Preserving and Restoring Function after Local Treatment

Andrea L. Cheville

INTRODUCTION

Primary breast cancer treatment is associated with long-term musculoskeletal problems in up to one third of patients. This is significant because of the favorable survival enjoyed by the majority of women diagnosed with breast cancer. Current estimates suggest that there are 2.9 million breast cancer survivors alive in the United States, and millions more worldwide (1). Physical impairments develop secondary to normal tissue damage inflicted through cancer removal and staging procedures. Nerves, muscles, stroma, and lymphatics fall within surgical and radiation treatment fields leaving them vulnerable to inadvertent injury. Musculoskeletal problems may develop within, adjacent to, or distant from treatment fields, manifesting as impairments in strength, flexibility, and integrated movement patterns (2). Table 39-1 lists impairments associated with breast cancer treatments, some of which may persist for decades following treatment. At all time points, impairments may be associated with disability and diminished health related quality of life (HRQOL) (3, 4, 5, 6 and 7). The likelihood of long-term disability correlates directly with the intensity and extent of breast cancer treatment. More surgery (e.g., axillary lymph node dissection [ALND] versus sentinel lymph node biopsy [SLNB]) and more radiation (e.g., four-field versus tangent beam configurations) increase the probability that patients will develop musculoskeletal problems (3, 8, 9).

Empirical data now reinforce theoretical concerns that musculoskeletal pathology at surgical and radiation sites will not spontaneously resolve independent of treatment. (10). Ninety percent of breast cancer survivors report one or more adverse treatment effects 6 months following their diagnoses, with 60% endorsing multiple problems (11). Unfortunately, such problems persist for the 30% of survivors who continue to report adverse sequelae 6 years after their diagnoses (11). Elderly patients and those with elevated body mass indices are at increased risk of developing lasting functional deficits following their breast cancer treatment (12).

Despite the clear correlation between breast cancer treatment and musculoskeletal problems, tissue-level changes remain ill defined. Radiation-induced fibrosis has been implicated on the basis of long-term follow-up studies (13, 14). Additional radiation-related problems include shoulder capsule and epimesial contractures, brachial plexopathies, lymphostasis leading to accumulation of inflammatory mediators (15), and muscle hypertonicity secondary to direct or neural irritation. However, no empirical links yet implicate these processes in the development of treatmentrelated impairments. Surgical procedures, even when limited to local tumor excision and SLNB, can produce maladaptive changes in posture and upper quadrant movement patterns. These changes are thought to be mediated through pain, scarring, and adaptive positioning in the postoperative period. Adjuvant chemotherapy may also contribute to musculoskeletal problems by reducing muscle mass (16) and oxidative capacity (17). The relative contributions of different cancer treatments and pathological processes to functional problems remain poorly characterized despite a growing understanding of treatment-related late toxicities. Manual treatments and therapeutic exercises may effectively address most problems (18), although systematic reviews, noting a paucity of rigorous randomized trials, have remarked the persistent need for better quality evidence (19).

Successful management of musculoskeletal problems depends on a patients’ willingness to perform therapeutic exercises. Because treatments are active and must often be continued for extended intervals, its success requires a high level of adherence. Patient “buy in” can be substantially enhanced by the strong endorsement of the entire breast
cancer treatment team. With increasing appreciation of latent treatment toxicities, prophylactic stretching and strengthening activities are now accepted as integral components of comprehensive survivorship care. In the absence of such preventative activities, breast cancer survivors, treated years previously, may become uniquely vulnerable to delayed morbidities that manifest when the musculoskeletal and other systems senesce (20). This chapter will outline the evidence base regarding the epidemiology and management of breast cancer treatment-related musculoskeletal morbidity.

TABLE 39-1 Physical Impairments Affecting the Shoulder, Cervical Spine, and Thoracic Spine Following Primary Breast Cancer Treatment

Shoulder Complex
Restricted scapulothoracic motion Glenohumeral joint contracture Pectoralis major and minor muscle shortening Muscle weakness
	Serratus anterior Middle trapezius Rhomboids Hand intrinsics
Myofascial dysfunction
	Middle trapezius muscle Rhomboid muscle
Maladaptive neuromuscular recruitment patterns
Cervical Spine
Exaggerated lordosis Myofascial dysfunction
	Upper trapezius muscle Levator scapulae muscle
Restricted range of motion
	Lateral rotation Lateral bending
Thoracic Spine
Exaggerated kyphosis Intercostal muscle contracture

EPIDEMIOLOGY

Upper quadrant disability following breast cancer treatment is primarily due to restricted range of motion (ROM), persistent pain and diminished strength. Reported incidences of these problems vary widely depending on the type of breast cancer treatment, measurement technique, and duration of follow-up. Systematic reviews consistently comment on the heterogeneity of measurement and reporting strategies that characterize the literature on treatment-related morbidity (14, 21, 22). None-the-less, all concur that late musculoskeletal effects are potentially prevalent and problematic among breast cancer survivors.

Loss of Range of Motion

Survivors who develop ROM deficits are more likely to report pain, reduced HRQOL and difficulty performing activities of daily living (23). Table 39-2 lists shoulder ROM deficits reported at different time points following surgery. Most patients experience an abrupt transient reduction in shoulder ROM after breast cancer surgeries (3, 24). Two weeks postoperatively, incidences of restricted ROM as high as 86% have been reported following ALND, and 45% following SLNB (25). However, it should be noted that some surgeons, to reduce the risk of seroma formation, restrict active shoulder abduction to 90° until drain removal which may occur as late as 3 to 4 weeks postoperatively (26).

By 6 weeks the postoperative incidence of restricted shoulder abduction is substantially lessened to 26.5% after ALND, and 24.8% after SLNB (27). Longitudinal studies suggest that restrictions in shoulder ROM gradually resolve to near baseline in a majority of patients (5, 28). However, a significant minority of patients do not recover normal shoulder ROM in abduction, forward flexion, and/or external rotation. A history of ALND, modified radical mastectomy, and radiation therapy are associated with more significant and lasting limitations (5, 27, 29, 30 and 31). Older age and elevated BMI also increase the risk of persistent ROM deficits (30).

Pain

Recent reports have highlighted the potential for persistent and severe upper quadrant pain following breast cancer treatment (32). The presence of moderate or worse pain among breast cancer survivors is strongly associated with poor mental and physical functioning (29, 33). Pain is more common after ALND and axillary/supraclavicular radiation (4, 32). Few studies differentiate musculoskeletal pain from neurogenic or lymphedema-related pain. Table 39-3 lists reported pain prevalence. Reports neither specify pain etiologies, nor report consistent outcome measures (e.g., presence/absence of pain versus visual analogue scores [VAS]). The data are therefore challenging to synthesize. However, the table clearly demonstrates that a significant percentage of patients experience persistent pain in the shoulder or arm. A unique study that integrated pain maps from 343 breast cancer survivors established that post-treatment pain may affect the entirety of the upper quadrant, but occurs most commonly in the axilla (34).

Loss of Strength

Strength deficits are less prevalent immediately following breast surgery but become increasingly problematic with time. This pattern has been appreciated for grip strength. In a longitudinal cohort, mean grip strength decreased by 16.9 Nm at 6 weeks and by 41.3 Nm at 24 months after ALND, relative to preoperative values (5, 27). A similar pattern was noted after SLNB though the reduction was less pronounced, 5.8 Nm at 6 weeks and 17.2 Nm at 24 months. These reductions agree with high reported prevalence of impaired grip strength, which range from 16% to 40% (23, 35). The influence of Lymphedema (LE) on grip strength remain inadequately characterized but may be an important mediating factor (36). Prevalence of reduced shoulder and arm strength are also high with self-reported limitations affecting up to 69% of patients (37). Objective reductions of 10 nM in shoulder abduction strength have been detected at 12 and 24 months following treatment (5, 23). Shoulder strength deficits are more common following modified radical mastectomy (38).

Musculoskeletal Syndromes

Axillary web syndrome, Figure 39-1, manifests as taut cords that extend distally along the medial arm from the treated axilla to the cubit and, at times, as far as the wrist. Incidence estimates range from 5.2% to 72%, with completion axillary dissection being a potential inciting factor (25, 39, 40, 41, 42). Retrospective studies produced lower incidence estimates (41). Pathological analyses suggest that superficial lymphatic

vessels and veins, together with their surrounding connective tissue, comprise the cords (41). The natural history of axillary web syndrome is self-limited with gradual resolution over the first year following surgery without residua (41). However, the cords can be quite painful and may discourage patients from performing needed shoulder ROM activities, thereby contributing to long-term ROM deficits (42).

TABLE 39-2 Prevalence and Severity of Shoulder Range of Motion Deficits at Different Time Points Following Breast Cancer Surgery

Outcome Measure

Author (Reference)

Elapsed Time after Breast Cancer Surgery^a

6 wks

3 mos

6 mos

9-12 mos

18-24 mo

>2 yrs

ALND

SLNB

ALND

SLNB

ALND

SLNB

ALND

SLNB

ALND

SLNB

ALND

SLNB

Mean decrease from ipsilateral baseline AB

Rietman et al. 2003, 2006 (27, 5)

26.4°

24.7°

21.0°

5.5°

Purushotham et al. 2005 (60)

6.3°

3.1°

Mansel et al. 2006 (28)

4.2°

1.9°

2.3°

1.5°

1.9°

2.5°

Husted Madsen et al. 2008 (61)

11.0°

5.0°

9.0°

4.0°

Mean difference in AB relative to untreated shoulder

Hack et al. 1999 (35)

6.4°

Kaya et al. 2010 (33)

14.4°

ROM <160° AB

Ernst et al. 2002 (38)

14.0%

8.0%

ROM <20° normal value ≥1 plane

Langer et al. 2007 (62)

11.3%

3.5%

Self-reported limitation ROM

Leidenius et al. 2005 (63)

34.0%

16.0%

Warmuth et al. 1998 (64)

8.0%

Veronesi et al. 2003 (65)

27.0%

0.0%

21.0%

0.0%

Land et al. 2010 (66)

3.0%

2.0%

3.0%

1.0%

2.0%

Decrease in lateral AB

Gill 2009 (67)

4.4%

2.8%

ROM <normative values any plane

Lauridsen et al. 2008 (9)

35%

Mean ROM (normal = 180°)

Rietman et al. 2004 (68)

156.6°

Gosselink et al. 2003 (3)

FF 126° MRM

150° BCT

Peintinger et al. 2003 (24)

143.8° AB

158.9° AB

Lateral AB <140°

Kopec et al. 2012 (69)

8.30%

140°-159°

21.20%

160°-179°

44%

Lateral AB (ipsilateral-contralateral)/(contralateral) × 100% 5-10%

Ashikaga et al. 2010 (70)

13.1%

10.1%

≥10%

9.0%

5.70%

^aFor studies that did not collect data at specified intervals, the elapsed time after surgery is the cohort average.
ALND, axillary lymph node dissection; SLNB, sentinel lymph node biopsy; FF, forward flexion; AB, abduction; BCT, Breast-conservation therapy; MRM, modified radical mastectomy.

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