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Upper-Limb Morbidity in Patients Undergoing a Rehabilitation Program After Breast Cancer Surgery

A 10-Year Follow-up Study

de Carlos-Iriarte, Esperanza, PhD1; Mosquera-González, Margarita, PhD, MPH2; Alonso-García, Marcos, MPH3; Andrés-Prado, María José, PhD, MPH4; Machota-Blas, Elizabeth, MD5; Hernández-García, José Manuel, PhD6; Rodríguez-Caravaca, Gil, PhD, MPH7

doi: 10.1097/01.REO.0000000000000131

Objective: To identify long-term predictive factors for upper-limb morbidity in patients who completed an early rehabilitation program after breast cancer surgery.

Material and Methods: Prospective cohort study. The study population comprised 659 female patients who were consecutively enrolled in a rehabilitation program shortly after breast cancer surgery between April 1999 and June 2010. The rehabilitation program comprised clinical evaluation, written information on hygiene measures, aerobic exercise, and physical therapy. Variables assessed for affected and contralateral limb included circumferential measurement for lymphedema, passive range of motion in the shoulder, pain intensity using a visual analog scale, and sensory loss by the pin-prick method and tactile sensitivity. Predictive variables covered age, body mass index, regular physical activity, previous shoulder pathology, type of breast surgery, side of surgery, postsurgical complications, sentinel lymph node biopsy/axillary lymph node dissection, tumor size and histology, chemotherapy, radiotherapy, and hormonal treatment. A multivariate logistic regression analysis was performed to control for confounding factors.

Results: The mean follow-up period was 72 months. A total of 306 patients (64.4%) showed upper-limb symptoms at some point during the follow-up period. Sensory loss and pain were the most relevant impairments. Predictive factors for shoulder and arm morbidity were obesity (odds ratio [OR] = 2.45; 95% confidence interval [CI], 1.18-5.08), previous shoulder pathology (OR = 6.05; 95% CI, 2.89-12.63), postsurgical complications (OR = 2.16; 95% CI, 1.05-4.43), and regional lymph node radiotherapy (OR = 3.42; 95% CI, 2.07-5.63).

Conclusions: Previous shoulder pathology, postsurgical events, obesity, and site of radiotherapy were significant risk factors for developing shoulder and arm morbidity.

1Head of Department, Service of Rehabilitation Medicine, University Hospital “12 de Octubre,” Madrid, Spain

2Consultant, Preventive Medicine Unit, University Hospital Fundación Alcorcón, Madrid, Spain

3Resident, Preventive Medicine Unit, University Hospital Fundación Alcorcón, Madrid, Spain

4Consultant, Preventive Medicine Unit, University Hospital Fundación Alcorcón, Madrid, Spain

5Consultant, Service of Rehabilitation Medicine, University Hospital “12 de Octubre,” Madrid, Spain

6Consultant, Service of Obstetrics and Gynaecology, University Hospital “12 de Octubre,” Madrid, Spain

7Consultant, Preventive Medicine Unit, University Hospital Fundación Alcorcón, Madrid, Spain

Correspondence: Margarita Mosquera-González, PhD, MPH, Preventive Medicine Unit, University Hospital Fundación Alcorcón, C/Budapest 1, 28922, Alcorcón, Madrid, Spain (

The authors declare no conflicts of interest.

Upper-limb morbidity is a common adverse effect after breast cancer surgery that is usually associated with more aggressive procedures such as extensive breast surgery or axillary lymph node dissection (ALND).1 However, upper-body symptoms and impairment remain common despite the introduction of sentinel lymph node biopsy (SLNB), a less invasive technique that can enable some patients to avoid extensive lymph node surgery.2,3

Lymphedema, limited shoulder and arm mobility, shoulder/arm pain, and scarring on the breasts and thorax are some of the most frequent upper-body complications after breast cancer surgery.4 Existing studies on dysfunction of the upper limb revealed a high prevalence of functional limitations at 3 months including chest pain and numbness,5,6 which resolve over time, and lymphedema, which worsens over time. These limitations typically present within the first 12 months after surgery.7,8

Shoulder-arm function at 6 weeks after surgery and age seem to be the strongest predictors of long-term shoulder-arm dysfunction.9 Sensory neuropathy and arm mobility restrictions are associated as well with self-reported limitations in activity and decreased health-related quality of life.10

Nevertheless, the postsurgical adverse effects involving the upper limb can be minimized by participation in a rehabilitation program including written information on prevention and hygiene measures11 (skin care: avoid wounds, burns; carry out daily exercises in all the range of movement of the arm), evaluation of the cause of shoulder and arm morbidity, regular and progressive physical activity (eg, restoration of range of motion and resistance/strength exercises), and strategies for control of pain and prevention of lymphedema.3,12

A greater understanding of contributing risk factors is essential to establish prevention and management strategies.13 In recent years, large-scale prospective studies have been conducted to evaluate the incidence of upper-body symptoms after breast cancer surgery, mainly lymphedema,14–16 although we are not aware of any long-term prospective cohort study in Spain reporting upper-body morbidity in patients enrolled in a rehabilitation program after breast cancer surgery.

The main objective of this study was to determine the long-term predictive factors for upper-limb morbidity in patients who underwent breast cancer surgery and completed an early rehabilitation program.

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A prospective cohort study has been conducted to determine the incidence of upper-limb morbidity years after surgery and associated prognostic factors covering patients undergoing breast cancer surgery from April 1999 to June 2010. All patients were consecutively enrolled as part of an early rehabilitation program during the immediate postoperative period according to the upper-limb diagnosis and rehabilitation protocol established in the hospital's clinical practice guidelines on breast cancer. All patients were periodically reviewed according to the rehabilitation program and depending on the individual clinical situation (Table 1) until discharge. In the immediate postoperative period, all patients performed the first-day breathing exercises including diaphragmatic-abdominal breathing. From the second to fifth days, they performed upper-limb aerobic exercises without resistance: full range of movement of the elbow, wrist, and hand; 90° flexion, 60° abduction; internal rotation with complete adduction; and external rotation with 30° abduction of the shoulder. During this period, they also received written information on hygiene measures. One month after surgery, patients who had undergone ALND received written instructions on prevention of lymphedema with exercises and self-care measures.



If lymphedema developed, patients were treated with kinesiotherapy, pneumatic compression, compression sleeves, and manual lymphatic drainage if the lymphedema volume increased by 30% over the contralateral side. Pulsed ultrasound was indicated in lymphedema-related fibrosis.

Restricted shoulder mobility was treated with kinesiotherapy. Transcutaneous electrical nerve stimulation and pulsed ultrasound were indicated in patients with associated shoulder pain.

Cycle of physiotherapy consisted of daily sessions during 2 weeks, 30 minutes per session (regardless of the comorbidity treated), as outpatients.

A sample size was estimated on the basis of a 95% confidence level, a precision of 5%, an expected maximum complication rate of 50%, and losses to follow-up of 30%. Thus, a study population of 535 was deemed to be necessary. The University Hospital “12 de Octubre” Research Ethics Committee approved the study as part of the upper-limb diagnosis and rehabilitation protocol. Informed consent was obtained, and the rights of the subjects were protected.

The inclusion criteria were as follows: breast tumor ablation (mastectomy or breast-conserving surgery) with ALND or SLNB, and at least a minimum follow-up period of 6 months after surgery.

Patients were excluded if they had a history of cancer, bilateral breast cancer (primary or recurrence), and massive nodal (tumor infiltration in more than 80% of the dissected axillary lymph nodes) and/or distant metastasis.

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Outcome Measurements

Bilateral measurements (affected and contralateral limb) were recorded for each patient by medical rehabilitation specialists 1 and 6 months after breast cancer surgery and at the end of the follow-up period (Figure 1). The areas assessed are set out in the following text.

Fig. 1

Fig. 1

Passive motion of the shoulder (flexion, abduction, internal rotation, and external rotation) was measured with a goniometer.6 Limited mobility was considered pathologic when the restriction to the range of movement exceeded 20° degrees of flexion or abduction in relation to the standard values and in comparison with the nonoperated side.17 The degree of limited mobility was classified as mild, moderate, or severe depending on whether the restriction to the range of movement was 10% to 20%, 20% to 30%, or 30% or more, respectively.18

Arm volume was evaluated using the obtuse cone model described by Kuhnke19 (Figure 2). Lymphedema was defined as an increase in volume of 5% relative to the previous value and a 5% difference in relation to the contralateral upper extremity, with a correction for the dominant arm (5% over the nondominant arm).20–22

Fig. 2

Fig. 2

Pain was assessed using a visual analog scale scored as 0 (no pain), 3 to 4 (mild), 5 to 6 (moderate), and 6 to 10 (severe pain).23 Sensory loss was measured in the upper limbs, chest wall, and breast region using the pin-prick method and assessment of tactile sensitivity.

Upper-limb dysfunction (difficulties in performing tasks due to tiredness, heaviness, tightness, pain, tingling sensation, and numbness) was recorded during the physical examinations when patient reported it,24 with an “ad hoc” questionnaire evaluating the presence or absence of at least 2 or more of these symptoms.

Predictive variables included age, body mass index (BMI), regular physical activity, previous shoulder pathology, type of breast surgery, surgery side, postsurgical complications, SLNB/ALND, tumor size and histology, chemotherapy, radiotherapy, and hormonal treatment.

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Statistical Analysis

A descriptive study was conducted to identify the clinical characteristics of patients. Patients were classified into 2 categories according to the presence or absence of upper-limb morbidity (at least one of the following adverse effects: pain, limited range of motion in the shoulder, lymphedema, and/or upper-limb function deficit). The association between the presence or absence of upper-limb morbidity and predictive factors was analyzed using the χ2 test or Fisher's exact test. Univariate relative risks and their 95% confidence interval (CI) were estimated to identify predictors of morbidity. Multivariate logistic regression analysis was performed to predict the probability of morbidity. Variables with significance levels less than .05 remained in the final model.

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Patient Characteristics

The study population comprised 659 patients, all women. Of these, 130 were not eligible, 40 did not complete the minimum follow-up period, and 13 were excluded because they did not fulfill inclusion criteria (Figure 1). Of the remaining 476 participants, 39 patients died of breast cancer before the end of the follow-up period and 7 died of other causes.

Maximum follow-up was 136 months (11.3 years), with a mean follow-up of 72 months. The mean age at diagnosis was 54 years (range, 27-84 years).

The characteristics of the study population are presented in Table 2; disease characteristics are presented in Table 3.





One month after surgery, the most frequent upper-limb symptoms were sensory loss (54.2%), limitation of mobility (40.1%), and pain (25.1%). At 6 months, the most frequent symptoms were sensory loss (39.9%) and pain (26.9%). The most frequently diagnosed conditions at the end of the follow-up period were sensory loss (31.9%) and pain (28.7%) (Figure 3).

Fig. 3

Fig. 3

The frequency of lymphedema increased from 1.9% (n = 9) at 1 month after surgery to 18.4% (n = 87) at the end of the follow-up period, mainly developed during the first 9 months (74.1% of patients presented with lymphedema within this period).

A total of 306 patients (64.4%) showed upper-limb symptoms at some point during the follow-up period.

During the first 6 months after surgery, 355 patients (74.6%) did not require additional rehabilitation. Thereafter, and until the end of the follow-up period, 179 patients (37.6%) required rehabilitation for any cause; of these, 29 (6.1%) fulfilled 1 cycle of physiotherapy, 75 (15.8%) 2 cycles, and 49 (27.4%) required 4 or more cycles of physiotherapy.

At the end of the follow-up, 8.9% patients (n = 42) had limitations for their daily life activities due to severe pain, 7% or more due to severe mobility restriction, and more than 30% due to lymphedema.

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Univariate Regression Analysis

Univariate regression analysis was conducted to identify the baseline variables that contributed to arm morbidity (Table 4). Statistically significant risk factors for restricted mobility included regional lymph node radiotherapy (relative risk [RR] = 1.98; 95% CI, 1.30-3.02) and removal of more than 15 lymph nodes (RR = 2.55; 95% CI, 1.61-4.04). Experiencing previous shoulder pathology was associated with restricted shoulder mobility (RR = 2.09; 95% CI, 1.76-2.49). Pain and upper-limb dysfunction were associated with previous shoulder pathology, chemotherapy, and removal of more than 15 lymph nodes.



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Multivariate Logistic Regression Analysis

The multivariate logistic regression revealed statistically significant predictors of arm morbidity (Table 5). In the model, previous shoulder pathology, postsurgical events (seroma, hematoma, wound dehiscence, or wound infection), obesity, and site of radiotherapy were predictive factors for arm symptoms during the follow-up period. Patients with previous shoulder pathology were 6 times more likely to be in the group with arm morbidity (odds ratio [OR] = 6.049; 95% CI, 2.89-12.63; P < .0001).



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The findings show that women with previous shoulder pathology, obesity, postsurgical complications (seroma, hematoma, wound dehiscence, or wound infection), and radiotherapy administered to regional lymph nodes were more likely to develop shoulder-arm symptoms after breast cancer surgery.

Multiple factors have been associated with arm morbidity in breast cancer. According to Kootstra et al,9 shoulder-arm function 6 weeks after surgery and age are the strongest predictors for shoulder-arm function in the long term.

The analysis of age groups revealed no statistically significant differences, with findings were similar to those reported by Yang et al5 in 2010.

It was found that BMI of 30 or more was associated with arm morbidity. Other authors also found obesity to be a significant risk factor for lymphedema, indicating that these patients should be more closely monitored.16,25 For example, Sagen et al26 evaluated 2 rehabilitation programs in 2009 and found BMI of 25 or more to be the only risk factor for arm disability.

The postsurgical complications examined in our study (seroma, hematoma, wound dehiscence, and wound infection) were significantly associated with overall morbidity. These results contrast with those of Kootstra et al,3 who found that complications of the surgical wound had no effect on arm function or volume.

Kootstra et al3,9 and other authors27,28 indicate that ALND, which continues to be the standard treatment in node-positive breast, can be associated with significant morbidity and abnormal accumulation of fluid. ALND was found to be a risk factor for overall morbidity (RR = 1.23; 95% CI, 1.07-1.40) in the univariate analysis, which showed that the incidence of arm morbidity was greater than that of SLNB.

Studies investigating the effect of SLNB and ALND on the incidence of lymphedema29–32 revealed similar results, namely, that the prevalence of lymphedema is lower when SLNB is performed.25,32,33

Hayes et al6 found that more extensive breast surgery increases the probability of lymphedema independently of the extent of axillary dissection. However, other authors specify that the type of surgery did not affect shoulder dysfunction, lymphedema, or arm function.3 In our study, radical surgery of the breast was significantly correlated with overall morbidity in the univariate analysis but did not remain in the final model in the multivariate analysis.

In their systematic review, Stuiver et al34 found that patients who received radiotherapy were more likely to have lymphedema and that residual morbidity was associated with radiotherapy administered to the axilla.32 The results did not show a correlation between radiotherapy and arm morbidity. However, we did find an association between irradiation of locoregional axillary nodes and overall morbidity.

Therefore, lymphedema remains a frequent problem (even years after treatment of breast cancer),35 although there is no evidence to suggest which approach (instructions on prevention of lymphedema, kinesiotherapy, pneumatic compression, compression sleeves, or manual lymphatic drainage) is most effective.36

The effects of conservative nonpharmacological interventions for preventing clinically detectable upper-limb lymphedema after treatment of breast cancer were recently assessed in a Cochrane systematic review,34 which stated that no firm conclusions can be drawn on the effectiveness of interventions involving manual lymph drainage. However, the review did mention that shoulder-mobilizing exercises early after surgery do not entail a higher risk of lymphedema and are better for shoulder mobility in the short term.

The finding that restricted shoulder mobility was greater in the immediate postsurgical period agrees with the findings of other authors.3 In addition, Scaffidi et al11 reported that the early rehabilitation program reduced the articular and functional limitation of the upper limb after breast cancer treatment in most patients. The authors stated that early assisted mobilization and home rehabilitation with written information on preventive and hygiene measures play a crucial role in reducing the occurrence of postoperative adverse effects in the upper limb. In our study, we found that after 1 month postsurgery, 40.1% of patients showed restricted shoulder, with mobility declining to 15.3% at 6 months and 14.5% after more than 6 months of follow-up; of these, 26.7% recovered their mobility after physiotherapy during the first month, 16.8% after 6 months, and 11.4% at the end of the follow-up period.

Pain is usually associated with restricted mobility, limitations in activities of daily living, and upper-limb dysfunction. Although this adverse effect remains the main impairment over the years,37 it was found that even if pain was the most frequent cause of upper-limb morbidity, its intensity was usually mild, suggesting that it could be relieved by rehabilitation.26

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Study Limitations

Our study is subject to a series of limitations. First, although the morbidity assessment was conducted as objectively as possible, assessment of upper-limb dysfunction and pain may have a subjective component.

Second, no specific questionnaire was applied to collect data on upper-limb dysfunction.

Third, additional factors such as social status, education, incomes, occupation, or race, none of which were recorded in our study, could influence the perception of morbidity.

However, we believe that one of the strengths of this study is that data are reported from a 10-year follow-up period and, despite the presence of losses, the prevalence and incidence of upper-limb morbidity are consistent with those reported elsewhere. In addition, assessments were based on objective parameters recorded during the clinical examination that were evaluated taking into account the difference between the affected and unaffected sides. This provided an objective view of upper-limb morbidity associated with breast cancer surgery.

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The main long-term predictive factors for shoulder-arm morbidity are previous shoulder pathology, postsurgical events, obesity, and regional lymph node radiotherapy. These factors must be taken into account during evaluation of patients diagnosed with breast cancer in order to enable early diagnosis of upper-limb impairment. This early diagnosis prevents worsening of adverse effects and reduces the number of patients who require additional rehabilitation.

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The authors thank Grünenthal Pharma S.A. for language translation resources.

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carcinoma of the breast; lymphedema; outcome assessment; predictive factors

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