Abstract
Abstract
Background:
After breast cancer surgery patients are at higher risk of lymphedema development and decreasing physical activity (PA), as well as decreasing health-related quality of life (HRQOL). The aim of the study was to compare the level of PA and HRQOL in women after breast cancer surgery using light arm compression with women not using compression 1 year after oncological treatment.
Methods and Results:
Forty-five women were preoperatively randomly assigned to a compression group (CG, n = 23) or to no compression group (NCG, n = 22). Arm volumes were measured before surgery and 12 months thereafter. The CG received circular-knit sleeves in compression class 1 for daily wearing in the postoperative period up to 1 year. Both groups underwent a standardized physical exercise program. PA with the short version of International Physical Activity Questionnaire (IPAQ), compliance, and HRQOL by EORTC QLQ-C30 and QLQ-BR23 questionnaires was assessed in both groups 1 year after surgery. After 1 year observation the CG showed significantly lower mean affected arm volume compared to NCG. The total PA (calculated as the sum of vigorous moderate exercises and walking) was markedly higher within the CG, with no difference in particular IPAQ items. There were no correlations between reported PA items and observed arm/edema volume or body mass index changes. The QLQ-BR23 revealed only better sexual functioning (p = 0.014) and greater upset by hair loss in NCG (p = 0.01).
Conclusions:
The available data indicate that wearing compression sleeves neither interfere with the level of PA nor decrease quality of life 1 year after breast cancer surgery.
Introduction
B
Breast cancer survivors are also at higher risk of decreasing physical activity (PA) and increasing sedentary behavior after cancer diagnosis. 5 LE and low level of PA lead to significant functional, psychological, and social morbidity decreasing health-related quality of life (HRQOL). 6
The majority of studies reported significantly poorer HRQOL outcomes in patients with LE resulting in decreased physical functioning, as well as psychological and social well-being, in comparison to breast cancer survivors without LE. This swelling can lead to an increase in breast and arm symptoms, shoulder stiffness, and functional limitations in activities of daily living, body image disturbance, anxiety, and negative future perspectives.6–8 Therefore efforts to prevent LE are very important. Preliminary research findings suggest that early diagnosis and initiating compression in the subclinical phase may reduce the development of clinical LE,3,4,9,10 but randomized controlled trials evaluating compression garments and quality of life (QoL) for LE prevention are lacking.
Appropriate physical exercises may have beneficial effects, including considerable improvement in range of shoulder motion after surgery,11,12 cardiorespiratory fitness, physical function, and QoL, in patients previously treated with chemotherapy and radiation therapy.13,14 Epidemiological evidence supports PA before and after breast cancer treatment as a contributing factor in decreasing risk of breast cancer recurrence and mortality among breast cancer survivors. 15
However, studies investigating the role of postoperative physical activities in combination with compression are lacking. The aim of the study was to compare the level of PA and QoL after breast cancer surgery in two groups of patients: in those using light arm compression sleeves and performing exercises and in women performing exercises but not using compression up to 1 year after oncological treatment.
Materials and Methods
Fifty-four women with recognized breast cancer without distant metastases, with no symptoms/signs of infection in the affected limb, without any signs of heart or renal failure, vein thrombosis, severe pulmonary insufficiency, or liver disease were preoperatively randomly assigned to a compression group (CG) or to a control group without compression (no compression group, NCG). Nine patients (one from CG, eight from NCG) resigned at the beginning of this study and 45 women were recruited (Table 1).
BMI, body mass index; CG, compression group; NCG, no compression group; IQR, interquartile range (25%–75%); SD, standard deviation.
For the 12 months' period postoperatively the CG received circular-knit sleeves in compression class 1 (ccl1, 15–21 mmHg) for daily wearing in the postoperative period. Compression sleeves (MEDI Bayreuth, Germany) were fitted to the subjects based on the preoperative individual limb measurements. Standard educational leaflets addressing wearing time, garment washing, and replacement intervals were provided. Arm sleeves were applied in the morning and removed before going to bed (average wearing time per day: 8–10 hours). Both groups received the same standardized physical exercise program: active upper limb exercises (flexion and extension, abduction and adduction of the shoulder, shoulder rotations, flexion and extension of the elbow, and fist clenching) combined with deep diaphragmatic breathing were performed initially with an instructor and recommended to be performed regularly once daily for 15 minutes.
In both groups preoperatively and 12 months afterward, the limb volumes were taken based on circumferential arm measurements using a simplified frustum formula. 16 Edema volume (mL) was calculated by subtracting the volume of the normal limb from that of the affected limb. An increase of >10% in limb volume was defined as LE. 17
Twelve months after the operation, PA was assessed with the International Physical Activity Questionnaire (IPAQ) (7-day short version available at www.ipaq.ki.se). The items in the IPAQ form were structured to provide separate scores on the time spent walking in moderate-intensity and vigorous-intensity activity. Computation of the total score for the short form requires summation of the duration (in minutes) and frequency (days) of walking, moderate-intensity and vigorous-intensity activities. All scores are expressed in MET (metabolic equivalent of task)-min/week. A MET is the resting metabolic rate while sitting quietly in a chair. One MET is approximately equal to resting oxygen consumption of 3.5 mL/kg/min. Thus exercise intensity is expressed in multiples of the resting metabolic rate. The following values continue to be used for the analysis of IPAQ data: walking = 3.3 METs, moderate PA = 4.0 METs, and vigorous PA = 8.0 METs. Total physical activity (TPA) in MET-min/week is calculated as sum of walking + moderate + vigorous MET-min/week. The duration of PA could not be less than 10 minutes. According to IPAQ it is easy to classify subjects into one of three PA categories of: insufficient (below 600), sufficient (600–1500 or 600–3000), and high (above 1500 or 3000 MET-min/week). Duration of sitting is an additional indicator variable of time spent in sedentary activity and is not included as part of any summary score of TPA.
Compliance assessment after 1 year observation was based on the International Compression Club Compression Questionnaire (ICC meeting, Maastricht 2014). HRQOL was measured 12 months after surgery with European Organization for Research and Treatment of Cancer (EORTC) QLQ-C30 and QLQ-BR23 questionnaires. 18
The research protocol was in accordance with the Helsinki Declaration, approved by the local ethics committee (no. 63/KBL/OIL/2014).
Statistics
The sample size calculation was based on our previous pilot study when a power of 80% in a clinically meaningful median limb volume difference of 200 mL was achieved. Actually the difference of the median volumes was 326 mL and the power reached 95%.
The categorical variable data were presented as proportion and the continuous variables as mean (standard deviation, SD) in normally distributed (according to Shapiro–Wilk test) or median (interquartile range 25%–75%). The associations between categorical variables were analyzed by chi-square test or Fisher's exact test, whereas continuous variables were compared within one group by paired t test (for normally distributed) or Wilcoxon rank-sum test (non-normally distribution). Means and SDs of normally distributed variables were compared, and paired t test was used to examine the differences. Linear regression analysis (ANCOVA) was identified to control for baseline differences. Correlations between affected arm volumes, edema volumes, BMI, and type of PA, as well as sitting time, were calculated using Spearman test. p-value of less than 0.05 was regarded as significant.
Results
Patients characteristics
Patient's characteristics according to wearing compression or not, including BMI, type of surgery and additional oncological modalities, level of PA, and arm edema volume changes, are summarized in Table 1.
Limb and edema volumes
After 1 year of observation the CG showed significantly lower mean affected arm volume compared to NCG. Four of 23 patients (17%) in CG versus 6/22 (27%) in NCG developed LE; significantly less edema could be seen in the CG versus NCG (p < 0.001). BMI has not changed markedly although in NCG patients initially were more often overweight compared to the women in CG (Table 2).
EORTC, European Organization for Research and Treatment of Cancer; QoL, quality of life.
Physical activity
The available data indicated no significant differences in the amount of vigorous and moderate physical activities, as well as walking between groups with compression (CG) and without (NCG) 1 year after oncological treatment; however, higher TPA was observed in CG compared to NCG (Table 3). Moderate-intensity activities (1440 MET-min/week vs. 420 MET-min/week) dominated in CG, while in NCG sitting time was more prevalent. Higher sedentary activity in NCG can be related with older age compared to the age in women from CG.
MET, metabolic equivalent of task; TPA, total physical activity.
There were no correlations between arm/edema volume or BMI changes after 12 months and type of PA in CG (Table 4).
Sleeve compliance and HRQOL
There was a good compliance observed within CG: 22 of 23 patients were wearing the sleeves over 12 hours, without any application/removal troubles. All women felt improvement in physical functioning (wrist/elbow movement ability, functional improvement enabling eating with the spoon, working, or practicing sports). There were only sporadic mild complications of compression (unpleasant feeling because of too high temperature in two patients, itching or sliding down the product—one patient each).
Better sexual functioning (QLQ-BR23 BRSEF subscale; p = 0.01) and greater upset by hair loss (BRHL subscale; p = 0.01) within NCG were found (Table 5). The global health status, functional and symptom scales of QLQ-C30 and the remaining of QLQ-BR23 functional aspects (body image, sexual enjoyment, future perspective), and symptom items (systemic therapy side effects, breast symptoms, arm symptoms) did not differ between groups.
HRQOL, health-related quality of life; EORTC QLQ-BR23, EORTC Quality of Life Breast Module Questionnaire.
Discussion
In patients with manifest breast cancer related LE compression combined with exercise regimes is a well-established method improving physical functioning and general health.19–21 This treatment requires lifelong management and the effectiveness depends on patient compliance. However, the prophylactic role of physical activities in combination with compression to reduce the incidence of postoperative arm-LE is less clear, since prospective randomized trials evaluating PA with or without compression for LE prevention are lacking.
Based on literature related with decongestive lymphatic therapy (DLT), exercises with compression bandaging/compression garments improve lymph outflow; however, some studies found insufficient evidence to support or refute the recommendation to wear compression sleeves during regular exercise in LE.22,23 In one study no exacerbation of LE with absence of compression during resistance exercise was observed 23 and in another report compression garments with exercises in LE maintained the effect after DLT. 21
As demonstrated in our study, PA levels were essentially equivalent between women wearing and not wearing compression garments; their QoL was not significantly diminished by this intervention. Evaluating our data by measuring the edema volume in both study arms we were able to demonstrate that wearing compression sleeves in ccl1 (15–21 mmHg) in addition to PA was able to reduce the incidence and amount of early postoperative edema and of LE, defined by an increase of the arm volume of more than 10% up to 12 months significantly. 24
Breast cancer survivors are at higher risk of decreasing PA 5 and often refrain from exercises to avoid or limit repetitive or strenuous use of limb on the side of the body treated for cancer because of the fear of developing LE. 25 Despite the majority of studies that have approved the safety of exercise for survivors with LE, 25 it is difficult to say with confidence if and which types of exercise reduce the risk of LE. Scientific evidence concerning prevention of LE incidence remains still poor.19,26,27
Strong evidence is now available on the safety of physical exercise during and after breast cancer treatment.14,28 Physical exercises have been shown to improve physical function, help maintain optimal BMI, and increase QoL, as well as decrease risk of comorbidities such as heart disease or new primary cancers and later cancer recurrence.13,15 Among LE patients participating in exercise physiotherapy programs, general health, vitality, and physical functioning were also reported. Significant improvements in physical and psychological function were noticed when DLT was combined with exercise regimens.29,30
Breast cancer survivors, who participate in regular PA, may improve their survival. 31 Current recommendations by American College of Sports Medicine encourage cancer survivors to follow exercise programs for healthy age-matched adults, which include 150 min/week of moderate or 75 min/week of vigorous aerobic exercise—it means at least 600 MET-min/week. 31 Our data indicate a sufficient level of PA 1 year after surgery—the activity levels were quite equivalent in both groups and wearing of sleeves did not have any negative influence. Only two women from CG and three women from NCG had an insufficient (<600 MET-min/week) level of TPA. Our data show also no significant differences in PA between the groups with and without compression despite the CG having a tendency to higher vigorous- and moderate-intensity activities compared to the NCG (Table 3). Differences in TPA observed between groups could be a result of older age in NCG women. A significant decrease of arm and edema volume was only observed in the CG. There was no correlation between arm volume after 12 months, type of PA, and sitting time in the CG. Decrease of arm volume seems to be a result of compression influence mainly.
The arm sleeves exerted a mean resting pressure of 15 mmHg and could be easily applied by the patients themselves. Our study shows that light circular knitted sleeves in combination with an exercise program may decrease the risk of secondary LE after lymph node interventions and that low pressure products seem to be sufficient. It might be that the relative high level of stiffness of the used product (the measured increase of pressure was between 7 and 11 mmHg during fist clenching) could explain the beneficial effect of the sleeve in combination with PA exercises. Significant decrease of subgarment pressure observed after 6 months is mainly due to the achieved edema reduction in addition to some fatigue of the material and should lead to the prescription of new sleeves. 24
In a recent review, patients with breast cancer-related LE reported a lower QoL score compared to those without LE due to resulting decrease in physical functioning and psychological and social well-being. 6 Using the EORTC QLQ-C30 and BR23 as a valuable instrument to assess the QoL in breast cancer patients, 18 we did not find any significant differences at any assessment point (global health status, functional scales, and symptom scales) in QLQ-C30 between the groups with and without compression. Analog results were also reported in other studies.32,33 The QLQ-BR23 data revealed only better sexual function (BRSEF) (p = 0.014) and greater upset by hair loss (BRHL) (p = 0.01) in the group without compression despite comparable cytostatic treatment (Table 5). The remaining functional aspects (body image, sexual enjoyment, and future perspective) and symptom items (systemic therapy side effects, breast symptoms, and arm symptoms) did not differ significantly between the groups. It seems that worse result of sexual functioning in CG can be related with more extensive surgery (mastectomy + ALND) in women who were younger compared to women in NCG.
The economic burden of prevention and therapy of LE should be further evaluated. It is in the interest of the patient, the therapist, and the insurance companies to make the LE prevention as cost effective and as acceptable as possible. Patients with LE may not be able to return to work and this may further diminish their HRQOL, as well as economic productivity. Changes in social well-being were most marked among younger patients with women under 40 experiencing decreased social well-being compared to the older patients. 34 Seventeen of 23 examined women in the group with compression started to work again. Compression was well tolerated and patients could not only carry out their jobs but also leisure activities and practice sport. None of the patients reported any complications related to the use of the sleeve. There were no problems with donning and doffing the compression device so that compression sleeves are very easy and safe option in the LE prevention. The use of compression garments in women at risk does not seem to worsen their QoL. Almost all women planned to continue to use the sleeve after completion of the study, so that we plan to follow the patients for at least 2 years. We suggest that low compression sleeves used in this study are acceptable for women at risk. For people who are otherwise healthy, lower pressure is preferable leading to a better compliance. Previous studies have shown that already low pressure stockings are able to prevent leg edema in standing professions 35 leading to a better QoL. 36
One major limitation of our study is the low number of patients who agreed to take part in the study, which does not allow to evaluate subgroups concerning the risk for the development of LE. Another weakness of this study was the noticeable number of dropouts (16.7%) in NCG and the restricted observation period of 1 year.
An important strength of the study is the preoperative assessment of limb volumes and the high level of compliance regarding self-application and wearing of the sleeves and concerning the attendance at follow-up visits.
Conclusion
The available data indicate that wearing compression sleeves neither interfere with the level of PA nor decrease QoL 1 year after breast cancer surgery.
Our data show that an exercise program involving all major muscle groups in the upper limb but performed together with light compression sleeves is well accepted, reduces the risk of secondary LE after lymph-node interventions in comparison to PA alone, and may be recommended as a routine procedure, starting immediately after surgery.
Footnotes
Acknowledgment
This work was supported by University of Physical Education, grant number: 51/BS/KRK/2014.
Author Disclosure Statement
No competing financial interests exist.
