negative errors, (3) level III--nonrandomized, concurrent cohort comparisons between contemporaneous subjects who did and did not receive the intervention, (4) level IV--nonrandomized, historical cohort comparisons between current subjects who received the intervention and former subjects who did not receive the intervention, and (5) level V--case series without controls. In level V studies, the clinical outcome of a group of subjects is described, but no control group or condition is included and thus no control of extraneous variables is undertaken. A case study on a single individual cannot be included in this category.

Considering the potential ethical conflicts of having a pure control group for the conditions being studied, Sackett's levels I through IV were modified. Studies in which 2 or more treatments were compared, as opposed to only those in which there was a control group that received no treatment, were also considered appropriate for inclusion in levels I through IV. This method was also suggested in the critical reviews by Piper[16] and Boyd and colleagues.[17]

Sacket[15] also outlined 3 grades of recommendations, based on the levels of evidence. Grade A recommendations are supported by at least one, but preferably more, level I study. Grade B recommendations are made for outcomes supported by at least one level II study. Grade C recommendations are supported by level III, IV, or V studies.

In order to evaluate the methodological rigor of the studies, the following criteria were adapted from Sackett's[19] rules for scientific evidence and Harris'[20] criteria for evaluating scientific merit: (1) inclusion and exclusion criteria were listed for the subjects and included an operational definition of lymphedema, (2) the treatment protocol was adequately described to be replicable, (3) the reliability of data obtained with outcome measures was investigated, (4) the validity of the outcome measures has been assessed, (5) the assessors were blinded to the treatment groups, and (6) all subjects enrolled in the study were accounted for.

Results

Initially, 42 articles were identified that referred to treatment for lymphedema. Many of these articles were reviews or descriptive reports. There were 19 articles that reported experimental or quasi-experimental studies.[7,8,10-12,21-34] To assess the reliability of different raters' judgments in classifying these studies according to Sackett's rules, we independently reviewed and classified them. Interrater agreement on level of evidence was attained for 15 of the 19 studies (78.9%). We discussed the 4 studies on which there was disagreement in determining the Sackett level, and we arrived at a consensus decision for each of the 4 studies.

Thirteen[7,8,10-12,21-28] of the 19 experimental studies also met the 4 study selection criteria. The 6 experimental studies that were excluded were those that involved subjects who had developed lymphedema from causes other than treatments for breast cancer and thus did not satisfy all of the study selection criteria.

Levels of Evidence

The levels of evidence and other study characteristics are summarized in Table 1. Of the 13 studies evaluated according to Sackett's levels, 1 study[21] was identified as a level II study, 5 studies[8,10,22,25,28] were categorized as level III studies, and the remaining 7 studies[7,11,12,23,24,26,27] were classified as level V studies.

[TABULAR DATA 1 NOT REPRODUCIBLE IN ASCII]

Scientific Rigor of the Studies

The scientific rigor of the studies was evaluated by the 6 criteria outlined earlier. These evaluative criteria for each study are summarized in Table 2.

Table 2. Evaluative Criteria for Studies Reviewed

                                                Reliability of
                                                Outcome
                                   Treatment    Measures
                      Defined      Can Be       Was
Author(s)             Lymphedema   Replicated   Assessed

Balzarini et al,[8]
  1993                Y            Y            N
Bertelli et al,[21]
  1991                Y            Y            N
Bertelli et al,[22]
  1992                Y            Y            N
Bunce et al,[23]
  1994                N            Y            N
Gan et al,[12] 1996   Y            Y            N
Kim-Sing and
  Basco,[24] 1987     N            Y            N
Matthews and
  Smith,[10] 1996     Y            N            N
Morgan et al,[11]
  1992                Y            N            N
Swedborg,[7] 1977     N            N            Y
Swedborg,[25]
  1980                Y            Y            Y
Swedborg,[26]
  1984                Y            Y            Y
Swedborg et al,[27]
  1993                Y            Y            Y
Zanolla et al,[28]
  1984                N            Y            N

                      Validity of
                      Outcome
                      Measures       Blind
                      Has Been       Assessment   Account for
Author(s)             Investigated   of Outcome   Attrition

Balzarini et al,[8]

  1993                N              N            Y
Bertelli et al,[21]
  1991                N              N            Y
Bertelli et al,[22]
  1992                N              N            Y
Bunce et al,[23]
  1994                N              N            N
Gan et al,[12] 1996   Y              N            Y
Kim-Sing and
  Basco,[24] 1987     N              N            Y
Matthews and
  Smith,[10] 1996     N              N            Y
Morgan et al,[11]
  1992                Y              N            Y
Swedborg,[7] 1977     Y              N            Y
Swedborg,[25]
  1980                Y              N            Y
Swedborg,[26]
  1984                Y              N            Y
Swedborg et al,[27]
  1993                Y              N            Y
Zanolla et al,[28]
  1984                N              N            Y

Subject inclusion and exclusion criteria. Inclusion and exclusion criteria were similar in most studies. In order to qualify for the review, each article chosen included subjects who had been treated for breast cancer and who had developed lymphedema following treatments. Inclusion criteria required that there be no evidence of active disease or metastases in the subjects. For all of' the studies, the inclusion criteria required subjects to have some degree of lymphedema. In only 9 of the studies,[8,10-12,21,22,25-27] however, were there operational definitions of lymphedema. Within these 9 studies, there were 5 different definitions for lymphedema. Three studies[10-12] based inclusion criteria on the International Society of Lymphology[35] definition, which provides a description of various levels of lymphedema but no measurable size differences. Reliability has not been investigated for the use of this scale. In 2 of the studies,[21,22] subjects had to have a cumulative circumferential difference between the 2 upper extremities of greater than 10 cm across 7 sites. In 2 studies,[26,27] the involved upper extremity had to have 110% of the volume of the uninvolved upper extremity. For 1 study,[8] the researchers required the circumference of the involved extremity to be more than 6.5% larger than that of the uninvolved extremity. In another study,[25] a volume difference of 150 mL was required between the 2 extremities. One group of researchers[24] used self-selected subjects who had requested treatment for lymphedema. These researchers[24] and the researchers in the remaining 3 studies[7,23,28] provided no operational definition for what constituted lymphedema.

Repeatability of the treatment protocol. When specific modalities (eg, ultrasound, pneumatic pressure therapy) were included in an investigation, all but one study[7] provided sufficient detail to allow repetition of the intervention protocol. Researchers using CPT[10,11] did not describe the actual exercises, thus preventing replication of the treatment.

Outcome measure reliability. Reliability of data obtained with the outcome measure was described in 4 of the studies. Swedborg[7] studied the intrarater reliability of measurements obtained by water displacement volumetry over 3 consecutive days in women without lymphedema and found that the greatest variation observed was 1.2% of the total limb volume. Swedborg and colleagues used the same technique in 3 later studies.[25-27] In the remaining 9 studies, there were no assessments of the reliability of data for the outcome measures.

Outcome measure validity. None of the studies included any indication of validity for any of the outcome measures used. Of the 13 studies reviewed, 8 different methods were used to measure the size of the upper extremities. Volume measurement by water displacement, a method used in 5 studies,[7,12,25-27] is considered by many researchers to be the gold standard for estimating the volume of an irregular shape. In the remaining 8 studies, circumferential measurements were used. In 2 studies, circumferential measurements were used to calculate the volume of a cylinder[23] and the volume of a truncated cone.[11] In 2 studies,[24,28] only a single circumferential measurement was compared for the involved and uninvolved extremities. In 4 studies,[8,10,21,22] the circumferences at a number of different sites were measured and summed. Next, the values for the involved and uninvolved extremities were compared. The number and location of sites at which circumferential measurements were taken vary greatly from study to study.

All of these methods appear to have face validity for estimating change in the size of a limb with treatment. Volume calculation by the truncated cone method, which is the method of volume calculation used by Morgan et al,[11] has been studied for the lower extremity[36] and the upper extremity[37] and has been shown to have good concurrent validity with water displacement volumetry (r =.93 and .99, respectively). The concurrent validity of volume calculation by the cylinder method compared with water displacement has been investigated in the lower extremity (r=.99)[29] but not in the upper extremity. Concurrent validity of measurements obtained with the other methods of upper-extremity size estimation has not been investigated.

Blind assessment. In none of the studies was the use of blinded outcome assessors explicitly described.

Account for attrition. In 12 of the 13 studies reviewed, subject attrition was described and the reason for the subject attrition was given. In the study by Bunce and colleagues.[23] one subject was not accounted for at the 1-year follow-up; no explanation was provided for the subject's absence.

Grades of Recommendation

Following Sackett's rules for creating grades of recommendations from the levels of evidence, 7 recommendations were developed. One grade B recommendation is provided from the single level II study. Six grade C recommendations are suggested, incorporating results of the studies evaluated to be at levels III through V.

Grade B recommendation arising from the level II study:

1. Compression garments appear to reduce limb size after 6 months of use. The addition of electrical stimulation does not improve the results.[21]

Grade C recommendations arising from level III to V evidence:

1. Elevation alone is not effective in controlling lymphedema.[27]

2. Microwave treatment, in combination with compression garment use, has demonstrated promising results in the reduction of limb size.[12]

3. Compression garments alone reduce limb size. Pneumatic pumps or electrical stimulation devices, in combination with compression garments, do not improve the results.[22]

4. Complex physical therapy, which combines exercise, Foldi massage, use of compression garments, and skin hygiene, is supported by 2 level V studies,[10,11] although "modified CPT" was found to be just as effective as regular CPT.[10] According to Matthews and Smith, the standard program of CPT requires "daily treatments of more than one hour in duration for a period of four weeks,"[10(p323)] whereas their modified program of CPT required only twice-weekly treatments and used pressure garments rather than compression bandaging.

5. Combinations of treatments including massage, pneumatic pump, and compression garments show promising results in the treatment of people with lymphedema.[23,25]

6. The Wright linear pneumatic pump, a 3-chamber, gradient pressure, sequential intermittent pump, is effective in reducing limb size.[24] as is the uniform pressure pneumatic pump,[28] when followed by the use of compression garments.

Discussion

By using Sackett's rules of evidence to evaluate research articles, some support for the use of various physical therapy interventions and techniques in the management of lymphedema, secondary to breast cancer treatments, has been found. It is important to note, however, that only 1 of the 13 studies reviewed was a randomized controlled trial. This study[21] was graded at level II because of the small sample size, creating low power to detect group differences. The remaining 12 studies were graded at level III or V. This finding is not to suggest that the treatment approaches used in level III to V studies are less effective, but only that the research designs used to study them were less rigorous and thus there is diminished confidence that the treatments themselves created the change in the outcome measure.

The large number of grade C studies indicates the prevalence of less rigorous research in the management of this condition. Further studies with better control and more rigorous designs will clarify the value of the tentative grade C recommendations. Randomized controlled trials provide the best evidence for treatment efficacy.[15] Controlling extraneous variables and randomly assigning subjects to groups to maximize equality between the groups improve the strength of experimental design. By applying strict controls on the experiment, confidence in the findings may increase.

The ability of the randomized controlled trial to capture the complexity of individuals or a unique clinical situation, however, may be overestimated.[38] True experiments are more controlled than typical clinical settings and situations, and results of these experiments may not apply in the clinical setting. Due to ethical considerations, a full randomized controlled trial is not always possible. Sackett's rules of evidence ensure that the' most rigorous research designs are acknowledged as such, but they also allow for other research designs to be recognized. By including observations through other less rigorous forms of research, potentially helpful treatment protocols are recognized, with the intention of increasing benefits to patients.[15] Optimally, recommendations would be similar, regardless of the type of research design or level of evidence of the study. Numerous studies of varying research designs but with similar results would provide the most confidence in recommendations.

The levels of evidence and scientific merit of a study must be considered together before making conclusions regarding the effectiveness of physical therapy intervention for the management of lymphedema. The 13 studies selected for review were analyzed for scientific rigor according to 6 criteria. None of the articles included in the review fulfilled all of the criteria for scientific rigor suggested in this article (see Tab. 2). One way to improve the believability of experimental findings is to include blinding in the assessment of outcomes. This blinding will prevent the researcher from incorporating expectations about the outcome while evaluating a subject. In studies with more than one group, random allocation attempts to control extraneous factors in subject pools, balancing variables throughout the groups.

Outcome measures allow for systematic documentation of the amount of change in the dependent variable in an experiment. In the 13 studies reviewed, 7 different methods were used to quantify the size of the limbs being treated. Investigation or use of outcome measures that give valid and reliable data is a critical component of a strong study. In order for an outcome measure to yield valid data, it must first yield reliable data. Only one investigator in 4 separate studies[7,25-27] demonstrated the reliability of the data obtained with the outcome measure chosen. Five groups of investigators incorporated the gold standard outcome measure into their studies,[7,12,25-27] and one other group of investigators[11] used a previously validated method for determining upperextremity volume. The remaining researchers did not demonstrate validity or reliability of the data for the outcome measures chosen, thus creating further cause for uncertainty in interpreting the results of these studies.

The grade B and C recommendations developed from the levels of evidence should be considered tentatively. First, none of the recommendations were based on many conclusive studies. Instead, recommendations were based on the results of 1 or 2 level II to V studies. Second, from the 13 articles included in the review, 7 different methods were used to quantify the size of the limbs, which does not allow comparison among different treatment protocols. Lastly, only one of the investigators demonstrated the reliability of the data obtained with the outcome measure chosen, which is a necessary, but not sufficient, prerequisite for validity of the data for an outcome measure. Without assurance of outcome measures that yield valid and reliable data, it cannot be determined whether the treatment results are due to the treatment protocol or whether they are a result of measurement error. The combination of these factors causes concern when considering the recommendations based on the available evidence in the conservative management of lymphedema following treatment for breast cancer.

Clinical Recommendations

Despite the relatively limited scientific evidence in support of physical therapy interventions for the management of lymphedema following breast cancer treatment, the following clinical recommendations are suggested:

* Physical therapists should encourage consistent and long-term use of compression garments in patients with lymphedema. Whether these garments need to be custom-fitted sleeves or standard-sized sleeves is not clear from the studies reviewed, nor is there consistency among the studies in the suggested amount of compression provided. A physical therapist with clinical expertise in the treatment of people with upper-extremity lymphedema has recommended a range of 3 compression classes: 20 to 30 mm Hg, 30 to 40 mm Hg, and 40 to 50 mm Hg.[39]

* Combined techniques, involving massage, sequential pneumatic compression, compression garments or compression bandaging, and exercise, may also be effective. It is not clear, however, whether such a combined program is actually more effective than a program involving pneumatic compression only followed by compression garments.

* Based on one study, modified CPT may be just as effective as standard CPT, and it is far less labor intensive and therefore less costly.

* Microwave therapy, used in conjunction with compression garments, may be effective in reducing limb volume, but electrical stimulation, used in combination with compression garments, is no more effective than compression garments alone.

Summary

Thirteen studies using physical therapy for the management of lymphedema following treatment for breast cancer were evaluated according to Sackett's 5 rules of evidence. The 13 studies were also assessed to evaluate scientific rigor according to 6 criteria. One study was evaluated at level II, 5 studies were evaluated at level III, and the remaining 7 studies were evaluated at level V, generating 1 grade B recommendation and 6 grade C recommendations. Caution must be exercised when considering these recommendations because none of them are supported by numerous, definitive studies. More rigorous research, incorporating blind assessment of outcomes and random assignment of subjects to groups, will enhance clarification of these tentative recommendations. Consensus on an outcome measure that yields valid and reliable data for the evaluation of limb size is critical to allow for comparison of results across studies.

References

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[36] Kaulesar Sukul DMKS, den Hoed PT, Johannes EJ, et al. Direct and indirect methods for the quantification of leg volume: comparison between water displacement volumetry, the disk model method, and the Frustrum sign model method, using the correlation coefficient and the limits of agreement. J Biomed Eng. 1993:15:477-480.

[37] Karges JR, Mark BE, Stikeleather SJ, Worrell TW. Assessing the relationship between water displacement and circumferential measurements in determining upper extremity volume in women with lymphedema. Phys Ther. 1997:77;S109-S110. Abstract.

[38] Domholdt E. Physical Therapy Research: Principles and Applications. Philadelphia, Pa: WB Saunders Co; 1993:153-161.

[39] Mark BE. Introduction to evaluation and treatment of lymphedema. Unpublished handout at: American Physical Therapy Association Combined Sections Meeting; February 18, 1996; Atlanta, Ga.

A Megens, PT, is a student in the Master of Science in Rehabilitation Sciences Program, School of Rehabilitation Sciences, University of British Columbia, Vancouver, British Columbia, Canada, V6T 2B5, and Clinician, British Columbia's Children's Hospital, Vancouver, British Columbia, Canada.

SR Harris, PhD, PT, FAPTA, is Professor, School of Rehabilitation Sciences, University of British Columbia, T325-2211 Wesbrook Mall, Vancouver, British Columbia, Canada, V6T 2B5 ([e-mail]). Address all correspondence to Dr Harris.

This work was supported, in part, by a research grant to Dr Harris from the Canadian Breast Cancer Foundation.

This article was submitted January 7, 1998, and was accepted July 7, 1998.