The Comparative Frequency of Breast Cancer-Related Lymphedema Determined by Perometer and Circumferential Measurements: Relationship with Functional Status and Quality of Life

Abstract

Background:

The aim of this study was to comparatively determine the frequency of breast cancer-related lymphedema (BCRL) by using prospective monitoring with perometer and circumferential measurements in a group of patients who underwent breast cancer surgery. We also aimed to evaluate the relationship between volume changes and functional status and quality of life (QoL) in patients with breast cancer-related subclinical lymphedema.

Materials and Methods:

Patients who had unilateral breast cancer surgery for breast were assessed with circumferential and perometer, respectively, for volumes at baseline, 3rd-month, 6th-month, 9th-month, and 12th-month by the same physiotherapist. Every patient was informed about lymphedema symptoms and prevention. The demographic and clinical properties were recorded. Functional status and QoL were evaluated by Q-DASH and the Lymphedema Quality of Life Questionnaire-Arm questionnaires.

Results:

A total of 101 female patients with a mean age of 49.02 + 10.59 years completed the 12-month follow-up. Most of the patients were overweight, had an axillary dissection in addition to breast surgery, and received radiotherapy. The frequency of subclinical and clinical BCRL at the end of 12 months was determined by 34.7% and 23.8% with circumferential measures and perometer, respectively. QoL and functional scores did not differ between patients with and without subclinical lymphedema.

Conclusion:

Introduction

Breast cancer is the most common type of cancer among women worldwide, and more than two million new cases are diagnosed annually.¹ Its incidence and mortality rates are gradually increasing in developing countries, including Turkiye.² With improved surgical procedures and enhanced effectiveness of breast cancer treatment, the number of breast cancer survivors is growing dramatically, and a significant number of women are dealing with the potential complications of treatment including breast cancer-related lymphedema (BCRL).^1–3

BCRL is characterized by the abnormal accumulation of excess water and plasma proteins, as well as extravascular blood and parenchymal cells in the affected upper and lower arm, chest, and trunk, due to the insufficiency of lymphatic transport capacity.⁴ More than 20% of women diagnosed with breast cancer develop BCRL.⁵

BCRL may manifest initially as transient swelling in the ipsilateral arm, breast, or trunk; it can chronically progress to irreversible fibrosis and interstitial hypertrophy.^5,6 It is associated with symptoms like pain, heaviness, tightness, decreased range of motion, adversely affected gross and fine motor skills, impaired daily function, depression, and decreased quality of life as well as causing substantial financial burdens to patients, caregivers, payers, and society.^6–8 BCRL carries a lifelong risk for breast cancer survivors, although there are a limited number of long-term follow-up studies.⁹ Early detection and treatment of BCRL can prevent progression to its chronic stage, eliminating morbidity and the need for more complicated treatments.

Fortunately, awareness of lymphedema has increased in recent years, and patients who have undergone breast surgery are referred to oncologic rehabilitation units of the Physical Medicine and Rehabilitation departments in the early period. However, there is significant variability in lymphedema measurement techniques. The best practice guidelines do not recommend a particular screening strategy, emphasizing only the importance of prevention, baseline measurements, regular follow-up, and patient education.¹⁰

There is no single tool to assess BCRL, but there are various objective tools and more subjective clinical examination methods. Among objective measurement instruments, perometer and circumferential tape measurements are both commonly used for volumetric measurement of lymphedema.^3,11 Perometer utilizes a frame of infrared light beam-receiver pairs to measure limb outline with sub-centimeter definition and thus derive limb volume by the disc model method.¹² Its advantages are being quick, accurate, and highly reproducible, but it is costly and difficult to access. In contrast, tape measurement is inexpensive and easily accessible but is time-consuming with inconsistent inter- and intra-rater reliability.^3,11

The aim of this study was to comparatively determine the frequency of subclinical and clinical lymphedema by using prospective monitoring with perometer and circumferential measurements in a group of patients who underwent breast cancer surgery. We also aimed to evaluate the relationship between volume changes and functional status and quality of life (QoL) in patients with BCRL.

Materials and Methods

Study sample

Female patients who underwent surgery for breast cancer were included in this prospective comparative cohort study. Patients were first evaluated by oncology doctors and then referred to the oncologic rehabilitation unit of Physical Medicine and Rehabilitation Hospital in Ankara City Hospital just after oncologic surgery. Patients were recruited consecutively.

This study was approved by the local ethics committee, and written informed consent was obtained from all participants. The study met the requirements of the Declaration of Helsinki and was approved by the Institutional Ethics Committee of Ankara City Hospital.

The inclusion criteria were as follows: (1) age 18 and over and (2) having unilateral breast cancer surgery. Patients were excluded according to the following criteria: (1) patients with a history of contralateral breast cancer surgery, (2) patients with other malignant disorders (5) patients having musculoskeletal or venous disorders on the affected arm which may simulate or mask symptoms of lymphedema, (6) patients having renal and/or heart failure, (7) pregnancy, (8) immobile patients, and (9) patients with cognitive or neurological disorder.

Demographic and clinical characteristics of the patients including age, body mass index (BMI), education status, marital status, occupation, regular exercise habits, and lesion site were recorded. Breast cancer treatments, type of surgery, histopathological diagnosis, type and stage of cancer (TNM staging: 0–4), adjuvant treatments such as radiation therapy, chemotherapy, or hormonal therapy, and duration of lymphedema were noted in all patients.

BMI was classified as normal (18.5–24.9), overweight (25–29.9), and obese (≥30).¹³ Every patient was informed about BCRL symptoms and prevention.

Volume measurements

Upper limb volumes were assessed with circumferential and perometer measurements, respectively, for volumes at baseline, 3rd month, 6th month, 9th month, and 12th month by the same physiotherapist, in the same place.

For circumferential measurements, subjects sat straight on a chair with their arms relaxed by their sides and elbows straight. Circumferential measurements were performed by a standard 1-inch retractable tape, starting at the level of the ulnar styloid, at 4 cm intervals along the arms, and converted to an approximate arm volume to enable estimation of volume.^4,14 Calculation of the limb segment volumes (millimeters) was undertaken using a simplified truncated cone formula. Excess limb volume comparing affected and unaffected limbs and the difference in excess volume (The excess limb volume is expressed as a percentage of the unaffected limb volume, indicating how much larger the affected limb is compared to the unaffected limb) were calculated. The threshold for subclinical lymphedema was determined as >5% excess-volume difference compared to unaffected arm and the threshold for clinical lymphedema was determined as >10% excess-volume difference compared to unaffected arm.¹⁵

Upper limb volumes were also measured using an optoelectronic perometer (Pero-System 350 NT Messgeräte GmbH, Wuppertal, Germany), which was connected to a personal computer. For measurement, the patient sat on the seat of the perometer with one limb inside and the other outside the frame. Infrared light transmitters located on two sides of the frame project light toward photosensors on the opposing two sites, and the limb effectively blocks the transmission of the light from one side of the frame to the other, creating an electronic image. As the frame is moved along the limb, a series of images are recorded every 0.5 cm, creating limb size and volume on the computer using the Peroplus 2000 Software (Pero-System Messgerate GmbH). Computer software allowed for the analysis of volume and excess volume at any stage of measurement.^12,14 For the perometric measurement method, the threshold for subclinical lymphedema was determined as a 100 mL volume difference compared to the unaffected arm, and the threshold for clinical lymphedema was determined as a 200 mL volume difference compared to the unaffected arm.¹⁶

QoL assessments

Quality of life was assessed by the Turkish version of the Lymphedema Quality of Life Questionnaire-Arm (LYM-QoL-Arm).¹⁷ The LYM-QoL-Arm has been developed by Keeley et al. to assess the impact of lymphedema of the arms on the QoL of the patients. It consists of four domains with 28 items. These domains are function, appearance, symptoms, and mood. The answers were evaluated on a four-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. The ‘overall QoL’ item was scored 0–10.¹⁸

Functional assessments

Functional disability of the affected extremity was evaluated using the quick Disability of Arm, Shoulder, and Hand questionnaire (Q-DASH).¹⁹ It is a self-report questionnaire evaluating the patients’ symptoms and functional tasks associated with limitations of the arm, shoulder, and hand. It is validated for the Turkish population with upper limb problems. It contains 11 items and results in a score ranging from 0 to 100 with higher scores indicating more functional disability.²⁰

Outcome measures

The difference in volumes, excess volumes, QoL, and functional assessment scores were evaluated at baseline, 3rd month, 6th month, 9th month, and 12th month in all patients.

Statistical analyses

Descriptive statistics were used to examine the frequency distributions and calculate the scores of scales and subscales, and defined with either mean ± standard deviation, median, or percentage values. The continuous variables have been tested for normal distribution using the Shapiro–Wilk test. Whether the categorical variables differed between groups was investigated by the Chi-square test or the Fisher exact test. Differences between two independent groups in terms of numerical variables were investigated with the independent samples t-test and Mann–Whitney U test. All tests of statistical significance were two-sided and considered statistically significant at p < 0.05. Analyses were conducted by SPSS 22.0 statistical package.

Results

From 188 patients included at the beginning of the study, 101 patients with a mean age of 49.02 ± 10.50 years completed the 12-month follow-up. Out of 188 patients at the beginning, 31 patients did not come to visits after the first evaluation, 47 patients were lost to follow-up, 6 patients changed the hospital, 2 patients moved to another city, and 1 patient died.

The total frequency of subclinical lymphedema and clinical lymphedema at the end of 12 months was determined by 34.7% and 23.8% with circumferential measures and perometer, respectively.

Most of the patients were overweight (31.7%) and obese (38.6%), had axillary dissection in addition to breast surgery (65.3%), and received radiotherapy (76.24%) and chemotherapy (86.14%). 15.8% of the patients were illiterate, and 17.8% of the patients had high school education. 95% of the patients did not have a regular exercise habit. Demographic and clinical characteristics of patients are shown in Table 1.

Table 1.

Demographic and Clinical Characteristics of Patients

Age (years) (mean±SD)	49.02 ± 10.59
Body mass index (kg/m²) (mean±SD)	28.72 ± 5.16
Normal	28 (27.7%)
Overweight	32 (31.7%)
Obese	39 (38.6%)
Morbid obese	2 (2%)
Education
Illiterate	16 (15.8%)
Primary school	53 (52.5%)
High School	18 (17.8%)
University	12 (11.9%)
Master’s degree	2 (2%)
Smoking
Yes	11 (10.9%)
No	89 (88.1%)
Exsmoker	1 (1%)
Exercise habit
Yes	5 (5%)
No	96 (95%)
Type of surgery
Radical mastectomy	15 (14.9%)
Modified radical mastectomy	19 (18.8%)
Lumpectomy	67 (66.3%)
Neoadjuvant therapy
Yes	32 (31.7%)
No	69 (68.3%)
Radiotherapy treatment
Yes	87 (86.14%)
No	14 (13.86%)
Chemotherapy treatment
Yes	77 (76.24%)
No	24 (23.76%)
Axillary dissection
Yes	66 (65.3%)
No	35 (34.7%)
Number of lymph nodes dissected (mean±SD)	8.68 ± 5.95
Number of positive lymph nodes (mean±SD)	1.75 ± 3.12

Patients with lymphedema were older in both circumferential and perometric measurement groups, but the differences did not reach a statistically significant level (p = 0.325, p = 0.409, respectively). Higher BMI was associated with the presence of lymphedema in perometric measurement group but not in the circumferential measurement group (p = 0.05, p = 0.702, respectively).

Patients with and without lymphedema diagnosed by perometer had similar scores in appearance, symptoms, mood, and overall domains of QoL questionnaire and Q-DASH questionnaire both at baseline and at 5th control. Patients with lymphedema had higher scores in the functional domain of QoL questionnaire at baseline; however, there was no statistical significance in the 5th control. Comparison of functional scores and QoL scores in patients with and without lymphedema diagnosed by perometer at baseline and 5th controls are shown in Table 2.

Table 2.

Comparison of Quality of Life of Patients with and Without Breast Cancer-Related Lymphedema Diagnosed by Perometer

	BCRL(+) (n = 24)	BCRL(−) (n = 77)	p value
LYM-QoL-Arm Function
Baseline	1.50 ± 0.45	1.32 ± 0.34	0.036
5th control	1.55 ± 0.37	1.58 ± 0.45	0.725
LYM-QoL-Arm Appearance
Baseline	1.10 ± 0.28	1.05 ± 0.22	0.411
5th control	1.08 ± 0.18	1.07 ± 0.20	0.754
LYM-QoL-Arm Symptom
Baseline	1.83 ± 0.66	1.62 ± 0.54	0.118
5th control	1.74 ± 0.61	1.78 ± 0.58	0.752
LYM-QoL-Arm Emotion
Baseline	1.67 ± 0.48	1.75 ± 0.71	0.626
5th control	1.59 ± 0.56	1.83 ± 0.80	0.175
LYM-QoL-Arm Overall
Baseline	6.42 ± 1.10	6.77 ± 1.28	0.230
5th control	6.96 ± 1.04	6.95 ± 1.19	0.970
Q-DASH
Baseline	29.81 ± 20.15	21.12 ± 13.44	0.017
5th control	28.11 ± 12.82	27.74 ± 14.33	0.910

(mean±SD).

BCRL, breast cancer-related lymphedema; LYM-QoL-Arm, the Lymphedema Quality of Life Questionnaire-Arm; Q-DASH, the quick Disability of Arm, Shoulder, and Hand questionnaire.

Similarly, patients with and without lymphedema diagnosed by circumferential measurements had similar scores in all domains of QoL questionnaire and Q-DASH questionnaire both at baseline and at 5th controls. These results are shown in Table 3.

Table 3.

Comparison of Quality of Life of Patients with and Without Breast Cancer-Related Lymphedema Diagnosed by Circumferential Measurements

	BCRL(+) (n = 35)	BCRL(−) (n = 66)	p value
LYM-QoL-Arm Function
Baseline^*	1.30 ± 0,43	1.39 ± 0.34	0.240
5th control^*	1.57 ± 0.35	1.58 ± 0.48	0.938
LYM-QoL-Arm Appearance
Baseline^*	1.08 ± 0.24	1.06 ± 0.24	0.644
5th control^*	1.07 ± 0.15	1.08 ± 0.21	0.816
LYM-QoL-Arm Symptom
Baseline^*	1.58 ± 0.58	1.71 ± 0.57	0.256
5th control^*	1.84 ± 0.63	1.75 ± 0.56	0.447
LYM-QoL-Arm Emotion
Baseline^*	1.86 ± 0.75	1.66 ± 0.60	0.137
5th control^*	1.73 ± 0.69	1.80 ± 0.79	0.682
LYM-QoL-Arm Overall
Baseline^*	6.60 ± 1.12	6.73 ± 1.31	0.626
5th control^*	7.03 ± 0.82	6.91 ± 1.30	0.622
Q-DASH
Baseline^*	24.66 ± 19.22	22.40 ± 13.46	0.492
5th control^*	27.64 ± 13.58	27.93 ± 14.21	0.922

(mean±SD).

Discussion

In our study, the frequency of lymphedema detected by circumferential measurements was higher than the frequency of lymphedema detected by perometer. In line with the literature, most of the patients were overweight and obese, had axillary dissection in addition to breast surgery, and received radiotherapy.^3,5,9,21 Women with mild lymphedema are three times more likely to have moderate or severe lymphedema than women without lymphedema.⁵ Therefore, it is essential to detect subclinical and clinical BCRL at the earliest time possible.

Various objective methods together with clinical examination are used in the assessment of BCRL. The use of these measures depends on institutional preferences and the availability of equipment. The lack of standardized methods and protocols for the evaluation of lymphedema has limited the determination of BCRL incidence and treatment outcomes. Objective measures of BCRL include bioimpedance spectroscopy, perometer, circumferential tape measurement, and water volumetry, all of which have different advantages and disadvantages.²² Newer modalities like perometer and bioimpedance spectroscopy have received increased attention in recent years. However, in routine clinical practice, many centers continue to use the more economical and accessible alternative of circumferential tape measurement.

Perometer uses an infrared optoelectronic device that can measure the volume of the swollen limb and then compare it to the healthy limb. The perometer works using infrared scanning to calculate the circumference of multiple areas of the limb, creating a three-dimensional image of the limb, with the limb volume calculated in milliliter.¹² Perometer has been shown to be a reliable and validated method for the measurement of lymphedema. However, the high cost of the optoelectric perometer limits its use in most clinical settings.^11,22 Circumferential tape measurement is economical and easily accessible but is time-consuming.^3,22

In our study, subclinical and clinical BCRL were detected in a higher percentage of patients by circumferential measurements than by perometer. Sun et al. found that there was no difference in total arm volume comparing circumferential measurement techniques to perometer in patients with BCRL.²³

In a meta-analysis, data from 83 studies were collated, in which different methods were used for the evaluation of lymphedema; circumference measurement was found to be the most frequently used method (38 studies), followed by questionnaires (19), perimetry (17), and bioelectric impedance analysis (3).⁵ In another more recent meta-analysis that included the results of five studies, circumference measurement was also found to be the most frequently used method (33 studies), followed by water displacement (20). Other methods were also noted, but they were less frequently used.²⁴

We think that circumferential tape measurement is still the most important measurement method for BCRL. Circumferential tape measurements give good results as long as they are applied carefully in an appropriate environment by the same person as we did in our study. Significantly higher BMI of lymphedema patients in perometric measurement group may have contributed to our results. Adriaenssens et al. compared perometer, water displacement, and volumetric circumferential measurements in a cohort of patients with varying degrees of BCRL. They suggested that scientific research and multidisciplinary clinical approaches may benefit from the use of the perometer, compared to the other arm volume evaluation tools for BCRL considering its ease of use, reproducibility, and volume calculations not at the extreme of all measurement methods, and circumferential measurements can also be used by private practices because they diagnose the same amount of BCRL patients.²⁵

BCRL impairs QoL, decreases physical functioning, and affects psychosocial well-being.^7,26 In our study, QoL and functional scores did not differ between patients with and without BCRL. These results may be related to a relatively small sample size, and patients may be prepared for symptoms of BCRL, which is an important goal of patient education. We informed all patients about the symptoms and triggers of BCRL starting from the first visit. A recent review on advances in the prevention and treatment of BCRL highlighted the importance of patient education, which many breast cancer survivors report they do not receive adequately, for the purpose of early surveillance and timely management aimed at reducing the incidence and progression of BCRL.¹¹ Also lymphedema symptoms may be mild at the beginning of the disease. The patients in our study have routinely visited the oncology and Physical Medicine and Rehabilitation departments. Upper extremity function and QoL may be worse in patients who do not regularly follow their doctor’s visits. A recent multinational guideline recommends screening for breast cancer-related lymphedema (BCRL) within 3 months following surgery, with subsequent assessments conducted every 3–4 months during the first year. After the initial year, screenings should be repeated every 6–12 months for at least 24 months post-surgery.²⁷

To the best of our knowledge, this is the first prospective study examining the prevalence of BCRL in this country with a 12-month follow-up. The limitations of our study include a relatively small sample size, a single-center design, and a follow-up period of only one year. Nevertheless, our study contributes to the existing literature by comparing two commonly used measurement methods for assessing lymphedema. Further studies with longer follow-up periods are needed to gain a more comprehensive understanding of the chronicity of this condition.

Conclusion

After the first 12 months after surgery, the frequency of BCRL assessed by circumferential measurements was higher than the frequency assessed by perometer. Periodic monitoring of women with breast cancer for the presence of lymphedema, preferably by the same person together with conservative interventions, is suggested in order to allow early detection and timely intervention for BCRL. Conservative interventions for the prevention of BCRL after breast cancer treatment include regular exercise, weight management, the use of compression garments, patient education, and techniques such as manual lymphatic drainage and skin care, all of which have been shown to reduce the risk or severity of lymphedema.^9–11

Footnotes

Authors’ Contributions

G.M.C.: Conceptualization, methodology, investigation, data curation, writing—original draft, supervision, P.B.: Methodology, investigation, data curation, writing—original draft, C.S.P.: Methodology, validation, formal analysis, investigation, A.Y.: Formal analysis, data curation, writing original draft preparation, G.U.: Methodology, investigation, D.U.: Methodology, investigation, supervision, S.K.: Methodology, investigation, M.D.: Investigation.

Author Disclosure Statement

The authors declare that they have no conflicts of interest.

Funding Information

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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