Exercise for Women With or at Risk for Breast Cancer–Related Lymphedema

Breast cancer accounts for approximately one third of all cancers diagnosed in American women. In 2005, it was estimated that 211,240 women would be diagnosed with invasive breast cancer in the United States and 58,490 would be diagnosed with in situ breast cancer.1 Although advancements in technology have led to early detection and a higher survival rate,2 approximately 40,410 US women were expected to die from this disease in 2005.1 Many women experience secondary complications of the disease and its treatments, including decreased quality of life (QOL), weight gain, sleep disturbances, poor body image, fatigue,3 increased risk for osteoporosis, cardiovascular disease, premature menopause, and lymphedema.4 Breast cancer is commonly treated by surgery, chemotherapy, or radiation. Axillary dissection or radiation can result in lymphedema due to obstruction, trauma, and inflammation of the lymphatic system.5Lymphedema has been defined as an abnormal accumulation of protein-rich fluid,4,6 edema, and chronic inflammation5,7 and can elicit pain, tightness, and heaviness in the upper extremity (UE), as well as lead to recurrent skin infections.8 Lymphedema is classified into 3 stages based on severity. Stage I lymphedema is spontaneously reversible9 and typically involves pitting edema, an increase in UE girth, and heaviness.8 Stage II is marked by a spongy consistency of the tissue without signs of pitting edema. Tissue fibrosis causes limbs to harden and increase in size. Stage III, lymphostatic elephantiasis, is the most advanced stage but is rarely seen following breast cancer treatment.9 Management of lymphedema in women with breast cancer has been a subject of debate for many years. Treatment options include elevation, massage, compression garments, pneumatic compression pumps, and complex physical therapy.8 Traditionally, women who had been treated for breast cancer and those with pre-existing lymphedema were advised to avoid strenuous or repetitive activities that required effort with the affected UE because these activities were assumed to initiate or exacerbate lymphedema.10 The purpose of this update is to review and critique recent studies investigating the effects of aerobic exercise and UE resistance training for women with or at risk for breast cancer–related lymphedema. The questions we will address are: (1) Does aerobic or resistance exercise lead to lymphedema in women who are at risk for the condition? and (2) Does aerobic or resistance exercise reduce or exacerbate pre-existing lymphedema? We begin by reviewing the prevalence, etiology and pathophysiology, and diagnosis of lymphedema and then review recent exercise studies. Because no standardized definition of lymphedema exists, breast cancer–related lymphedema may be underreported.5 Erickson and colleges2 and McKenzie and Kalda11 reported that approximately 25% of patients develop lymphedema after breast cancer surgery, with an increase to 38% for those who also undergo radiation therapy. Other risk factors include extensive axillary disease, previous cancer in axillary lymph nodes, and obesity.8 According to Petryk and colleagues,12 a 2-cm difference between the surgical-side UE and contralateral UE is the most common definition of lymphedema, although the visibility of this difference may go unnoticed in women who are obese yet be more obvious in thinner women. Although a difference greater than 2.0 cm at any point has been defined by some authors13,14 as “clinically significant,” other authors15,16 have classified this degree of lymphedema as mild. Management of lymphedema in women with breast cancer has been a subject of debate for many years. Surgical resection of the axillary lymph nodes is used to stage and control breast cancer.5 This procedure alone, or in conjunction with radiation therapy, places patients at high risk for developing lymphedema.17 Lymph node dissection disrupts lymphatic flow and results in a build-up in pressure in the vessel walls, causing them to distend and leading to deficient lymphatic valves that allow backflow of fluid and blockage in fluid transport. This blockage obstructs the main lymphatic route for fluid to exit the UE, resulting in lymphedema.5 Breast cancer–related lymphedema can affect the trunk and any remaining breast tissue, as well as the UE.5,18 A new, less invasive surgical procedure involves dissection of one or more sentinel nodes, the first lymph nodes that drain the breast region. A biopsy is performed to determine the extent of metastasis. If these nodes do not contain malignant cells, additional dissection may be avoided.5 Sentinel node biopsy, however, has yet to become standard practice. Lymph nodes are especially susceptible to radiation, leading to vessel wall fibrosis. This condition impedes the lymph nodes’ ability to filter the fluid that normally flows through.5 Because lymph drainage is impaired, the lymph provides a breeding ground for bacteria, making these individuals susceptible to infection.18,19 Additional problems associated with lymphedema include decreased range of motion (ROM), slower healing of injuries or infections, tightness and heaviness, paresthesia, and pain, all of which can lead to functional impairment.2,7,18 Clinicians use a variety of strategies to diagnose UE lymphedema. The most widely used strategy is circumferential UE measurements using specific anatomical landmarks.8 Arm circumference measurements are used to estimate volume differences between the affected and unaffected UEs. A more accurate measure of volume difference is the water displacement technique.10 A newer method, multifrequency bioelectrical impedance (MF-BIA), measures the rate of resistance of extracellular and intracellular fluid to different frequencies of electrical current.2 This method is used infrequently in research and clinical settings even though it has a false positive rate of zero,2,3 likely due to the time required to set it up, position the electrodes, and so on. Lymphoscintigraphy, another measure of peripheral lymphatic function, also is rarely used2 because it involves injection of a radiotracer. Computed tomography, magnetic resonance imaging (MRI), ultrasound, and observation also can be used to help confirm the diagnosis of lymphedema20 but are used less commonly than anthropometric measures.21 Contraindications, as well as potential benefits, of upper-body exercise for women with or at risk for breast cancer–related lymphedema have recently received attention in the research literature, including examination of the effects of both aerobic and UE resistance exercise. As recently as 2000 and 2001, review articles by leading oncology experts have advised that “violent exercise and strenuous exertion” (arm and hand precautions) should be avoided in an effort to prevent lymphedema12(p298) and that the affected limb should be used in moderation with repetitive motion to be avoided.2 These warnings were based on the belief that vigorous exercise would increase lymph production, leading to an increase in UE volume.22 As these authors noted, however, there was no scientific evidence or data at that time to support these preventive strategies.2,12 Exercise encourages skeletal muscle contractions to provide the primary pumping mechanism for lymphatic and venous drainage23 and therefore should stimulate the contraction of lymph vessels because these vessels are innervated by the sympathetic nervous system.11 As McKenzie and Kalda11 have suggested, upper-body exercise may “re-set” the sympathetic drive to lymph vessels and thus assist in the long-term management of lymphedema. The use of compression bandaging in combination with exercise may improve venous and lymphatic return6 and minimize fluid from leaking into the interstitial space.5 Compression also may provide a protective component of lymphedema during exercise and, consequently, has been recommended8 and used4 as a precautionary measure during exercise. In February 2006, we searched the databases CINAHL, EMBASE, MEDLINE, PEDro, and PubMed (back to their originating dates) using the search terms “breast cancer,” “exercise,” and “lymphedema” (and their associated MeSH terms), with the searches limited to human, female, and English-language studies. After a review of the abstracts by the first 5 authors, irrelevant articles were excluded (ie, review articles, clinical practice guidelines, studies in which exercise was not an independent variable, and studies in which the type of exercise therapy was not defined). If there were discrepancies as to whether a study should be included, the parties in disagreement discussed the studies until a resolution was attained. “Gray literature,” such as unpublished studies, dissertations, and conference proceedings, were not included in our search. Eight studies were located that related directly to breast cancer–related lymphedema and aerobic or resistance exercise. The 6 studies that involved women who were at risk for breast cancer–related lymphedema will be presented first, in the order in which they were published, followed by the 2 studies involving women with pre-existing lymphedema. The type of design used, Sackett level of evidence,24 and methodological quality of the studies reviewed will be described. Sackett’s rules of evidence rank studies according to 5 hierarchical levels: (1) level I—large randomized controlled trial with low false positive or false negative errors; (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.24 A case series published by Harris and Niesen-Vertommen4 in 2001 (level V) suggested that women who had undergone treatment for breast cancer could engage in UE exercise without developing lymphedema. Data from 20 women, aged 31 to 63 years, were included. Six women reported that they currently had lymphedema (although no measurable differences were seen at baseline), and 7 women reported having feelings of heaviness or tightness. At the beginning of the study, time since breast cancer diagnosis ranged from 1 to 17 years. All women had undergone level I or II axillary node dissection, and 13 women also had undergone radiation treatment. The training program consisted of 20 to 30 minutes of aerobic exercise (eg, brisk walking, jogging, bicycling, or swimming), plus stretching and resistance training for the UE and back muscles (eg, bench press, seated row, latissimus dorsi muscle pull-downs). Exercises were conducted 3 times a week, for 9 months, in preparation for and during dragon boat racing. The women were advised to wear compression sleeves, although adherence to this advice was not reported. Upper-extremity circumference measurements were taken at the beginning of training, before racing, and 7 to 8 months after the end of the dragon boat racing season. Interrater reliability of the circumferential measurements was assessed for 3 women (15% of participants), and percentage of agreement was 96%. A clinically important change of greater than 0.5 in was reported in the involved UE for 2 women. However, there were no clinically important differences (≥1 in) in circumference between the ipsilateral and contralateral upper limbs for any of the women. Limitations reported by the authors included recording in inches rather than centimeters, lack of control for the type and intensity of aerobic activities in which the participants were engaged outside of the standardized strength-training program, nonstandardized time of day that UE measurements were taken, and lack of a control group. An additional limitation that we identified was lack of reporting on patients’ adherence in wearing compression garments. As the authors noted, case reports represent the lowest level of experimental evidence in Sackett’s 5 original levels of evidence24 because there is no control for potential threats to internal validity. They stated further that the research question posed as to safe levels of exercise for women who are at risk for lymphedema could only be “answered definitively through a prospective, well-controlled trial.”4(p98) In a pilot study published in 2002, Kolden et al25 the and of a exercise In this study (level women who had been treated for breast cancer were included. These women had been diagnosed with stage I to breast cancer with no reported lymphedema. of the women were months of most were currently a 3 times intervention of a to of and 20 minutes of aerobic and 20 minutes of resistance training and The aerobic component consisted of walking, and and as well as aerobic training was through use of resistance and resistance measures included body aerobic and of of life also was assessed using a variety of A rate the of the and were by the that participants an of of the were in aerobic and on the bench and press, as well as in of the 5 the measure of and of on all 3 measures (ie, and of the participants reported any including lymphedema. Limitations identified by the authors were the that the participants were women who were especially and therefore may not have been of all women with breast that there was no control and that there was no to long-term effects of the An additional limitation that we was the lack of of measurements of the UE were taken to measure lymphedema, although the authors reported at the no reliability data were for any of the measures used in the In and published a randomized controlled trial (level the effects of exercise training using on and in women with breast cancer in the experimental due to participants 3 times for of training from minutes for the first 3 to minutes for the 3 The control participants did not The of lymphedema was not an that was in this study but was as an participants in the exercise lymphedema during the of the study with no of lymphedema in the control a difference that was not but the of a type II Although the of lymphedema between the 2 to the difference was likely of clinical leading the authors to that exercise should lymphedema We with this and that UE circumference should be in all exercise involving women with or at risk for lymphedema. a design (level et the and effects of a exercise program for women who had been treated for breast The participants in their study were women between the of and years, with a of 17 months since breast cancer circumference measurements and of the impedance that 2 of the women had pre-existing lymphedema of 8 and based on a of at 6 on the All participants had undergone surgery, radiation, and All women to an exercise program that with aerobic including and use of This of the exercise program was followed in and 5 by exercise that on aerobic training with the water resistance as the weight training using and was The women exercise a and on their 2 additional times following a Exercise intensity was at a level as by using rate measurements and the of an that exercise and of the were taken at at of the program, then at and A of with measures for was used to determine the of the of lymphedema, body and were were in of lymphedema as by circumference and bioelectrical the 2 women with pre-existing lymphedema, there were no in the of their lymphedema. was no in aerobic or body although the women stated that to and had them the long-term that can be from an exercise A increase in was reported and at all In in their a increased and although the authors did not this was Many women also that they an increase in Although the data did not in lymphedema in women with breast cancer–related lymphedema, the use of a program did not lead to any identified by the authors were and lack of a control group. Although was of reliability having been for body in the of bioelectrical the authors reported that the of such measurements is was no of reliability for the UE circumference In a study (level et women who had been diagnosed with stage I to breast cancer and had undergone a or The women were at 6 months and had no of lymphedema. The study consisted of a exercise program that included both resistance and aerobic training 3 times the program and included the following seated row, bench press, latissimus dorsi muscle muscle and muscle exercise of the also was 3 times for to the boat training was at body UE UE and upper-body were at and 20 were used to any in UE circumference and Upper-extremity and the These however, were to have from muscle because there were no differences between the affected and unaffected UEs. The resistance training program was to that in a previous that a increase in UE circumference after to 6 and results that women treated for breast cancer may be to engage in UE resistance training without lymphedema. A limitation of this study (and 2 previous by the authors was that the assessed only UE volume and the results could not directly a change in lymphatic An additional that we identified was the that only the dragon boat training was to the resistance and aerobic training program was not no reliability data were reported for any of the measures In a trial (level and the effects of a and therapy program for women with breast women, aged to years, who had been diagnosed with breast cancer and had undergone a or more extensive breast were through the and the of The women were to the and therapy program or the control group. women during the of the study due to other or At the and performed the and therapy program the and therapy the program and their in the and therapy program, 7 women had UE circumference differences of greater than 5 cm between the affected and unaffected but only 3 women 1 who a compression had reported having lymphedema. The and therapy program consisted of 2 for the first 6 and then one for the remaining 6 with a of stretching and then were to including of and or with resistance at such as with and also were These activities were followed by to 30 minutes of with the women and to following the by The with a of and The of and were at and as well as measurements of and by an physical who was of the An of was used to in were no in circumference at 13 or in any of the women. The treatment at the with the control the the the treatment had and at 13 and and in Although it that the and therapy program did not affect lymphedema or the UE with resistance were not well described. Other of the study include the and to include a the 6 studies that the effects of exercise on lymphedema in women who were at risk for developing lymphedema, were Sackett level the lowest level of experimental evidence and a design that to control for due to lack of a control group. The study, a randomized controlled trial (level did not include lymphedema as an but rather as an The study also was level As by the authors of of these studies, further research is using experimental with and that will provide on in lymphatic to UE circumference and studies have the effects of aerobic or resistance exercise on women with breast cancer–related lymphedema and will be presented in the order in which they were McKenzie and in the of upper-body exercise on women with breast cancer–related lymphedema. women were to treatment or control level due to and no were included they had more than 6 months of treatment for stage I or II breast cancer and had lymphedema. were excluded they had stage lymphedema, breast or were that could affect UE The women in the experimental an upper-body program that included a series of resistance training and as 3 times resistance training included the following seated row, bench press, latissimus dorsi muscle muscle and muscle After 2 an additional upper-body aerobic exercise was on an the exercise the women in the experimental compression (and both of women these The control was no specific subject was at and 2 for UE and volume by water were no differences in UE as by water or UE circumference as a result of the exercise of life was using the on the first and of the increased in the exercise physical function, and This upper-body exercise program did not affect UE volume in women with breast cancer–related lymphedema. According to the authors, study included the and intensity of the intervention to elicit an and the that and may have circumference and volume measurements of the subjects were or Other that we identified were to reliability of the circumference measurements and lack of of a In a study (level V) published in 2005, and the effects of with on UE lymphedema in 31 women who had been treated for breast cancer and had or lymphedema greater volume than the unaffected of the UE was water with reliability of this measure to the The of of the participants also were with a A standardized exercise program of and and and using was on 1 and extremity volume was before the exercise directly after exercise and to the exercise program, volume was greater in the affected UE In all women were to wear a compression on day 1 or day of exercise following the exercise the volume of the affected UE a increase with measurements without compression and with compression but there was no difference after without compression and with compression This that exercise may have effects on lymphedema. However, there were no differences in UE volume the women wearing or not wearing the compression of high levels of reliability on UE volume data before the study was Limitations include the lack of a control and the to data on all 31 In the authors that their results could not be to women with lymphedema. In the 2 studies that the effects of exercise on women with pre-existing only women with lymphedema were included. was as a pilot and only one study included reliability of UE Although the study by McKenzie and Kalda11 included a control no was reported. However, the authors stated that was set at to for the of conducted on this the that aerobic exercise and UE resistance training should be for women with breast cancer was widely studies, although limited in and have evidence to that exercise may be The studies reviewed in this the effects of exercise and that exercise lymphedema, although more of lymphedema were reported as in the exercise in one the 8 studies 5 were Sackett level the type of experimental studies could be as level randomized controlled one of which lymphedema as an rather than as an Additional research with more (eg, randomized controlled and more to measure lymphatic flow (eg, is to address the and of for women with breast cancer–related lymphedema, one of the most and secondary complications of breast cancer

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