Abstract
Objectives
To compare gait parameters, functionality (muscle strength, balance, exercise capacity) and health status (kinesiophobia, fatigue, quality of life) in lower extremity lymphedema patients and healthy controls and to determine correlations between exercise capacity, gait parameters, muscle strength, balance, quality of life and lymphedema severity.
Methods
Twenty-two lymphedema patients and 20 healthy controls participated in the study. Participants’ demographic and medical characteristics were recorded. Muscle strength, endurance, balance, functional exercise capacity, gait parameters, kinesiophobia, fatigue and quality of life were assessed with dynamometer, 30-s chair stand test, Biodex, 6-min walk test (6MWT), 8-m test (8-MWT), Tampa Scale, Fatigue Severity Scale and Short Form-36, respectively.
Results
Lymphedema patients had lower muscle strength and endurance, 6MWT distance, speed, cadence and stride length, 8-mWT speed, cadence and left stance phase, and higher swing phase-left and single support phase-right compared to healthy controls (p < .05). Balance parameters were worse in lymphedema patients compared to healthy controls (p < .05). Quality of life was lower and kinesiophobia and fatigue levels were higher in lymphedema patients compared to healthy controls (p < .05). Significant correlations were found between 6MWT distance, speed and stride length, 8-mWT speed and stride lengths and lymphedema severity, muscle strength, balance, and quality of life (p < .05). Multiple regression analyses identified balance and lymphedema severity as predictors for 6MWT distance, speed, and stride length.
Conclusions
Lymphedema patients have reduced muscle strength, exercise capacity, quality of life, and increased kinesiophobia and fatigue. Lymphedema negatively impacts gait and balance. Gait parameters are correlated with muscle strength, balance, quality of life and lymphedema severity in lymphedema patients.
Introduction
Lower extremity lymphedema (LEL) is chronic, progressive swelling of the legs caused by impaired lymphatic circulation due to primary (e.g., genetic defects) or secondary (e.g., surgery, cancer treatments) factors. 1 Despite uncertainties regarding the incidence of primary LEL, secondary LEL occurs in 29%–70% of cancer patients.2–4 Clinical symptoms are swelling, sense of limb heaviness, cosmetic impairment, physical discomfort, pain, recurrent infections, fatigue and functional impairment. 1 The presence of these symptoms was associated with worsening quality of life. 5 Altered weight distribution in LEL may cause the center of gravity (CoG) to shift to the lymphedema side, and affect balance. 6 These changes may lead to fear of falling and kinesiophobia, reducing mobility, 7 and contributing to peripheral muscle weakness and gait impairment. 8
Gait depends on the coordinated function of the neurological, musculoskeletal, and other body systems, and its quality can be assessed through specific gait parameters. Spatiotemporal parameters, the main components of the gait cycle, are widely used to evaluate gait disorders/asymmetries. 9 Conditions causing asymmetric weight distribution, such as unilateral amputation or volume changes, can impair balance and lead to spatiotemporal asymmetry.9–12 However, it remains unclear whether such asymmetry occurs in LEL patients. Objective gait analysis enables goal-oriented treatment and helps assess mobility, exercise capacity, fall risk, disease severity, and treatment efficacy.9,13,14 Research on gait in lymphedema is limited and mostly focuses on treatment effects.8,15 Forner-Cordero et al., 16 reported slower walking speeds in LEL patients compared to healthy population data, but whether spatiotemporal gait parameters differ from controls is still unknown.
Although few studies report that edema-related increases in volume and weight impair walking and functional performance, 17 there is a lack of evidence on the extent to which muscle strength and endurance, functional exercise capacity and gait parameters are affected in LEL patients compared to healthy controls. Therefore, the primary aim was to determine gait parameters, functionality (muscle strength, endurance, balance, functional exercise capacity) and health status (kinesiophobia, fatigue, quality of life) in LEL patients and compare them with healthy controls. The secondary aim was to determine the relationship between lymphedema severity, muscle strength, balance, quality of life, and functional exercise capacity and gait parameters in LEL patients.
Methods
This study was conducted between March 2023-March 2024 at Dokuz Eylül University, Physical Therapy and Rehabilitation Faculty with regularly followed-up LEL patients and healthy controls (CG). Ethical approval was obtained from the Dokuz Eylül University Non-invasive Ethics Committee (decision no.:2023/08–06). All participants gave written informed consent.
LEL group inclusion criteria were age≥18, unilateral LEL, Turkish literacy, and voluntary participation. The CG included relatives of participants or the researcher, aged≥18 and willing to participate. Exclusion criteria were as follows: Additional disorders that prevent walking, orthopedic and neurological diseases, mental and cognitive disorders and lymphangitis. The G*Power 3.1.9.7 (Franz Foul, Kiel University, Germany) program was used to determine the sample size. The smallest sample size for 95% power at the 95% confidence interval was 26 participants (13 per group). 18
Participants’ demographic characteristics were recorded. Medical characteristics of LEL patients, including diagnosis, side, severity and duration of lymphedema and infection history were recorded. All assessments were conducted by a single physiotherapist.
Circumference measurement was performed to assess lymphedema severity in LEL group, following 30 minutes of rest with the lower limbs elevated to 30–45°. Circumference measurements were made at 5 cm intervals, starting from the lateral malleolus and continuing for 60 cm proximally, with the patients supine and legs in an elevated position. Limb volumes were calculated using the Frustum formula, and lymphedema severity was classified by volume difference between limbs (5%–20%, mild; 20%–40%, moderate; >40%, severe) per International Society of Lymphology guidelines. 19
Quadriceps femoris (QF) strength was evaluated bilaterally using a digital dynamometer (JTECH Power Track Commander II, USA). 20 The test was performed in a seated position with the assessor assisting in stabilizing the knee. The test was repeated three times, and the highest value was recorded.
30-s chair stand test (30-sCST) was used to evaluate lower extremity endurance. Participants were asked to perform as many sit-to-stand movements as possible within 30 seconds while seated on an armless chair (height = 43 cm) with their hands crossed over their chest. The number of sit-to-stand repetitions completed within 30 seconds was recorded. 21 The 30-sCST has a moderate-high test-retest reliability (ICC = 0.89) and moderate construct validity (r = 0.77). 22
Biodex Balance System (Biodex Inc., New York) was used to assess balance.23,24 Postural stability (PS), limits of stability (LoS), fall risk, static balance (SB) with eyes-open/closed on firm and foam were evaluated. For PS, fall risk, and LoS, three 20-s trials were performed, with average scores calculated automatically. SB was assessed with four 30-s trials on firm and foam surfaces with eyes-open/closed. During PS and SB (eyes-open), participants aimed to keep a screen-displayed ball centered and steady. In LoS testing, participants followed directional targets via controlled sways. Fall risk involved measuring postural sway on a movable platform. For SB with eyes closed, balance shifts were recorded without visual input. 25 Lower PS, fall risk and SB scores indicate better stability and balance. Higher LoS scores indicate better stability limits.
The 6-min walking test (6MWT) was used to evaluate functional exercise capacity. The 6MWT was carried out according to the ATS criteria. 26 Participants were asked to walk as fast as possible for 6 minutes on a 30-m straight corridor. During the 6MWT, standard encouragement phrases and the remaining time were told to the participants every minute. 26 6MWT-distance, mean gait speed, cadence, and stride length were measured using an accelerometer (G-Walk, BTS, Italy) worn on the subject’s waist. 27
Gait parameters including speed, cadence, stride length, stance, swing, single support and double support phases were measured with the accelerometer (G-Walk, BTS, Italy) used during 8-m walking test (8-mWT). 27 Participants were asked to walk at normal gait speeds during the 8-mWT. The gait parameters measured with G-Walk had high or excellent test-retest reliability (ICC: 0.84–0.98) and were correlated with muscle strength and range of motion parameters. 27
Symmetry Index (SI) is a method for percentage evaluation of the differences between the right and left lower extremity spatio-temporal parameters during walking. 28 The calculation of SI is a method used for gait asymmetries in healthy individuals, in patients with unilateral impairments such as cerebral palsy, hemiplegia, and unilateral total hip arthroplasty.29–31 SI was calculated for the stance and swing phases, as well as for the single and double support phases of gait parameters. An SI result of 0 indicates symmetry, while an SI ≥100% indicates asymmetry. 28
The Tampa Kinesiophobia Scale (TKS) was used to evaluate the individuals’ fear of movement. TKS consists of 17 questions and a 4-point Likert-type scoring (1 = I strongly disagree, 4 = I completely agree) is used. The total score is between 17 and 68. A high score indicates a high kinesiophobia. In our study, the cut-off value for high kinesiophobia was accepted as 37. 32
The Fatigue Severity Scale contains 9 items and evaluates fatigue. Each question is scored between 0 and 7. The total score is divided by 9 and more than 4 points is considered as the presence of fatigue. 33
Quality of life was assessed using the Short Form-36 (SF-36). 34 The SF-36 assesses eight health domains; physical function and role, bodily pain, general health, vitality, social function, emotional role, and mental health. Scores in the range of 0–100 are calculated for each of the eight health areas, and a low score indicates poor health. 35
Statistical analysis
The statistical analysis was carried out using SPSS-v.27 (IBM, Armonk, NY). Participants’ clinical and sociodemographic characteristics were analyzed using descriptive statistics. Shapiro-Wilk test was used to determine the normal distribution. Student’s t test was used to examine the differences between groups. The variables determined by counting were compared by the Chi-Square test. Pearson correlation coefficient (r) was used for the correlation between muscle strength, balance, kinesiophobia, fatigue, quality of life and gait parameters and functional exercise capacity, and was classified as weak (<0.40), moderate (0.40–0.60) and strong correlation (>0.60). Multiple linear regression (stepwise regression) models were constructed to determine the variables that independently explained the variance in the best 6MWT-distance, speed, and stride length. Model fit was assessed using appropriate residual and goodness-of-fit statistics. The statistical significance was set at p < .05.
Results
Demographic and medical characteristics of the participants.
LEL, Lower extremity lymphedema group; CG, Control group; SD: standard deviation, n: number, BMI: Body Mass Index, cm: centimeter, kg: kilogram, m: meter;
aIndependent samples t test;
bFisher Chi-Square test; NA: not applicable.
Comparison of participants’ muscle strength and endurance, functional exercise capacity, gait parameters, balance, kinesiophobia, fatigue and quality of life.
Bold values indicate statistically significant differences (p < 0.05). LEL, Lower extremity lymphedema group; CG, Control group; SD: standard deviation, QF, Quadriceps femoris; kg: kilogram, L, left; R, right; 30-sCST, 30-s chair stand test; n: number, 6MWT, 6-min walking test; m: meter; s, second; min, minute; 8-mWT, 8-m walking test; SI, Symmetry Index; PS, Postural stability; AP, Anterior Posterior; ML, Medial Lateral; LoS, limits of stability; SB, static balance; EO, Eyes Open; EC, Eyes Closed; TKS, Tampa Kinesiophobia Scale; FSS, Fatigue Severity Scale; SF-36, Short Form-36; PF, physical function; PR, physical role; BP, bodily pain; GH, general health; V, vitality; SF, social function; ER, emotional role; MH, mental health;
Independent samples t test;
*p < .05.
Correlations between muscle strength, balance, kinesiophobia, fatigue, quality of life and gait parameters and functional exercise capacity in the LEL group.
Bold font indicates significant moderate to high correlation (<0.40, weak correlation; 0.40-0.60, moderate correlation; >0.60, high correlation). 6MWT, 6-min walking test; 8-mWT, 8-m walking test; L, left; R, right; QF, Quadriceps femoris; 30-sCST, 30-s chair stand test; PS, Postural stability; AP, Anterior Posterior; ML, Medial Lateral; LoS, limits of stability; SB, static balance; EO, Eyes Open; EC, Eyes Closed; TKS, Tampa Kinesiophobia Scale; FSS, Fatigue Severity Scale; SF-36, Short Form-36; PF, physical function; PR, physical role; BP, bodily pain; GH, general health; V, vitality; SF, social function; ER, emotional role; MH, mental health.
Multiple Linear Regression Analyses of 6MWT parameters.
6MWT, 6-min walking test; PS, Postural stability; ML, Medial Lateral; LoS, limits of stability.
Discussion
This study, to the best of our knowledge, is the first to compare muscle strength, functional exercise capacity and gait parameters in LEL patients and controls, and to examine the relationship between gait parameters, functional exercise capacity, and lymphedema severity, muscle strength, balance, and quality of life. Compared to controls, LEL patients showed reduced muscle strength and endurance, impaired functional capacity, poorer gait and balance, lower quality of life, and increased kinesiophobia and fatigue. Functional exercise capacity and gait parameters are correlated with lymphedema severity, muscle strength, balance and quality of life in LEL patients. Multiple linear regression identified balance and lymphedema severity as predictors of 6MWT-distance, speed, and stride length in LEL patients.
LEL patients are often inactive due to discomfort from edema, kinesiophobia, and fear of worsening the condition with movement. This inactivity causes weakness in muscles such as the gluteus and QF and thus negatively affects walking. 8 Lee et al., 36 found that 36.3% of upper extremity lymphedema patients developed muscle weakness in the affected arm, associated with fear of use. In the current study, LEL patients had lower QF muscle strength compared to CG.
Reduction in physical function and mobility, difficulty in performing activities of daily living, and avoidance of activities such as exercise and walking may decrease functional exercise capacity in LEL patients.17,18,37,38 Several previous studies have reported that lymphedema severity in LEL patients is correlated with 6MWT-distance and also serves as a predictor of 6MWT performance.39,40 The lower functional exercise capacity in LEL patients may be explained by the predominance of severe lymphedema and lower muscle strength.
LEL reduces lower extremity muscle strength and functional performance, limiting range of motion and altering gait parameters, which leads to walking difficulty.16,41 As increased cadence exerts greater load on the lower extremities, cadence decreases in conditions affecting lower extremity kinematics. 42 In the current study, LEL patients had significantly lower cadence than controls. Altered muscle function in chronic diseases affects joint kinetics, contributing to reduced stride length and width. 43 While 6MWT-stride length was significantly lower in LEL patients, 8-mWT stride length showed no difference between groups. In LEL patients, faster walking resulted in a shorter step length, possibly due to altered gait kinematics compared to healthy individuals. 44 Forner-Cordero et al., 16 noted that LEL patients walked at a slower speed compared to data from the healthy population. In the present study, gait speed was also lower in LEL, potentially reflecting a compensatory strategy to reduce joint and muscle loading caused by edema. A short stance and prolonged swing phase in one limb indicates an increased stance and single support phase in the opposite limb. 45 In the current study, 54.55% of LEL patients had left-sided lymphedema. In unilateral LEL, the stance phase may be reduced to minimize load on the affected limb. Compared to CG, LEL patients showed significantly lower stance phase-left and higher swing phase-left and single support phase-right. As prolonged single support is linked to increased postural sway, 46 this may be associated with significantly higher postural sway in LEL patients than in CG.
Altered weight distribution and asymmetric load bearing due to LEL may shift CoG toward the lymphedema-affected side, leading to increased postural sway and changes in spatiotemporal parameters.6,9,10,47 Asymmetry in spatiotemporal parameters has been reported in individuals with unilateral upper extremity amputation and lymphedema.9,12 Consistent with these findings, in the present study, LEL group showed significantly higher symmetry indices of stance, swing, single support, and double support phases compared to CG. Basar et al., 23 reported that unilateral upper extremity lymphedema causes low overall, AP and ML postural stability, but does not increase the fall risk. In the current study, overall and ML postural stability of LEL patients were significantly higher than CG, and the two groups were similar in terms of fall risk. Unlike studies reporting that the eyes-closed firm surface and eyes-open and closed foam surface balance were affected in LEL patients compared to CG,7,48 in the present study, only the eyes-closed foam surface balance was impaired in LEL patients. In eyes-closed static balance on foam surface, visual information and somatosensory system are disabled and the vestibular system comes to the fore. 48 In the current study, the impairment of eyes-closed foam surface balance in LEL patients may be due to the low vestibular dominance of patients with LEL. 48
Most LEL patients reported that they avoided physical activities such as exercise and housework, and that activities such as standing, walking, and exercise worsened LEL. 37 Similar to this study, LEL patients were reported to have higher kinesiophobia than than CG.17,18,49 Low muscle strength and functional exercise capacity negatively affect fatigue levels. Similar to previous studies,49,50 in the present study, LEL patients had high levels of fatigue. Clinical symptoms such as swelling and heaviness in the extremity, recurrent infections, physical discomfort, cosmetic and functional deterioration affect many domains of quality of life in patients with LEL.5,38,49 In the current study, LEL patients had lower quality of life parameters than CG. Considering that increasing the severity of LEL worsens the quality of life, 51 the low quality of life parameters of the LEL patients may be due to the fact that the majority of them have severe lymphedema (63.6%).
Examining the relationship between gait parameters and lymphedema severity, muscle strength, balance, and quality of life may enhance understanding of the importance of gait quality in rehabilitation. In the present study, 6MWT-distance, speed, and stride length, 8-mWT speed and stride lengths, were significantly correlated with lymphedema severity, muscle strength, balance, and quality of life in LEL patients. 6MWT is considered an indicator of postural balance and reflects mobility, including sensorimotor, balance and muscle strength. 52 Since walking and balance involve similar system functioning such as postural stability, musculoskeletal and the sensorimotor system, the relationships between the two parameters are not surprising. 53 Greater lymphedema severity was associated with impaired gait and reduced functional capacity.39,40 Angst et al., 54 reported that 6MWT was associated with quality of life in lipedema patients, unlike LEL patients. Pedrosa et al. found that mobility and quality of life were correlated in LEL patients. 55 In the current study, SF-36 physical function, role and general health were associated with gait parameters in LEL patients. Çakır et al. identified lymphedema severity, muscle strength, and lower extremity functionality as predictors of 6MWT-distance in LEL patients. 39 Gait speed is key determinant of balance, fall risk, and functional performance.14,56,57 Balance control, particularly medial-lateral postural stability, is closely associated with changes in step width and step length. 58 In the present study, postural stability-ML, lymphedema severity, and LoS-Backward predicted 6MWT-distance; lymphedema severity, LoS-Backward, and LoS-Forward predicted 6MWT-speed; and postural stability-ML, lymphedema severity, LoS-Backward, and LoS-Forward predicted 6MWT-stride length in LEL patients.
This study has several limitations. Kinematic evaluation of the lower extremity in LEL patients could be useful in explaining the changes in gait. Additionally, participants could be recruited and evaluated homogeneously based on their physical activity levels.
In conclusion, muscle strength, functional exercise capacity, gait parameters, balance, kinesiophobia, fatigue and quality of life are impaired in LEL patients. Functional exercise capacity and gait parameters correlate with lymphedema severity, muscle strength, balance and quality of life in LEL patients. Balance and lymphedema severity are predictors of 6MWT-distance, speed and stride length in LEL patients. As gait parameters significantly impact daily life, incorporating gait and balance training into complex decongestive therapy, aerobic and strengthening exercises, may enhance functional exercise capacity and health parameters in LEL patients. Further research is needed on the effects of LEL on gait parameters.
Footnotes
Acknowledgements
The authors would like to thank the participants in this study.
Author contributions
EE: Conceptualization, Methodology, Formal analysis, Investigation, Writing- Original draft. DK: Conceptualization, Methodology, Supervision, Writing- Reviewing and Editing, MC: Methodology, Formal analysis, Investigation, Writing- Reviewing and Editing. All authors read and approved the final manuscript.
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
Ethical statement
Guarantor
EE.
Data Availability Statement
The research data for this study cannot be shared as it contains sensitive or confidential information, such as patient data.
