The Reliability and Validity of Lymphedema Quality of Life Questionnaire-Leg in Turkish Patients with Lower Limb Lymphedema

Abstract

Background:

Accurate information on quality of life (QoL) outcomes among patients with lower limb lymphedema (LLL) is substantially needed to capture lymphedema-specific impairments and make clinical decisions for the management of this suffering condition. No specific instrument for QoL in patients with LLL has been translated to Turkish and validated. This study aims to adapt the Lymphedema Quality of Life Questionnaire-leg (LYMQOL-Leg) to Turkish and to test its reliability and validity in patients with LLL.

Methods and Results:

The Turkish-LYMQOL-Leg was obtained using forward–backward translation and administered to 138 patients with LLL, along with Short Form 36 (SF-36), and Lower Extremity Functional Scale (LEFS), between May 2015 and October 2017. A test–retest interval of 7 days was used to assess the reliability. Descriptive analysis was applied for demographic variables and validation studies were conducted by means of construct validity using Spearman's rank correlation coefficient. Internal consistency and test–retest reliability were assessed using Cronbach's α and intraclass correlation coefficient (ICC), respectively. All patients with LLL completed the questionnaires. The mean age and lymphedema duration were 52.01 ± 14.73 years and 95.6 ± 108.6 months, respectively. Internal consistency and test–retest reliability of the Turkish-LYMQOL-Leg were good with Cronbach's α (0.85–0.90) and test–retest ICC (0.68–0.85). External construct validity was highly confirmed by expected correlations with comparator scales SF-36 and LEFS (p < 0.01).

Conclusion:

The Turkish version of the LYMQOL-Leg is a valid and reliable tool for evaluating QoL in patients with LLL that can readily be applied as an outcome measure both in clinical practice and research studies.

Introduction

Lymphedema is a debilitating disorder characterized by accumulation of excessive fluid and protein in the interstitium due to the impairments in lymphatic system and results in chronic swelling in different parts of the body. Lymphedema is commonly seen in extremities but may involve the trunk, head, and genital area in some cases.¹ Lymphedema of the lower limbs can be classified as primary or secondary, depending on the underlying cause.

Primary lymphedema of the legs may be diagnosed immediately after birth or puberty, or may have a long latency period from onset to diagnosis. Secondary lymphedema of the lower limbs may manifest mostly due to the cancer surgeries of abdominopelvic organs, melanomas or regional lymphomas, and/or radiation therapies. Progressed chronic venous insufficiency, lipedema, gravitational/dependency edema, obesity, trauma, or infections may also cause lower extremity lymphedema to a lesser extent.^1–3

Lower limb lymphedemas (LLLs) are incurable and progressive conditions that can cause life-long physical, psychosocial, and emotional problems and have impact on individual's well-being and quality of life (QoL).^4–8 Many patients suffering from chronic LLL also experience a range of physical symptoms including heaviness, pain, discomfort, difficulty in ambulation, in finding fitted clothing and footwear, as well as associated conditions including skin ulceration, cellulitis, and immobility. All these problems can be challenging and frustrating for many individuals and may lead to feelings of self-consciousness, embarrassment, depression, and social isolation^5–7

The diminishing effect of LLL on QoL has previously been evaluated using generic QoL instruments^8–10 or cancer-specific instruments^4,7,11 and rarely with lymphedema-specific questionnaires^5,8,12 Accurate information on health-related QoL outcomes among patients with LLL is substantially needed to capture lymphedema-specific impairments and make clinical decisions for the management of this suffering condition.^4,5 The majority of lymphedema-specific QoL instruments measure only the impact of upper limb lymphedema. In recent years, there has been more interest in developing questionnaires designed and validated specially for limb lymphedema, such as “the lymphedema quality of life inventory (LyQLI),”¹³ “Freiburg QoL assessment for lymphatic disorders,”⁸ “lymphedema functioning, disability, and health questionnaire (Lymph-ICF),”¹⁴ and “Lymphedema Life Impact Scale (LLIS).”¹⁵ But none of them has separate parts assessing the different aspects of upper and lower extremity lymphedema. Keeley et al.¹⁶ have designed and validated a short and simple lymphedema quality of life questionnaire (LYMQOL) that consists of two distinct questionnaires; for upper and lower lymphedema LYMQOL-Arm and LYMQOL-Leg.

LYMQOL is a disease-specific patient-reported outcome measure developed in the United Kingdom, used and validated in different cultures^5,17,18 and consists of 27 perceived items. Turkish language is spoken by some 84 million people worldwide. Previously no specific instrument for LLL has been translated to Turkish and validated and as far as we have known, there exists no QoL study for Turkish patients with LLL. The aim of this study was to translate and validate LYMQOL-Leg for Turkish patients with LLL.

Materials and Methods

In this study, we undertook a descriptive and methodological study for validation of the LYMQOL-Leg among Turkish patients with LLL, similar to the procedures that have been undertaken for the validity of LYMQOL-Arm.¹⁹ The study was conducted in the Lymphedema Unit, Physical Medicine and Rehabilitation Department of a university hospital, and Lymphedema Research and Practice Center of the same university between June 2015 and May 2017. The study was approved by the Clinical Research Ethics Committee of the University School of Medicine. All patients gave verbal and written informed consent for inclusion in the study. LLL patients having mental incapacity, having psychiatric diagnoses requiring medications, and those younger than 18 years and older than 65 years were not included. Patients were excluded if they are illiterate or involved in intensive lymphedema treatment during the test period, or if they have life-threatening or terminal illness. All the patients who have lymphedema due to cancer treatments had completed their chemotherapy and radiotherapy sessions and did not have active malignancy. The diagnosis of LLL was verified by symptoms, anamnesis, history, imaging, and bilateral volumetric measurements depending on the circumferential measurements.¹⁸ For patients having unilateral leg lymphedema, the circumferential measurements were performed by a standard 1 inch retractable tape at 4-cm intervals along the leg, from malleoli to groin and converted to an approximate leg volume using the truncated cone formula to enable estimation of volume. The presence of lymphedema was assessed by interlimb volume difference (>10%) based on the serial circumferential measurements in both affected and nonaffected extremities.¹ Also the circumferential measurements of second toe base and metatarsophalangeal areas were recorded for patients with feet edema. Lymphedema was defined as an increase in feet circumference at any level by 1.5 cm or more compared with the contralateral side. In bilateral disease, the diagnosis was made depending on inspection and lymphoscintigraphy results derived from the patient files.^1,2

The demographic properties (age, gender, education and marital status, occupation, and body mass index) and disease characteristics (causes, duration of lymphedema, involvement side, treatments, and stage of lymphedema) were recorded.

Translation and cross-cultural adaptation

After obtaining written permission (2015) from the researcher who developed the LYMQOL, the forward–backward translation method was initiated. Four steps were used in the linguistic validation of the questionnaire. Two lecturers graduated from departments of foreign languages of Bilkent University and two lymphedema specialists, who were competent and fully bilingual in both Turkish and English, participated in the translation process. One of the lecturers translated the English version into Turkish to produce an understandable and conceptually equivalent translation. The back translation of the Turkish version into source language was done by the second lecturer who was unaware about the purpose of translation. The original form and the one translated form from Turkish to English were compared by the two lecturers, and the final form of the Turkish version was prepared. Finally the two lymphedema specialists, who were fully competent in both languages, controlled and revised the lecturers' final Turkish version to obtain the Turkish version used in this study. To avoid misunderstanding and to obtain difficulties in understanding, the instrument was given as a pretest to 30 patients with LLL. Face-to-face interviews with the patients showed that all the indices were clear and the instrument was understandable. We made no cross-cultural validation in the translation because feedback from the pretest study group did not identify any concerns. The Turkish version of LYMPQOL-Leg was answered by the patients themselves. One lymphedema specialist was in the interview room to help the patients in case they needed assistance, which was the case only in a few patients with difficulty in reading. The scale was completed by each patient twice with 1-week interval.

Questionnaires

The LYMQOL-Leg has been developed to assess the impact of lymphedema of the legs on the QoL of the patients and consists of 27 items: 26 multiple-choice questions and 1 rating question.¹⁶ It covers four domains: symptoms, appearance, function, and mood. The answers were evaluated on a 4-point Likert scale (1 = not at all, 2 = a little, 3 = quite a bit, 4 = a lot). Each item received a score between 1 and 4, with higher scores indicating a worse QoL. Domain totals were calculated by adding the individual scores and dividing the total by the number of questions answered. (If >50% of questions per domain were not answered, this cannot be calculated * and = 0). If the item was not scored and left blank or not applicable, this was scored with a 0. The four domains and their corresponding questions are Function 1 (a–h), 2,3; Appearance 4,5,6,7,8; Symptoms 9,10,11,12,13,14; and Emotion 15,16,17,18,19,20. A visual analog scale for “overall quality of life” (Q21) is scored between 0 and 10, as the value marked by the respondent. If the item is not scored, left blank, or not applicable, it is scored as 0. Previous reports indicated that the LYMPQOL-Leg was easy to complete with clear face validity and good internal consistency.^5,16

Patients with LLL were also administered Short Form 36 (SF-36) and Lower Extremity Functional Scale (LEFS) QoL tools, for comparisons with the new instrument. They were chosen as criterion standards, since they are suggested and used frequently^6,15,20 for QoL studies for lymphedema patients, and their Turkish versions have been evaluated for test–retest reliability and validity.^21,22

SF-36 is a standard 36-item self-administered generic QoL questionnaire designed to measure health-related QoL during the previous month.²³ It consists of 36 items within 8 subscales, which evaluate physical functioning (10 items), mental health (5 items), social health (2 items), physical role (4 items), emotional role (3 items), vitality (4 items), pain (2 items), and general health (6 items). These eight domains can be aggregated into two summary measures: the physical component score and mental component score. Each domain is scored according to a standardized scoring protocol in the range of 0–100, where higher scores indicate better health status. The Turkish validity and reliability have previously been conducted²¹

LEFS is a self-report measure assessing lower extremity function in patients with any musculoskeletal impairment, developed by Binkley et al.²⁴ It is a single-page questionnaire containing 20 items: each had five possible numeric response categories (0–4). The total score ranges from 0 to 80, with higher scores indicating better functional status. The Turkish cross-cultural adaptation and validation have previously been made by Citaker et al.²²

Procedure

The participants completed the LYMPQO-Leg, SF-36, and LLFS concurrently, whereas the LYMPQOL-Leg was completed for patients twice within 7 days.

Statistical analyses

The sample size is determined as at least fivefold of item numbers, for the reliability and validity studies. According to this information, 135 patients were required for the study. Descriptive analyses were applied to calculate means and standard deviations and median of the demographic variables.

For test–retest reliability, all patients completed the questionnaires, as a second time within 7 days, at the same time of day, during a nontreatment period. Intraclass correlation coefficients (ICCs) with one way random effects model were used to determine test–retest reliability of the scores on five domains of LYMQOL-Leg and of the score on each question separately. Cronbach's α coefficients were used to determine internal consistency of the entire questionnaire and of each domain. As recommended, internal consistency of a magnitude of 0.70 or greater was sought. Cronbach's α was determined as high correlation if values in range of 0.80–0.95 were obtained, where a value >0.95 indicated excessive internal consistency.

Confirmatory factor analysis was used to show the convenience of factor structure to the original scale. Construct validity was tested by convergent–divergent validity approach comparing the correlation of the similar scales of the SF-36 and LLFS. It was expected that conceptually related scales would correlate better with the functioning scales of the LYMQLQ-Leg and vice versa. We used the Pearson correlation coefficient for normally distributed scores and the Spearman correlation coefficient for the other scores. The correlation coefficients are interpreted as follows: <0.4 was weak, 0.4–0.74 was moderate, 0.75–0.9 was strong, and >0.9 was very strong.²⁵

We have also performed subgroup analysis according to the causes (primary and secondary). Independent samples t-test and one way analysis of variance were used to compare subgroups.

All the analyses were conducted using IBM SPSS 22.0. The level of significance was set at p < 0.05.

Results

A total of 138 patients with LLL were included to the study. All the subjects completed tests 1 and 2 for LYMQOL for test–retest analyses. The time between tests 1 and 2 was within 7 days. The demographic and clinical characteristics of the patients are given in Table 1.

Table 1.

Demographic and Clinical Properties of the Patients

	Patients, N = 138
Age (years), mean ± SD (min–max)	52.01 ± 14.73 (16–85)
Gender, n (%)
Female	119 (86.2)
Male	19 (13.8)
Marital status, n (%)
Unmarried/single	23 (16.7)
Married	104 (75.4)
Divorced/widowed	11 (8)
Education, n (%)
Illiterate	11 (8)
Primary school	56 (40.6)
Secondary school	13 (9.4)
Lycee	29 (21)
University	29 (21)
Occupation, n (%)
Housewife	79 (57.2)
Retired	18 (13)
Officer	21 (15.2)
Self-employment	10 (7.2)
Student	6 (4.3)
Unemployed	4 (2.9)
Involved side, n (%)
Right	24 (17.4)
Left	36 (26.1)
Bilateral	78 (56.5)
BMI, kg/m²	33.95 ± 8.99 (19.53–59.1)
Duration of lymphedema (months), mean ± SD (min–max)	95.6 ± 108.6 (1–480)
Exercise habit, n (%)
Yes	12 (8.7)
No	126 (91.3)
Etiology, n (%)
Primary lymphedema	65 (47.1)
Secondary lymphedema	73 (52.9)
Initial side, n (%)
Proximal leg	29 (21)
Distal leg/feet	109 (79)
Causes, n (%)
Cancer treatment and/or radiotherapy	47 (34.1)
Lipolymphedema	58 (42)
phelobolymphedema	26 (18.9)
Trauma	2 (1.4)
İnfection<	1 (0.7)
Congenital/hereditary	4 (2.9)
Surgery, n (%)	46
TH/BSO/omentectomy/inguinal lymph node dissection	36 (78.2)
Melanoma/inguinal lymph node dissection	3 (6.5)
Local colon resection + omentectomy	3 (6.5)
Lymphoma	1 (2.17)
Prostatectomy/node dissection	1 (2.17)
Metastatic cancer surgery	2 (4.34)
Lymphedema stage, n (%)
1	19 (13.8)
2	104 (75.4)
3	15 (10.9)
Type, n (%)
Reversible	18 (13)
Spontaneous irreversible	105 (76.1)
Elephantiasis	15 (10.9)

BMI, body mass index; BSO, bilateral salpingooferectomy; max, maximum; min, minimum; SD, standard deviation; TH, total hysterectomy.

Majority of the patients were female and had pelvic or abdominal cancer surgery followed by lipolymphedema and phlebolymphedema. Concomitant venous disease was present in 45% of patients. A great number of them were married and housewives. Nearly half of the participants were lycee or university graduated. The median duration of lymphedema was 60 months. Symptoms such as skin ulceration and cellulitis were present in 8% of the patients.

Reliability

Internal consistency (based on a Cronbach's α score of (0.89–0.92) and test–retest reliability (based on an ICC of 0.86–0.95 of the LYMQLQ-Leg) were found to be high (p < 0.001; Table 2). The test–retest reliability of all the subscores and overall scores of LYMQOL-Leg were strong.

Table 2.

Internal Consistency and Test–Retest Reliability of the Turkish Quality of Life Measure for Limb Lymphedema-Leg Instrument (N = 138)

LYMQOL-Leg scores	Test–retest			Consistency	Paired t-test
LYMQOL-Leg scores	Pearson	ICC	95% CI	Cronbach's α	p
Function	0.947^*	0.947	0.922–0.963	0.918	0.157
Appearance	0.907^*	0.907	0.866–0.936	0.899	0.819
Symptom	0.863^*	0.863	0.805–0.905	0.890	0.637
Mood	0.904^*	0.903	0.861–0.933	0.908	0.045
Overall	0.935^*	0.935	0.906–0.955		0.078

p < 0.001.

CI, confidence interval; ICC, intraclass correlation coefficient; LYMQOL, quality of life measure for limb lymphedema.

Confirmatory factor analysis

Confirmatory factor analysis was applied to the factor structure. Specifically, we expected a best-fit model with the following indices: a Satorra–Bentler scaled χ²/degrees of freedom ratio (CMIN/DF) of 2.0 or less; a Trucker Lewis index (TLI) of 0.90 or higher; a comparative fit index (CFI) of 0.90 or higher; a Incremental Fit Index (IFI) of 0.90 or higher; and a low root mean square error of approximation (RMSEA) of 0.08 or less. These values were calculated as CMIN/DF: 1.417, RMSEA: 0.055, IFI: 0.959, CFI: 0.958, TLI: 0.952. Accordingly, this factor structure was found acceptable.

Construct (convergent–divergent) validity

Table 3 gives an overview of interscale Spearman correlation coefficients between the different domains of SF-36 and the LEFS. All 138 patients completed the three questionnaires. All domains of LYMQOL-Leg had the strongest correlation with the expected and related like domains of SF-36 (LYMQOL-function/SF-36-physical component, LYMQOL-mood/SF-36 mental component) and moderate correlation with overall LYMQOL-Leg scores and mental and physical component summary scores. Concurrently, LEFS scores had correlated with all subscores of LYMQLQ-Leg, having the strongest correlation with functional subscore of LYMQOL, as expected and moderately correlated with appearance symptom and mood scores of LYMQOL (Table 3).

Table 3.

Correlation Coefficients Between Quality of Life Measure for Limb Lymphedema-Leg and the Short Form-36 and Lower Extremity Functional Scale Questionnaires (Construct Validity)

	LYMQOL function	LYMQOL appearance	LYMQOL symptom	LYMQOL mood	LYMQOL overall
LEFS score	−0.791^**	−0.413^**	−0.552^**	−0.437^**	0.585^**
SF-36
Physical functioning	−0.712^**	−0.274^**	−0.509^**	−0.344^**	0.471^**
Role physical	−0.519^**	−0.367^**	−0.477^**	−0.417^**	0.552^**
Bodily pain	−0.601^**	−0.303^**	−0.639^**	−0.444^**	0.537^**
General health	−0.513^**	−0.452^**	−0.494^**	−0.499^**	0.583^**
Vitality	−0.444^**	−0.432^**	−0.448^**	−0.553^**	0.633^**
Social functioning	−0.599^**	−0.493^**	−0.579^**	−0.615^**	0.570^**
Role emotional	−0.361^**	−0.293^**	−0.291^**	−0.525^**	0.429^**
Mental health	−0.299^**	−0.419^**	−0.436^**	−0.558^**	0.541^**
Physical component summary (n = 62)	−0.711^**	−0.352^**	−0.638^**	−0.378^**	0.639^**
Mental component summary (n = 62)	−0.291^*	−0.442^**	−0.350^**	−0.738^**	0.471^**

p < 0.05, ^**p < 0.01.

LEFS, Lower Extremity Functional Scale; SF-36, Short Form 36.

In subgroup analysis, no statistical difference was found between the scores of LYMQOL-Leg in patients with primary and secondary lymphedema (Table 4). Also the mean values of subscores of LYMQOL-Leg were similar between female and male patients (p > 0.05, in all domains, data not shown)

Table 4.

The Mean Values of Quality of Life Measure for Limb Lymphedema-Leg Scores According to the Etiology of Lymphedema

LYMQOL-Leg	All group (N = 138)	Primary (n = 65)	Secondary (n = 73)	p
Function	2.36 ± 0.82	2.33 ± 0.83	2.39 ± 0.82	0.670
Appearance	2.57 ± 0.84	2.60 ± 0.87	2.54 ± 0.82	0.656
Symptom	2.38 ± 0.81	2.41 ± 0.81	2.36 ± 0.81	0.684
Emotion	2.16 ± 0.85	2.16 ± 0.85	2.16 ± 0.85	0.984
Overall	5.20 ± 2.51	5.51 ± 2.67	4.93 ± 2.35	0.180

Discussion

Lower limb is the most commonly affected area in patients developing lymphedema worldwide.²⁶ LLL is an incapacitating disease and more morbid than upper extremity lymphedema. Although the incidence of LLL remains unknown, both in our country and in the world,²⁷ this condition is seen commonly in our routine daily practice. There is no cure for lymphedema, and multimodal treatment approaches focus on symptom control and complex decongestive therapy.^1,2 Since this chronic disease may have great impact on several areas of life such as physical and mental well-being, the lack of information on different aspects of QoL influences the treatment outcomes of this detrimental condition. The use of LLL-specific QoL tools can give a general picture of the deficits in QoL experienced by the patients and may help to manipulate resources accordantly and guide therapeutic approaches comprising the patient education.

Although many instruments have previously been used to assess health-related QoL in patients with lymphedema, no consensus has been made on the gold-standard tool. Thomas et al.²⁶ compared three QoL instruments in lymphatic filariasis and recommended the use of lymphatic filariasis quality of life questionnaire with further modifications in this population. A systematic review identified only six studies measuring the health-related QoL in the English literature. Most of the studies in this review utilized generic or cancer-specific QoL tools.⁴Recently new QoL measures specific to lymphedema are developed and are in use to gain more accurate insight into the burden of this suffering condition.^13–16 LYMPQOL has a unique structure that comprises two separate questionnaires: for upper and lower lymphedema—LYMQOL-Arm and LYMQOL-Leg. The tool is short, understandable, practical, and easily applicable.¹⁶

In our study, we tested the reliability and validity of the LYMQOL-Leg in Turkish LLL patients and found that all subscales of LYMQOL-Leg had good internal consistency and test–retest reliability. As far as we have known, this is the first and the only validated Turkish Lymphedema-Specific Questionnaire for LLL. The validation of this questionnaire has previously been made in different cultures comprising Dutch,¹⁷ Irish,⁵ and Japanese¹⁸ LLL patients. In the original study, Keeley et al.¹⁶ indicated an internal consistency using Cronbach's α scores ranging from 0.87 to 0.91 across all domains of the tool in patients with LLL. Dutch validation study determined good internal consistency scores. The internal consistency of our study was observed to be high with values between 0.89 and 0.91 similar to the original study and more than those reported by previous studies.^16,17 The construct validity was confirmed by high correlation coefficients with the LYMPQOL-Leg and related like domains of SF-36 and LEFS. The construct validity was not fully confirmed in the original study as there was no significant correlation between initial limb volume and QoL, but we have found correlation between LYMQOL-Leg scores and lymphedema severity, indicating worse QoL in advanced lymphedema and a strong construct validity.

As is well known that lymphedema severity and outcome may show variability due to the awareness and education of the health professionals and public. In addition, socioeconomic and cultural factors as well as quality and access to medical services for lymphedema may vary from country to country and affect the course and outcomes of this debilitating condition. In our study, the mean values of LYMQOL-Leg subscale scores were higher than in some previous studies, indicating a worse QoL than in other cultures.^16–18

Although the female-to-male ratios of our study were consistent with other previous studies,^14–16 a limitation of this study might be that majority of the subjects were female. But subgroup analysis evaluating the scores of LYMQOL with regard to gender indicated no difference between the groups. Another limitation might be the exclusion of patients with cognitive and psychiatric dysfunctions (as assumed that they have not a full comprehension of all the questions), which may lead to limitations in generalizability of our results for all LLL patients. But most of the previous studies conducted on LLL patients used a similar exclusion criterion.^13–17 We did not assess the responsiveness of this instrument as it was outside the context of our study, future studies that address the responsiveness of this questionnaire would be beneficial for the extensive use of this tool.

Conclusion

In conclusion, assessment of QoL of LLL patients is important and our findings demonstrate that LYMQOL-Leg is a valid and reliable instrument for the assessment of the QoL in Turkish patients with LLL. Turkish LLL patients found the Turkish version of LYMQLQ-Leg questionnaire easy to understand, respond, and complete. In the absence of any other validated lymphedema-specific QoL questionnaire in Turkish language, the Turkish LYMQOL-Leg appears to be a promising tool that can be readily applied as an outcome measure both in clinical practice and research studies.

Footnotes

Acknowledgments

The authors thank Dr. İpek Genç and Bahar Tezer Alanya for their effort during backward and forward translation processes.

Author Disclosure Statement

No competing financial interests exist.

References

International Society of Lymphology. The Diagnosis and treatment of peripheral lymphedema. 2013 Consensus Document of the International Society of Lymphology. Lymphology, 2013; 46:1–11.

Jensen

, Simonsen

, Karlsmark

, et al. Lymphoedema of the lower extremities-background, pathophysiology and diagnostic considerations. Clin Physiol Funct Imaging, 2010; 30:389–398.

Paskett

, Dean

, Olivieri

, Harrop

. Cancer-related lymphedema risk factors, diagnosis, treatment and impact: A review. J Clin Oncol, 2012; 30:3726–3733.

Cemal

, Jewell

, Albornoz

, Pusic

, Mehrara

. Systematic review of quality of life and patient related outcomes in patients with oncologic related lower extremity lymphedema. Lymphatic Res Biol, 2013; 11:14–19.

Greene

, Meskell

. The impact of lower limb chronic oedema on patients' quality of life. Int Wound J, 2017; 14:561–568.

Franks

, Moffatt

, Doherty

, Williams

, Jeffs

, Mortimer

. Assessment of health-related quality of life in patients with lymphedema of the lower limb. Wound Rep Reg, 2006; 14:110–118.

Kim

, Lim

, Lee

, Park

, et al. Impact of lower limb lymphedema on quality of life in gynecologic cancer survivors after pelvic lymph node dissection. Eur J Obstet Gynecol Reprod Biol, 2015; 192:31–36.

Huggenberger

, Wagner

, Lehmann

, Aeschlimann

, Ammann-Vesti

, Angst

. Health and quality of life in patients with primary and secondary lymphedema of the lower extremity. Vasa, 2015; 44:129–137.

Blumberg

, Berland

, Rockman

, Musa

, Brooks

, et al. Pneumatic compression improves quality of life in patients with lower extremity lymphedema. Am Vasc Surg, 2016; 30:40–44.

10.

Katz

, Dugan

, Cohn

, et al. Weight lifting in patients with lower-extremity lymphedema secondary to cancer: A pilot and feasibility study. Arch Physc Med Rehabil, 2010; 91:1070–1076.

11.

de Vries

, Hoekstra

, Hoekstra-Weebers

. Quality of life after axillary or groin sentinel lymph node biopsy, with or without completion lymph node dissection, in patients with cutaneous melanoma. Ann Surg Oncol, 2009; 16:2840–2847.

12.

Carmeli

, Bartoletti

. A retrospective trial of complete decongestive physical therapy for lower extremity secondary lymphedema in melanoma patients. Support Care Cancer, 2011; 19:141–147.

13.

Klernas

, Johnson

, Horstmann

, Krisjanson

, Johansson

. Lymphedema Quality of Life Inventory (LyQLI) Development and investigation of validity and reliability. Qual Life Res, 2015; 24:427–439.

14.

Devoogdt

, van Kampen

, Geraerts

, Coremans

, Christiaens

. Lymphoedema functioning, disability and Health Questionnaire (Lymph-ICF): Reliability and validity. Phys Ther, 2011; 91:944–957.

15.

Weiss

, Daniel

. Validation of the lymphedema life impact scale (LLIS): A condition specific measurement tool for persons with lymphedema. Lymphology, 2015; 48:128–138.

16.

Keeley

, Crooks

, Locke

, Veigas

, Riches

, et al. A quality of life measure for limb lymphedema (LYMQOL). J Lymphoedema, 2012; 5:345–349.

17.

van de Pas

, Bieamns

, Boonen

, Viehof

, Neumann

. Validation of the Lymphoedema Quality of Life Questionnaire (LYMQOL) in Dutch patients diagnosed with lymphedema of the lower limbs. Phelobology, 2016; 31:257–263.

18.

Iuchi

, Dai

, Sanada

, Okuwa

, Naktani

, Sugama

. Associations between the treatments and outcomes of patients with upper and lower lymphedema in Japan: A cross sectional observational study. Int J Nurs Stud, 2015; 52:913–919.

19.

Borman

, Yaman

, Denizli

, Karahan

, Özdemir

. The reliability and validity of Lymphedema Quality of Life Questionnaire-Arm in Turkish patients with upper limb lymphedema related with breast cancer. Turk J Phys Med Rehabil, 2018; 64:1–8.

20.

Durutürk

, Tonga

, Gabel

, Acar

, Tekindal

. Cross-cultural adaptation, reliability and validity of the Turkish version of the lower limb functional Index. Disabil Rehabil, 2015; 37:2439–2444.

21.

Koçyiğit

, Aydemir

, Fişek

. Reliability and validity of Turkish version of Short Form-36. Med Ther Mag, 1999; 12:102–106.

22.

Citaker

, Kafa

, Hazar-Kanik

, Ugurlu

, Kafa

, Tuna

. Translation, cross-cultural adaptation and validation of the Turkish version of the Lower Extremity Functional Scale on patients with knee injuries. Arch Orthop Trauma Surg, 2016; 136:389–395.

23.

Ware

, Snow

, Kosinski

, Gandek

. SF-36 Health Survey: Manual and Interpretation Guide. Boston, MA: The Health Institute, New England Medical Center; 1993.

24.

Binkley

, Stratford

, Lott

, et al. The lower extremity functional scale (LEFS): Scale development, measurement properties and clinical application. Phys Ther, 1999; 79:371–383.

25.

Koo

, Li

. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med, 2016; 15:155–163.

26.

Thomas

, Narahari

, Bose

, Vivekananda

, New

, et al. Comparison of three quality of life instruments in lymphatic filariasis: DLQI, WHODAS2.0, LFSQQ. PLOS Neglected Tropical Diseases, 2014; 8:e2716–e2718.

27.

Hopp

, Osborne

, Schneidler

, Bojar

, Uyar

. A prospective pilot study on the incidence of post-operative lymphedema in women with endometrial cancer. Gynecol Oncol Rep, 2015; 24:25–28.