Complex Decongestive Therapy Enhances Upper Limb Functions in Patients with Breast Cancer-Related Lymphedema

Abstract

Background:

We aimed to evaluate the effects of complex decongestive therapy (CDT) on upper extremity functions, the severity of pain, and quality of life. We also searched the impact of the sociodemographic and clinical characteristics on the improvement in upper extremity functions.

Methods:

A total of 37 women with breast cancer-related lymphedema (BCRL) [age, 53.6 ± 11.2 (28–72)] were included in this study. All patients underwent CDT-phase 1 program, including meticulous skin care, manual lymphatic drainage, remedial exercises, and compression bandages. Arm volume was calculated by a formula for truncated cone using circumferential measurements. A baseline questionnaire, including sociodemographic and clinical properties, was used for each patient. Short Form-36 (SF-36), Disabilities of the Arm, Shoulder and Hand (DASH) questionnaire, and Visual Analog Scale (VAS) for pain and heaviness were used as clinical assessment scales.

Results:

The mean of the posttreatment volume of the affected limb was lower compared to pretreatment volume (2741.81 ± 696.85 and 2990.67 ± 745.49, respectively), and the mean percentage change in edema volume was 38.1% ± 26.5%. We observed a statistically significant reduction in pain and heaviness VAS scores and improvement of shoulder mobility among upper extremities with lymphedema (p < 0.001) after CDT. The mean of posttreatment DASH score was lower compared to pretreatment score (37.19 ± 16.01, 49.81 ± 18.84, respectively, p < 0.001). All subgroups of the SF-36 parameters were increased after the CDT application (p < 0.01). Besides being under 65 years old, having a body mass index above 30 and short duration of lymphedema were found to be related to greater improvement in upper extremity functions.

Conclusions:

CDT provides enhancement of upper extremity functions and quality of life in patients with BCRL. The reduction in lymphedema volume, pain, and heaviness and the improvement in shoulder mobility may be the contributed factors.

Introduction

Breast cancer is the most frequently diagnosed cancer in women worldwide. Because of the increase in early detection and the improvements in treatments, more women survive breast cancer. The survival rate varies from 40% to 80% depending on the development level of the countries.¹ Breast cancer survivors are at increased risk for the long-term treatment-related sequela such as breast cancer-related lymphedema (BCRL). BCRL is a pathological condition characterized by the accumulation of protein-rich lymphatic fluid in the extracellular spaces. It may occur in almost 40% of the patients who have undergone breast cancer surgery or radiation therapy due to the lymphatic system defects.^2–5 BCRL may appear in the upper extremity, as well as in the ipsilateral upper quadrant and remaining breast tissue.⁶ The related risk factors are the number of removed axillary nodes, radiotherapy, the presence of axillary hematoma, seroma or infection, overweight, and reduced physical activity.^7–10

In lymphedema, there is no cure, but for optimal benefits, early detection and initiation of the treatment are essential.^5,11,12 Today, complex decongestive therapy (CDT) is recognized as the primary treatment of lymphedema. CDT is carried out in two phases (intensive and maintenance), and it consists of multicomponents such as manual lymphatic drainage (MLD), compression therapy, remedial exercises, meticulous skin care, and patient education. The aims of the CDT are to reduce the extremity volume by transferring lymph fluid with the residual lymphatics; to reduce the fibrosis; and to prevent the complications and recurrences. The benefits gained in the intensive phase are tried to be conserved in the maintenance phase.^3,5,12–14

Lymphedema leads to psychological problems, reduced upper extremity functions, and deterioration in health-related quality of life (HRQoL).^4,15–18 Up to now, the studies related to the effectiveness of CDT are focused on extremity volume reduction and improvement in the quality of life.^19–23 However, the studies investigating the effects on the upper extremity functions are limited.^24–26 Although it is important to show the decrease in the lymphedema volume, the improvements in upper extremity functions should also be demonstrated to accept that a treatment is effective in lymphedema. Therefore, in this study we aimed to evaluate the following: (1) the effect of CDT on upper extremity functions, severity of pain, and quality of life and (2) the impact of the sociodemographic and clinical characteristics on the improvement in upper extremity functions.

Materials and Methods

Subjects

Participants were recruited from the lymphedema follow-up clinic in Ankara Physical Medicine and Rehabilitation Training and Research Hospital from August 2014 to February 2015. Subjects who developed a difference of 2 cm or more in circumferential measurements between the lymphedematous and the contralateral limb and had at least one of the symptoms of tension, heaviness, pain, and functional impairment were accepted as sufficient for BCRL diagnosis. All patients were required to be more than 18 years old and had a history of breast cancer treatment at least 3 months ago. The exclusion criteria were as follows: (1) bilateral breast cancer and bilateral upper limb lymphedema, (2) recurrence or metastasis of breast cancer, (3) edema due to other reasons such as heart, kidney, or liver diseases and filariasis, (4) stage 3 lymphedema according to the lymphedema staging system of International Society of Lymphology,²⁷ (5) patients with the contraindications for application of CDT (active cutaneous infection, deep vein thrombosis, cardiac edema, and peripheral artery disease), and (6) coexistence of neuromuscular diseases, which could affect the upper extremity functions. A total of 52 consecutive women with the diagnosis of BCRL were evaluated. Of those, four patients had metastasis, three patients had stage 3 lymphedema, four patients had cellulitis, and two had bilateral lymphedema. Therefore, these 13 patients were excluded from the study, and a total of 39 patients were enrolled. However, during the treatment period, two patients dropped out of the study because of the new onset of cellulitis. In consequence, 37 patients completed the treatment and were included in the final analysis. The study was approved by the local ethics committee, and the written informed consent was provided for all participants.

Treatment protocol

Complex decongestive therapy-phase 1 program, consisting of meticulous skin and nail care, MLD, compression bandages, and remedial exercises, was applied to all participants. All patients received MLD for five times a week (Monday–Friday) during 3 weeks (a total of 15 sessions) by a physiotherapist trained in the Vodder method. Each MLD session lasted ∼45–60 minutes. Multilayered short-stretch bandaging was performed after the application of MLD. The bandaging process was started with placing the stockinette over the arm and hand. Then it was followed by padding made of cotton and multiple overlapping layers of short-stretch bandages. The patients kept the bandages on for 21–24 hours a day. Remedial exercises were done with the bandages in place to increase lymphatic drainage through the contraction and relaxation periods of the muscles. Abdominal breathing exercise was also added to the rehabilitation program. At the end of the 3-week CDT-phase 1 program, an education was given to the patient and family for the maintenance phase (phase 2) of CDT. Sleeve and glove were provided for wearing during daytime only. In addition, patients were trained for multilayered nocturnal bandaging (at least 3/week) and self-massage techniques.

Assessment and outcome measures

A baseline questionnaire, including sociodemographic (age, body mass index [BMI] and marital, work, and educational status) and clinical properties (type of surgery, time of surgery, duration, and side of the lymphedema), was used for each patient. Clinical symptoms of pain and heaviness in the affected arm were evaluated with visual analog scale (VAS). Ranges of motion of the shoulder (flexion, abduction, and external rotation) were measured by a goniometer. All participants completed the Disabilities of the Arm, Shoulder and Hand (DASH) questionnaire and Short form-36 (SF-36). The circumferential measurements of the upper extremities were carried out bilaterally. The assessments were performed at baseline (before the treatment) and 1 week after the end of the 3-week CDT-phase 1 program.

DASH questionnaire

The DASH is a self-report questionnaire, which assesses physical function and symptoms in people with musculoskeletal disorders of the upper extremity. The DASH has 30 items, and each item is scored on a Likert scale from 1 to 5 where 1 reflects “no difficulty” and 5 “severe difficulty.” Scores are transformed to a 0–100 scale with higher DASH scores indicating greater disability. This instrument assesses physical functions, symptoms, and social functions. The optional four items related to work or sports activities were not used for this study. Test–retest reliability for the DASH exceeds to 0.96 in musculoskeletal population. The Turkish validity and reliability study of DASH were conducted by Duger et al.²⁸

Medical outcomes study 36-item short-form health survey (SF-36)

The SF-36 was used to assess the HRQoL. This measure is a 36-item survey consisting of 8 multi-item scales such as physical function, role physical, mental health, role emotional, vitality, bodily pain, social functioning, and general health. Each section is directly transformed into a 0–100 point scale with higher scores demonstrating better health status. The scores of the subscales can also be summarized as the physical component score (PCS) and mental component score (MCS).

Circumferential measurements

The circumferential measurements (cm) were carried out at five anatomic landmarks (wrist, 10 cm below the elbow, elbow, 10 cm above the elbow, and axilla) by a plastic tape with light pressure. The upper limb was divided into four segments with the mentioned anatomic landmarks, and the arm volume was calculated with a truncated cone formula. The formula was “V = h (C2 + Cc + c2)/12π” (V: the volume of an extremity segment, C/c: circumferences at each end, and h: the distance between the ends). The total volume of the extremity was calculated by summing up these four segments. The measurements were taken before and after the CDT application on both affected and unaffected sides to evaluate the reduction in lymphedema volume. The percentage change in edema (%) was calculated with the following formula: percentage change in edema = (V_i − V_f)/(V_i − V_n) × 100 (V_i: the initial volume of the lymphedematous limb, V_f: the final volume of the lymphedematous limb, and V_n: volume of the normal limb).

Statistical analysis

SPSS software package (version 20.0; SPSS Inc., Chicago, IL) was used for statistical analysis. Distributions of continuous variables were assessed by Shapiro–Wilk test. Descriptive statistics was determined as mean ± standard deviation for continuous variables, median (minimum–maximum) for discrete variables, and number (n) and percentage (%) for categorical variables. The significances of the difference in median values between the affected and unaffected arms were analyzed with the Mann–Whitney U test. The Wilcoxon test was used to express significant changes on the arm volumes between before and after CDT. Spearman correlation analysis was performed to evaluate the relationship between the decrease in DASH scores and the possible associated parameters. A p-value of <0.05 was considered significant.

Results

The average age of all 37 patients was 53.6 ± 11.2 (28–72). Table 1 shows the sociodemographic and the clinical characteristics of the patients. The mean of the pretreatment volume of the affected limb was 2990.67 ± 745.49 (1515–5093) mL, and the posttreatment volume was 2741.81 ± 696.85 (1386–4772) mL (p < 0.001). The mean of the percentage change in edema was calculated as 38.1% ± 26.5%. Statistically significant reduction in pain and heaviness VAS scores and improvement in shoulder mobility were observed in the affected upper extremities with the CDT application (p < 0.001). The mean of the posttreatment DASH scores was found to be lower compared to the pretreatment DASH scores (37.19 ± 16.01, 49.81 ± 18.84, respectively, p < 0.001) (Table 2). All subgroup scores of the SF-36 questionnaire showed a significant increase with the treatment (p < 0.01) (Table 3). The impacts of the sociodemographic and clinical properties on the improvement in DASH scores were also evaluated. Being under 65 years old and having a BMI above 30 were found to be related to the greater difference in DASH scores (respectively, p = 0.03 and p = 0.04) (Table 4). The correlation analysis between the decrease in DASH scores and age, BMI, and the edema reduction rate was not found to be significant (p > 0.05). Besides, a significant correlation was found between the decrease in DASH scores and the duration of lymphedema (r = −0.306, p = 0.04). The study also revealed a significant correlation with the decrease in DASH scores and the increase in PCS of SF-36 (r = 0.355, p = 0.03), but not with the increase in the MCS (r = 0.159, p > 0.05).

Table 1.

Sociodemographic and Clinical Characteristics of the Patients, n = 37

Variables	n (%)	Mean ± SD
Age, years		53.5 ± 11.1
BMI, kg/m²		29.5 ± 5.5
Marital status
Married	27 (73)
Single	10 (27)
Work status
Employed	30 (81.1)
Unemployed	7 (18.9)
Education status
Low	27 (73)
High	10 (27)
Type of surgery
RM+LND	2 (5.4)
MRM+LND	30 (81.1)
BCS+LND	5 (13.5)
Time from surgery, months		47.6 ± 31
Duration of lymphedema, months		21.5 ± 19
Side of surgery
Dominant	18 (48.6)
Nondominant	19 (51.4)
Chemotherapy	36 (97.3)
Radiotherapy	33 (89.2)
Lymphedema stage
Stage 1	7 (18.9)
Stage 2	30 (81.1)
Lymph node metastasis+	26 (70.3)

BCS, breast-conserving surgery; BMI, body mass index; LND, lymph node dissection; MRM, modified radical mastectomy; RM, radical mastectomy

Table 2.

The Efficacy of Complex Decongestive Therapy on Lymphedema Volume, Upper Extremity Functions, and the Severity of Pain and Heaviness, n = 37

Variables	Pretreatment	Posttreatment	p
Lymphedema volume, mL	2990.67 ± 745.49	2741.81 ± 696.85	<0.001
DASH score	49.81 ± 18.84	37.19 ± 16.01	<0.001
Pain VAS score	4 (3–6)	1 (0–3)	<0.001
Heaviness VAS score	5 (3–6)	2 (0–3)	<0.001
Shoulder mobility
Forward flexion	170.27 ± 16.07	175.13 ± 9.01	0.001
Abduction	168.10 ± 19.83	172.97 ± 12.66	0.003
External rotation	81.62 ± 14.04	84.32 ± 9.87	0.008

Values are mean ± SD or median (IQR1–IQR3).

DASH, Disabilities of the Arm, Shoulder and Hand questionnaire; VAS, Visual Analog Scale.

Table 3.

The Efficacy of Complex Decongestive Therapy on Health-Related Quality of Life, n = 37

Variables	Pretreatment (mean ± SD)	Posttreatment (mean ± SD)	p
Physical functioning	38.3 ± 8.65	42.5 ± 7.09	<0.001
Role physical	33.7 ± 6.81	37.70 ± 7.87	0.001
Bodily pain	41.39 ± 11.25	49.22 ± 8.73	<0.001
General health	41.79 ± 8.30	47.6 ± 8.65	<0.001
Vitality	45.99 ± 8.86	51.4 ± 8.91	<0.001
Social functioning	35.15 ± 8.85	40.9 ± 8.4	<0.001
Role emotional	34.24 ± 8.62	38.10 ± 9.66	0.009
Mental health	39.55 ± 12.76	45.9 ± 8.8	0.001
Physical component scores	39.37 ± 8.83	42.8 ± 7.3	<0.001
Mental component scores	39.47 ± 9.93	43.8 ± 9.52	<0.001

Table 4.

The Impact of Sociodemographic and Clinical Characteristics on the Improvement in DASH Scores, n = 37

Variables	DASH score difference mean ± SD	p
Age, years
<65	13.26 ± 8.08	0.04
>65	7.33 ± 6.23	0.04
BMI, kg/m²
<30	10.03 ± 9.47	0.03
>30	17.33 ± 8.85	0.03
Education level
Low	12.05 ± 9.12	0.24
High	9.76 ± 8.76	0.24
Type of surgery
RM/MRM+LND	10.06 ± 8.76	0.46
BCS+LND	8.68 ± 7.89	0.46
Lymphedema stage
Stage 1	13.3 ± 9.83	0.86
Stage 2	12.46 ± 10.22	0.86
Lymph node metastasis
Yes	14.33 ± 10.79	0.56
No	11.89 ± 9.86	0.56

Boldface denotes significance at p < 0.05.

Discussion

BCRL is a condition that generally leads to long-term sequela such as psychological distress, physical impairments, and deterioration in HRQoL in breast cancer survivors.^4,17,18,29 Today, CDT is accepted as the gold standard therapy of BCRL.⁵ The aims of our study were to evaluate the effects of CDT on upper extremity functions, severity of pain, and quality of life and to investigate the impact of sociodemographic and clinical characteristics on the degree of improvement in upper extremity functions. Our results revealed that CDT has positive effects on the mentioned clinical parameters. Besides, being under 65 years old, having a BMI above 30, and short duration of lymphedema were found to be related to greater improvement in upper extremity functions.

In the literature, several studies revealed positive effects of CDT on lymphedema volume and HRQoL in BCRL.^19–22 In our study, we found the mean of the percentage change in edema as 38.1% compatible with the previous studies suggesting 20% to 73%.³⁰ Mondry et al. investigated the effects of 2–4 week of CDT on quality of life (QoL) and severity of pain in the same population and demonstrated that the degree of the decrease in girth had a significant correlation with the reduction in pain VAS scores, but not with the increase in QoL. In another study, Kim et al. also showed that during the maintenance phase of CDT, QoL significantly improved and in contrast with the study of Mondry et al., it was correlated with the reduction in limb volume.¹⁹ In our study, we found significant improvements in all subgroups of the PCS and MCS of SF-36 and severity of pain after the application of 3-week CDT program. We focused on the upper extremity functions, so we did not do further investigations or comparisons among the HRQoL and sociodemographic and clinical factors. Besides, we found that the improvements in upper extremity functions were correlated with the improvements in HRQoL.

After the breast cancer treatment, it was suggested that physical impairment appears on the affected upper limb and this limitation was greater in patients with lymphedema.^15,16 Lymphedema related arm swelling, heaviness, pain, restriction in the upper extremity joints, and reduced strength may be the causal factors for the decreased upper extremity functions.^15,16,31,32 In this population, the studies evaluating the upper extremity limitations are mostly cross-sectional studies, and the comparisons were made between patients with and without lymphedema.^15,33 In one of these studies, Dawes et al. demonstrated that women with lymphedema had higher scores of the DASH questionnaire as an indicator of activity limitation and participation restriction.¹⁵ They also showed that severity of pain was correlated with higher DASH scores and suboptimal HRQoL. This study also pointed out that the treatments decreasing only lymphedema volume without a reduction in pain may not provide improvements in activity, participation, or HRQoL. In another study, being older was shown to be related to upper extremity dysfunction.³³ In these studies, the DASH questionnaire was used to assess the upper limb functions. It contains 5 impairment items, 19 activity limitation items, and 3 participation restriction items, which are compatible with each of the three International Classification of Functioning, Disability and Health Model (ICF) outcomes with discriminant validity.¹⁷

In the literature, a limited number of studies evaluated the effects of lymphedema treatments, especially CDT on upper extremity functions, and the results were contradictory.^24–26 One of these studies, Buragadda et al. compared patients with BCRL receiving CDT and a home program or conventional treatment.²⁴ The conventional treatment group performed MLD, a low elastic compression garment, glenohumeral mobilization, and deep breathing exercise. And the 1-hour home program included self-lymphatic drainage, skin care, and remedial exercises. The results of this study indicated significant improvements in the arm function, pain, and lymphedema volume in both groups but greater improvements were seen in the group receiving the home program. In another study, King et al. compared the effects of compression garments versus compression bandaging within the initial treatment phase of a decongestive lymphatic therapy for a total of 10 treatment sessions in BCRL.²⁶ The results of this study revealed greater volume reduction, but worse upper extremity functions in compression bandaging group compared to compression garment group. Dayes et al. also compared two groups receiving compression garments or daily MLD and bandaging followed by compression garments. But unlike the results of the mentioned studies, no differences were found in mean scores for both the PCS and MCS of the SF-36 and DASH scores at baseline or any of the follow-up periods between and within the treatment groups.²⁵

In our study we had only one study group of BCRL receiving CDT, and we demonstrated significant improvements in DASH scores compatible with the Buragadda et al.'s study.²⁴ To reveal the gains provided by CDT application, we did the posttreatment evaluation 1 week after the end of the 3-week CDT phase 1 program, when the patient began to wear compression garments in daily routine. Because, with the compression bandages, the daily activities and the use of upper extremities were obviously limited and if we did the second evaluation immediately after the CDT phase 1, we may find less or similar conclusions in posttreatment DASH scores compared with the pretreatment scores. In addition to the significant decrease in DASH scores, we also found significant improvement in shoulder mobility and upper extremity pain VAS scores in the posttreatment evaluation. Shoulder disorders and pain are mostly seen in patients with BCRL who underwent axillary dissection and radiation and may be the causal factors of the deterioration in upper extremity functions and quality of life.³⁰ Devoogdt et al. revealed that 31% of the patients who underwent breast cancer treatment had impaired shoulder mobility, and 51% had the limitation of daily living activities.³⁴ The improvements in these parameters may be contributing factors for the decrease in DASH scores.

To our knowledge, the factors influencing the improvement in upper extremity functions following CDT have not been evaluated. The previous studies investigating the predictive factors for the effectiveness of CDT only used the lymphedema volume reduction as the treatment outcome. In these studies, most of the clinical and sociodemographic factors were not found to be associated with the effectiveness of CDT.^{20,23,30,35,36} Liao et al. showed that longer duration of lymphedema was correlated with higher baseline percentage of excess volume (PEV) and, greater PEV and older age were associated with worse CDT efficacy demonstrated with a lower percentage reduction of excess volume.³⁷ In our study, we showed that being under 65 years old and short duration of lymphedema were related to a greater increase in upper extremity functions consistent with the mentioned study. It was known that in the later stages of lymphedema CDT was less effective because of the adipose and fibrotic changes within the soft tissue.^3,38 Application of CDT in patients with early lymphedema would provide better recovery for upper extremity functions, as well as better volume reduction.

Considering that weight gain and higher BMI are risk factors for development and increased severity of lymphedema, the association between higher BMI and better recovery of upper extremity functions is a surprising finding of our study.^39,40 Previously, Vignes et al. revealed that higher BMI was a predictor for absolute reduction of lymphedema volume after intensive decongestive physiotherapy.³⁰ It was suggested that patients with high BMI might have larger volumes of lymphedema due to the containment of higher extracellular water proportion than intracellular water compartment in fat tissue. It was known that CDT could only mobilize extracellular fluid of the tissue. Therefore, the potential to lose absolute amounts is larger, and the benefits may be more evident.^30,41 But in our study, we were not able to show a correlation between the edema reduction rate and the degree of the improvement in DASH scores. So the reasons underlying to identify this relation remained unclear, and further studies are needed. In this study, we emphasize to take into account the upper extremity functions in addition to the volume reduction while determining the prognostic factors for the treatment efficacy.

Study limitations

The results of this study reflected only the initial phase of CDT. Because of the lack of long-term follow-up evaluations, we could not comment on the efficacy of maintenance phase. In addition, we enrolled patients with stage 1 and stage 2 lymphedema into the study. Therefore, we could not generalize the results for stage 3 lymphedema. Another limitation of this study was not inclusion of objective methods to assess the upper extremity functions. We used only DASH questionnaire because of the easy applicability.

Conclusion

As shown in our study, CDT provides enhancement of upper extremity functions and quality of life in patients with BCRL. The reduction in lymphedema volume, pain, and heaviness and the improvement in shoulder mobility may be the contributed factors. This study would lead to further long-term follow-up studies, including objective upper extremity function assessment methods.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

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