The Effect of Manual Lymph Drainage and Compression Bandaging for Stage 2 Breast Cancer-Related Lymphedema: A Randomized Controlled Trial

Abstract

Aim:

To explore the effect of manual lymph drainage (MLD), compression bandaging (CB), or combined decongestive therapy (CDT), including MLD and CB, on stage 2 breast cancer-related lymphedema (BCRL).

Methods:

Sixty women with stage 2 BCRL were enrolled. They were randomly divided into the MLD group, the CB group or the CDT group. Each group, respectively, received MLD alone, CB alone, or CDT composed of MLD and CB, for 2 weeks. The volume and the local tissue water (LTW) of affected arms were measured before and after treatment. Arm circumferences were measured at 4 cm interval starting from the wrist to the shoulder with a tape measure. LTW was detected using the (tissue dielectric constant, TDC) method and was expressed as TDC value in two sites on the ventral midpoint of upper arm and forearm.

Results:

The volume of affected arms in each group after 2-weeks' treatment was lower than their baseline and the difference was statistically significant (p < 0.05). But there was no significant difference in volume change among three groups. The TDC value of the upper arm and forearm in the group CB and the group CDT decreased distinctly compared with baseline (p < 0.05). But the TDC value of the upper arm and forearm after MLD did not change (p > 0.05). Compared with the group MLD and the group CDT, the reduction of the TDC value in the group CB was more significant (p < 0.05).

Conclusions:

MLD or CB alone could effectively reduce the volume of affected arms for patients with stage 2 BCRL, and CB also could reduce the LTW more significantly. CDT did not seem to show an extra advantage. Therefore, CB may be the first choice for stage 2 BCRL. But for patients who are unwilling or intolerant to CB, MLD can be selected.

Introduction

Breast cancer-related lymphedema (BCRL) is a common sequela of surgical or radiation therapy of breast cancer. Clinical manifestations of BCRL vary widely and include swelling, pain, discomfort, reduced joint dexterity due to fibrosis and hardening of affected tissues, as well as enhanced infection risk caused by static protein-rich ambience fostering bacteria.¹ There is no cure for lymphedema till now. It is widely believed that the optimal management to efficiently relieve lymphedema is combined decongestive therapy (CDT), a conservative treatment of choice for lymphedema. It generally consists of skin care, a specific manual lymph drainage (MLD), exercises, and compression with multilayered compression bandaging (CB). Many studies have shown that CDT is effective for secondary lymphedema.

A myriad of advantages is attained by a CDT approach that reduces edema volume, intensity of pain and arm heaviness, reinforces lymphatic function, improves quality of life, and lowers the incidence of cellulitis.^2–6 However, the effectiveness of using different components of CDT alone or in combination is still uncertain.⁷

Although MLD is quite welcome by patients, well tolerated, and harmless, it is time consuming and usually requires skilled therapists. Furthermore, there are conflicting results about the effectiveness of MLD across individual studies. Some research concluded that there was no effectiveness when combined with compression, some suggested additional benefit, but studies investigating MLD use alone (with no other concurrent treatment) were small.^6,7 Although compression therapy is noninvasive, during the treatment process, patients may need to tolerate various discomfort caused by this, such as bandage allergy or skin damage, and even the edema at the distal end of the limb may be aggravated due to improper pressure distribution. Therefore, patient compliance is a major challenge and one of the factors affecting the efficacy of long-term stress therapy.

Due to the differences in study design, the small scale of the trial, nonstandard measurement techniques, diagnosis and treatment thresholds, and the current studies on CDT have not provided decisive evidence for the superiority of any scheme, the combination of CDT components or the length of treatment time.⁸ MLD or CB needs to be evaluated both within the context of CDT and as a stand-alone modality. Therefore, the objective of this study was to determine whether the MLD or CB alone had an independent therapeutic effect and MLD combined CB could manage BCRL more effectively.

Patients and Methods

Conduct of study

The study was approved by the Medical Ethics Committee of Peking Union Medical College Hospital, Beijing, China, and was conducted following the Declaration of Helsinki. Written informed consent was obtained from each patient before the initiation of the study.

Study design and study population

This study was a single-center interventional study of randomized controlled trials executed at the Peking Union Medical College Hospital. Sixty female breast cancer survivors who underwent axillary lymph node dissection and radiotherapy, complained of swelling in the affected side, and were diagnosed as stage 2 BCRL were eventually enrolled.

Inclusion criteria

Breast cancer survivors with a history of mastectomy who complained of swelling or heaviness in the affected side and diagnosed as lymphedema stage 2 using the grading standard issued by the International Society of Lymphology (ISL) in 2016,^9,10 and willing to receive conservative treatment for BCRL were included in this study.

Exclusion criteria

The followings were excluded from participation in the data collection: survivors who had any evidence of cancer metastases or recurrences; acute inflammation; acute allergy; acute thrombosis; and cardiac decompensation.

Sixty-three women with stage 2 BCRL enrolled in this study initially. Three patients with cancer metastases (n = 1), combined with acute lymphangitis (n = 1) or being allergic to bandages, and unable to tolerate compression therapy (n = 1) were excluded. Finally, 60 eligible patients were investigated. The mean age was (54.8 ± 9.4) years (range 36–68 years). All patients had completed radiotherapy before they participated in this study.

They belonged to three groups, including the MLD group, the CB group, and the CDT group, respectively. Each group consisted of 20 patients. There was no significant difference in age, body mass index (BMI, kg/m²) as well as the baseline volume, and tissue dielectric constant (TDC) value of affected limbs among three groups, as shown in Table 1.

Table 1.

Age, Body Mass Index, Baseline Volume, and Tissue Dielectric Constant Value of 60 Breast Cancer–Related Lymphedema Patients in Three Groups (Mean ± Standard Deviations)

Parameter ^a (x ± s)	MLD	CB	CDT	p
N	20	20	20
Age (years)	54.5 ± 10.0	57.3 ± 9.2	51.4 ± 10.1	0.594
BMI (kg/m²)	25.9 ± 3.9	26.0 ± 3.0	26.3 ± 1.8	0.981
Volume (cm³)	3109.6 ± 666.2	2898.4 ± 579.0	2965.8 ± 317.6	0.457
TDC value of the upper arm	38.5 ± 7.0	38.3 ± 7.1	38.4 ± 6.8	0.997
TDC value of the forearm	41.9 ± 5.7	40.7 ± 5.0	41.1 ± 7.9	0.824

There are no significant differences in all baseline parameters among the three treatment groups.

MLD, manual lymph drainage, performed once a day, five times a week during 2 weeks; CB, compression bandaging, a compression therapy performed once a day, five times a week during 2 weeks; CDT, combined decongestive therapy, a conservative treatment, including manual lymph drainage and compression therapy with compression bandaging, performed once a day, five times a week during 2 weeks; BMI, body mass index; TDC, tissue dielectric constant; BCRL, breast cancer–related lymphedema; x ± s, mean ± standard deviation.

Scoring

Two doctors certified by the Dr. Vodder School- International performed MLD for patients in the MLD group and the CDT group. MLD consisted of four basic techniques (stationary circle, rotary technique, pump technique, scoop technique) initiated from the unaffected trunk quadrants (neck and chest) and after preparation of these regions, the affected areas of the trunk were treated. Then MLD was applied to the edematous limb starting proximally at the shoulder, moving in segments progressively down the limb, using specific edema techniques. Finally, the trunk was cleared, including the affected chest and back. Compression therapy was given to the patients in the CB group and the CDT group by the certified doctors with short stretch bandages. CB was worn soon after MLD and was kept day and night in the CDT group. MLD and CB were performed once a day, five times a week during 2 weeks.

The volume and the TDC value were measured at baseline and after 2 weeks' treatment. The TDC value reflecting the local tissue water (LTW) and edema of the affected arm was measured in the ventral midpoint of the affected upper arm and forearm with moisture meter (Moisture Meter D Compact; Delfin Technologies LTD, Kuopio Finland).^10–16 A probe with diameter of 23 mm and detection depth of 2.5 mm was selected in this study. Every point was measured three times and then averaged. Volume was calculated using circumferential measurements at every 4 cm from the styloid process to the shoulder.

Statistical analysis

A matched t test was used to compare the volume and the TDC value before and after treatment. One-way ANOVA and S-N-K were used to determine the difference among three groups. Significant statistically difference is p < 0.05.

Results

The volume of the affected limbs in each group after 2 weeks' treatment was all lower than baseline and the difference was statistically significant (p < 0.05).The TDC value of the upper arm and forearm in the CB group and the CDT group decreased distinctly compared with baseline (p < 0.05). But the TDC value of the upper arm and forearm after MLD did not change (p > 0.05), shown in Table 2.

Table 2.

Comparison of the Volume and the TCD Value in Upper Arm and Forearm Between Baseline and 2 Weeks' Follow-Up

Group statistic	N	Time	Volume (x ± s)	TCD value in upper arm (x ± s)	TCD value in forearm (x ± s)
MLD	20	Baseline	3109.6 ± 666.2	38.5 ± 7.0	41.9 ± 5.7
MLD	20	after 2 weeks	2974.1 ± 657.3^a	38.4 ± 6.7	41.9 ± 5.7
Change from baseline Mean (95% CI)			135.45 (117.28 to 153.62)	0.10 (−0.19 to 0.38)	0.02 (−0.61 to 0.64)
p value			0.000	0.494	0.961
CB	20	Baseline	2898.4 ± 579.0	38.3 ± 7.1	40.7 ± 5.0
CB	20	after 2 weeks	2760.9 ± 559.0^a	33.4 ± 4.9^a	36.0 ± 4.5^a
Change from baseline Mean (95% CI)			137.49 (100.98 to 173.99)	4.90 (2.68 to 7.12)	4.63 (2.73 to 6.52)
p value			0.000	0.000	0.000
CDT	20	Baseline	2965.8 ± 317.6	38.4 ± 6.8	41.1 ± 7.9
CDT	20	after 2 weeks	2829.7 ± 290.6^a	36.7 ± 5.6^a	39.7 ± 6.6^a
Change from baseline Mean (95% CI)			136.05 (118.67 to 153.42)	1.67 (0.90 to 2.43)	1.39 (0.55 to 2.22)
p value			0.000	0.000	0.003

denotes a p-value <0.05, showing a significant difference between the baseline and the 2nd week measurements.

MLD, manual lymph drainage, performed once a day, five times a week during two weeks; CB, compression bandaging, a compression therapy performed once a day, five times a week during two weeks; CDT, combined decongestive therapy, a conservative treatment, including manual lymph drainage and compression therapy with compression bandaging, performed once a day, five times a week during 2 weeks; TDC, tissue dielectric constant; x ± s, mean ± standard deviation.

Compared with the MLD group and the CDT group, the reduction of TDC value in the upper arm and forearm in the CB group was more significant (p < 0.05). However, there was no significant difference in volume change among the three treatment groups, shown in Table 3.

Table 3.

Comparison of Changes of Volume and TCD Value in Upper Arm and Forearm After 2 Weeks' Follow-Up Among the Three Treatment Groups

Group	N	Changes of volume (x ± s)	Changes of TCD value in upper arm (x ± s)	Changes of TCD value in forearm (x ± s)
MLD	20	135.5 ± 38.8	0.10 ± 0.61	0.02 ± 1.34
CB	20	137.5 ± 78.0	4.90 ± 4.74^a	4.63 ± 4.04^a
p values		NS	p < 0.05	p < 0.05
MLD	20	135.5 ± 38.8	0.10 ± 0.61	0.02 ± 1.34
CDT	20	136.0 ± 37.1	1.67 ± 1.64	1.39 ± 1.78
p values		NS	NS	NS
CB	20	137.5 ± 78.0	4.90 ± 4.74^a	4.63 ± 4.04^a
CDT	20	136.0 ± 37.1	1.67 ± 1.64	1.39 ± 1.78
p values		NS	p < 0.05	p < 0.05

denotes a p-value <0.05, showing a significant difference between the group CB and another two groups.

MLD, manual lymph drainage, performed once a day, five times a week during two weeks; CB, compression bandaging, a compression therapy performed once a day, five times a week during 2 weeks; CDT, combined decongestive therapy, a conservative treatment, including manual lymph drainage and compression therapy with compression bandaging, performed once a day, five times a week during 2 weeks, TDC, tissue dielectric constant; x ± s, mean ± standard deviation; NS, not statistically significant.

Discussion

As a universal treatment, CDT including MLD, compression therapy (consisting of compression bandages, compression sleeves, or other types of compression garments), skin care, and lymph-reducing exercises, has been regarded as the standard conservative treatment for lymphedema. Among these, MLD and CB are the key therapeutic techniques and have high professional requirements for operation, which need to be implemented by experienced doctors, physiotherapists, or nurses who have received strict training. MLD is a massage technique that uses a special rhythmic pumping through gentle, directed stretching of skin to massage the affected area and stimulate lymphatic contractility, thus enhancing lymphatic drainage without increasing capillary filtration.¹⁷ As a result, MLD reduces the tissue swelling and softening fibrosis in the trunk and arm.^18,19 However, results about the effect of MLD on the treatment and prevention of BCRL were inconsistent.

Some of research revealed that MLD did not significantly reduce or prevent the risk of lymphedema. Other research showed that MLD could add benefit in reducing the arm volume of the affected side.^20–27 So far, three systematic review and meta analysis, conducted, respectively, by Mining et al., Ezzo et al. and Huang et al., stated that a systematic analysis of previous randomized controlled trials revealed little distinction in the treatment or prevention of BCRL by comparing MLD with other interventions.^27–29 It is worth noting that heterogeneity across the analyzed studies was considerable and the sample size was limited. Paradoxically, subgroup analyses was significant showing that participants with mild-to-moderate BCRL were better responders to MLD than moderate-to-severe participants.^29,30

In addition, MLD could significantly reduce lymphedema in patients younger than the age of 60 years and an intervention time of 1 month.²⁸ A study believed that when fibrosis and concavity edema began to appear in early stage 2, standard CDT including MLD was better than CB alone.³¹

Although the area of lymphedema can be restored to a normal or near-normal situation with appropriate treatment including MLD, the lymphatic vessel system cannot return to its normal state and the skin cannot fully regain its elasticity. There is always a risk of restasis of lymph fluid at the site of the lesion. Therefore, providing external support to the affected area is an important step in the management of lymphedema. The main goal of compression therapy is to maintain the swelling reduction effect achieved during MLD and prevent lymphatic fluid from accumulating again.³² Compression raises tissue pressure, reduces the effective ultrafiltration pressure and helps reduce interstitial fluid by decreasing its formation and preventing lymph back flow into the interstitial space. Compression also improves the muscle pump function by creating a resistance against which muscles can work. Distinct variations within the subbandage pressures can enhance lymphatic and venous function.

Moreover, compression increases reabsorptive surface and softens tissues with fibrotic changes.³³ Studies have shown that the complete CDT of compression bandage combined with MLD has more advantages than that of compression bandage alone.³¹ However, some studies have found that compression bandages without MLD are still effective in reducing lymphedema.^21,34 Also, CB used with a compression garment could significantly reduce the volume of the edematous limb compared with the usage of a compression garment alone.¹⁷

In this study, we found that MLD alone or CB alone could effectively reduce the volume of affected arms in patients with stage 2 BCRL and CB as well as CDT could effectively reduce LTW of affected arms. Therefore, CB seemed to have more advantages, because it could not only significantly reduce the volume and LTW of affected arms but also more significantly improve LTW of affected arms compared with MLD alone or CDT. The combination of MLD and CB seemed to have no obvious advantage. In our previous studies, we found that MLD had an immediate therapeutic effect of reducing LTW of affected limbs in patients with BCRL,³⁵ but for patients with stage 2 lymphedema with fibrosis, MLD alone might not be able to maintain the improvement of LTW.

During the course of CB treatment alone, for the edema area with severe fibrosis, the local pressure would be appropriately increased during the dressing process to obtain better treatment effect. In the combined treatment, the fibrotic area usually was treated with fibrosis manipulation first. When CB followed immediately, because the local skin stiffness had been immediately improved, the local pressure was generally no longer deliberately increased during the dressing process, which might be related to the fact that the local LTW improvement after the combined treatment was not as significant as that of CB alone. These results suggested that the pressure gradient should be adjusted according to the individual differences of patients when CB therapy was performed after MLD in the combined treatment.

For local fibrotic areas, in the case of skin hardness and the LTW improvement from manual manipulation, it is still necessary to appropriately increase the pressure in this area to obtain better maintenance of treatment effect. If the CDT for BCRL can be individualized according to the evaluation results of the affected limb and in combination with the specific conditions and wishes of the patient, including whether they are willing to receive CB therapy, whether they are allergic to the fabric of CB, or whether they can tolerate the discomfort of compression treatment and inconvenience to life from this, it will be more ideal and can optimize benefits and cost efficiency.

The deficiency of this study is that the sample size is slightly small, and it is necessary to increase the sample size for further observation. Whether there will be different results after prolonging the course of treatment remains to be clarified by further research. It is also worth mentioning that the observed differences in TDC values after different treatment may be reasonably explained by differences in edema detection methods rather than differences in treatment effects because the moisture meter is a very sensitive tool used to detect LTW. If we use bioelectrical impedance analysis (BIA) to observe the extracellular water of limb segments, we probably get the same results as volume measurement.

However, BIA can only check the edema of the whole limb and is not sensitive to the edema with serious fibrosis but not significant volume increase. So it was not involved in this study. In the future, further research can be conducted to explore whether the observation results by different detection technologies are different. In addition, it would be important to identify other subgroups, and more than one possible subgroup can be examined in the same trial. For instance, will patients with stage 1 BCRL respond differently to MLD or CB? Are radiation-induced stenotic/fibrotic changes less responsive to MLD or CB than lymphatic damage from surgical scarring? To sum up, more high-quality studies are warranted on the differences in the therapeutic effects of CDT components and the choice of combination mode.

In conclusion, for stage 2 BCRL, MLD or CB alone could effectively reduce the volume of affected arms, and CB also could reduce the LTW of affected arms more significantly. CDT did not seem to show an advantage. Therefore, CB may be the first choice, and for patients who are unwilling or intolerant to CB therapy, MLD can be selected.

Footnotes

Acknowledgments

The authors thank Dr. Lixia Chen, Dr. Qiang Sun, and Dr. Shaofeng Yang for their kind support and help. We are grateful to the patients participating in this study. The work reported in this article would be incredible without them.

Authors' Contributions

Y.L.: Writing–original draft (lead) and review and editing (lead). X.Z.: Conceptualization (lead) and writing–review and editing (equal). J.S.: Software (lead) and writing–review and editing (equal). W.Z.: Conceptualization (supporting) and writing–review and editing (equal). Y.G.: Writing–original draft (supporting) and writing–review and editing (equal). J.G.: Methodology (lead), formal analysis (lead), and writing–review and editing (equal).

Author Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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