The risk factors and prevalence of upper extremity
impairments and an analysis of effects of lymphoedema
and other impairments on the quality of life of breast
cancer patients
S. KIBAR,MD,ASSISTANT PROFESSOR, Department of Physical Medicine and Rehabilitation, Ufuk University School of Medicine, Ankara, and Department of Physical Medicine and Rehabilitation, Ankara Physical Medicine and Rehabilitation Education and Research Hospital, Ankara, M. DALYAN ARAS, MD, ASSOCIATE PROFESSOR, Department of Physical Medicine and Rehabilitation, Ankara Physical Medicine and Rehabilitation Education and Research Hospital, Ankara, & S. €UNSAL DELIALIO GLU, MD, ASSOCIATE PROFESSOR, Department of Physical Medicine and Rehabilitation, Ankara Physical Medicine and Rehabilitation Education and Research Hospital, Ankara, Turkey
KIBAR S., DALYAN ARAS M. & €UNSAL DELIALIO GLU S. (2017) European Journal of Cancer Care 26, e12433, doi: 10.1111/ecc.12433
The risk factors and prevalence of upper extremity impairments and an analysis of effects of lymphoedema and other impairments on the quality of life of breast cancer patients
This study aimed to determine the prevalence and identify the risk factors associated with upper extremity impairments (UEIs) in breast cancer patients and to investigate the degree to which these impairments and other characteristics influence quality of life (QoL). A total of 201 women over the age of 18 who underwent breast cancer treatment at least 6 months were included in this cross-sectional study. All of the patients were evaluated for the presence of lymphoedema and any UEIs. UEIs divided into five subgroups: pain, restriction of shoulder range of motion (ROM), numbness and heaviness, loss of strength, and sensory deficit. QoL of the patients was evaluated by SF-36. The prevalence of the upper extremity impairments was as follows: pain 31.8%, restriction of shoulder ROM 23.9%, numbness and heaviness 35.3%, loss of strength 8.5%, and sensory deficit 18.4%. Furthermore, lymphoedema was seen in 41.3% of patients. The multivariate model showed that lymphoedema is the only statistically significant risk factor that affects the development of UEIs (P= 0.001). However, it also revealed that lymphoedema (P = 0.001) and increased age negatively affect QoL, whereas prolongation of the follow-up period has a favourable impact (P= 0.016). Therefore, lymphoedema diminishes QoL via an increased number of UEIs.
Keywords: breast cancer, quality of life, upper extremity impairment, prevalence, lymphoedema.
INTRODUCTION
Shoulder and arm problems after breast cancer operations and axillary lymph node dissection (ALND) produce a complex spectrum of symptoms (Kuehn et al. 2000). There are hypotheses concerning the factors that con-tribute to the development of upper extremity impair-ments (UEIs) and the most factors most often considered are the surgical method, the extent of the ALND,
radio-Correspondence address: Sibel Kibar, Ufuk €Universitesi Tıp Fak€ultesi Fizik Tedavi ve Rehabilitasyon Anabilim Dalı Mevlana Bulvar No:86-88 Balgat, 06520, Ankara, Turkey (e-mail: sibelkbr@gmail.com).
The manuscript submitted does not contain information about medical device.
Accepted 24 November 2015
DOI: 10.1111/ecc.12433
European Journal of Cancer Care, 2017, 26, e12433, DOI: 10.1111/ ecc.12433
therapy, lymph node (LN) metastasis and obesity. In stud-ies that compared ALND and sentinel lymph node dissec-tion (SLND), more UEIs were usually found in the ALND group (Kwan et al. 2002; Crane-Okada et al. 2008). In addition, UEIs have been found to occur more frequently after mastectomies than breast-conserving surgery (Nes-vold et al. 2008) and have been seen more after axillary radiotherapy than breast/chest radiotherapy (Kwan et al. 2002).
Lymphoedema still remains a troublesome complica-tion of breast cancer treatment since patients can receive partial relief but not complete resolution. The presence of upper extremity symptoms, for example discomfort in arm, is thought to be predictive on the development of lymphoedema (Norman et al. 2009). Additionally, early evaluation of UEIs at the sixth post-operative month is important in order to provide information to assess long-term prognosis (Albert et al. 2006). Therefore, evaluating patients with an eye towards UEIs during the follow-up process can aid in the diagnosis of lymphoedema at an early stage, especially since there is a higher likelihood of recovery with early diagnosis.
There are previous studies that have indicated that shoulder problems impair the quality of life (QoL) of patients after breast cancer treatment (Voogd et al. 2003; Montazeri 2008). While some studies have investigated the adverse effects of lymphoedema on QoL (Beaulac et al. 2002; Ridner 2005), others have examined how it is affected by UEIs (Beaulac et al. 2002; Kwan et al. 2002; Ridner 2005; Sagen et al. 2009; Park et al. 2012). Early rehabilitation has also been influential in improving the functional level and QoL of patients after surgery (Gordon et al.2005).
While swelling and mild discomfort are dominant at the initial stage of lymphoedema, as this condition progresses, symptoms such as pain and restricted range of motion (ROM) start to emerge (Park et al. 2012). In long-term fol-low-up, upper extremity problems may improve, but lym-phoedema continues (Engel et al. 2003). Many studies have been conducted with respect to lymphoedema, its incidence, and its impact on QoL (Ridner 2005; Park et al. 2012); however, there have been only a few studies focus-ing on UEIs other than lymphoedema (Hawker et al. 2011; Nesvold et al. 2011). The effect of lymphoedema on the development of UEIs has also not been adequately investi-gated. The most important limitation of previous UEI studies is that the majority have been based on subjective questionnaires (Bosompra et al. 2002; Kwan et al. 2002; Engel et al. 2003; K€arki et al. 2005; Norman et al. 2009).
This study aimed to assess upper extremity problems along with the associated risk factors in patients with
breast cancer patients via objective methods, which may be applied easily in outpatient clinics and to investigate the degree to which UEIs, lymphoedema, and other clini-cal and demographic characteristics of patients influence QoL. In view of the aforementioned issues, we tried to elu-cidate the points that should not be ignored in the treat-ment process in order to increase the QoL by enabling decreased morbidity in the early stages.
MATERIALS AND METHODS
Between 2008 and 2011, 287 Caucasian women with breast cancer who had a modified radical mastectomy or lumpectomy in conjunction with chemotherapy and/or radiotherapy were evaluated for the development of UEIs and lymphoedema at the Hospital. All patients have been undergone level III ALND. Level III is the highest level of the ALND. Level I LNs are lateral and inferior to the toralis minor muscle, level II LNs are behind the pec-toralis minor muscle, level III LNs are medial and superior to the same muscle (Berg 1955).
Patients over the age of 18 with a minimum post-treat-ment period of 6 months were included cross-sectional in the study. Sixty-five patients with bilateral breast cancer, regional recurrence or distant metastasis along with those with any shoulder or UEI before surgery, systemic disease causing oedema of the extremities, or a history of upper extremity fracture or surgery that might affect the evalua-tion process were excluded. In addievalua-tion, 21 patients refused to participate in the study. In the end, a total of 201 patients (mean age 52.5 10.4) who were operated on for unilateral breast cancer fulfilled the criteria and were included in the study.
The socio-demographic characteristics, such as age, edu-cation level and marital status of all of the patients, were recorded, and the body mass index [BMI (W-kg)/(H2-m2)] was calculated. The operation duration, surgical method, complications, number of extracted LNs, number of metastatic LNs and adjuvant treatment methods, includ-ing breast–chest radiotherapy, axillary radiotherapy, chemotherapy and comorbidities (such as hypertension, diabetes mellitus) were also documented through the medical records of the patients and patient interviews.
The study was approved by the Ethics Committee of the Hospital. In addition, written consent forms were obtained from all patients; if the patient was illiterate the consent form was obtained from her literate relatives. They were all informed about lymphoedema, UEIs, preventive measures, positioning, and skin care via an information brochure and exercise form. Furthermore, those diagnosed with lymphoedema or UEI were included
in a physical therapy and rehabilitation programme. The rehabilitation programme was determined according to the patients’ clinical features. Lymphoedema was treated by manual lymphatic drainage massage, pneumatic compression device and multilayer compression ban-dages. Shoulder problems were treated by appropriate physical therapy agents and exercises supervised by a physiotherapist.
Assessment of UEIs
The UEIs were divided into the following five subgroups: pain, restriction in shoulder ROM, numbness, loss of strength and sensorial deficiency. The patients were eval-uated by an experienced physiatrist who questioned them about upper extremity pain in their shoulders, arms, wrists and hands. Their pain level was evaluated by a visual analogue scale (VAS), and since pain scores of less than three have no effect on QoL a score of three or over in a single location indicated a positive response for pain (Tengrup et al. 2000; K€arki et al. 2005; Hawker et al. 2011).
Shoulder ROM was determined by a standard goniometer to measure abduction, flexion, and external and internal rotation since lack of mobility in this joint has a significant negative impact on daily activities (Gerhardt & Rodinelli 2001), especially when compared with the contralateral shoulder. To measure flexion, the patient sat with the arm at the side with the elbow extended. The plane of motion was sagittal, and the goniometer placement axis was centred on the lateral shoulder. The stationary arm remained at 0° while the other arm remained parallel to the humerus. Abduction measurements were gathered with the patient in a simi-lar position in that the plane of motion was frontal, and the goniometer placement axis was centred on the ante-rior shoulder. To measure the shoulder internal and external rotation, each patient was placed in the supine position with the shoulder at 90° of abduction and the elbow at 90° of flexion. The arm was in the pronation position. The plane of motion was transverse, and the goniometer was positioned on an axis on the elbow through the longitudinal axis of the humerus. The sta-tionary arm remained at 0°, and the other arm remained parallel to the forearm. All of these movements were evaluated twice in both extremities. If the difference between two of the measurements was 5°, a third mea-surement was taken, and the highest value was accepted as the reference (Palmer et al. 1998; Hayes et al. 2005). The normal ROM for flexion and abduction is 180° while it is 90° for internal and external rotation. A
restriction score of 20° or over was regarded as positive for restriction in ROM (Voogd et al. 2003). If the same restriction was found at the contralateral shoulder, the result was attributed to the patient’s physical stature and was not deemed as positive.
Assessment of muscle strength was made by manual muscle testing using the Medical Research Council (MRC) scale (Palmer et al. 1998). For each movement, two measurements were taken twice at each shoulder. When there was a difference between these measurements, it was repeated. After comparing the results with the con-tralateral shoulder, a movement value of 4 or below on the MRC was considered as loss of strength.
The feelings of numbness and heaviness were evaluated according to a self-reported light touch examination focus-ing on normal dermatomal and peripheral nerve distribu-tion. While avoiding excessive pressure, the examiner touched the skin lightly with a fine wisp of cotton. The patient was then asked to respond about how this felt and to determine whether or not there was a difference between the two sides. If necessary, a third test was per-formed.
All patients were also evaluated for lymphoedema of the upper extremity by a circumferential measurement method (Norman et al. 2001; Ahmed et al. 2011). This was carried out via flexible non-stretch tape at the metacarpophalangeal joint and wrist and at 10 cm distal to the lateral epicondyle and 15 cm proximal to the lateral epicondyle. A 2 cm or more circumferential difference at any of these four points between the affected and non-affected arms was defined as lymphoedema (Norman et al. 2001; Kwan et al. 2002; Ahmed et al. 2011). Patients were then questioned about how long it took for the lym-phoedema to develop and about when they first noticed the differences in size between their right and left hands as well as their upper and lower arms (Ahmed et al. 2011).
Quality of life
The Medical Outcomes Study 36-item Short Form Health Survey (SF-36â) (QualityMetric, Lincoln, RI, USA), which has previously been used to evaluate QoL in many other studies, was also employed in our study for the same purpose (Freitas-Silva et al. 2010). The SF-36â is one of the most commonly used QoL scales in breast cancer patients, and its validity and reliability has been proven (Hawker et al. 2011). It is a multidimen-sional questionnaire with eight parts: physical function-ing, physical role functionfunction-ing, bodily pain, general health perceptions, vitality, social role functioning, emo-tional role functioning and mental health, and these
components can be divided into two subsets: the physi-cal component summary (PCS) and the mental compo-nent summary (MCS). Each compocompo-nent is measured with a value ranging from 0 to 100, with 0 and 100 cor-responding to the poorest and optimal health statuses respectively (Ware et al. 2000).
Statistical analysis
Statistical analyses were conducted using the Predictive Analytic SoftWare (PASW) version 18.0 for Windows sta-tistical software package (SPSS, Chicago, IL, USA). Descriptive statistics were expressed as mean, standard deviation (SD), minimum and maximum, and median for continuous variables, and percentages (%) for categorical variables. The Mann–Whitney U and chi-squared tests were used to determine the risk factors that have an impact on UEIs in univariate analysis. Afterwards, the variables with a value of P< 0.25 were entered into the multivariate model, and multivariable backward stepwise logistic regression was used to identify the effects of clini-cal factors which affect UEIs together with some risk fac-tors (Hosmer & Lemeshow 2000). For every variable, the odds ratio (OR) and 95% confidence intervals (CIs) were calculated. A P< 0.05 was considered to be statistically significant.
A one-way analysis of variance (ANOVA) test was used in the univariate analysis of the risk factors of QoL. For independent cohorts, Student’s t-test and Spearman’s cor-relation coefficient were utilised. After univariate analy-sis, the variables with a value of P< 0.25 were entered into the multivariate model, and multivariable linear regression was performed. For every variable, the coeffi-cient of regression and 95% CIs were calculated. A P< 0.05 was considered to be statistically significant.
RESULTS
The mean follow-up period for the study participants was 47.9 48.7 months. 137 (62.8%) of these patients were between the ages of 40 and 60. In addition, the BMI was over 25 in 176 (87.5%) of the patients.
High percentage of participants are illiterate or have only a primary school education (n= 147, 73%), are unem-ployed (n= 181, 90%), and are overweight or obese (n= 176, 87.5%). Since all these items are concordant with low socioeconomic status, this study demonstrated the features of the patients with breast cancer in low socioeconomic status. A modified radical mastectomy was performed on 94.53% of the patients in this study, and all patients underwent level III ALND as mentioned
before. The clinical and demographic characteristics of the patients are shown in Table 1.
The prevalence and risk factors of UEIs
With respect to UEIs, 107 of 201 patients (53.23%) had at least one of the UEIs. Thorough results are shown in Table 2.
Lymphoedema was identified in 83 (41.3%) patients. A univariate analysis for UEI risk factors showed a statisti-cally significant negative effect on UEIs with regard to the number of metastatic LNs (P = 0.004), breast/chest radio-therapy (P = 0.018), axillary radiotherapy (P = 0.009) and presence of lymphoedema (P ˂ 0.001). The results of the univariate analysis are shown in Table 3.
Table 1. Demographic variables and patient treatments
Variables Categories N %
Total 201 100
Age ≤40 22 10.9
41–60 137 68.2
>60 42 20.9
Educational level University 13 6.5
High school 28 13.9
Middle school 13 6.5
Primary school 67 33.3
Illiterate 80 39.8
Marital status Bachelor/widowed 24 11.9
Married 177 88.1
Work status Employed 20 10
Unemployed 181 90 BMI BMI≤25 25 12.5 BMI>25 176 87.5 Comorbidity 114 56.7 + 87 43.3 Operation MRM 190 94.53 Lumpectomy/other 11 5.47 Cancer treatment Surgery 201 100
Breast–chest RT 116 57.8
Axillary RT 68 33.8
Chemotherapy 95 47.2 BMI, body mass index; MRM, modified radical mastectomy; RT, radiotherapy.
Table 2. The prevalence of upper extremity impairments
Variables Category N % Pain 137 68.2 + 64 31.8 Restriction of ROM 153 76.1 + 48 23.9 Numbness–heaviness 130 64.7 + 71 35.3 Loss of strength 184 91.5 + 17 8.5 Sensory deficit 164 81.6 + 37 18.4
Multivariate analysis of the variables with a value of P˂ 0.25, showed that the only variable that had an impact on UEIs was lymphoedema (OR: 3.941; P˂ 0.001). Addi-tionally, the patients with lymphoedema had a 3.941 times greater risk of UEI development compared with those without this condition. All of the multivariate anal-ysis results are given in Table 4.
Effective factors on QoL
We investigated the effects of the socio-demographic and clinical characteristics, UEIs and lymphoedema of the patients as they related to QoL in terms of the PCS and MCS of the SF-36â. Those with at least one upper
extrem-ity issue were placed in the UEI group, and the UEI effects were also evaluated one by one.
In univariate analysis, while age (P˂ 0.001), BMI (P= 0.005), post-operative complications (P = 0.026), axil-lary radiotherapy (P= 0.022), the number of extracted LNs (P= 0.033), the presence of lymphoedema (P ˂ 0.001) and the existence of any other UEI (P= 0.013) had an effect on the PCS, it was determined that the comorbidities (P= 0.05), follow-up period (P = 0.041), breast/chest radio-therapy (P = 0.047), axillary radiotherapy (P = 0.003), lym-phoedema (P ˂ 0.001) and UEIs (P = 0.018) affected the MCS. The results of the univariate analysis for QoL are shown in Table 5. However, pain, restriction in ROM, and numbness and heaviness had a negative effect on both the PCS and MCS. The relationship between the UEIs and QoL is shown in Table 6.
Variables with a value of P< 0.25 in the univariate anal-ysis were used in the multivariate analanal-ysis, and while lymphoedema had a statistically significant negative effect on the MCS (b = 7.087; P ˂ 0.001) and PCS (b = 7.087; P ˂ 0.001), older age only affected the PCS (b = 7.567; P ˂ 0.001). In addition, statistically
signifi-Table 3. Assessment of risk factors for UEIs
Variables Category UEIs ( ) (n= 94) UEIs (+) (n = 107) P
Surgery MRM 89 (46.8) 101 (53.2) Lumpectomy 5 (45.5) 6 (54.5) 1.000 Extracted LNs 20.87 7.497 21.93 7.888 0.261 Metastatic LNs 2.10 3.921 4.63 7.754 0.004* RT (breast/chest) 48 (56.5) 37 (43.5) – + 46 (39.7) 70 (60.3) 0.018* Axillary RT 71 (53.4) 62 (46.6) – + 23 (33.8) 45 (66.2) 0.009* Chemotherapy 14 (56.0) 12 (44.0) – + 80 (45.7) 95 (54.3) 0.334 Post-operative complication 72 (46.2) 84 (53.8) – + 22 (53.8) 23 (46.2) 0.473 Knowledge of lymphoedema 56 (46.7) 64 (53.3) – + 38 (46.9) 43 (53.1) 0.973 Lymphoedema 71 (60.2) 47 (39.8) – + 23 (27.7) 60 (72.3) <0.001* Age (years) 52.5 10.4 51.5 10.5 53.4 10.3 ≤40 12 (55.4) 10 (45.5) 41–60 65 (47.4) 72 (52.6) >60 17 (40.5) 25 (59.5) 0.541 Follow-up period 47.9 48.7 44.8 43.1 51.5 54.4 ≤12 months 13 (43.3) 17 (56.7) 13–36 months 41 (48.2) 44 (51.8) >36 months 40 (46.5) 46 (53.5) 0.0897 BMI 30.2 4.9 29.2 4.6 31.1 5.0 BMI≤25 13 (52.0) 12 (48.0) BMI>25 81 (46.0) 95 (54.0) 0.729 Comorbidity 52 (45.6) 62 (54.4) – + 42 (48.3) 45 (51.7) 0.708
UEIs, upper extremity impairments; MRM, modified radical mastectomy; LN, lymph node; RT, radiotherapy; BMI, body mass index. Values within parentheses were expressed in percentage. Bold and*: p < 0.05
Table 4. Results of multivariable logistic regression analysis
Variables Odds ratio P
95% CIs Lower Limit Upper Limit Lymphoedema 3.941 <0.001* 2.150 7.222 Bold and*: p < 0.05
cant improvement was demonstrated in the PCS (b = 2.348; P = 0.016) and MCS (b = 2.694; P = 0.005) with a prolonged follow-up period. The results of the multivari-ate model are shown in Table 7.
DISCUSSION
The study population’s characteristics are consonant with low socioeconomic status. In this study, development of at least one UEI and lymphoedema were determined in the patients with breast cancer who underwent level III
ALND, 53.1% and 41.3% respectively. Additionally, the only significant risk factor of upper extremity problems is lymphoedema. While lymphoedema and patient age have unfavourable effect on QoL of these patients, long follow-up period has favourable effect.
After breast cancer treatment, pain is an important issue since it stimulates fears of recurrence and thoughts about cancer (Passik & McDonald 1998). Patients mostly com-plain about shoulder and neck pain for 6 months post-operatively (Tengrup et al. 2000; K€arki et al. 2005). It is believed that the laceration of the branches of the
inter-Table 5. Assessment of risk factors for quality of life
Variables Category Physical health P Mental health P
Age (years) ≤40 43.96 8.02 <0.001* 38.10 10.71 0.486 41–60 38.95 10.41 40.53 10.38 >60 28.42 9.08 41.31 9.69 BMI BMI≤25 43.07 11.39 0.005* 38.62 10.86 0.349 BMI>25 38.62 10.86 76 (96.2%) Comorbidity 38.48 10.47 0.81 39.19 10.25 0.05* + 36.48 10.71 40.68 10.18
Follow-up period (months) ≤12 33.26 10.26 0.061 37.50 8.12 0.041*
13–36 37.25 10.85 39.47 11.08 >36 38.76 11.13 42.39 9.81 Surgery MRM 37.08 10.91 0.232 40.11 10.18 0.066 Lumpectomy 41.16 12.11 45.95 10.62 Post-operative complication 38.22 10.63 0.026* 41.16 10.49 0.057 + 34.09 11.71 37.86 9.09 RT (breast/chest) 39.06 12.50 0.063 42.10 10.35 0.047* + 36.01 9.58 39.20 10.07 Axillary RT 38.48 11.64 0.022* 41.87 10.53 0.03* + 34.98 9.22 37.59 9.16 Chemotherapy 34.14 13.88 0.226 42.42 8.96 0.287 + 37.71 10.50 40.08 10.42 Lymphoedema 39.76 11.59 <0.001* 43.31 9.93 <0.001* + 33.81 9.03 36.33 9.34 Knowledge of lymphoedema 36.14 10.67 0.069 40.63 9.96 0.729 + 39.01 11.29 40.12 10.76 Extracted LNs 0.150† 0.033* 0.045† 0.529 Metastatic LNs 0.077† 0.729 0.085† 0.228
QoL, quality of life; BMI, body mass index; MRM, modified radical mastectomy; RT, radiotherapy; LN, lymph node. †Spearman’s correlation coefficient. Bold and*: p < 0.05
Table 6. The relationship between upper extremity impairments and quality of life
Variables Category Physical health P Mental health P
UEIs 39.34 12.13 0.013* 42.25 10.30 0.018* + 35.50 9.58 38.82 10.01 Pain 38,58 11,25 0.015* 41,90 9.67 0.003* + 34.55 9.93 37.26 10.86 Restriction in ROM 38.40 11.31 0.011* 41.23 10.24 0.047* + 33.78 9.12 37.86 10.01 Numbness–heaviness 38.25 11.65 0.077* 42.06 10.59 0.001* + 35.55 9.48 37.43 8.97 Loss of strength 37.60 11.21 0.101 40.74 10.26 0.152 + 34.08 7.76 37.01 9.97 Sensory deficit 37.51 11.41 0.563 40.77 10.25 0.322 + 36.35 8.95 38.91 10.33
costobrachial nerve is the source of the shoulder/arm pain in these patients (Vecht et al. 1989). In a cross-sectional study by Nesvold et al. (2008), in which all of the patients underwent ALND, a pain incidence of 32% was reported, which is in compliance with the 31.8% rate in our study. Another study by Devoogdt et al. (2011) reported a high pain incidence rate of 79% following ALND, and VAS pain scores of one and above were evaluated as having the pres-ence of pain. In our opinion, the lower VAS pain scores that signified the pain threshold in that study led to the higher incidence rates.
Movement restriction may develop, especially in the shoulder region, after breast cancer, but the results of the few studies that have investigated the prevalence of this condition are contradictory (Freitas-Silva et al. 2010). Many studies evaluate upper extremity mobility based on the self reports of patients. However, the goniometric eval-uation methods vary in the different studies. We preferred to use goniometric method and 20° as the threshold of movement restriction because in values higher than this, QoL is impaired, and daily activities are limited (Tengrup et al.2000; Voogd et al. 2003). It is thought that the resec-tion of the pectoral fascia during mastectomies culminates in shoulder movement restriction by causing adherence to subcutaneous tissue (Lauridsen et al. 2005). All of our patients underwent level III ALND, and a great majority had modified radical mastectomy. The prevalence of restricted ROM was 23.9%. In another study by Nesvold et al. (2008) that used treatment protocol and evaluation methods similar to ours, the prevalence rate of restricted ROM was reported as 24%. In addition, 12% of patients with breast-conserving surgery in that study reported restricted ROM. Furthermore, in a study by Kuehn et al. (2000) that included 306 patients in which the majority underwent breast-conserving surgery followed by ALND, it was reported that the rate of ROM restriction was as low as 14% with no significant difference between ALND levels I–II and ALND levels II–III. These findings and ours demonstrate that mastectomy has a significant impact on ROM restriction and that ALND has no effect.
While in many studies muscle strength was evaluated through questioning the patients about their sense of loss of strength in the affected extremity, we employed an
experienced physiatrist who used the MRC scale for this purpose and determined that 8.5% of our patients had loss of strength. This rate was reported as 10% in a study by Bosompra et al. (2002) which evaluated 222 patients via a verbal questionnaire and 13% in another prospective study by Isaksson and Feuk (2000), that featured a smaller cohort of 48 patients.
The risk of intercostobrachial and medial cutaneous nerve damage increase with ALND, causing sensorial impairment (Jung et al. 2003). Crane-Okada et al. (2008) also found that sensorial impairment and numbness were more common in patients with ALND. Mansel et al. (2006) investigated the intercostobrachial nerve region via a pinprick test, and impairment was reported in 31% of the patients with ALND and 11% with SLND. In our study, only light touch was used to evaluate sensorial distur-bance, and impairment was seen in 18% of the patients. The disparate results could be the result of the different evaluative methods that were utilised in these studies.
We also determined that 35% of the patients in our study complained of numbness and heaviness. K€arki et al. (2005) reported incidence rates at the post-operative sixth and 12th months of 35.4% and 32.2%, respectively, while 24% experienced numbness in a study by Bosompra et al. (2002). In our opinion, it is very difficult to diagnose numbness and heaviness in patients with lymphoedema. The incidence rate of lyphoedema was 41.3% in our study, and this rate is also close to the incidence of numbness found in other studies.
The risk factors of UEIs
After investigating the risk factors of lymphoedema, axil-lary radiotherapy and ALND, some studies have shown an increase in the rate of lymphoedema that mimics the rise in the development of UEIs (Kwan et al. 2010; Bar Ad et al. 2012). As previously mentioned, mastectomies result in UEIs due to the devastation incurred by the mus-cles required for upper extremity ROM (Lauridsen et al. 2005; Nesvold et al. 2008). While studies by Petrek et al. (2001) and Mak et al. (2008) showed that mastectomies alone produce no significant effects in the development of lymphoedema, concurrent ALND and axillary
radiother-Table 7. Multivariate linear regression analysis for quality of life Variables
Physical health Mental health
UC (b) (95% CIs lower–upper limit) P UC (b) (95% CIs lower–upper limit) P Lymphoedema 4.527 ( 7.298 to 1.756) 0.001* 7.087 ( 9.781 to 4.393) <0.001* Follow-up period 2.348 (0.447–4.249) 0.016* 2.694 (0.818–4.571) 0.005*
Age 7567 ( 10.024 to 5.11) <0.001* – –
apy were reported to be risk factors (Kwan et al. 2010). In the light of these findings, we evaluated the effects of lym-phoedema and other possible risk factors on the develop-ment of UEIs and demonstrated that lymphoedema is the only significant risk factor, a fact this has also been veri-fied by the results in other studies (Hayes et al. 2005; Smoot et al. 2010).
Quality of life
Our data also indicated that lymphoedema has an impact on QoL. In a study by Beaulac et al. (2002) with a 27.8% lymphoedema rate in 105 patients, the UEIs were found to have no effect on QoL, but lymphoedema was reported to be a risk factor just as it was in our study. It has also been reported by Ridner (2005) that lymphoedema lowers the QoL because it causes more UEIs. While it is true that improvement can be seen in UEIs in the later phases of fol-low-up, once lymphoedema develops, that improvement stops (Engel et al. 2003).
In the present study, the prolonged follow-up period was found to have a favourable impact on QoL. Sagen et al. (2009) emphasised the improvement in QoL after a 5-year follow-up period. In addition, it is known that 90% of the late effects of RT emerge after 3.9 years (Bentzen et al. 1989); thus, evaluations that take place after 4 or more years would be beneficial in order to investigate the extent to which the QoL of breast cancer patients has been affected. The mean follow-up period of our study was approximately 4 years.
It is inevitable that the incidence of UEIs increases in conjunction with older age (Kuehn et al. 2000; Park et al. 2012). In addition, QoL can decrease on account of the higher number of comorbidities in the elderly and the increased likelihood of lymphoedema development with a prolonged follow-up period. In this study, we demon-strated the adverse effects of older age on QoL and showed that upper extremity functions were impaired by lym-phoedema and advanced age (Hayes et al. 2005).
There are some limitations for this study. The study population’s characteristics are consonant with low socioeconomic status. Most of the patients of this study were illiterate or had primary school education,
unem-ployed and overweight or obese. Because of these features of the patients, results of this study prevail in populations with low socioeconomic status.
Even though we demonstrated that lymphoedema has a negative effect on QoL and the development of UEIs, the cross-sectional design of our study means that lym-phoedema cannot be regarded as a precise cause of these conditions. In addition, no evaluations were conducted before surgery, resulting in patients with pre-existing shoulder symptoms being ruled out. Since patients with UEIs might come to the outpatient clinic more than the other patients, they might be overrepresented in the study. This may be a bias in patient’s selection.
The prominent reason of the high prevalence of lym-phoedema and the lymlym-phoedema-induced UEIs may be related with low socioeconomic status of the patients, combination of mastectomy, level III ALND and the other therapy methods. UEIs have no statistically significant impact on QoL. Lymphoedema, is a major risk factor for the development of UEIs and it also impairs the QoL of breast cancer patients. Therefore, untreatable, established lymphoedema diminishes QoL via an increased number of UEIs. If possible and appropriate for the patient the usage of new treatment methods for ALND should be encouraged and mastectomies should be avoided by the clinicians.
CONFLICT OF INTEREST
The authors declare that they have no conflict of interest and no disclosures. The authors have full control of all pri-mary data and agree to allow the journal to review the data if requested.
ACKNOWLEDGEMENTS
We certify that no party having a direct interest in the results of the research supporting this article has or will confer a benefit on us or on any organisation with which we are associated AND, if applicable, we certify that all financial and material support for this research (e.g., NIH or NHS grants) and work are clearly identified in the title page of the manuscript.
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