The Effect of Education on Upper Extremity Function in Patients with Lymphedema after Breast Cancer Treatments

Abstract

Background:

The aim of this study was to evaluate the effects of education on the upper extremity functions of patients with lymphedema (LE) after breast cancer treatments.

Methods:

Thirty-eight patients with LE after breast cancer treatments participated in the study. The patients were separated into two groups. Group 1 (n = 19) was educated about the causes and symptoms of LE and the methods for minimizing complications from LE, such as skin care, changes that must be made in daily life activities, exercises, and protective clothing. Group 2 (n = 19) was treated through standard means (surgical, chemotherapy, radiotherapy). A universal goniometer was used to assess the range of motion of the upper extremity of the patients. The Disabilities of the Arm, Shoulder and Hand questionnaire (DASH) and the Shoulder Pain and Disability Index (SPADI) were used to assess shoulder function. The measures were carried out once by the same physiotherapist. The chi-square and Mann–Whitney U tests were used to analyze the data.

Results:

Group 1, educated about LE, performed better than the other group in shoulder flexion range. When shoulder abduction, internal–external rotation, and elbow flexion motions were compared by using the DASH and SPADI, no significant difference was observed between the groups (p > 0.05). However, when shoulder function was compared, Group 1 was better. There was no significant difference between the groups when the severity of LE was compared.

Conclusion:

This study underscores the need to develop and implement strategies for LE prevention and education for all breast cancer patients.

Introduction

Breast cancer is the most common type of cancer among women, and more people are diagnosed every day. On average, one out of eight women worldwide is at risk of developing breast cancer.¹ Breast cancer in women represented 24.4% of all cancer cases in 2004, 23.3% in 2005, and ranked first with 23.7% in 2006, according to an article published by the Ministry of Health, Turkey.²

Arm lymphedema (LE) has long been recognized as a complication of surgical treatment or radiotherapy of the axilla for breast cancer. Approximately 5% to 42% of patients with breast cancer develop LE following treatment.³ LE is a chronic and progressive condition resulting from an abnormality of or damage to the lymphatic system.⁴ Any reduction in the capacity of the lymphatic system to drain fluid from the interstitium and return it to the blood circulation will cause fluid to build up in the skin and subcutaneous tissues of the affected part of the body. LE may be one of several arm symptoms that adversely affect quality of life and functional status; other impairments may result from muscle, tendon, or ligamentous damage as a consequence of treatment. Delaying intervention in reducing LE may result in poor quality of life and greater emotional distress.^3–5

Patients require optimal upper extremity function to carry out routine daily activities and to return to work.⁶ The most common and life-limiting problems after breast cancer treatment are related to the upper extremities. Most patients who have undergone axillary dissection and breast cancer surgery have reported at least one upper extremity problem.⁷ LE may cause limb swelling, heaviness, pain, pitting of skin, tightness or hardness in the limb, inflammation, and reduced mobility in the shoulder and arm. Breast cancer patients with LE are more adversely affected by the functions of the upper extremity following the treatment.⁸

LE requires lifelong attention.⁹ However, there are not enough studies about the importance of educating patients who develop LE after breast cancer treatment. Patient education focusing on risk-reduction strategies holds great promise. More studies are needed in this area. Therefore, this study was designed to assess the impact that education can have on upper extremity functions in patients who develop LE after breast cancer treatment.

Methods

This study involved 38 women who developed LE after breast cancer treatments. They had completed cancer therapies, including surgery, radiotherapy, and chemotherapy, and had stopped all medical treatments at least 3 months before the beginning of the study.

The women included in the study were classified by degree of LE symptoms, that is, mild, moderate, or severe. Women were ruled ineligible according to the following exclusion criteria: severe pain in the axillary node dissection scar; severe cardiac disease; uncontrolled hypertension; malignant LE; recurrent cancer or infection in the arms; disorders related to muscles or joints; difficulties in participating in the study; and irregular attendance. All participants were informed about the study purpose and procedures.

Study design

This study was planned as cross-sectional and prospective. Two open-ended questions were asked to determine the education levels of the LE patients.

The first question was “Have you received information about LE from any healthcare professional (doctor, physiotherapist, nurse)? If yes, from whom? Explain the information you received.” Patients who answered yes to the first question were included in the group that was educated about preventative measures (Group 1). If the answer was no, the second question was asked: “Have you ever obtained any information about the proposed reduction of risk factors for lymphedema?” Patients who answered no were included in the group who received standard care for LE (Group 2).

Ethical approval

All procedures involving human participants were in accordance with institutional and national guidelines and the Declaration of Helsinki, 1975, revised in 2007 (approved by the Clinical Research Ethics Committee of Dokuz Eylul University School of Medicine; March 3, 2011; protocol no: 70-GOA; decision no: 2011/06-22).

Assessments

At the time of enrollment, a complete history was obtained from each woman, including the type and side of the operation; the number of excised axillary lymph nodes; the results of a sentinel lymph node biopsy; the number of tumor-positive lymph nodes; the radiotherapy technique used; the presence and type of systemic adjuvant treatment; the duration of LE; and the previous episodes of infections and complications (radiation-induced brachial plexopathy, erysipelas, etc.).

All assessments were performed by the same physiotherapist.

Arm mobility

An experienced physiotherapist assessed arm mobility with standard universal goniometry. Flexion–extension, abduction–adduction, external–internal rotation of the shoulder, and flexion–extension of the elbow and wrist were measured. Three positions (sitting, supine, and prone) were used for measurements. The tests were performed three times, according to the literature,¹⁰ and with respect to minimum pain threshold. The mean of the three measurements was taken as the reference value. Based on the clinical examination, a reduced range of motion of greater than or equal to a 25° difference between the affected side and the unaffected side was defined as impaired mobility.

Circumference measurement

Edema of the arm was assessed by circumference measurements. A standard 1-in retractable fiberglass tape measure was used to perform the circumference measurements. Subjects were measured while in a supine position with their arms relaxed by their sides and elbows straight. Both arms were measured at each test date. The circumference was measured every 5 cm beginning at the third phalanx nail fold and continuing 45 cm proximally. All measurements were recorded in centimeters. The severity of LE was classified according to a modification of the original definitions of the American Physical Therapy Association. Circumference differences less than 3 cm between arms were defined as mild, differences of 3–5 cm were defined as moderate, and differences greater than 5 cm were defined as severe.¹¹

Volumetric measurement

The volume of the arm was measured by water displacement. The arm was placed in a water-filled cylinder, and the overflowing water was measured. Both arms were measured, and the difference was calculated. Subjects were instructed to lower the arm slowly into the volumeter and stop when the top of the volumeter came in contact with the axilla. At this point, a rod was placed at the level of the second and third finger web space. This rod became the stopping point that determined the depth of immersion for repeated measurements. All measurements were recorded in milliliters. Volume differences less than 250 mL between arms were defined as mild, differences of 250–500 mL were defined as moderate, and differences greater than 500 mL were defined as severe.^12,13

Shoulder Pain and Disability Index

The Shoulder Pain and Disability Index (SPADI) consists of two dimensions (pain and disability), with a total of 13 questions. The pain dimension consists of five questions pertaining to severity. Disability is assessed with eight questions designed to measure the degree of difficulty an individual has with the various activities of daily living that require the use of the upper extremities. To answer the questions, the patients placed a mark on a 10-cm visual analog scale for each question. Verbal anchors for the pain dimension were “no pain at all” and “worst pain imaginable” and those for the disability dimension were “no difficulty” and “so difficult it requires help.” Scores from both dimensions were then averaged to derive a total percentage score. Higher scores reflected more pain and greater disability.¹⁴

The Disabilities of the Arm, Shoulder and Hand

The Disabilities of the Arm, Shoulder and Hand (DASH) questionnaire was used to determine the functional level of the upper extremities. It consists of a 30-item disability/symptom scale that asks about a patient's health status during the preceding week. The items ask about the degree of difficulty in performing various physical activities because of an arm, shoulder, or hand problem (21 items); the severity of each of the symptoms of pain, activity-related pain, tingling, weakness, and stiffness (5 items); and the problem's effect on social activities, work, and sleep and its psychological impact (4 items). Each item had five response choices, ranging from “no difficulty or no symptom” to “unable to perform activity or very severe symptom,” and was scored on a 1- to 5-point scale.

The DASH scores for all items were then used to calculate a scale score ranging from 0 (no disability) to 100 (most severe disability). The score for the disability/symptom scale is called the DASH score. A Turkish validity and reliability study of DASH was performed by Düger et al.¹⁵

Statistical analysis

Data were analyzed in the SPSS 16.0 program. Descriptive statistics were summarized as frequencies and percentages for categorical variables. Continuous variables were presented as the mean and standard deviation where normally distributed. Descriptive data were determined by the Mann–Whitney U test, and categorical variables were analyzed using the chi-square test. A p-value of less than 0.05 was considered statistically significant.

Results

Demographic data for both groups are presented in Table 1. We initially enrolled 43 patients, but one subject withdrew from the study because of breast cancer recurrence; two subjects withdrew from the study because of muscle disorders; and two subjects declined to participate in the study. This allowed data collection from 38 patients.

Table 1.

Demographic Features

	Group 1, n = 19	Group 2, n = 19
Age (years) (mean ± SD)	52.58 ± 9.84	55.26 ± 9.33
BMI (kg/m²) (mean ± SD)	28.32 ± 5.27	29.48 ± 4.20
Effect arm (%)
Dominant	57.9	47.4
Nondominant	36.8	52.6
Bilateral	5.3	0.0
Occupation (%)
Housewife	42.1	57.9
Worker	26.3	15.8
Retired	31.6	15.8
Education level (%)
Not literate	0.0	15.8
Primary	36.8	47.4
Secondary	21.1	10.5
Higher	42.1	26.3
Infection (%)
Never	63.1	73.7
1–2 times	15.8	10.5
3–4 times	15.8	15.8
5–↑	5.3	0.0
Treatments (%)
Never	0.0	10.5
CT	0.0	5.3
HT	0.0	5.3
RT + CT	15.8	10.5
RT + CT + HT	73.7	68.4
RT + HT	10.5	0.0
Type of operation (%)
Modified radical mastectomy	26.3	47.4
Radical mastectomy	36.8	26.3
Lumpectomy + ALND	36.8	26.3
Risk factors (%)
Absent	47.3	36.8
HT	26.3	15.8
Cigarette	15.8	15.8
DM	5.3	0.0
HT + DM	0.0	26.3
HT + cigarette	5.3	5.3

ALND, axillary lymph node dissection; BMI, body mass index; DM, diabetes mellitus; HT, hypertension; SD, standard deviation.

The mean age of Group 1 was 52.58 ± 9.84 years, and the mean body mass index (BMI) was 28.32 ± 5.27 kg/m². The mean age of Group 2 was 55.26 ± 9.33 years, and the mean BMI was 29.48 ± 4.2 kg/m². The characteristics of the patients in the two groups were similar (Table 1).

There was no significant difference between the groups in terms of the severity of LE (Table 2).

Table 2.

Lymphedema Severity of Groups

	Group 1, n = 19	Group 2, n = 19	p ^*
Duration of lymphedema (months), mean ± SD	24.21 ± 2.36	20.76 ± 2.77	0.860
Lymphedema severity (%)
Mild	42.1	42.1	0.879
Moderate	15.8	10.5
Severity	42.1	47.4

p < 0.05.

Compared to the normal range of motion in each of the two groups, a statistically significant difference was found in terms of shoulder flexion (p < 0.047). There was no statistically significant difference in the shoulder abduction, external rotation, internal rotation, and elbow flexion movements (Table 3).

Table 3.

Compared Range of Motions of Groups

Range of motion (°)	Group 1 (mean ± SD), n = 19	Group 2 (mean ± SD), n = 19	p ^*
Shoulder flexion	163.16 ± 1.35	140.00 ± 4.29	0.047^*
Shoulder abduction	146.32 ± 3.21	124.05 ± 4.70	0.126
Shoulder external rotation	82.10 ± 1.52	70.52 ± 3.02	0.240
Shoulder internal rotation	87.10 ± 8.71	71.84 ± 3.10	0.050
Elbow flexion	134.21 ± 8.21	123.1 ± 3.18	0.170

p < 0.05.

The results of the DASH and the SPADI measurements of the two groups were not statistically significant. However, Group 1 was observed to be better than Group 2 (Table 4).

Table 4.

Compared Functional Level of Upper Extremity in Two Groups

	Group 1 (mean ± SD), n = 19	Group 2 (mean ± SD), n = 19	p ^*
DASH (0%–100%)	28.1 ± 1.51	30.37 ± 2.17	0.861
SPADI pain (0%–100%)	21.10 ± 2.23	32.73 ± 3.26	0.277
SPADI disability (0%–100%)	27.57 ± 2.13	38.15 ± 2.9	0.249
SPADI total (0%–100%)	24.82 ± 2.06	35.95 ± 2.9	0.184

p < 0.05.

DASH, The Disabilities of the Arm, Shoulder and Hand Questionnaire; SPADI, Shoulder Pain and Disability Index.

Discussion

In this study, we assessed the effect of education on the upper extremity functions in patients who developed LE after breast cancer treatments. We observed that the upper extremity functions were better in the patients who were educated about LE.

An educational program may increase the awareness of LE, reduce the risk of BCRL, and increase upper extremity functions through lifestyle modifications. Lu et al. evaluated whether education in combination with physiotherapy can reduce the risk of breast cancer-related LE (BCRL).¹⁶ They analyzed 1217 women diagnosed with unilateral breast cancer who underwent tumor resection and axillary lymph node dissection in three groups (who received neither education nor physiotherapy postsurgery; who received an educational program on BCRL between days 0 and 7 postsurgery; and who received an educational program on BCRL between days 0 and 7 postsurgery, followed by a physiotherapy program). They emphasized that patient education was effective if it began within the first week postsurgery and was followed by physiotherapy in reducing the risk of LE in women who undergo breast cancer surgery with axillary lymph node dissection (ALND).¹⁶ Fu et al. also demonstrated that patients who received LE information reported significantly fewer symptoms and more practice of risk-reduction measures than those who did not.¹⁷ In our study, there was not a strong difference about their upper extremity functions in two groups. It was known that poor adherence to LE self-care programs was a major impediment to treatment success and it was possible that patients did not implement the program's advice into their daily lives as Fu et al. said.^17,18

In some studies, more frequent and severe LE was observed after heavy work or excessive use of an affected extremity.¹⁹ Tahan et al. studied 55 patients, with an occupation that required vigorous use of the upper limbs, who had a high grade of BCRL after breast cancer surgery. In that study, Group 1 included patients who worked continuously less than 30 minutes at a time and equal to or less than 8 hours per day. Group 2 included patients working continuously between 30 and 60 minutes at a time and equal to or less than 8 hours per day. Group 3 included patients working continuously for more than 1 hour and at least 8 hours per day. According to this study, the progressive stage and grade distribution of the BCRL in Group 3 was higher than Groups 1 and 2. In addition, these results show that occupations requiring more upper extremity activity had the worst LE clinical stage and grade status, as well as arm pain complaints, and physiotherapy and pain medicine needs. Also, prolonged use of the affected limb was found to increase the severity of LE.¹⁹ In our study, 19 participants (50.0%) were housewives, 8 (21.1%) working actively and 11 (28.9%) not working actively. LE was found to be more common in housewives who, in their daily work, often use extremities and engage in heavy lifting. These findings were similar to the results reported in the literature.

Although there are not enough studies in the literature that indicate the incidence of infection, it is known that recurrent infections accelerate the development of subcutaneous tissue fibrosis and increase edema.^20,21 In our study, 12 of 38 patients (31.6%) had an infection at least once and at the most six times. Their increased frequency of infection increased the development of fibrotic tissue.

Risk factors associated with LE have been divided into three groups in recent studies. The first of these groups includes the treatment-related risk factors (type of surgery, radiotherapy, or chemotherapy), the second includes disease-related risk factors (phase of pathological nodal involvement, affected number of lymph nodes, and tumor breast localization), and the third includes clinical-related risk factors (age, obesity, BMI, hypertension, history of infection, and the dominant extremity effective resistance).^20–22 According to Ozaslan et al., risk factors for the development of LE are infection, BMI, and the required use of hands for an hour or more in the course of working.²³ Risk factors of the patients in our study are consistent with the literature.

The most common and life-limiting problems are those related to upper limb function after the treatment of patients with breast cancer. Many researchers reported at least one upper extremity problem in 42%–82% of patients who underwent surgery of the breast or lymph node.²⁴ Ewertz et al. reported that 10%–70% of patients experienced limitations of the arms and shoulders, depending on the evaluation methods, the post-treatment time, and the type of surgery.²⁵ Westrup et al. found that 25% of 485 patients with breast cancer had upper extremity problems, and this problem was associated with BMI, type of surgery, and lymph node dissection.²⁶ Maunsell et al. found that the frequency of upper extremity problems was not affected by the type of surgical axillary lymph node dissection but reported significantly more arm and shoulder problems in patients.²⁷ Devoogdt et al. investigated short-term (3 months) and long-term (3–4 years) outcomes of patients and demonstrated that 31% experienced shoulder mobility impairment and 51% experienced limitations in activities of daily living according to long-term outcomes.

As the follow-up period increased, the risk and incidence of LE also increased, reducing mobility of the shoulder.²⁸ Ozçinar et al. investigated the late period effects (9–12 months) of treatments, and in 51 (24.8%) of 218 patients, the development of shoulder movement impairments was determined to be statistically significant in patients with LE.²⁹ Ewertz et al. studied the late period effects of breast cancer treatment and demonstrated a 35% reduction in shoulder function in the third postoperative year.²⁵ In our study, 78.9% of the patients had shoulder problems (i.e., there was a difference of 10° or more between the two extremities).

Shoulder and upper extremity stiffness is an important factor that affects the quality of life of patients after breast surgery.³⁰ The incidence of limitation of motion has ranged from 2% to 51% after breast surgery.³¹ Suden et al. reported limitation of motion in the shoulder in 48% of 141 breast cancer patients 18 months after operation.³² Hack et al. reported that 73% of study participants experienced limitation of motion in the shoulder and arm.³⁰ Rietman et al. also reported that 12%–51% of study participants experienced limitation of motion.³¹ Levangie et al. studied the magnitude of the late effects of shoulder function after breast cancer treatment by investigating the abduction and flexion movements of the shoulders that were affected and by comparing the contralateral side of the stiffness; they found that there was a 10% or 10°–20° limitation of motion.³³ Isasson et al. reported 20° restrictions in shoulder abduction and flexion after breast and axillary surgery and demonstrated that shoulder and arm problems also increase after radiotherapy.³⁴

Radiotherapy significantly reduces the mobility of the shoulder in patients undergoing axilla radiotherapy. Compared with patients who underwent breast-conserving surgery, patients who underwent mastectomies experienced a significantly decreased range of motion.³¹ Levangie et al. studied the effects of the stage of breast cancer after treatment and reported that the pectoralis major and minor muscles are affected after the application of radiotherapy, with particular impairments in shoulder flexion and abduction.³³ Radiation therapy caused destruction of the related tissues leading to fibrosis, which then leads to the restriction of shoulder movements.²⁰ Ozçinar et al. identified statistically significant limitations in shoulder flexion, abduction, and internal and external rotation movements in the early period of breast cancer treatment (week 1). They also showed a significant limitation of the ongoing internal rotation measurements by 9–12 months after surgery.²⁹ In our study, shoulder flexion was significantly better among the group receiving education than it was among the standard care group. Shoulder abduction, internal and external rotation, and elbow flexion were not significantly different.

In the literature, the most affected joint movements were shoulder abduction, shoulder flexion, shoulder external rotation, wrist flexion, and flexion of the proximal interphalangeal joints.³ In our study, the most affected movements were shoulder flexion (71.1%), shoulder abduction (68.4%), elbow flexion (44.7%), shoulder external rotation (34.2%), and shoulder internal rotation (23.7%).

Smoot et al. evaluated the shoulder function of patients with and without LE after breast cancer by using the DASH questionnaire and reported that the group that developed LE had significantly higher DASH scores.³ Dawes et al. studied upper extremity function and quality of life in women after breast cancer surgery and demonstrated that the DASH scores were significantly higher in patients with LE.⁸

Smoot et al. examined disorders of upper extremities after breast cancer treatment and found that the DASH scores were significantly higher in the LE group than in the group that had not developed LE.³ In our study, DASH scores were not significant in the group receiving training compared with the standard care group, but they were lower than the standard care DASH scores. Training breast cancer treatment patients on how to manage LE has been reported to be a priority.⁵ Fu et al. investigated the impact of informing patients about the symptoms of LE after breast cancer treatment. In this study, 57% of 136 patients were provided information about LE and how to reduce its symptoms. The authors reported a significant decrease in LE and its symptoms in the group that was provided information.¹⁷ In our study, there was no statistically significant difference between the groups in terms of upper extremity function, even though upper extremity function was observed as better in the education group.

There are strengths and limitations in our study. One strength is that there are not enough studies related to the effect of education on the upper extremity functions in patients who develop LE after breast cancer treatments. One limitation is that education about LE was given by different health professionals, such as doctors, physiotherapists, and nurses, and because of that, there might have been differences in the content and time of education. In addition, the relatively small number of patients included might have limited the study's power.

Conclusion

This study underscores the need to develop and implement strategies for LE prevention and education for all breast cancer patients.

LE adversely affects the lives of individuals. It has become a health problem not only for the individual but also for society. Therefore, it is extremely important that patients with breast cancer receive information about LE that can improve their quality of life and functional levels.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

References

Ahmedin

, Siegel

, Ward

, Hao

, Xu

, Thun

. Cancer statics. CA Cancer J Clin, 2009; 59:225–249.

Eser

, Olcayto

, Karakılınç

. Population-based cancer registry centers repository: Eight Provinces, 2004–2006 evaluation. Cancer Control Department of the Ministry of Health in 2004–2006 the incidence of cancer in Turkey.

Smoot

, Wong

, Cooper

, et al. Upper extremity impairments in women with or without lymphedema following breast cancer treatment. J Cancer Surviv, 2010; 4:167–178.

Preston

, Seers

, Mortimer

. Physical therapies for reducing and controlling lymphoedema of the limbs. Cochrane Database Syst Rev, 2004:CD003141.

Maclean

, Miedema

, Tatemichi

. Breast cancer-related lymphedema. Can Fam Physician, 2005; 51:246–247.

Hayes

, Battistutta

, Newman

. Objective and subjective upper body function six months following diagnosis of breast cancer. Breast Cancer Res Treat, 2005; 94:1–10.

Leidenius

, Leppanen

, Krogerus

, von Smitten

. Motion restriction and axillary web syndrome after sentinel node biopsy and axillary clearance in breast cancer. Am J Surg, 2003; 185:127–130.

Dawes

, Meterissian

, Goldberg

, Mayo

. Impact of lymphoedema on arm function and health-related quality of life in women following breast cancer surgery. J Rehabil Med, 2008; 40:651–658.

Park

, Lee

, Chung

. Incidence and risk factors of breast cancer lymphoedema. J Clin Nurs, 2008; 17:1450–1459.

10.

Hayes

, Walton

, Szomor

, Murrell

GAC

. Reliability of five methods for assessing shoulder range of motion. Aust J Physiother, 2001; 47:289–29.

11.

Karadibak

, Yıldırım

, Kara

, Saydam

. Effect of complex decongestive therapy on upper extremity lymphedema. Fizyoter Rehabil, 2009; 1:3–8.

12.

Ramos

, O'Donnell

, Knight

. Edema volume, not timing, is the key to success in lymphedema treatment. Am J Surg, 1999; 178:311–315.

13.

Beek

, te Slaa

, van der Laan

, Mulder

, Rutten

, Voogd

, Gobardhan

. Reliability of the inverse water volumetry method to measure the volume of the upper limb. Lymphat Res Biol, 2015; 13:126–130.

14.

Bumin

, Tüzün

, Tonga

. The Shoulder Pain and Disability Index (SPADI): cross-cultural adaptation, reliability, and validity of the Turkish version. J Back Musculoskelet Rehabil, 2008; 21:57–62.

15.

Düger

, Yakut

, Öksüz

, Yörükan

, Kol, omuz ve El Sorunları. (Disabilities of arm, shoulder and Hand-DASH). Anketi türkçe uyarlamasının güvenirliği ve geçerliği. Fizyoter Rehabil, 2006; 17:99–107.

16.

, Hong

, Chou

, Hsiao

. Role of physiotherapy and patient education in lymphedema control following breast cancer surgery. Therap Clin Risk Manage, 2015; 11:319.

17.

, Chen

, Haber

, Guth

, Axelrod

. The effect of providing information about lymphedema on the cognitive and symptom outcomes of breast cancer survivors. Ann Surg Oncol, 2010; 17:1847–1853.

18.

Vignes

, Porcher

, Arrault

, Dupuy

. Factors influencing breast cancer-related lymphedema volume after intensive decongestive physiotherapy. Support Care Cancer, 2011; 19:935–940.

19.

Tahan

, Johnson

, Mager

, Soran

. The role of occupational upper extremity use in breast cancer related upper extremity lymphedema. J Cancer Surviv, 2010; 4:15–19.

20.

Quiron

. Recognizing and treating upper extremity lymphedema in postmastectomy/lumpectomy patients: A guide for primary care providers. Am Acad Nurse Pract, 2010; 22:450–459.

21.

Waren

, Barson

, Borud

, Slavin

. Lymphedema a comprehensive review. Ann Plast Surg, 2007; 59:464–472.

22.

Monleon

, Murta-Nascimento

, Bascuas

, Macia

, Duarte

, Belmonte

. Lymphedema predictor factors after breast cancer surgery: A survival analysis. Lymphatic Res Biol, 2015; 13:268–274.

23.

Ozaslan

, Kuru

. Lymphedema after treatment of breast cancer. Am J Surg, 2004; 187:69–72.

24.

Keramopoulos

, Tsionou

, Minaretzis

, et al. Arm morbidity following treatment of breast cancer with total axillary dissection: A multivariated approach. Oncology, 1993; 50:445–449.

25.

Ewertz

, Jensen

. Late effects of breast cancer treatment and potentials for rehabilitation. Acta Oncologica, 2011; 50:187–193.

26.

Westrup

, Lash

, Thwin

, Silliman

. Risk of decline in upper-body function and symptoms among older breast cancer patients. J Gen Intern Med, 2006; 21:327–333.

27.

Maunsell

, Brisson

, Deschenes

. Arm problems and physiological distress after surgery for breast cancer. CJS, 1993; 36:315–320.

28.

Devoogdt

, Van

, Christiaens

, Troosters

, et al. Short and long term recovery of upper limb function after axillary lymph node dissection. Eur J Cancer Care, 2011; 20:77–86.

29.

Ozçinar

, Guler

, Özmen

, et al. Morbidities after local/regional treatment of breast cancer and patients’ quality of life. J Breast Health, 2010; 6:1.

30.

Hack

, Cohen

, Katz

, et al. Physical and physiological morbidity after axillary lymph node dissection for breast cancer. J Clin Oncol, 1999; 17:143–149.

31.

Rietman

, Dijkstra

, Hoekstra

, Eisma

, et al. Late morbidity after treatment of breast cancer in relation to daily activities and quality of life: A systematic review. EJSO, 2003; 29:229–238.

32.

Suden

, Rezveni

, Harrison

. Shoulder movement after the treatment of early stage breast cancer. Clin Oncol, 1998; 10:173–181.

33.

Levangie

, Drouin

. Magnitude of late effects of breast cancer treatment on shoulder function: A systematic review. Breast Cancer Res Treat, 2009; 116:1–15.

34.

Isasson

, Feuk

. Morbidity from axillary treatment in breast cancer: A follow-up study in a District Hospital. Acta Oncol, 2000; 39:335–336.