Psychometric Evaluation of a Brazilian Version of the Lymphedema Functioning,Disability and Health Questionnaire for Lower Limb Lymphedema in Patients After Cancer Treatment

Abstract

Background:

The aim of this study was to evaluate psychometric properties of the Lymphedema Functioning, Disability and Health Questionnaire for lower limb lymphedema (Lymph-ICF-LL) in Brazilian patients with secondary lower limb lymphedema after cancer treatment.

Methods and Results:

A diagnostic test study was performed in 30 patients with lower limb lymphedema. To assess the reliability, the intraclass correlation coefficient (ICC) was analyzed through test–retest, Cronbach alpha coefficient, magnitude of intrasubject variability by standard error of measurement (SEM), and smallest real difference (SRD). To assess the face and content validity, a specific questionnaire was applied to assess the clarity of the scoring system and comprehensiveness of questions. To assess construct validity, correlations between the final Brazilian version of the Lymph ICF-LL and the quality of life questionnaire SF-36 (36-Item Short Form Health Survey Questionnaire) were analyzed. The ICCs and general internal consistency scores of Lymph-ICF-LL were high (ICCs >0.90 and the Cronbach alpha coefficient >0.90, respectively). Measurement variability between the tests was acceptable (SEM 5.9) with SRD of 16.4. Face and content validity were considered excellent by the patients as the scoring system was clear and questions were understandable for 97% and 90% of the patients, respectively. Construct validity was classified as good and all hypotheses for assessing convergent validity were accepted (medium to strong correlation, from −0.69 to −0.84).

Conclusion:

The Brazilian version of the Lymph-ICF-LL is a reliable and valuable instrument for assessing Brazilian patients with secondary lower limb lymphedema associated with cancer treatment.

Introduction

Lower limb lymphedema is a chronic and debilitating complication caused by cancer treatment, common after lymphadenectomy and radiotherapy.^1,2 It is defined as lymphatic system dysfunction and impaired lymphatic transport, thus leading to an increase in interstitial fluid, which is protein rich and characterized by lower limb swelling.^3,4

Patients with lymphedema can present with associated symptoms in their limbs, including pain, feeling of heaviness, sensibility changes, physical dysfunction, decreased mobility, and also psychological, social, and financial concerns.^5–7 Patients with lower limb lymphedema have a lower quality of life due to physical, psychosocial, esthetic, and emotional impairment. All these problems can be arduous and frustrating, which may lead to feelings of anguish, abandonment, embarrassment, depression, social isolation, and fear of possible illness progression.^8,9

Lymphedema, when lacking proper treatment, is a chronic and progressive disease. Once it manifests, it will persist throughout an individual's life.¹⁰ The first-line treatment for lymphedema has been conservative management with complex decongestive therapy, which includes special attention to skin care, manual lymphatic drainage, exercises of the extremities (muscle pumping exercises), and compression therapy (compression bandages and low-stretch elastic stocking).^4,11 This type of treatment aims to minimize and control the swelling and increase the function.

The impact and deteriorating effects of lymphedema were studied extensively in breast cancer patients.^12–15 Nonspecific, health-related quality-of-life instruments, specific outcome measures, and, rarely, specific questionnaires for lower limb lymphedema have evaluated the quality of life and functional limitations of lymphedema in the lower limbs after cancer treatment.^8,9,16–22 The main disadvantage of the current questionnaires is that they are inaccurate and therefore provide limited information about patients' experiences with lower limb lymphedema. Thus, the instruments must be multidimensional and evaluate specific deficiency outcomes of lymphedema to make clinical decisions.²³

The Functioning, Disability and Health Questionnaire for lower limb lymphedema (Lymph-ICF-LL) is a specific instrument that assesses problems in functioning, such as impairment in function, activity limitations, and participation restrictions, associated with the development of secondary lower limb lymphedema.²³ Its validity and reliability were good when applied in Dutch. The original questionnaire²³ was also translated and validated for the Chinese population²⁴ and the German population.²⁵ Ferreira et al.²⁶ translated and performed the cross-cultural adaptation of the Lymph-ICF-LL into (Brazilian) Portuguese for patients with secondary lower limb lymphedema after cancer treatment. The aim of this study was to evaluate psychometric properties of Lymph-ICF-LL in Brazilian patients with secondary lower limb lymphedema after cancer treatment.

Methods

A diagnostic study was performed to evaluate psychometric properties of the Brazilian version of Lymph-ICF-LL. Thirty patients with secondary lower limb lymphedema after gynecological cancer or melanoma treatment, followed up at the Physical Therapy Clinic of the Gynecological and Bone and Connective Tissue Cancer Department in Hospital of Cancer II, the Brazilian National Cancer Institute, were included in this study. If the patients had one of the following conditions, they would be excluded: active neoplastic disease; visual, cognitive, or intellectual impairment that would not enable them to read and understand the questionnaires; walking disability; and refusal to sign an informed consent form.

Eligible patients answered four questionnaires: the clinical and sociodemographic variables questionnaire, final Brazilian version of the Lymph-ICF-LL, face and content validity questionnaire, and 36-Item Short Form Health Survey Questionnaire (SF-36) quality of life questionnaire to evaluate the construct validity. Moreover, patients were submitted to physical examination to obtain the clinical assessment for lymphedema, and oncological data from the medical records were collected. While the Lymph-ICF-LL and SF-36 were self-applied, interviews were conducted to collect data for the other questionnaires.

The Lymph-ICF-LL²³ comprises 28 questions based on information collected from patients with lower limb lymphedema. The interviewees choose their answers on a numeric scale, ranging from 0 to 10, where 0 indicates that the patient has not shown any symptoms regarding the question proposed and 10 indicates that the patient showed extreme symptoms concerning the question proposed. For each question, the interviewee chooses the number that best describes their situation. The answer option “not applicable” must be chosen in case the question does not apply to the interviewee. The questions are divided into three categories: physical function, mental function, and mobility function.

To evaluate the test–retest reliability, participants answered the Lymph-ICF-LL a second time within 24–48 hours. This period was considered because changes in functioning were not expected due to lymphedema.²³

The questionnaire to assess the face and content validity comprised two questions: 1. Was the scoring system clear? 2. Were all complaints related to your lymphedema mentioned in the Lymph-ICF-LL questionnaire? The participants who answered negatively to any of the questions were asked to explain their choices. Later, during the interview, they were asked to clarify their answers.

The SF-36 is a reliable and valuable questionnaire to assess the quality of life of the general population. It comprises 36 questions about eight subjects related to the quality of life. A low score in the SF-36 indicates a low level of quality of life.²⁷

Through the interview and analysis of the information in the medical records of all participants, it was possible to collect data on age, race, educational attainment, type of occupation, type of cancer (cervical cancer, endometrial cancer, ovarian cancer, vulvar cancer, vaginal cancer, or melanoma), cancer treatment (surgery with lymphadenectomy or sentinel lymph node biopsy, chemotherapy, or radiotherapy), and physical therapy treatment for lymphedema (skin care, manual lymphatic drainage, compression bandages, low-stretch elastic stocking, or exercises of the extremities).

During the physical examination, information about mass and height (to determine the body–mass index) was collected along with specific information to evaluate the lower limbs (venous disease, skin changes, degenerative process, perimetry to measure the difference between the volumes of the lower limbs, side and the severity of lymphedema, and the presence of pain and its intensity using a visual numeric scale, where 0 indicates that the patient did not have pain and 10 indicates the highest level of pain).²⁸

Perimetry was conducted with the patient lying in the supine position with the lower limbs exposed. A measuring tape was used to measure the circumference of limbs in centimeters; it was executed from 21 and 14 to 7 cm above the patella and from 14, 21, and 28 to 35 cm under the patella.

The volume of the lower limb was estimated from several circumference measurements, by measuring each segment of the limb between each pair of circumferences (truncated cone). It was calculated as follows: V = h × (C² + Cc + c²)/(π × 12), where V is the final volume of the limb segment; C and c are circumferences between two measuring points; and h is the distance between the circumferences (C and c) in each segment. The sum of the volume for each point corresponds to the estimated final volume (V); then, the average of the difference between the volumes of the lower limbs (in milliliters) is calculated and the side with lymphedema (unilateral or bilateral)²⁹ is assessed. The severity was measured according to the International Society of Lymphology⁴ as weak (>5 to <20% of increased limb volume), moderate (an increase of 20%–40%), or very strong (>40% increase).

Data analysis

Data were analyzed with IBM SPSS, version 23.0. Descriptive analysis of the participants in this study was performed using a measure of central tendency of the quantitative variables and absolute and relative frequencies of the qualitative variables.

Reliability

The reliability of the total score, scores on the five domains, and score on each question separately on the Brazilian version of Lymph-ICF-LL was assessed by test–retest, in which the intraclass correlation coefficient (ICC) was calculated. The internal consistency of the entire questionnaire and of each domain was determined by the average of the Cronbach alpha coefficient. To interpret the magnitude of intrasubject variation of the two scores from the Brazilian version of Lymph-ICF-LL, the standard error of measurement (SEM) was calculated with the following formula: $S E M = S D_{12} \sqrt[]{1 - I C C}$ where SD₁₂ is the average standard deviation of the two ratings.³⁰

To evaluate clinically important changes, the smallest real difference (SRD) was calculated with the following formula: SRD = 1.96 × SEM × √2.³⁰ To obtain a reference range of 95% of the SRD for the mean difference between scores on the two occasions, the mean difference between the two scores plus or minus the SRD was calculated.

Validity

Face validity, content validity, and construct validity were analyzed. It was not possible to analyze the criterion validity since there is no gold standard in the literature. Face validity was evaluated qualitatively when asked whether the questions in the questionnaire were understandable and whether the scoring system was clear. The content validity was examined by the answers given by participants to questions about the comprehensiveness of the questionnaire.³¹

The construct validity was obtained by evaluating the correlation between scores on the domains of the SF-36 and the Brazilian version of Lymph-ICF-LL, by applying the Pearson correlation coefficient for interval-level data, and by the Spearman correlation coefficient for ordinal-level data. To evaluate the distribution of interval scale data, the Kolmogorov–Smirnov test was performed.³²

When analyzing the construct validity to determine convergent and divergent validity, the same hypothesis as posed by the authors for validation of the Lymph-ICF-LL questionnaire in English²³ was employed. In case of agreement between the Lymph-ICF-LL and SF-36, the domains were included to assess convergent validity. In case of disagreement, they were included in the hypothesis for assessing divergent validity.

The ICC, Cronbach alpha coefficient, and correlation coefficient were interpreted as follows: weak (<0.40), moderate (0.40–0.74), strong (0.75–0.90), and very strong (>0.90) [30]. The construct validity was defined as very good (>90% for the proved hypothesis), good (between 75% and 90% for the proved hypothesis), and moderate (between 40% and 74% for the proved hypothesis).³³

This study was approved by the Research Ethics Committee (number 814.262/2014). All participants signed a consent form setting out the terms of agreement before they were included in this study.

Results

The 30 participants with lower limb lymphedema (3 men and 27 women) were, on average, 52.1 years old (standard deviation = 11.3) with a body–mass index of 30.4 kg/m² (standard deviation = 8.5). Table 1 indicates the frequency of the variables related to the type of cancer and cancer treatment. Table 2 indicates the variables related to lymphedema.

Table 1.

Characteristics of the Participants with Lower Limb Lymphedema

Variables	N	%
Sex
Women	27	90
Men	3	10
Age, years
Average (±SD)	52.1 (11.3)
BMI at the physical examination (kg/m²)
Average (±SD)	30.4 (8.5)
Type of cancer
Cervical	8	26.7
Endometrial	9	30
Ovarian	6	20
Vulvar	2	6.6
Melanoma	5	16.7
Lymphadenectomy or sentinel lymph node biopsy
Yes	25	83.3
No	5	16.7
Chemotherapy
Yes	16	53.3
No	14	46.7
Radiotherapy
Yes	11	36.7
No	19	63.3

BMI, body–mass index; SD, standard deviation.

Table 2.

Characteristics of Lymphedema and Current Physical Therapy Treatment

Variables	N	%
Lymphedema
Difference of volume in mL (±SD)^a	942 (1100)
Mean duration of lymphedema	12.5 (110)
Affected side
Right	11	36.7
Left	12	40
Bilateral	7	23.3
Severity of lymphedema
Weak	27	90
Moderate	2	6.7
Strong	1	3.3
Current physical therapy treatment
Skin care
Yes	29	96.7
No	1	3.3
Manual lymph drainage
Yes	1	3.3
No	29	96.7
Compression bandages or low-stretch elastic stocking
Yes	29	96.7
No	1	3.3
Exercises of the extremities
Yes	27	90
No	3	10

Represents only the participants with unilateral lymphedema (13 participants).

SD, standard deviation.

Reliability

Table 3 indicates the ICC, Cronbach alpha coefficient, SEM, and SRD for the total score on Lymph-ICF-LL and the score on each question of Lymph-ICF-LL separately. The test–retest reliability was very strong (ICCs >0.90) for the total score of the questionnaire and the scores of all domains.

Table 3.

Reliability of the Total Score and Domain Scores of the Functioning, Disability and Health Questionnaire for Lower Limb Lymphedema (Lymph-ICF-LL) (N = 30)

Lymph-ICF-LL score	Test–retest		Consistency (α)	Variability (SEM)	Clinically important changes
Lymph-ICF-LL score	ICC	95% CI	Consistency (α)	Variability (SEM)	SRD	95% SRD
Total	0.96	0.92–0.98	0.96	5.9	16.4	−19.6 to 13.2
Physical function	0.91	0.82–0.96	0.92	5.4	14.9	−18.3 to 11.5
Mental function	0.92	0.84–0.96	0.93	6.2	17.1	−21.1 to 13.1
General tasks/household activities	0.92	0.83–0.96	0.92	7.6	21.2	−23.9 to 18.5
Mobility	0.92	0.82–0.96	0.91	6.5	17.9	−19.4 to 16.4
Life domains/social life	0.91	0.80–0.96	0.92	6.8	18.9	−25.7 to 12.1

Lymph-ICF-LL, Lymphedema Functioning, Disability and Health Questionnaire for lower limb lymphedema; ICC, intraclass correlation coefficient; CI, confidence interval; α, Cronbach alpha coefficient; SEM, standard error of measurement; SRD, smallest real difference.

For all 28 questions of the Lymph-ICF-LL, the test–retest reliability was strong or very strong for 25 of them (ICCs >0.75). The reliability of two questions (concerning participation in social activities with friends and the presence of skin infection) was moderate (ICCs = 0.66 and 0.67, respectively). To the question concerning the capacity of riding a bicycle, the reliability was weak and negative (ICC = −0.22), due to the negative mean covariance between the answers. In this specific question, only 6 participants indicated an answer, while 24 participants said that they had never performed this activity or did not apply to their cotitidan. The data regarding the reliability of each question of the Lymph-ICF-LL, were not presented.

The general internal consistency of scores of the Lymph-ICF-LL was considered very strong, with a Cronbach alpha coefficient of 0.96 for the total score and 0.91–0.96 for scores of the various domains.

The total score of Lymph-ICF-LL had variability (SEM) of 5.9 between tests. However, the SRD was 16.4 and the confidence interval of the SRD, 95%, ranged from −19.6 to 13.2. Therefore, a reduction in the total score on the Lymph-ICF-LL of 20 or more and an increase of 13 or more should be considered clinically relevant. The general tasks/household domain indicated major variability (7.6) and major SRD (21.2).

Validity

To 29 participants (97%), the scoring system (11-point scale) for the questions on the Lymph-ICF-LL was clear. One participant mentioned that it is necessary to provide space for justifying the symptoms in each question. In the case of 27 participants (90%), all complaints were referred on the Lymph-ICF-LL. One participant commented that there should be a question about skin changes (for example, dry skin). Another participant mentioned sexual dysfunction because of leg volume and weight. In addition to these aspects, one participant mentioned burning and paresthesia in the limb with lymphedema.

Two questions concerning the mobility domain from the Lymph-ICF-LL require attention: 80% (24) and 83.3% (25) of participants marked “not applicable” for questions 20 (ride a bike) and 21 (drive a car), respectively, as they had never performed any of these activities.

Moreover, in five questions of the life domains/social life domain, many participants answered that these questions did not apply to their lives or that they have never done any of them. Only 43.3% (13) of participants answered the question related to the whether they can fulfill their job, 60% (12) said that they have never practiced sports, 23.3% (7) did not carry out any leisure-time activities or did not go out on holidays, and 13.3% (4) did not participate in social activities with friends.

Table 4 indicates the Pearson correlation coefficients of various domains of Lymph-ICF-LL and SF-36 and their p values. All data had normal distribution. Concerning convergent validity, all domains of the Lymph-ICF-LL were significantly correlated with the expected corresponding domains of SF-36. The correlation coefficient ranged from −0.69 to −0.84 (moderate to strong correlation), with p-values <0.01. Thus, all five hypotheses to assess the convergent validity were accepted. Concerning divergent validity, the domains of Lymph-ICF-LL were moderately correlated with the domains of SF-36. The correlation coefficient ranged from −0.60 to −0.73, with p-values <0.01. Therefore, all five hypotheses to assess divergent validity were not substantial.

Table 4.

Correlation Between the Values of the Domains of the Lymph-ICF-LL and SF-36 (n = 30)

SF-36 domain	Pearson correlation coefficient (P)
	Lymph-ICF-LL domains
	Impairment in function		Activity limitations and participation restrictions
	Physical function	Mental function	General tasks/household activities	Mobility	Life domains/social life
Physical functioning	−0.71 (<0.01)	−0.73 (<0.01)	−0.79 (<0.01)	−0.84 (<0.01)	−0.80 (<0.01)
Role—physical	−0.74 (<0.01)	−0.69 (<0.01)	−0.82 (<0.01)	−0.79 (<0.01)	−0.79 (<0.01)
Bodily pain	−0.72 (<0.01)	−0.69 (<0.01)	−0.66 (<0.01)	−0.67 (<0.01)	−0.64 (<0.01)
General health	−0.35 (0.06)	−0.46 (0.01)	−0.42 (0.02)	−0.37 (0.05)	−0.39 (0.04)
Vitality	−0.67 (<0.01)	−0.73 (<0.01)	−0.76 (<0.01)	−0.75 (<0.01)	−0.73 (<0.01)
Social functioning	−0.67 (<0.01)	−0.69 (<0.01)	−0.76 (<0.01)	−0.63 (<0.01)	−0.69 (<0.01)
Role—emotional	−0.65 (<0.01)	−0.72 (<0.01)	−0.66 (<0.01)	−0.55 (<0.01)	−0.60 (<0.01)
Mental health	−0.65 (<0.01)	−0.70 (<0.01)	−0.60 (<0.01)	−0.67 (<0.01)	−0.68 (<0.01)

SF-36, 36-Item Short Form Health Survey Questionnaire.

Discussion

The Lymph-ICF-LL is the first specific instrument translated and adapted to Brazilian Portuguese with a great number of individuals with secondary lymphedema after cancer treatment. Its psychometric evaluation was satisfactory when applied to the Brazilian population.

The questionnaire Lymph-ICF-LL was translated and validated before for the Chinese population²⁴ and German population²⁵ in addition to validation for the Dutch population.²³ Following these studies, the reliability of Lymph-ICF-LL was good for the individual with lower limb lymphedema. In the case of test–retest reliability, the Brazilian questionnaire obtained better results than the questionnaires validated for Dutch, German, and Chinese populations.

Unlike the Dutch study,²³ in which the domains of mental function and life domains/social life obtained ICCs classified as strong (0.87 and 0.81, respectively), in this study, all domains had very strong ICC values (≥0.90). The ICC for the total score on the questionnaire was very strong in both populations.

In the German population,²⁵ except for the domain, general tasks/household, which obtained weak correlation (0.36), the other domains had moderate to very strong correlation (0.54–0.95). In the Chinese population,²⁴ ICC values for all domains were classified as strong (0.80–0.84), except the domain, mental function, which obtained moderate correlation (0.55). The test–retest reliability for the total score on the questionnaire was moderate (0.67) and strong (0.90) for the German and Chinese populations, respectively.

Concerning internal consistency, the Brazilian Portuguese questionnaire obtained Cronbach alpha coefficients that were very strong for the total score (0.96) and all domains (0.91–0.93), similar to the results in the Dutch²³ and Chinese²⁴ questionnaires (coefficients 0.89–0.97 and 0.85–0.95, respectively). However, the German questionnaire²⁵ indicated an internal consistency between 0.23 and 0.88 (weak and strong) due to lack of many values, which compromised its calculation.

Following the study by Devoogdt et al.,²³ the variability and clinically important changes were evaluated. In the two questionnaires, the SEM and SRD for the total score and for the score on each domain were similar. The questionnaires validated for German²⁵ and Chinese²⁴ populations did not analyze the SEM and SRD.

Regarding face validity, the results were similar to the questionnaires validated for the Dutch and German populations²⁵ concerning the clarity of the scoring system. Whereas 97% of Brazilian participants considered the scoring system clear, for the Dutch population, the frequency was 90%, and for the German population, it was 100%. Concerning the data about the scope of the questions, the result of this study was the same as for Dutch patients²³ (90%); however, it was 77.3% for the German patients.²⁵

In this study, one participant mentioned that there should be space to justify their symptoms beside each question. In this case, the health professional understood the importance of understanding the questions on the questionnaire and left space to record patients' complaints. Other patients said that there should be questions about skin changes, sexual dysfunction, and symptoms of burning and paresthesia in the lower limb with lymphedema. In the study that assessed the incidence and intensity of symptoms and angst in patients with lower limb lymphedema, questions about dry and peeling skin and feeling of burning and paresthesia in the limb, as well as questions about impaired sexual activity and sexual interest, for instance, were prevalent.²¹ Therefore, it clearly indicates the importance of inquiring at the end of the questionnaire whether the patient has any more symptoms/complaints related to lymphedema.

Concerning the construct validity, the current results were better than the Dutch study²³ for convergent validity. The correlation coefficient in the Dutch study ranged from −0.46 to −0.86 (moderate to strong correlation), with p-values <0.01, whereas for Brazilian patients, the correlation ranged from −0.69 to −0.84 (moderate to strong correlation), with p-values <0.01. For the German population,²⁵ the convergent validity could also be deduced in almost all correlations, but some hypotheses showed weak or null correlation.

For the divergent validity, none of the hypotheses could be deduced as the correlation on the hypotheses ranged from −0.60 to −0.73 (moderate correlation) with p-values <0.01. In the study by Devoogdt et al.,²³ the domains of Lymph-ICF-LL were not significantly correlated with the expected corresponding domains of SF-36, ranging from 0.04 to −3.32 (weak to null correlation), with p-values ranging from 0.08 to 0.83. The results for the Brazilian population were similar to the German population,²⁵ in which it was not feasible to assess the divergent hypotheses since the 95% confidence intervals of correlations included moderate to very strong correlations.

Strengths and limitations of the study

This study has several strengths. First, there was a good understanding of all questions on the questionnaire, and the majority of the participants considered that the instrument comprised all aspects related to lymphedema. Second, different aspects of reliability and validity of the Brazilian version of Lymph-ICF-LL were assessed, obtaining remarkable results. Moreover, the sample in this study comprised 30 participants, following the recommendations of including at least 30 heterogeneous participants for reliability studies.³³

The population in this study was heterogeneous as participants with various types of cancers and with lymphedema prevalence (ranging in months and volumes) were considered. In addition, the validation of Lymph-ICF-LL for the Brazilian population followed the same process of validation of the original questionnaire for the Dutch population.

However, the study also had potential limitations. The majority of the patients were women with gynecological cancer, thus it might limit its applicability to other populations, for instance, men with prostate cancer or patients with primary lymphedema. Moreover, another limitation was exclusion of patients with visual or cognitive impairment, which could interfere in reading or understanding the questionnaire. Those patients were excluded based on the perception that they would be unable to fully understand all questions, thus limiting the generalization of the results to all patients with lower limb lymphedema. It is worth mentioning that moderate/severe lymphedema prevalence was weak, therefore also limiting assessment by this instrument.

Conclusion

The Brazilian version of Lymph-ICF-LL is a reliable and valuable instrument to assess the problems related to functioning and experiences derived from secondary lower limb lymphedema after cancer treatment. The Brazilian patients considered the instrument easy to understand, and according to the results of this study, it is recommended to use the Brazilian version of Lymph-ICF-LL in addition to clinical research.

Footnotes

Acknowledgments

The authors are very grateful to the hospital collaborating in this study. The authors also extend their thanks to the study participants.

Authors' Contributions

All authors contributed to the conception and/or planning of the study. They contributed to collecting, analyzing, and/or interpreting data, as well as writing and/or critically revising the manuscript. All authors critically revised the article for important intellectual content and approved the final version of the article.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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