Abstract
Abstract
Background:
The purpose of this study is to investigate the effects of the aqua-lymphatic therapy (ALT) on unilateral lower extremity lymphedema in the maintenance phase.
Materials and Methods:
This is a randomized controlled trial with a blinded assessor. The study was completed with 30 ALT and 27 control group participants. Foot volume was assessed by a water displacement device, limb volume by circumference measurements, functional capacity by a 6-minute walk test, quality of life by Short Form-36, and social appearance by Social Appearance Anxiety Scale and hopeless by Beck Hopeless Scale. The ALT and the control group had group sessions twice in a week for 6 weeks directed by a physiotherapist.
Results:
The mean age of ALT patients was 44.50 ± 13.69 years, whereas that of the control patients was 47.66 ± 16.82 years. After the intervention, both groups' measurement of edema, functional level, quality of life, as well as social and future concerns improved significantly but this improvement was higher in the ALT group (p < 0.05, p ≤ 0.001).
Conclusions:
ALT was found to be a safe effective method for unilateral lower extremity lymphedema patients during the maintenance phase of Complex Decongestive Physiotherapy.
Introduction
A
As the lymphatic system constricts, protein-like macromolecules fail to transport back into the blood vascular system eventually causing swelling and other symptoms such as heaviness, tightness, and pain develop.1,5–7 The most common signs and symptoms for leg lymphedema are pain, swelling, reduced range of motion, muscle weakness, genital lymphedema, and difficulty with such activities of daily living as sitting or walking. Along with physical discomfort, this condition causes high levels of psychological stress because patients' perceptions change negatively and symptoms prevent them from participating in their usual activities. Thus, the aims of the therapy modalities are maintaining the stability of the lower extremities to increase mental health (MH) and quality of life.5–9
There is no known cure for lymphedema. The aim of the accepted therapies has been to control the lymphedema, and for that the common gold standard method is complex decongestive physiotherapy (CDP). CDP contains four complementary elements: skin care, manual lymph drainage, compression therapy, and remedial exercises. The treatment involves two stages; the first one is the intensive phase where a reduction of the majority of the edema occurs, and the second is the maintenance phase in which results of the intensive treatment must be continued by the patients themselves.1,10–12 According to the literature, after the intensive therapy phase, there was a 31%–73.4% reduction of edema reported; these results were compared with the initial status of the limb. 13 After stabilizing the volume, patients must carry on with the self-directed maintenance phase in which they need to wear compression garments, for compression, continue with the skin care, self-massage, and remedial exercises.14,15 Patients' adherence is the most important issue in the maintenance phase. There are only few studies assessing the relationship between adherence to maintenance therapy and lymphedema. These studies involve follow-up results of upper extremity lymphedema patients and they reported improvement of lymphedema during follow-up, especially in patients who were wearing an elastic sleeve and overnight bandage, whereas nonadherence may cause aggravation of the edema.16–19
The recent method for the lymphedema maintenance phase is aqua-lymphatic therapy (ALT), which provides a group setting for the patients to treat themselves in a social and entertaining environment. The ALT involves exercises and self-massage, which is performed in a hydrotherapy pool with specific characteristics. ALT combines the anatomic principles of the lymphatic system and the physical properties to maintain and even enhance the treatment effects that are accomplished during the intensive treatment phase with CDP.20,21 Physical properties of water might provide an effective, satisfying, and inexpensive environment for lymphedema patients and might be a good option for their maintenance phase to increase treatment adherence.20–22 Viscosity of the water provides resistance in any direction of the limb; on the other hand, hydrostatic pressure gradually increases with a greater depth that helps the lymphatic flow. Also, altering hydrostatic pressure on the skin during movements of the extremity may improve pumping of the lymphatic vessels.20–22
Aquatic therapy has been used to reduce edema in patients with musculoskeletal conditions and upper lymphedema.23,24 Only one article described the ALT technique on lower extremity lymphedema by using a case description of a woman with vulvar cancer. 21 No randomized study has investigated the effects of the ALT method in the maintenance phase on lower extremity lymphedema in the searching databases. The purpose of this study is to investigate the effects of ALT on unilateral lower extremity lymphedema in the maintenance phase.
Materials and Methods
Between January 2012 and January 2015, 63 lower extremity lymphedema patients gave their informed consent and enrolled in the study. After the baseline assessment, participants were randomly assigned to either the ALT group or the control group by using the simple random sampling method. Assignment was revealed by an independent researcher who was not involved in the assessment. The therapist who performed the outcome assessments was unaware of the group allocation throughout the study.
Ethical approval
All procedures involving human participants were in accordance with institutional and national guidelines, and the Helsinki Declaration of 1975, revised in 2007 (approved by Noninvasive Research Ethics Board of Dokuz Eylul University School of Medicine; protocol no.: 412-GOA; decision no.: 2014/31-14).
Setting and participants
The ALT sessions were conducted at a special hydrotherapy pool and the control group sessions were conducted at the Lymphedema Unit of Dokuz Eylul University, School of Physical Therapy and Rehabilitation, Izmir, Turkey.
Participants in this study were recruited from the Lymphedema Unit of Dokuz Eylul University, School of Physical Therapy and Rehabilitation.
• Inclusion criteria:
○ Suffered from primary or secondary unilateral lower extremity lymphedema ○ Had undergone or completed the minimum 2 weeks intensive phase of CDP in the past ○ Received approval to participate in ALT by their physician ○ Was a volunteer ○ Was older than 18 years of age
• Exclusion criteria:
○ Had undergone sentinel lymph node biopsy ○ Had active metastatic disease ○ Had cardiac insufficiency ○ Had acute infection anywhere in the body ○ Had urinary incontinence ○ Had hydrophobia ○ Had psychological disease
Study procedure
Before randomization, both groups went through an assessment that included a personal details form (exp; age, body mass index [BMI]) and volume of two legs. All filled out a quality-of-life questionnaire (Short Form-36 [SF-36]), a social anxiety scale (Social Appearance Anxiety Scale [SAAS]), and a future hopelessness scale (Beck Hopelessness Scale [BHS]); all performed a submaximal exercise test (6-minute walk test [6MWT]) and received exercise and self-massage instruction booklets. Approximately 1 hour of training, including the maintenance phase of the CDP, was provided to all patients before treatment. After the randomization process, all group patients (ALT and control) started the intervention program for 6 weeks (12 sessions) and 2 days per week as five to eight patients in each group. The ALT patients came twice a week to the pool, and the control group came twice a week to the lymphedema unit. All patients were advised to carry on with their self-management treatment during the rest of the week. At the end of the 6 weeks (12 sessions) follow-up, all participants were reassessed (Fig. 1).

Flowchart.
Description of the ALT method
ALT is based on the anatomic principles of the lymphatic system. The viscosity of water provides resistance to body movement. ALT comprised gentle exercises, which are performed in a low-resistance manner. Hydrostatic pressure may be used to protect the leg from swelling and reduces edema. ALT is performed in a group setting in a 1.4-m deep pool with a temperature between 32°C and 33.5°C. 20 Each session lasts 45–60 minutes. First, healthy lymphotomes are activated proximally to clear the reservoir, by breathing exercises. Second, proximal movements of chest and trunk and manual techniques of self-massage are performed. Lastly, work is performed to clear the affected lymphotomes into the healthy ones and self-massage and distal movements are performed that involve the hips, knees, ankles, and toes. Then, remedial exercises are performed proximal to distal. The program was designed by two CDP specialists (one has an instructor certificate of CDP since 2004, and one has a practice certificate of CDP since 2008) and one aqua-therapy specialist (since 2005) according to the base on the Tidhar methods and CDP principles (first proximal work and then distal to proximal work).20–22
Control group
Self-lymphatic drainage and remedial exercises (proximal to distal) were performed in the control group in the lymphedema unit by a specialist CDP physiotherapist. Each session lasts 45–60 minutes.
Assessments
At the time of enrollment, a complete history was obtained from each patient. Safety was assessed by an absence of related infections. Patients were instructed to report any infection during the study period, and any increase of limb volume among the study group subjects was defined as an adverse event.
Circumference measurement
Edema of the leg was assessed by circumference measurements. A standard 2.54 cm (1″) retractable fiberglass tape measurement was used to perform the circumference measurements. Patients were first rested for ∼30 minutes, whereas their lower extremity was elevated 30°–45°. Then, patients were measured in this position. The circumference was measured every 5 cm, beginning at the lateral malleoli and continuing 55 cm proximally. All measurements were recorded in centimeters. Then, they were calculated with Frustum Formula as 12 different truncated cones (malleol–5 cm = V1, 5–10 cm = V2,…, 50–55 cm = V12) and, subsequently, were added together to calculate the individual's limb volume (V1 + V2 … +V12 = VT25,26). Volume differences less than 250 mL between the legs were defined as mild, differences of 250–500 mL were defined as moderate, and differences greater than 500 mL were defined as severe. 27
Volumetric measurement
Ankle and foot are not suitable to the conical formula. So, the lower leg was measured by water displacement. The foot was placed in a water-filled container, and the overflowing water was measured (volumetric measurement [VM]). Both lower legs were measured, and the difference was calculated. Subjects were instructed to place the foot slowly into the volumeter and to stop when the top of the volumeter came into contact with the footpad. All measurements were recorded in milliliters. 27
Short Form-36
The SF-36 was constructed to survey health status in the Medical Outcomes Study. The SF-36 was designed for use in clinical practice and research, and it assesses eight health domains: limitations in physical activities because of health problems; limitations in social activities because of physical or emotional problems; limitations in routine activities because of physical health problems; bodily pain; general MH (i.e., psychological distress and well-being); limitations in usual role activities because of emotional problems; vitality (i.e., energy and fatigue); and general health (GH) perceptions. Scores in the range 0–100 are calculated for each of these different aspects of health, with a low score indicating poor health status. 28
Social Appearance Anxiety Scale
This scale was developed by Hart et al. to measure the social appearance anxiety level of adolescence and it was adapted into Turkish.28,29 The scale consists of 16 items and with one factor and five Likert types (1 = totally disagree, 5 = totally agree). The examples of items are “I feel nervous when having my picture taken” and “I worry people will judge the way I look negatively.” The higher score of the scale demonstrated a high level of social appearance anxiety. The lowest score of the test is 16, and the highest score of the test is 80. And the first item was scored reversely.29,30
The Beck Hopelessness Scale
The BHS was assessed with the Turkish version of the BHS. This scale includes a 20-item questionnaire that assesses hopelessness by measuring participants' negative expectancies about future events. The response format for the BHS is true/false. The BHS scores can range from 0 to 20. Higher score indicates a high feeling of hopelessness. The scale developed by Beck et al. was adapted for Turkey by Durak. 31
Six-minute walk test
The 6MWT was performed according to the guidelines published by the American Thoracic Society. 32 The test conducted in a long corridor, researchers placed two cones 29 m apart from each other, the rationale being that the patients needed 1 m to turn around the cone, to ensure a 30-m-long course. Before each test trial, the physiotherapist gave standardized verbal instructions to the patients on how to perform the 6MWT and instructed the patients to walk as long a distance as possible in 6 minutes. Patients were informed to walk as fast as possible, but were not allowed to run or jog. Standardized encouragement and the time left of the 6MWT were called out to the patients at each minute mark. Finally, the total distance walked by the patients in 6 minutes was calculated and recorded. Patients were allowed to rest standing or leaning against the wall during the test trial, but the time would still be running.33,34
Statistical analysis
Data were analyzed in the SPSS 15.0 program. Mean and standard deviation were analyzed by using descriptive analyses with normally distributed variables, and median and the minimum–maximum values were analyzed for nonparametric values. The data, determined by the number, were presented as number and percentage.
Because the number of people was less than 30 in the control group, differences between the before and after treatment results within groups were analyzed by using the Wilcoxon Rank Sum test. For independent samples, the Mann-Whitney U test was used to determine the differences between groups. p < 0.05 was considered statistically significant. Spearmen correlation was used to determine the correlation of ordinal data.
Results
Demographic data for both groups are presented in Table 1. At the beginning of the study, 63 patients enrolled; however, two of the ALT and four of the control group patients withdrew from the study. This allowed data collection from 57 patients (Fig. 1).
ALT, aqua-lymphatic therapy; SD, standard deviation.
p < 0.05.
The mean age of the ALT group was 44.50 ± 13.69 years, and the mean BMI was 29.43 ± 7.90 kg/m2. The mean age of the control group was 47.66 ± 16.82 years, and the mean BMI was 29.64 ± 8.07 kg/m2.
There was no significant difference between the groups in terms of the severity of lymphedema (Table 1), and the characteristics of the patients in the two groups were similar except for infection history (Table 1). Infection history was a risk factor of lymphedema, and it was statistically higher in the ALT group (Table 1) (p < 0.05). These results strengthen our randomization process.
Despite having infection history before treatment, there was no infection history during the treatment sessions in both groups.
Compared with before and after the therapy values of limb volumes calculated by the Frustum Formula, in the ALT group, all volumes (V1–V12), VT, and VM showed a statistically significant decrease (p ≤ 0.001) (Table 2). In the control group, although there was a reduction in all volumes, only V1, V2, V3, V9, V10, VT, and VM were decreased statistically significantly (p < 0.05) (Table 2). Compared with the volume changes between the groups, a reduction of VT, V3, V4, V5, V6, V7, V11, and V12 volumes was statistically higher in the ALT group than the control group (p < 0.05).
p < 0.05, **p ≤ 0.001.
V1 = 0–5 cm; V2 = 5–10 cm; V3 = 10–15 cm; V4 = 15–20 cm; V5 = 15–20 cm; V6 = 20–25 cm; V7 = 25–30 cm; V8 = 30–35 cm; V9 = 35–40 cm; V10 = 40–45 cm; V11 = 45–50 cm; V12 = 50–55 cm; VT: V1 +…+ V12.
VM, volumetric measurement.
According to the first measurements of 6MWT of 57 patients, a moderate negative correlation was found between the severity of edema and 6-minute walk distance (6MWD) (r = −0.567, p < 0.01). The ALT group patients' 6MWD ranged from 160 to 600 m, and the median was calculated as 500 m. The control group patients' 6MWD ranged from 160 to 600 m, and the median was calculated as 490 m. The comparison of the before and after therapy results of 6MWT, 6MWD was improved statistically significantly in both groups (p < 0.001) (Table 3), and there was no statistically significant difference between the groups (p > 0.05).
p < 0.05, **p ≤ 0.001.
6MWD, 6-minute walk distance; 6MWT, 6-minute walk test; BHS, Beck Hopeless Scale; ER, emotional role; GS, general health; MH, mental health; PF, physical function; PR, physical role; SAAS, Social Appearance Anxiety Scale; SF, social function.
The SF-36 scores of the patients were statistically significantly increased in all subscales of the SF-36 (p ≤ 0.001, p < 0.05). In the control group, there was a positive increase in all subscales of SF-36, but only physical function and vitality subscales were found to improve statistically significantly (p < 0.05) (Table 3). Compared with before and after therapy results of the SF-36 between the groups, physical role, pain, GH, social function, emotional role, and MH subscales were improved statistically significantly in the ALT group rather than the control group (p < 0.05).
After the therapy sessions, there was a statistically significant decrease in scores of SAAS and BHS in both groups (p ≤ 0.001, p < 0.05) (Table 3). Although there was a higher improvement in the ALT group, however, there was no statistically significant difference between the groups (p > 0.05).
Discussion
In this study, we investigated the effects of the ALT in the maintenance phase on edema severity, exercise capacity, quality of life, fear of the future, and social anxiety on unilateral lower extremity lymphedema patients. As a result of these findings, both in the ALT group and in the control group, unilateral lower extremity volume decreased, the functional exercise capacity increased, quality of life increased, and social appearance anxiety and future anxiety decreased. Results were found to be better in the ALT group than in the control group. It has been found that the ALT is an effective and reliable method for the maintenance phase of the CDP.
The most important problem for lymphedema patients is infection. Erysipelas infection is a well-recognized complication of lymphedema. It is mainly caused by β-hemolytic streptococci and rarely caused by Staphylococcus aurous. 35 The bacterium that causes erysipelas is not described in the literature as being present in pool water, but it colonizes on the skin. 36 Patients were instructed not to come to the ALT sessions if they had a skin wound, infection, cuts, or bruises. Unfortunately, public warm water therapy pools are implicated as environments with a high exposure to common waterborne and airborne pathogens such as Legionella and Mycobacterium spp. Therefore, pool cleanliness is essential to avoid ear, sinuses, and respiratory infections. Katz et al. assessed the feasibility of recruiting patients with lower limb lymphedema into an exercise intervention. In this uncontrolled pilot study, cellulitic infections developed in two patients during the intervention. They were told that infection might be a result of hygiene or hydrosis. 37 In another research study that was published in 2010, 20 women with upper extremity lymphedema participated in 12 weekly sessions of the ALT and reported that no infection problems occurred during the treatment. Similarly, in our study, none of the ALT group patients reported any infection of the leg during the study period. Also, none of the control group patients declared any infections during the study period.
The hydrostatic pressure may be the most important advantage of the water in terms of lymphedema. Hydrostatic pressure generates a similar pressure mechanism applied by the compression garment (high to low pressure). It also creates an equal pressure to the body parts in each level. Water also provides equal and effective pressure to body segments such as chest, genitals, hands, and toes that cannot be ensured by stockings.38,39 Johansson et al. studied upper extremity lymphedema and followed patients in two groups (15 aqua–15 control) for 8 weeks. Patients did not utilize self-drainage applications, and the aqua group mostly used swimming exercises. As a result, there was no change in edema in the aqua group despite doing exercises. 40 It is apparent that there is no hydrostatic pressure while swimming. The aim of the lymphedema treatment is to be redirected to healthy lymph nodes, lymphatic fluid, but hydrostatic pressure alone cannot lead to healthy lymph nodes.1,14 In their study, Tidhar et al. provided aquatic self-drainage to upper lymphedema patients and reported a significant reduction in the limb volume. 20 In this study, both groups (ALT and control groups) of patients performed self-draining applications. There was a significant reduction in limb volume in both groups; in addition, the decrease was higher in the ALT group. Our results supported the fact that self-drainage implemented with hydrostatic pressure may be more effective, which is in parallel with Tidhar et al. 20
Water temperature is another factor that can affect the results of the ALT in patients with lymphedema. Water temperature from 31°C to 33.5°C is the most appropriate.24,41 In the study by Tidhar, exercises were also performed in warm water (32°C–33°C) and there were improvements in the limb volume. 20 In our study, the pool water temperature used was from 32°C to 33.5°C and patients were given a mild exercise program. At the end of the study, there was a significant reduction in the limb volume in the ALT group. The reason of the differences between the studies might be due to the differences in the exercise protocols and the slow pace of the ALT exercises that need a thermoneutral temperature. Patients cannot relax and perform the exercises correctly when they are feeling too cold. 20 With our findings, it seems that performing an exercise that targets a reduction in limb volume and that is done in a warm temperature environment has a positive influence on limb volume, as reported by Tidhar et al. 20
In this study, patients with mild, moderate, and severe lymphedema who completed the 12 sessions of the therapy program were evaluated. There was a 391.14 mL (minimum −199.18–maximum 1351.18) decrease in the ALT group, and a 97.58 mL (minimum −1924–maximum 1205) decrease in the control group. Our study shows a significant reduction in the total volume of the limb in the ALT and the control group patients. However, we noticed some increase only in a few patients. We believe that variable characteristics of lymphedema play a role in this condition. Many different reasons, in particular the effect of gravity as well as activities of daily living, emotional moods, and unhealthy nutrition habits (salty foods, alcohol use, etc.), can increase the swelling in lower extremity lymphedema patients.42,43 When investigating the literature about lower extremity lymphedema, limb volume of patients is not common practice in the maintenance phase of CDP. In this respect, our findings provide an important contribution to the literature.
Lower extremity lymphedema patients are known to have difficulty in walking and daily activities due to an increase in volume and a feeling of heaviness in the affected limbs.14,21 In this study, according to findings, there was a moderate relationship between the severity of edema and 6MWD (r = −0.567). It means that while edema severity increases, the 6MWD of patients decreases. These findings of our study are important because there has been no study that has investigated the relationship between 6MWD and the severity of edema in the literature. After 12 sessions, both the ALT and the control groups had a significant increase in 6MWD and these findings supported the importance of the maintenance phase of CDP.
All participants in this study reported an improvement in their quality of life according to the quality-of-life questionnaire (SF-36). These findings are similar to the findings of Tidhar et al., which described an improvement in quality of life after the ALT. 20 On the other hand, Tidhar et al. reported some patients in the control group whose quality of life worsened. 20 Unlike Tidhar et al., quality of life of the control group of this study did not change negatively and there was no difference in the improvements of the groups. It is possible that being “in treatment” alone improves emotional and social well-being.
Social appearance defined as anxiety and worrying that other people are assessing their physical appearance. The deterioration of the physical image appeared with the rise in volume, and it returned once the negative body image in lymphedema patients was indicated in the studies. 44 Therefore, in our study, the social aspect of anxieties has been evaluated. As a result, there was a significant reduction in the perception of social anxiety in both groups, but it has been shown to be superior in the ALT group. In the recent literature, there was a gap about directly assessing the impact of the social aspect and the treatment of an anxiety. Thus, we believe that our work done on this subject could serve as a precursor to other work.
When we take into consideration our clinical observations, particularly in the lower extremity lymphedema patients, concerns regarding the future seem to be even higher. Therefore, BHS is used to evaluate future concerns. In both groups, there was a significant decrease in the future anxiety as there were no significant differences between the groups. There were no studies found in the literature that investigated the effect of direct concern on the future in patients with upper and lower limb lymphedema who had undergone CDP.
Limitations
The menstrual cycle of the patients involved in the ALT is one of the limitations faced by the study. Some of the patients did not wish to enter the pool during this period; however, they completed 12 sessions of therapy in 7 weeks as a result. According to our excluding criteria, the number of patients that could be reached was a small number of lower extremity lymphedema patients. And we could not be selective in the parameters that can influence the reduction or increase of edema. Another limitation of this study was the transportation problems faced by the patients. Due to transportation problems, few patients had to withdraw from the therapy sessions.
Consequently, a new approach, ALT is a feasible and reliable treatment program in patients with lower limb lymphedema. We believe that it is useful both physically and psycho-socially for the patients to be included in the group treatment program with physiotherapists periodically.
Footnotes
Author Disclosure Statement
No competing financial interests exist.
