Abstract
Background:
Impaired mobility and musculoskeletal dysfunctions are commonly seen in patients with lymphedema and can affect the balance system in patients in whom the lower limb is affected. This study aims at comparing postural stability between patients with lower limb lymphedema (LLL) and healthy subjects.
Methods and Results:
This controlled study included 36 patients with LLL (LLL group) and 36 healthy subjects (control group). Fall risk, stability index, and Fourier index measurements of Tetrax® Interactive Balance System were compared. There were no statistically significant differences between groups in terms of demographics parameters (p > 0.05). Some stability and Fourier index measurements were significantly higher in subjects in the LLL group than in the control group. However, the fall risk was not statistically different in patients with LLL than healthy subjects (p > 0.05).
Conclusion:
LLL may cause balance impairments. However, this impairment may not lead to increased fall risk. The evaluation of postural stability in LLL patients would be a useful addition to routine clinical practice due to the relationship between LLL and balance impairments.
Introduction
Balance is the ability of the body to know its location in an environment and to maintain a desired position. It is key in the performance of daily activities and locomotor system function. 1 For these reasons, the International Classification of Functioning, Disability and Health has classified balance as an activity. 2 The central nervous system, somatosensorial system, proprioceptive system, vestibular system, visual system, musculoskeletal system, and cognitive functions are related to postural stability. The decreased ability to maintain postural stability manifests as high postural sway, impaired balance and falling, a greater risk of fracture and/or musculoskeletal injury and resultant physical, mental, and social problems, and high costs. For these reasons, daily clinical practice should place emphasis on postural pathologies and their diagnosis and rehabilitation and on fall prevention.3–6
Lymphedema is a chronic and progressive disease characterized by the accumulation of macromolecules and liquids in the interstitial space, and it is the result of impairment of the lymphatic system. It is clinically characterized by chronic gross swelling, pain, skin changes, and susceptibility to infections of the affected limb.7–9 Lymphedema may cause decreased joint activity and muscle strength, musculoskeletal pathologies, physical dysfunction, gait abnormalities, and limited mobility.10–12 Such problems can precipitate postural instability in patients with lower limb lymphedema (LLL).
This study aims at comparing balance and fall risk between LLL patients and healthy subjects. To the best of our knowledge, this is the first study investigating whether there are balance changes in patients with LLL.
Materials and Methods
This controlled study was approved by the local ethics committee, and written informed consent was obtained from all participants. Power analysis during the biostatistical preliminary assessment indicated a study population of 72 patients (36 patients for each group) with a 95% confidence level and 80% power. 6
Participants were divided into two groups: the LLL group and the control group. Patients who had been diagnosed with LLL were screened for eligibility from our outpatient clinics. After this stage, 36 patients (35 women and 1 man) were included in the LLL group. The control group included 36 healthy subjects (35 women and 1 man) randomly selected from individuals in the hospital employee population.
Participants with neurologic or musculoskeletal disorders, vestibular/visual/hearing pathologies, or severe bone or rheumatologic disease that might the effect of balance system were excluded from the study.
Age, gender, body mass index (BMI) (body weight [kg]/height 2 [m2]), and static posturography measurements of all participants were recorded. For the LLL group, etiology of lymphedema, stage of lymphedema, duration of LLL, and the diametric measurement differences among lower limbs were recorded. All measurements were assessed by the same assistant health staff using the same method.
Static posturography
Static posturography was measured by using the Tetrax® Interactive Balance System (Sunlight Medical Ltd., Ramat Gan, Israel). Static postural balance was evaluated by recording vertical pressure fluctuations. The subject was asked to position their bare feet in a comfortable position on four power plates with their arms hanging freely next to their body. If necessary, stability was provided by hand pieces positioned on either side of the device. The Tetrax Interactive Balance System was used to evaluate the fall risk, stability index (SI), and Fourier index measurements.
Fall risk was given as a numerical hypothetical risk value of 0–100, with 0–35 indicating low fall risk, 36–57 moderate fall risk, and 58–100 high fall risk. The SI indicates the degree of postural sway and tests an individual's overall stability and capability of controlling and compensating for changes in posture. Higher fall risk and SI scores reflect diminished postural performance.
The Fourier index is a regression analysis used to measure postural sway intensity through the Fourier transform, which shows a different frequency for each lesion that causes instability. Normal comfortable posture is represented by fluctuations of 0.01–0.1 Hz (F1), abnormalities in the vestibular organ or musculoskeletal system fatigue by fluctuations of 0.1–0.5 Hz (F2–F4), somatic sensory impairment from declined spinal and lower extremity motor function by fluctuations of 0.5–1 Hz (F5–F6), and postural instability from abnormalities in the central nervous system by fluctuations of more than 1 Hz (F7–F8).
Static posturography can be measured and evaluated in eight different postures: NO = head straight, eyes open, on hard ground; NC = head straight, eyes closed, on hard ground; PO = head straight, eyes open, on soft ground; PC = head straight, eyes closed, on soft ground; HR = head turned to right, eyes closed, on hard ground; HL = head turned to left, eyes closed, on hard ground; HB = cervical extension, eyes closed, on hard ground; HF = cervical flexion, eyes closed, on hard ground.3,5 Static posturography measurement recordings took ∼5 minutes to complete. Each of the eight positions was held for 32 seconds, and the recovery time between measures was 2–4 seconds.
Lymphedema measurements
Lower limb size difference measurements were taken by using a flexible nonstretch tape at the following levels: the metatarsophalangeal joint, ankle, 10 cm distal to the distal margin of the patella, 10 cm proximal to the proximal margin of the patella, and 20 cm proximal to the proximal margin of the patella.
LLL patients were evaluated with respect to lymphedema stage defined as follows: Stage I presents with reversible pitting edema that subsides with limb elevation; in Stage II, the edema progresses and becomes more intense, may not pit, is irreversible, and is rarely reduced by limb elevation alone; and in Stage III, tissue is hard and pitting is absent, with skin changes such as thickening, hyperpigmentation, fibrosis, increased skin folds, fat deposits, and warty overgrowths.13–15
Statistical analysis
Statistical analysis was performed by using the statistical package SPSS (Version 17.0, SPSS, Inc., Chicago, IL). Normal continuous variables were described as the mean ± standard deviation (p > 0.05 in Kolmogorov–Smirnov test or Shapiro–Wilk [n < 30]), and non-normal continuous variables were described as the median. Comparisons between groups were applied by using the Student's t-test for normally distributed data and the Mann–Whitney U test for data that were not normally distributed. Categorical variables between the groups were analyzed by using the chi-square test. p-Values of 0.05 and lower were considered significant.
Results
The mean age of patients was 52.53 ± 9.71 years in the LLL group and 52.95 ± 10.41 years in the control group. Age and gender were similar between groups (p > 0.05). BMI was higher in the LLL group (p = 0.046). Characteristics of the study populations are summarized in Table 1.
Clinical Characteristics of the Study Population
Mean ± standard deviation.
Bold values indicate statistical significance.
Descriptive variables of LLL patients are shown in Table 2.
Descriptive Data of Lower Limb Lymphedema Patients (n = 36)
Median (minimum–maximum).
Lower limb size difference measurements, centimeter.
Comparisons of posturography results between groups
Mean fall risk values were in the moderate range in the LLL group (46.93 ± 32.43) and in the low range in the control group (29.45 ± 22.79). However, fall risk was not statistically different between groups (p = 0.161).
The SI at the NC and HF postures was different between groups (p < 0.05), whereas other SI parameters were similar (p > 0.05). SI measurements are given in Table 3.
Stability Index Results (Mean ± Standard Deviation)
Bold values indicate statistical significance.
The Fourier index measurements of F1 and F3 in HL posture, F2 and F4 in NC posture, F1–F2–F4 in HB posture, and F5–F6 in HF posture were different among groups (p < 0.05). Other Fourier index parameters were not statistically different (p > 0.05).
Discussion
To the best of our knowledge, this is the first study in the literature focusing on balance in patients with LLL. We found that some balance parameters are negatively affected in patients with LLL when compared with healthy subjects. Although the mean fall risk value was within the moderate fall risk range in the LLL group and the low risk range in the control group, when the fall risk was compared between groups, the findings were not statistically different according to static posturography results. Our findings demonstrate that patients with LLL have balance system pathologies but these pathologies are not observed in all balance parameters. This balance impairment does not appear to lead to increased fall risk.
All NO posture scores were similar among groups, suggesting that patients with LLL have normal and comfortable posture. However, when LLL patients were evaluated in the eyes closed positions on hard ground, some SI scores increased. This increasing of postural sway may lead to poor postural performance.
Some F1–F4 Fourier index measurements were significantly higher in subjects in the LLL group than in the control group. These results suggest that the musculoskeletal system can by partially affected by lymphedema. The F5–F6 Fourier index measurements in the HF posture were higher in patients with LLL than in the control group. This result may be due to sensorial impairment from lower extremity dysfunctions in patients with LLL.
Pain, musculoskeletal pathologies and related comorbidities such as weakness and edema of the muscles, limited joint activity and mobility, structural and functional abnormalities of the lower extremity, physical dysfunction, and gait abnormalities may be caused by lymphedema.9–12 We believe that these problems can impair the balance system in patients with LLL as physical dysfunctions, musculoskeletal abnormalities, and comorbidities are related with postural stability.
Angin et al. 6 evaluated postural stability in patients with unilateral upper limb lymphedema and found that postural sway increased in their patients. They reported that abnormal sensations, limitations in fine balancing movements of the upper extremity, and asymmetrical volume increases in the extremity caused by lymphedema may lead to inability of maintaining postural stability. These hypotheses and highlights may be valid for LLL patients and affect their balance system.
Higher body weight may negatively affect static postural control. 16 In this study, BMI was higher in patients with LLL, whereas fall risk was similar between the groups. Hence, we believe that obesity is not a main factor behind the fall risk.
Limitations of the sample in this study are its small size, concentration of low grade lymphedema in the sample group, and the fact that all but two participants were female. Further studies with larger, gender-equal sample sizes, including patients with high grade LLL, may lead to more specific and significant results. In addition, future studies in this area can be performed by using more objective lymphedema assessment methods such as perometry. Similarly, this study analyzed static balance and further studies evaluating dynamic balance and daily activities may contribute to our understanding of balance in patients with LLL. Finally, the number of participants' previous falls was not recorded.
Conclusion
Balance pathologies may be identified in patients with LLL, although this postural instability may not lead to increased fall risk. The evaluation of postural stability would be a useful inclusion as part of routine clinical practice in LLL patients. Further studies including dynamic and static balance evaluations with a mix of lymphedema grades and studies using more objective methods of lymphedema may provide more objective results.
Footnotes
Acknowledgments
The authors would like to thank Cagla Sariturk for the statistical evaluation and Kevser Aydar for the evaluation of the balance measurements.
Informed consent: Human patients and healthy controls were tested, and the study was carried out with the informed consent from all participants.
Animal and human rights: The study did not involve any animal experiments or animal samples.
Ethical approval: All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study was not funded by any company.
Author Disclosure Statement
No competing financial interests exist.