Original Article
Weight Lifting in Women with Breast-Cancer–Related Lymphedema
N Engl J Med 2009; 361:664-673August 13, 2009
- Abstract
Background
Weight lifting has generally been proscribed for women with breast-cancer–related lymphedema, preventing them from obtaining the well-established health benefits of weight lifting, including increases in bone density.
Methods
We performed a randomized, controlled trial of twice-weekly progressive weight lifting involving 141 breast-cancer survivors with stable lymphedema of the arm. The primary outcome was the change in arm and hand swelling at 1 year, as measured through displaced water volume of the affected and unaffected limbs. Secondary outcomes included the incidence of exacerbations of lymphedema, number and severity of lymphedema symptoms, and muscle strength. Participants were required to wear a well-fitted compression garment while weight lifting.
Results
The proportion of women who had an increase of 5% or more in limb swelling was similar in the weight-lifting group (11%) and the control group (12%) (cumulative incidence ratio, 1.00; 95% confidence interval, 0.88 to 1.13). As compared with the control group, the weight-lifting group had greater improvements in self-reported severity of lymphedema symptoms (P=0.03) and upper- and lower-body strength (P<0.001 for both comparisons) and a lower incidence of lymphedema exacerbations as assessed by a certified lymphedema specialist (14% vs. 29%, P=0.04). There were no serious adverse events related to the intervention.
Conclusions
In breast-cancer survivors with lymphedema, slowly progressive weight lifting had no significant effect on limb swelling and resulted in a decreased incidence of exacerbations of lymphedema, reduced symptoms, and increased strength. (ClinicalTrials.gov number, NCT00194363.)
Media in This Article
Figure 1
Enrollment, Randomization, and Follow-up of the Study Participants.Table 1
Baseline Characteristics of the 141 Study Participants with Lymphedema, According to Study Group.Article Activity
- Article
There are more than 2.4 million survivors of breast cancer in the United States.1 Approximately 184,000 women are diagnosed with breast cancer each year in the United States, and 90% of these women will live at least 5 years.2 Improvements in immediate treatment outcomes have led to an increased focus on morbidity among survivors. Lymphedema ranks high among the serious concerns of survivors, as it is chronic, progressive, and incurable.3 Lymphedema causes limb swelling and discomfort, considerably impairing arm function.4 The incidence of lymphedema after breast-cancer surgery varies across studies from 6 to 70%, depending on the criteria used for diagnosis and the follow-up interval.5-7 Sentinel-lymph-node biopsy is associated with a lower risk of lymphedema than axillary dissection,8 but one study reported a 17% incidence after sentinel-lymph-node biopsy alone.9
Breast-cancer survivors with lymphedema may limit the use of their affected arm out of fear and on the basis of guidance from commonly accessed cancer-information Web sites,10,11 which suggest that risk of lymphedema is decreased by avoiding lifting children, heavy bags, or other objects with the affected arm. Although this advice is intended to prevent harm, adherence to these precautions may limit physical recovery after breast-cancer surgery, alter activities, and adversely affect employment. Conversely, a program of controlled exercise through weight lifting may increase the physical-work capacity of the affected arm, thereby protecting it from injury sustained during common daily activities. Weight lifting offers additional benefits particularly relevant to breast-cancer survivors, including control of body fat12,13 and improved functional outcomes and bone health.14-16 We performed a 1-year randomized, controlled trial involving breast-cancer survivors with lymphedema to assess the effects of controlled weight lifting.
Methods
Patients
A total of 141 women with a history of breast cancer and current lymphedema were recruited from October 2005 through March 2007; follow-up was completed by August 2008. Recruitment methods included letters sent by state cancer registries, advertisements and interviews, and flyers. Eligible women had a history of unilateral nonmetastatic breast cancer 1 to 15 years before study entry and a body-mass index (BMI, the weight in kilograms divided by the square of the height in meters) of 50 or less, were not actively trying to lose weight, and had no current evidence of cancer, no medical conditions that would limit exercise, no history of weight lifting during the previous year, at least one lymph node removed, and a clinical diagnosis of stable breast-cancer–related lymphedema. Lymphedema was defined as a difference in the volume or circumference between the affected and unaffected limb of 10% or more or, according to Common Toxicity Criteria,17 arm swelling, obscuration of the anatomical architecture of the arm, or pitting edema. If a woman reported having lymphedema but it was not evident at study entry, she was required to provide written documentation of a previous clinical diagnosis of lymphedema and treatment from a certified lymphedema therapist.18 Stable lymphedema was defined as the absence in the past 3 months of therapist-delivered treatment, more than one arm infection requiring antibiotics, change in ability to perform activities of daily living, and verified changes in arm swelling of more than 10%.
Figure 1Figure 1
Enrollment, Randomization, and Follow-up of the Study Participants. shows the enrollment, randomization, and follow-up of the study participants. Women were assigned to either of two equal-size groups through a computerized process called minimization,19,20 in a manner that was unpredictable and was concealed from the study staff who determined eligibility. This approach balanced important potential confounders at baseline: age (<54 years vs. ≥54 years), difference in the volume between the affected and unaffected limbs (<10% vs. 10 to 20% vs. >20%), number of lymph nodes removed (<6 vs. ≥6), obesity (BMI <30 vs. ≥30), months since diagnosis (<60 vs. ≥60), and history of radiation treatment (yes vs. no).The Institutional Review Board of the University of Pennsylvania approved the protocol. Before participating, women provided written informed consent and written clearance from a physician.
Measurements
Measurements were obtained for all participants at baseline and at 12 months by trained staff who were unaware of the study-group assignments, using standardized methods. Limb volume was measured by submerging the arm and hand in water and measuring the displaced water volume.21,22 All participants were also evaluated by a certified lymphedema therapist18 using the Common Toxicity Criteria, which assess the tone, texture, and anatomical architecture of the arm tissue, in addition to swelling.17 Participants completed a validated survey assessing the presence and severity of 14 lymphedema-related limb symptoms (including swelling, leathery skin texture, heaviness, pain, pitting, and difficulty writing).23
Lymphedema exacerbations were ascertained by certified lymphedema specialists18 who were unaware of the study-group assignments, using a standardized evaluation. The participant was deemed to have an exacerbation if there was an increase in the volume of the affected limb of 5% or more, accompanied by an increase of 5% or more in the difference in the volume or circumference between the affected and unaffected limbs and by indications of sustained tissue changes such as fibrosis (sponginess, pitting, or hard, nonpitting fibrosis), altered skin color, or alteration of activities of daily living over the previous week because of symptoms (e.g., heaviness, inability to grip, tiredness, or achiness). Participants were evaluated for possible exacerbation if they reported a change in symptoms lasting 1 week or longer or if interim measurements at 3 or 6 months, by staff who were unaware of the study-group assignments, indicated an increase in the volume of the affected limb and an interlimb difference of 5% or more.
For each participant, the maximum amount of weight that could be lifted once was assessed for the bench press and leg press at baseline and 12 months; these tests are considered safe for most populations if properly supervised.24-26 The initial weight attempted for this test was based on the participant's rating of the difficulty of a warm-up set of four to six repetitions (40 lb [18.1 kg] for leg press, 5 lb [2.3 kg] for bench press), performed after stretching and familiarization with the equipment. Resistance was added until the participant rated the difficulty as maximal and refused to try to lift more, was clearly unable to lift more with proper biomechanics, or reported a symptom that required stopping. Trained study staff encouraged participants according to a standardized script. Compliance with the weight-lifting intervention was evaluated by means of attendance logs completed by fitness trainers.
Demographic characteristics were self-reported by patients at baseline. The cancer stage was obtained for each patient from state registries. Treatment history was self-reported, except for the number of lymph nodes removed, which was derived from pathology reports. Measurements assessed at baseline and at 12 months included weight and height, whole-body dual-energy x-ray absorptiometry (Hologic Discovery), adherence to common lymphedema self-care activities (e.g., compression, massage, bandaging), physical activity outside of weight lifting (according to the International Physical Activity Questionnaire)27; and diet (according to the Diet History Questionnaire).28,29
Weight-Lifting Program
Participants assigned to the weight-lifting group received a 1-year membership at a community fitness center (e.g., a YMCA) near their home. For the first 13 weeks, women were instructed, in small groups in a 90-minute session, twice weekly. Certified fitness professionals employed by the fitness centers led these sessions, which included stretching, cardiovascular warm-up, abdominal and back exercises, and weight-lifting exercises. Upper-body exercises included seated row, chest press, lateral or front raises, bicep curls, and tricep pushdowns. Lower-body exercises included leg press, back extension, leg extension, and leg curl. Weight-lifting exercises were introduced with little-to-no resistance. One to three new exercises were taught per session.
During the first 5 weeks, participants increased their number of sets of each exercise per session from two to three, with 10 repetitions per set. If no changes in symptoms were noted for a particular exercise after two sessions at a given weight, the resistance was increased by the smallest possible increment. If fatigue prevented the completion of a third set of 10 repetitions of a given exercise with proper biomechanical form, resistance for that exercise would remain the same at the next session. After two sessions at which three sets of 10 repetitions could be performed with proper form at a given level of resistance, without changes in arm and hand symptoms, the trainer guided the participant to increase the resistance by the smallest possible increment at the next session. No upper limit was placed on the weight to which women could progress in any exercise. During lymphedema exacerbations, women continued all exercises except the upper-body exercises, which were resumed only after approval of their lymphedema therapist, with resistance reset to the lowest possible level and then increased again as described above.
After the first 13 weeks, participants continued twice-weekly unsupervised exercise for 39 additional weeks. Throughout the study, fitness trainers telephoned women who missed more than one session per week. Participants in the control group were asked not to change their exercise level during study participation and were offered a 1-year fitness-center membership, with 13 weeks of supervised instruction, after study completion. The exercise protocol and the sequence in which the exercises were taught are available on request.
Safety
Trainers who worked with participants underwent 3 days of training, including an overview of lymphedema prevention, symptoms, and treatment30-32 and the exercise protocol. At baseline and 6 months, participants in both groups were given a custom-fitted compression garment (Jobst, BSN Medical). Participants in the weight-lifting group were required to wear these garments during weight lifting. Trainers asked the participants about changes in symptoms weekly, and measured the circumference and water volume of both limbs monthly, to ensure that any changes were detected promptly. Finally, participants in both groups were required to attend a 1-hour educational lecture that reviewed the National Lymphedema Network guidelines for risk reduction, treatment, and exercise.30-32 The 2005 guidelines included the statement that strength training is the type of exercise that “poses the greatest risk to individuals with lymphedema” and that modifications to strength training (e.g., adequate rest intervals or appropriate and sufficient compression of the affected limb) may be indicated.
Study Outcomes
The prespecified primary comparison between the weight-lifting group and the control group was the proportion of participants with an absolute increase of 5 percentage points or more in the interlimb volume discrepancy (the interlimb difference over time). Prespecified secondary outcomes included lymphedema exacerbation and symptoms, as well as strength and anthropometric measures.
Statistical Analysis
Descriptive statistics reported for baseline variables include rates for binary variables and means or medians and standard deviations for continuous variables. Data for two participants (one with a second primary cancer and one with recurrent cancer) were excluded. Data on the interlimb volume difference for nine women who were lost to follow-up were imputed with the use of predicted values from a multiple linear regression analysis that included baseline predictors. Continuous outcomes were compared between the two study groups by means of the Wilcoxon rank-sum test. For the analysis of data on exacerbations, simple imputation-based sensitivity analyses were conducted, in which the nine participants lost to follow-up were assumed to have had an exacerbation and then not to have had an exacerbation. Binary outcomes were compared between the two study groups using Fisher's exact test, with a two-sided significance level of 0.05.
Sample-size calculations were based on the aim of demonstrating equivalence between the weight-lifting group and the control group with respect to the primary outcome of changes in arm and hand swelling, as measured by displaced water volume. The statistical power of the study was set at 80%, with a significance level of 0.05, allowing for loss to follow-up of 20% of participants. Given these parameters and a null hypothesis of nonequivalence (a between-group difference of >20% in the proportion of women who had an increase of 5 percentage points in the interlimb volume discrepancy), we sought to recruit 144 women with lymphedema to provide adequate power against an alternative equivalence hypothesis (a between-group difference of <5% in the proportion of participants who had an absolute increase of at least 5 percentage points in the interlimb volume discrepancy).
Results
Table 1Table 1
Baseline Characteristics of the 141 Study Participants with Lymphedema, According to Study Group. summarizes baseline characteristics of all participants, including the two (1%) who were excluded from the analyses because of a second primary or recurrent cancer and the nine (6%) who were lost to follow-up. All participants had a clinical diagnosis of lymphedema; 12 had lymphedema classified as grade 0 at baseline but were included because, once diagnosed, lymphedema is considered to be manageable but not curable. The median rates of exercise-session attendance were 96%, 88%, 81%, and 75% in the first, second, third, and final quarters of the year-long study, respectively. There were no significant differences between the two groups in the baseline values of measures of strength, anthropometric data, diet, and physical activity (Table 2Table 2
Strength, Anthropometric, Diet, and Physical-Activity Data at Baseline and 12 Months, According to Study Group.).At 12 months, the weight-lifting participants had increased their strength, as measured with the bench press and leg press, more than controls (Table 2). Changes in diet, physical activity and anthropometric measures over the 12-month period were not significantly different between the two groups.
There was no significant difference between the two groups in the proportion of women who had a change in limb swelling of 5% or more (Table 3Table 3
Lymphedema Outcomes at 12 Months, According to Study Group.). This result did not materially change when the analysis was repeated without any imputed data from participants who were lost to follow-up (results not shown). Among the 130 women who had no second primary or recurrent cancers and were not lost to follow-up, 23 in the control group and 20 in the weight-lifting group were evaluated for exacerbation. Of these, 19 and 9 participants, respectively, were found to have had an exacerbation (83% vs. 45%). The total number of treatment sessions for exacerbation was 195 in the control group, as compared with 77 in the weight-lifting group. The number and severity of symptoms reported decreased more in the weight-lifting group than in the control group. No significant differences were noted between the two study groups with regard to self-reported adherence to prescribed lymphedema self-care therapies (results not shown). Post hoc analyses that excluded participants with grade 0 lymphedema yielded results similar to those reported in Table 3 (results not shown). Adjustment for baseline variables (cancer stage, number of nodes removed, race, physical activity, diet, and body-mass index) did not materially alter these results. There were no serious adverse events related to the intervention.Discussion
Contrary to common guidelines to avoid lifting with the affected limb, we found that weight lifting did not significantly affect the severity of breast cancer–associated lymphedema (as assessed by the primary outcome, an absolute increase of ≥5 percentage points in the interlimb volume difference). In addition, weight lifting reduced the number and severity of arm and hand symptoms, increased muscular strength, and reduced the incidence of lymphedema exacerbations as assessed by a lymphedema specialist.
Several previous studies, including a case series33 and small randomized, controlled trials,34-37 have also suggested that weight lifting is safe for breast-cancer survivors with lymphedema. The current trial was larger and of longer duration than those previously reported and also differed by testing a weight-lifting protocol with no upper limit on the resistance level to which participants could progress. A strength of this trial is its delivery in community fitness centers, primarily YMCAs, by trainers employed by these fitness centers. We adopted this approach with the goal of dissemination of the weight-lifting program if it proved effective. The ongoing LIVESTRONG at the YMCA program (a collaboration of the YMCA and the Lance Armstrong Foundation) includes the protocol described here as an intervention that can be offered to cancer survivors in YMCAs across the United States. Additional strengths of the present trial are the inclusion of a racially diverse population with a wide range of time since diagnosis (1 to 15 years) and the high rate of follow-up.
There are also potential limitations of the study. Evaluations for exacerbations were not completed by a single therapist, although the six lymphedema therapists assessing exacerbations followed a standardized algorithm for evaluation and had completed the 135-hour course recommended by the National Lymphedema Network.18 Therapists were unaware of which patients had been assigned to the weight-lifting group, as specified in the study design, but some participants in this group may have disclosed their recent weight lifting during evaluations for perceived exacerbations. Though the number of women evaluated for exacerbation was approximately equal in the two groups (23 in the control group and 20 in the weight-lifting group), the proportion of evaluated women who were found to have had an exacerbation was higher in the control group. One possible explanation for this observation is that some assessors may have become aware of the study-group assignments, resulting in biased assessments. However, the finding that symptom severity improved more in the weight-lifting group than in the control group supports a benefit of the intervention. An alternative explanation is that participants in the weight-lifting group, concerned about the potential for worsening of lymphedema with weight lifting, were more likely to seek care in the absence of objective evidence of exacerbation.
Although reporting bias cannot be ruled out as a possible explanation for the decrease in confirmed lymphedema exacerbations, several physiological effects of exercise might alternatively explain these findings. There is evidence that exercise enhances the flow of lymph38,39 and improves protein resorption40 and that the increased pulmonary work associated with exercise assists with lymph flow.41 It is also possible that increased muscle strength reduces the relative effect of common daily stresses to the limb.
The substantive treatment-related increases in strength, coupled with the lack of change in lean mass, indicate that the program was more focused on building muscle strength than on hypertrophy, as intended. Further research is needed to determine the critical components of this intervention in order to facilitate its optimal use by breast-cancer survivors with lymphedema.
In conclusion, the results of this study reduce concerns that weight lifting will worsen arm and hand swelling associated with lymphedema in breast-cancer survivors. These findings support the potential benefits of a slowly progressive weight-lifting program in women with breast-cancer–related lymphedema, in conjunction with appropriate use of compression garments and close monitoring for arm and hand swelling.
Supported by grants from the National Cancer Institute (R01-CA106851, to Dr. Schmitz) and the National Center for Research Resources (UL1RR024134, to the University of Pennsylvania). BSN Medical provided custom-fitted compression garments, and the fitness centers where the weight-lifting sessions took place (YMCA of Philadelphia and Vicinity, Sisters in Shape, and the Family YMCA of Burlington County, NJ) provided discounted membership fees for study participants.
No potential conflict of interest relevant to this article was reported.
We thank Jesse L. Chittams, M.S., for statistical support; the lymphedema therapists at Penn Therapy and Fitness who evaluated the participants in this study, including Joy C. Cohn, P.T., C.L.T.-L.A.N.A., Nicole L. Dugan, P.T., D.P.T., C.L.T.-L.A.N.A., Bernadette Erikson, P.T., C.L.T.-L.A.N.A., Beth Anne Morris, M.S.P.T., C.L.T.-L.A.N.A., Nancy Stewart, P.T., M.Ed., M.P.T., C.L.T., and Bryan Spinelli, P.T., M.S., O.C.S., C.L.T., each of whom also treated at least one of the exacerbations that occurred during the study; Rebecca Maurer, D.P.T., P.T., C.L.T.-L.A.N.A., treated one participant but did not evaluate participants for exacerbations.
Source Information
From the Center for Clinical Epidemiology and Biostatistics, University of Pennsylvania School of Medicine and Abramson Cancer Center, Philadelphia (K.H.S., A.T., R.S., L.L.-G., C.J.B., C.T.W.-S., Q.P.G.); the Department of Dermatology, University of Minnesota Medical School, Minneapolis (R.L.A.); and the Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN (A.C.).
Address reprint requests to Dr. Schmitz at the Department of Biostatistics and Epidemiology, University of Pennsylvania, 423 Guardian Dr., 903 Blockley Hall, Philadelphia, PA 19104-6021, or at schmitz@mail.med.upenn.edu.
- References
References
1
SEER Cancer Statistics Review (CSR). Bethesda, MD: National Cancer Institute, 2003. (Accessed July 20, 2009, at http://seer.cancer.gov/csr/1975_2000.)
2
Cancer facts and figures. Atlanta: American Cancer Society, 2008.
3
Hayes SC ,Janda M ,Cornish B ,Battistutta D ,Newman B . Lymphedema after breast cancer: incidence, risk factors, and effect on upper body function. J Clin Oncol 2008;26:3536-3542
CrossRef | Web of Science | Medline4
Warren AG ,Brorson H ,Borud LJ ,Slavin SA . Lymphedema: a comprehensive review. Ann Plast Surg 2007;59:464-472
CrossRef | Web of Science | Medline5
Vignes S ,Arrault M ,Dupuy A . Factors associated with increased breast cancer-related lymphedema volume. Acta Oncol 2007;46:1138-1142
CrossRef | Web of Science | Medline6
Armer JM ,Stewart BR . A comparison of four diagnostic criteria for lymphedema in a post-breast cancer population. Lymphat Res Biol 2005;3:208-217
CrossRef | Medline7
Ronka RH ,Pamilo MS ,von Smitten KA ,Leidenius MH . Breast lymphedema after breast conserving treatment. Acta Oncol 2004;43:551-557
CrossRef | Web of Science | Medline8
Golshan M ,Martin WJ ,Dowlatshahi K . Sentinel lymph node biopsy lowers the rate of lymphedema when compared with standard axillary lymph node dissection. Am Surg 2003;69:209-211
Web of Science | Medline9
Francis WP ,Abghari P ,Du W ,Rymal C ,Suna M ,Kosir MA . Improving surgical outcomes: standardizing the reporting of incidence and severity of acute lymphedema after sentinel lymph node biopsy and axillary lymph node dissection. Am J Surg 2006;192:636-639
CrossRef | Web of Science | Medline10
Lymphedema: what every woman with breast cancer should know. Atlanta: American Cancer Society, 2009. (Accessed July 20, 2009, at http://www.cancer.org/docroot/MIT/content/MIT_7_2x_Lymphedema_and_Breast_Cancer.asp.)
11
Understanding breast cancer: after treatment: life issues: lymphedema. Dallas: Susan G. Komen for the Cure, 2009. (Accessed July 20, 2009, at http://ww5.komen.org/BreastCancer/Lymphedema.html.)
12
Werner RS ,McCormick B ,Petrek JA , et al. Arm edema in conservatively managed breast cancer: obesity is a major predictive factor. Radiology 1991;180:177-184
Web of Science | Medline13
Schmitz KH ,Hannan PJ ,Stovitz SD ,Bryan CJ ,Warren M ,Jensen MD . Strength training and adiposity in premenopausal women: Strong, Healthy, and Empowered Study. Am J Clin Nutr 2007;86:566-572
Web of Science | Medline14
Phillips SM . Resistance exercise: good for more than just Grandma and Grandpa's muscles. Appl Physiol Nutr Metab 2007;32:1198-1205
CrossRef | Web of Science | Medline15
Nelson ME ,Fiatarone MA ,Morganti CM ,Trice I ,Greenberg RA ,Evans WJ . Effects of high-intensity strength training on multiple risk factors for osteoporotic fractures: a randomized controlled trial. JAMA 1994;272:1909-1914
CrossRef | Web of Science | Medline16
Bjarnason NH ,Hitz M ,Jorgensen NR ,Vestergaard P . Adverse bone effects during pharmacological breast cancer therapy. Acta Oncol 2008;47:747-754
CrossRef | Web of Science | Medline17
Cheville AL ,McGarvey CL ,Petrek JA ,Russo SA ,Thiadens SR ,Taylor ME . The grading of lymphedema in oncology clinical trials. Semin Radiat Oncol 2003;13:214-225
CrossRef | Web of Science | Medline18
Training of lymphedema therapists. Oakland, CA: National Lymphedema Network National Advisory Committee, 2005. (Accessed July 20, 2009, at http://www.lymphnet.org/lymphedemaFAQs/positionPapers.htm.)
19
Evans SJW, Day SJ, Royston P. MINIM: minimisation program for allocating patients to treatments in clinical trials, version 1.5. London: London Hospital Medical College, 1990.
20
Pocock SJ ,Simon R . Sequential treatment assignment with balancing for prognostic factors in the controlled clinical trial. Biometrics 1975;31:103-115
CrossRef | Web of Science | Medline21
King TI II . The effect of water temperature on hand volume during volumetric measurement using the water displacement method. J Hand Ther 1993;6:202-204
Medline22
Waylett-Rendell J ,Seibly DS . A study of accuracy of a commercially available volumeter. J Hand Ther 1991;4:10-1323
Norman SA ,Miller LT ,Erikson HB ,Norman MF ,McCorkle R . Development and validation of a telephone questionnaire to characterize lymphedema in women treated for breast cancer. Phys Ther 2001;81:1192-1205
Web of Science | Medline24
Barnard KL ,Adams KJ ,Swank AM ,Mann E ,Denny DM . Injuries and muscle soreness during the one repetition maximum assessment in a cardiac rehabilitation population. J Cardiopulm Rehabil 1999;19:52-58
CrossRef | Medline25
Fleck SJ, Kraemer WJ. Designing resistance training programs. 2nd ed. Champaign, IL: Human Kinetics, 1997.
26
Shaw CE ,McCully KK ,Posner JD . Injuries during the one repetition maximum assessment in the elderly. J Cardiopulm Rehabil 1995;15:283-287
CrossRef | Medline27
Craig CL ,Marshall AL ,Sjostrom M , et al. International Physical Activity Questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 2003;35:1381-1395
CrossRef | Web of Science | Medline28
Subar AF ,Midthune D ,Kulldorff M , et al. Evaluation of alternative approaches to assign nutrient values to food groups in food frequency questionnaires. Am J Epidemiol 2000;152:279-286
CrossRef | Web of Science | Medline29
Subar AF ,Thompson FE ,Kipnis V , et al. Comparative validation of the Block, Willett and National Cancer Institute food frequency questionnaires: the Eating at America's Table Study. Am J Epidemiol 2001;154:1089-1099
CrossRef | Web of Science | Medline30
Exercise. Oakland, CA: National Lymphedema Network, 2005. (2007 Update accessed July 20, 2009, at http://www.lymphnet.org/pdfDocs/nlnexercise.pdf.)
31
Treatment. Oakland, CA: National Lymphedema Network, 2006. (Accessed July 20, 2009, at http://www.lymphnet.org/pdfDocs/nlntreatment.pdf.)
32
Lymphedema risk reduction practices. Oakland, CA: National Lymphedema Network, 2008. (Accessed July 20, 2009, at http://www.lymphnet.org/pdfDocs/nlnriskreduction.pdf.)
33
Harris SR ,Niesen-Vertommen SL . Challenging the myth of exercise-induced lymphedema following breast cancer: a series of case reports. J Surg Oncol 2000;74:95-99
CrossRef | Web of Science | Medline34
Ahmed RL ,Thomas W ,Yee D ,Schmitz K . Randomized controlled trial of weight training and lymphedema in breast cancer survivors. J Clin Oncol 2006;24:2765-2772[Erratum, J Clin Oncol 2006;24:3716.]
CrossRef | Web of Science | Medline35
Johansson K ,Tibe K ,Weibull A ,Newton RC . Low intensity resistance exercise for breast cancer patients with arm lymphedema with or without compression sleeve. Lymphology 2005;38:167-180
Web of Science | Medline36
Courneya KS ,Segal RJ ,Mackey JR , et al. Effects of aerobic and resistance exercise in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial. J Clin Oncol 2007;25:4396-4404
CrossRef | Web of Science | Medline37
McKenzie DC ,Kalda AL . Effect of upper extremity exercise on secondary lymphedema in breast cancer patients: a pilot study. J Clin Oncol 2003;21:463-466
CrossRef | Web of Science | Medline38
Mortimer PS. Assessment of peripheral lymph flow before and after clinical intervention. In: Progress in lymphology. Amsterdam: Elsevier Science, 1990:215-522.
39
Mortimer PS . Evaluation of lymphatic function: abnormal lymph drainage in venous disease. Int Angiol 1995;14:Suppl 1:32-35
Web of Science | Medline40
Bourgeois P, Leduc O, Leduc A. Manual of lymphatic drainage: scintigraphic demonstration of its efficacy on colloidal protein resorption. In: Progress in lymphology. Amsterdam: Elsevier Science, 1988:551-4.
41
Brennan MJ ,Miller LT . Overview of treatment options and review of the current role and use of compression garments, intermittent pumps, and exercise in the management of lymphedema. Cancer 1998;83:Suppl:2821-2827
CrossRef | Web of Science | Medline
- Citing Articles (50)
Citing Articles
1
Sharon L. Kilbreath, Kathryn M. Refshauge, Jane M. Beith, Leigh C. Ward, MiJoung Lee, Judy M. Simpson, Ross Hansen. (2012) Upper limb progressive resistance training and stretching exercises following surgery for early breast cancer: a randomized controlled trial. Breast Cancer Research and Treatment
CrossRef2
Emily Jo Rajotte, Jean C. Yi, K. Scott Baker, Lindsey Gregerson, Andréa Leiserowitz, Karen L. Syrjala. (2012) Community-based exercise program effectiveness and safety for cancer survivors. Journal of Cancer Survivorship
CrossRef3
S. M. Halberstadt, K. H. Schmitz, M. D. Sammel. (2012) A joint latent variable model approach to item reduction and validation. Biostatistics 13:1, 48-60
CrossRef4
Paul D. Loprinzi, Bradley J. Cardinal. (2012) Effects of physical activity on common side effects of breast cancer treatment. Breast Cancer 19:1, 4-10
CrossRef5
K. Steindorf, M. Schmidt, C. Ulrich. (2012) Welche Effekte hat körperliche Bewegung auf das Krebsrisiko und auf den Krankheitsverlauf nach einer Krebsdiagnose?. Bundesgesundheitsblatt - Gesundheitsforschung - Gesundheitsschutz 55:1, 10-16
CrossRef6
S. Vignes. (2012) Prise en charge des lymphœdèmes des membres. La Revue de Médecine Interne
CrossRef7
Kerri M. Winters-Stone, Jessica Dobek, Jill A. Bennett, Lillian M. Nail, Michael C. Leo, Anna Schwartz. (2011) The effect of resistance training on muscle strength and physical function in older, postmenopausal breast cancer survivors: a randomized controlled trial. Journal of Cancer Survivorship
CrossRef8
Roger T. Anderson, Gretchen G. Kimmick, Thomas P. McCoy, Judith Hopkins, Edward Levine, Gary Miller, Paul Ribisl, Shannon L. Mihalko. (2011) A randomized trial of exercise on well-being and function following breast cancer surgery: the RESTORE trial. Journal of Cancer Survivorship
CrossRef9
Baukje Miedema, Ryan Hamilton, Sue Tatemichi, Roanne Thomas-MacLean, Thomas F. Hack, Elizabeth Quinlan, Anna Towers, Andrea Tilley, Winkle Kwan. (2011) Do breast cancer survivors' post-surgery difficulties with recreational activities persist over time?. Journal of Cancer Survivorship 5:4, 405-412
CrossRef10
Rehana L. Ahmed, Kathryn H. Schmitz, Anna E. Prizment, Aaron R. Folsom. (2011) Risk factors for lymphedema in breast cancer survivors, the Iowa Women’s Health Study. Breast Cancer Research and Treatment 130:3, 981-991
CrossRef11
Takumi Yamamoto, Nana Matsuda, Takeshi Todokoro, Hidehiko Yoshimatsu, Mitsunaga Narushima, Makoto Mihara, Gentaro Uchida, Isao Koshima. (2011) Lower Extremity Lymphedema Index. Annals of Plastic Surgery 67:6, 637-640
CrossRef12
Marilyn L. Kwan, Joy C. Cohn, Jane M. Armer, Bob R. Stewart, Janice N. Cormier. (2011) Exercise in patients with lymphedema: a systematic review of the contemporary literature. Journal of Cancer Survivorship 5:4, 320-336
CrossRef13
Chirag Shah, Frank A. Vicini. (2011) Breast Cancer-Related Arm Lymphedema: Incidence Rates, Diagnostic Techniques, Optimal Management and Risk Reduction Strategies. International Journal of Radiation Oncology*Biology*Physics 81:4, 907-914
CrossRef14
Sandra C. Hayes, Rebecca M. Speck, Elizabeth Reimet, Azadeh Stark, Kathryn H. Schmitz. (2011) Does the effect of weight lifting on lymphedema following breast cancer differ by diagnostic method: results from a randomized controlled trial. Breast Cancer Research and Treatment 130:1, 227-234
CrossRef15
S. Aebi, T. Davidson, G. Gruber, F. Cardoso, . (2011) Primary breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Annals of Oncology 22:Supplement 6, vi12-vi24
CrossRef16
Carolyn Casey, Lee-may Chen, Michael W Rabow. (2011) Symptom management in gynecologic malignancies. Expert Review of Anticancer Therapy 11:7, 1079-1091
CrossRef17
Stamatakos Michael, Stefanaki Charikleia, Kontzoglou Konstantinos. (2011) Lymphedema and breast cancer: a review of the literature. Breast Cancer 18:3, 174-180
CrossRef18
Carolyn C. Schook, John B. Mulliken, Steven J. Fishman, Frederick D. Grant, David Zurakowski, Arin K. Greene. (2011) Primary Lymphedema: Clinical Features and Management in 138 Pediatric Patients. Plastic and Reconstructive Surgery 127:6, 2419-2431
CrossRef19
Kerri M. Winters-Stone, Jessica Dobek, Lillian Nail, Jill A. Bennett, Michael C. Leo, Arpana Naik, Anna Schwartz. (2011) Strength training stops bone loss and builds muscle in postmenopausal breast cancer survivors: a randomized, controlled trial. Breast Cancer Research and Treatment 127:2, 447-456
CrossRef20
Marta I. Korpan, Richard Crevenna, Veronika Fialka-Moser. (2011) Lymphedema. American Journal of Physical Medicine & Rehabilitation 90:Suppl 1, S69-S75
CrossRef21
Margaret L. McNeely, Carolyn J. Peddle, Janice L. Yurick, Ian S. Dayes, John R. Mackey. (2011) Conservative and dietary interventions for cancer-related lymphedema. Cancer 117:6, 1136-1148
CrossRef22
Marianne Ewertz, Anders Bonde Jensen. (2011) Late effects of breast cancer treatment and potentials for rehabilitation. Acta Oncologica 50:2, 187-193
CrossRef23
Dorothy W. Pekmezi, Wendy Demark-Wahnefried. (2011) Updated evidence in support of diet and exercise interventions in cancer survivors. Acta Oncologica 50:2, 167-178
CrossRef24
Erik D. Hanson, Ben F. Hurley. (2011) Intervening on the Side Effects of Hormone-Dependent Cancer Treatment: The Role of Strength Training. Journal of Aging Research 2011, 1-8
CrossRef25
S. Vignes. (2011) Gestione dei linfedemi degli arti. EMC - Tecniche Chirurgiche Vascolare 16:3, 1-9
CrossRef26
D.C. Hughes, C.M. Mojica. (2011) Weight Lifting for Women at Risk for Breast Cancer–Related Lymphedema: A Randomized Trial. Breast Diseases: A Year Book Quarterly 22:2, 124-125
CrossRef27
Do Sung Kim, Young-Joo Sim, Ho Joong Jeong, Ghi Chan Kim. (2010) Effect of Active Resistive Exercise on Breast Cancer–Related Lymphedema: A Randomized Controlled Trial. Archives of Physical Medicine and Rehabilitation 91:12, 1844-1848
CrossRef28
Terry P. Haines, Patricia Sinnamon, Neil G. Wetzig, Margot Lehman, Euan Walpole, Tony Pratt, Amanda Smith. (2010) Multimodal exercise improves quality of life of women being treated for breast cancer, but at what cost? Randomized trial with economic evaluation. Breast Cancer Research and Treatment 124:1, 163-175
CrossRef29
M. López-Martín, E. De Carlos Iriarte. (2010) El papel de la escuela de linfedema y la cinesiterapia en la prevención y el tratamiento del linfedema. Rehabilitación 44, 49-53
CrossRef30
Linda L. McCausland. (2010) Dragon Boat Racing: Life After Breast Cancer Treatment. AJN, American Journal of Nursing 110:10, 48-54
CrossRef31
Randi S Lite, Stephanie Mejia. (2010) Resistance Training for Breast Cancer Survivors. Strength and Conditioning Journal 32:5, 60-62
CrossRef32
Kristen E. Adams, John C. Rasmussen, Chinmay Darne, I-Chih Tan, Melissa B. Aldrich, Milton V. Marshall, Caroline E. Fife, Erik A. Maus, Latisha A. Smith, Renie Guilloid, Sunday Hoy, Eva M. Sevick-Muraca. (2010) Direct evidence of lymphatic function improvement after advanced pneumatic compression device treatment of lymphedema. Biomedical Optics Express 1:1, 114
CrossRef33
Kathryn H. Schmitz, Kerry S. Courneya, Charles Matthews, Wendy Demark-Wahnefried, DANIEL A. GALVÃO, Bernardine M. Pinto, Melinda L. IRWIN, KATHLEEN Y. WOLIN, ROANNE J. SEGAL, ALEJANDRO LUCIA, CAROLE M. SCHNEIDER, VIVIAN E. VON GRUENIGEN, ANNA L. SCHWARTZ. (2010) American College of Sports Medicine Roundtable on Exercise Guidelines for Cancer Survivors. Medicine & Science in Sports & Exercise 42:7, 1409-1426
CrossRef34
Mei R. Fu, Constance M. Chen, Judith Haber, Amber A. Guth, Deborah Axelrod. (2010) The Effect of Providing Information about Lymphedema on the Cognitive and Symptom Outcomes of Breast Cancer Survivors. Annals of Surgical Oncology 17:7, 1847-1853
CrossRef35
Elana Katz, Nicole L. Dugan, Joy C. Cohn, Christina Chu, Rebecca G. Smith, Kathryn H. Schmitz. (2010) Weight Lifting in Patients With Lower-Extremity Lymphedema Secondary to Cancer: A Pilot and Feasibility Study. Archives of Physical Medicine and Rehabilitation 91:7, 1070-1076
CrossRef36
Rebecca M. Speck, Cynthia R. Gross, Julia M. Hormes, Rehana L. Ahmed, Leslie A. Lytle, Wei-Ting Hwang, Kathryn H. Schmitz. (2010) Changes in the Body Image and Relationship Scale following a one-year strength training trial for breast cancer survivors with or at risk for lymphedema. Breast Cancer Research and Treatment 121:2, 421-430
CrossRef37
Julie Chu, Subhashni D. Singh Joy. (2010) Weight Lifting for Breast Cancerrelated Lymphedema. AJN, American Journal of Nursing 110:6, 64
CrossRef38
Rebecca M. Speck, Kerry S. Courneya, Louise C. Mâsse, Sue Duval, Kathryn H. Schmitz. (2010) An update of controlled physical activity trials in cancer survivors: a systematic review and meta-analysis. Journal of Cancer Survivorship 4:2, 87-100
CrossRef39
Loren L Rourke, Kelly K Hunt, Janice N Cormier. (2010) Breast cancer and lymphedema: a current overview for the healthcare provider. Women's Health 6:3, 399-406
CrossRef40
P. Grätzel. (2010) Onko Update 2010. Der Onkologe 16:4, 417-419
CrossRef41
(2010) Scientific Surgery. British Journal of Surgery 97:4, 623-623
CrossRef42
Sharon L. Kilbreath, Leigh C. Ward, Kirstin Lane, Margaret McNeely, Elizabeth S. Dylke, Kathryn M. Refshauge, Don McKenzie, Mi-Joung Lee, Carolyn Peddle, Katie J. Battersby. (2010) Effect of air travel on lymphedema risk in women with history of breast cancer. Breast Cancer Research and Treatment 120:3, 649-654
CrossRef43
L. Zelek, T. Bouillet, P. Latino-Martel, N. Pecollo, E. Barrandon, S. Czernichow, P. Galan, S. Hercberg. (2010) Mode de vie et cancer du sein: quels conseils pour la prise en charge de l’après cancer ?. Oncologie 12:4, 289-297
CrossRef44
Kathryn H Schmitz, Rebecca M Speck. (2010) Risks and benefits of physical activity among breast cancer survivors who have completed treatment. Women's Health 6:2, 221-238
CrossRef45
Gulgun Tahan, Ronald Johnson, Lisa Mager, Atilla Soran. (2010) The role of occupational upper extremity use in breast cancer related upper extremity lymphedema. Journal of Cancer Survivorship 4:1, 15-19
CrossRef46
Barbara A. Springer, Ellen Levy, Charles McGarvey, Lucinda A. Pfalzer, Nicole L. Stout, Lynn H. Gerber, Peter W. Soballe, Jerome Danoff. (2010) Pre-operative assessment enables early diagnosis and recovery of shoulder function in patients with breast cancer. Breast Cancer Research and Treatment 120:1, 135-147
CrossRef47
J.-C. Ferrandez. (2010) Kinesiterapia despu??s del c??ncer de mama. EMC - Kinesiterapia - Medicina F??sica 31:4, 1-14
CrossRef48
Kathryn H. Schmitz. (2010) Balancing Lymphedema Risk. Exercise and Sport Sciences Reviews 38:1, 17-24
CrossRef49
L.R. Rourke, R.L. Askew, J.N. Cormier. (2010) Weight Lifting in Women with Breast-Cancer–Related Lymphedema. Breast Diseases: A Year Book Quarterly 21:1, 36-38
CrossRef50
Demark-Wahnefried, Wendy, . (2009) A Weighty Matter — Lifting after Breast Cancer. New England Journal of Medicine 361:7, 710-711
Full Text
