Introduction
Shoulder dysfunction is a common complication seen in breast cancer survivors. The incidence of ipsilateral shoulder pain, stiffness, swelling, and numbness is in over 80% of survivors. The patients often present with difficulties with the movement of the affected upper extremity limiting their ability to carry objects, reach overhead, push or pull, as well as perform activities of daily living, such as grooming and self-feeding. These functional deficits can affect breast cancer survivors’ productivity and their ability to return to work. Breast cancer survivors with decrease range of motion of the shoulder have 2.5 more likelihood to loose productivity compared to survivors who do not present shoulder dysfunction. Women who have arm and shoulder morbidity after breast cancer treatment report higher levels of disability, which ultimately limits their ability to return to work. This is especially the case of musicians, who even 5 years after treatment feel their identity and livelihood are threatened by the presence of shoulder pathology after breast cancer treatment. Furthermore, more than a third of breast cancer survivors feel less capable and less confident to use their arm due to a shoulder problem, which interferes with their ability to participate in recreational activities such as golf or tennis.
Anatomy and Biomechanics
The shoulder is the most mobile joint in the human body. It is composed of three bones and four articular surfaces: (1) the clavicle, which articulates with the sternum and the acromion to form the sternoclavicular and acromioclavicular joints, respectively; (2) the scapula, which articulates with the thorax to form the scapulothoracic joint; and (3) the proximal humerus, which articulates with the glenoid fossa to form the glenohumeral joint. Even though this is a “ball-and-socket” type of synovial joint, its stability comes from several different sources: static and dynamic restraints. The synovial capsule, labrum, and ligaments constitute the static restraints. Static restraints are important at rest and at the end of range of motion.
However, static structures alone are insufficient to stabilize the shoulder motion. Dynamic restraints play an important role during midrange of motion and are based on three general principles: concavity compression, muscle stiffness, and tendon compliance. Concavity compression refers to compression of the humeral head into the glenoid fossa. This action is primarily accomplished by rotator cuff muscles (supraspinatus, infraspinatus, teres minor, and subscapularis), although, the deltoid and long head of the biceps also contribute. Most of the rotator cuff muscles are helpful in stabilizing the shoulder anteriorly during abduction, while the subscapularis muscles stabilize the shoulder posteriorly.
Joint stability also depends on the interplay between the forces of the muscles, which is also known as torque. The strength during shoulder adduction is the highest, which is two times the torque force of abduction. Extension, flexion, abduction, and internal and external rotations follow adduction from the strongest to the weakest. These forces contribute to maintain the stability of the shoulder during active motion and during the influence of external forces. The last component of the dynamic restraints is the tendons. The tendon compliance allows them to store energy while they are being elongated and use it when they return to its original length, which contribute to keeping the head of the humerus in the right position.
Breast cancer survivors have increased internal rotation of the scapula and reduced external rotation. The change in the alignment of these structures results in a smaller subacromial space and compression of the rotator cuff structures. Scapula internal rotation also forces the head of the humerus joint into external rotation, which causes further impingement of the rotator cuff.
Patient Assessment
History and Self-Reported Function
As with other musculoskeletal complaints, a thorough evaluation and a detailed history are key elements when identifying the source of the dysfunction. Symptom characteristics, onset, intensity, exacerbating/alleviating factors as well as associated functional limitations provide important clues about the source of the complaints. Preexisting shoulder pathology can often be exacerbated by breast cancer and its treatments; therefore it is important to understand the onset of the symptoms, history of trauma, occupation, and functional deficits present prior to the breast cancer diagnosis.
The oncologic history, including staging and oncologic treatments, is indispensable when evaluating shoulder dysfunction. In cases of advanced breast cancer and worsening shoulder pain, metastatic disease to the proximal humerus or the scapula should be taken into consideration. They frequently present with functional pain and/or pathologic fractures. Pain aggravated by movements and limitations in the range of motion can be observed during the physical examination. However, with the increasing survival rate in breast cancer patients, most of the cases of shoulder dysfunction are consequences of the cancer treatment, rather than progression of the disease. The extent of the cancer treatment is related to the risk of shoulder dysfunction. Patients who need conservative breast cancer surgery have less risk of developing shoulder dysfunction when compared to those who need more aggressive surgeries (i.e., mastectomy, lymph node dissection) or radiation therapy.
Questionnaires to asses self-reported disability levels are commonly used to evaluate the impact of the symptoms in the functional level of the patients. The Disability of the Arm, Shoulder and Hand (DASH and Quick-DASH) is a validated tool that has been utilized to measure the self-reported upper extremity function in breast cancer patients. One study found that up to 36% of breast cancer patients feel less capable of using their upper extremity and have moderate-to-severe difficulties participating in recreational activities that involve the use of the upper extremities, such as tennis or golf. Although the results of the DASH could be influenced by the presence of lymphedema in the affected upper extremity, it is a tool that when used with a good history and examination can provide valuable information.
Physical Examination
Inspection
Unlike other patients, the breast cancer population frequently has clear evidence of asymmetries due to the presence of a mass, changes in the skin pigmentation due to radiation, or changes in the anatomy due to surgical interventions. In these cases, knowing the muscles involved during the surgical procedure could help understand the changes in a patient’s biomechanics. In addition, changes such as muscle atrophy can be the result of nerve injury, causing an imbalance of the forces of the shoulder muscles, critically important for its mobility and stability. Evaluation of the angle of the scapula for the presence of protrusion or winging could be another indication of injury of a peripheral nerve, such as the long thoracic nerve.
Palpation
Palpation of the shoulder girdle is useful to identify points of tenderness, masses, deformities, or crepitus. Deformities in the bony structure and crepitus are suggestive of possible fractures, while masses can be the result of enlarged lymph nodes, abscess, seroma, or presence of a tumor. Tendinopathy is often associated with tenderness along the trajectory of the tendon. Furthermore, the presence of tender areas and palpable bands in the skeletal muscles, known as myofascial trigger points, is another cause of tenderness in this patient population. During the palpation of the axillary area findings such as superficial tight cords are indicative of axillary web syndrome. Although cording can be found in the chest or the arm, the axilla is the most common place. It is usually observed in patients that have undergone axillary node dissection.
Range of Motion
The large mobility of the shoulder is one of its most distinctive characteristics. Therefore it is not a surprise that the evaluation of the range of motion is a critical component of the physical examination. The shoulder is the most mobile joint in the body. It allows 150–180 degrees of forward flexion and 40–60 degrees of extension in the sagittal plane. In the coronal plane, abduction ranges between 150 and 180 degrees; and in the axial plane, external rotation ranges between 60 and 90 degrees, while internal rotation ranges between 50 and 70 degrees. Breast cancer survivors have up to 60% reduction in flexion and abduction mobility 1 month after surgery, and 10% reduction at the 12-month mark. A loss of 3–17 degrees of external rotation and 1–4 degrees of internal rotation have also been reported. Decreased mobility with passive motion is more indicative of pathologies such as adhesive capsulitis, degenerative changes of the glenohumeral joint, pectoralis tightness, or radiation fibrosis. On the contrary, preserved passive mobility with evidence of limitations during active range of motion is suggestive of rotator cuff dysfunction.
Surgical interventions increase the risk of developing adhesive capsulitis. Patients with this pathology present with multidirectional restrictions in the passive evaluation of the shoulder range motion. However, limitations are typically pronounced during external rotation. Similarly, tightness of the pectoralis muscles can decrease the shoulder’s range of motion in breast cancer survivors. Anterior chest wall tightness in conjunction with scar tissue formation, radiation fibrosis, and patient acquisition of a protective posture causes malalignment of the shoulder structures. These forces result in a forward depression of the shoulder girdle, which prompts a decrease in the size of the subacromial space and compression of the supraspinatus tendon and long head of the biceps tendon, subacromial bursa, and a portion of the glenohumeral joint capsule. This is known as the subacromial impingement syndrome and it is associated with rotator cuff dysfunction.
Rotator cuff disease is the leading cause of shoulder pain in the general population. Shoulder malalignment is a major contributor to the development of rotator cuff pathology in the breast cancer population. Dysfunction of the rotator cuff muscles presents with pain and weakness during shoulder active range of motion. In addition, patients report pain in the lateral and anterior aspect of the shoulder, which on occasion radiates to the ipsilateral elbow. The pain is usually exacerbated by overhead movements and is known to have an important impact in patient function. Additional tests can be used for the evaluation of possible subacromial impingement syndrome and the integrity of the rotator cuff muscles. Neer and Hawkins-Kennedy are well-known impingement tests, while positive painful arc, drop arm, job tests, and pain with resisted internal and external rotation are suggestive of a rotator cuff pathology, likely involving the supraspinatus tendon. For the evaluation of a possible subscapularis tear, the belly off test is the most sensitive test described by the literature.
As the patient performs active range of motion of the shoulder, close attention needs to be given to the patient’s general posture and bilateral scapula movements. The imbalance of the shoulder girdle muscles, pain and changes in the shoulder girdle alignment are likely to alter the motion of the scapula over the posterior chest wall. Evaluation of the scapula alignment also includes the push-off wall test, which is useful to determine the presence of scapular winging caused by injury to the serratus anterior muscle or the long thoracic nerve (medial winging); or to the trapezius or cranial nerve XI (lateral winging).
Steven D. Waldman MD, JD, in Atlas of Uncommon Pain Syndromes (Third Edition), 2014
©2019 Elsevier B.V. or its licensors or contributors. ScienceDirect® is a registered trademark of Elsevier B.V.
Kennedy-Hawkins: fig 5.87B from Magee DJ: Orthopedic Physical Assessment, 6 th edition, St Louis, Saunders/Elsevier, 2014, p318, ISBN: 978-1-4557-0977-9.
Empty can: fig 20.36 from Mark H. Swartz, Darwin Chen and Jimmy Chan, The Musculoskeletal System; in: Swartz (ed): Textbook of Physical Diagnosis: History and Examination, 8 th edition, Elsevier, 2021, ch20, pp429–472, ISBN: 978-0-323-67292-4.
Motor Exam
Bilateral evaluation of the shoulder girdle muscle strength is necessary for comparison. Isolation of the specific action(s) of each muscle is recommended to identify possible isolated muscle weakness due to nerve damage or injury to the muscle itself. Weakness and decreased active range of motion are suggestive of tears of the muscle tendons. In the breast cancer population, changes in the shoulder’s biomechanics described previously put the supraspinatus muscle and its tendon at a higher risk of injury. Similarly, examination of the anterior chest wall muscles should be included. Pain in the anterior chest or anterior shoulder is suggestive of a pectoralis muscle pathology.
Sensory
Sensory innervation of the shoulder is provided by the axillary, supraclavicular, and suprascapular nerves. The axillary nerve originates from the brachial plexus and provides sensation to the lateral, anterolateral, and posterolateral aspect of the shoulder. The supraclavicular nerve is originated out of branches of C3 and C4 nerve roots and provides sensation along the clavicle up to the superior aspect of the trapezius muscle region. Lastly, the suprascapular nerve, a branch of the upper trunk of the brachial plexus, carries the sensory inputs of the acromioclavicular joint and glenohumeral joint.
The intercostal nerves have an important role in the development of postmastectomy pain. The intercostal brachial nerve, which is branch of the second intercostal nerve, provides sensory innervation to the upper thoracic dermatomes (T1 and T2), including the axilla, medial upper arm, and chest. These sensory branches are often scarified during axillary dissections in the presence of positive lymph nodes. Chronic pain and postmastectomy pain syndrome are closely associated with injury to the intercostal brachial nerve. Furthermore axillary lymph node dissection is associated with pain, numbness, and stiffness, which negatively affect the quality of life of breast cancer survivors. Perineural injections of the intercostal brachial nerve have shown benefits in the management of postmastectomy pain syndrome secondary to intercostal brachial neuralgia. These findings confirm the role that injuries caused to this nerve have in the development of chronic pain syndrome in cancer survivors.
Tumor-Related Impairments
Increasing efforts in breast cancer screening have resulted in earlier detection of the disease. Therefore impairments secondary to the tumors are less frequently seen. There is lack of studies that evaluate the direct effects of breast cancer mass to the function of the ipsilateral shoulder. However, it is believed that once diagnosed, there is a tendency for survivors to protect the affected side, limiting the level of activity that they are used to perform with the ipsilateral upper extremity. In a study performed by Flores and Dwyer, the shoulder range of motion of 33 women was tested after biopsy but before surgery. Surprisingly, they found a significant reduction of the range of motion of the shoulder. Furthermore, African-American survivors were found to have greater reduction of shoulder flexion when compared to Whites. More research needs to be conducted to understand the implication of breast cancer in shoulder function prior to the start of oncological treatments.
Surgical-Related Impairments
Functional limitations are believed to be at its peak in the first couple of months of surgery but have been reported even 6 years after surgery. The most prevalent complaint is the difficulty to perform overhead activities, reported in 42%–56% of survivors followed by pain, which is present in 22%–38% of the patients. Flores and Dwyer measured the shoulder range of motions before and after breast cancer surgery. In this study, all shoulder motions, except internal rotation, had a statistically significant reduced range of motion. However, abduction was found to be the most affected shoulder movement. Two weeks after surgery, the patients were able to achieve only 83 degrees of abduction, which is significantly below the 150–180 degrees that are considered normal.
However, it is not only a matter of timing. The extent of the surgical intervention, conservative versus nonconservative surgery, and lymph node involvement plays a role in the risk of developing shoulder functional impairments. A cross-sectional study performed in 150 breast cancer survivors reported greater pain and movement deviations in those patients that underwent mastectomy.
Conserving Surgery
Breast-conserving surgery, including lumpectomy, partial mastectomy, or wide local excision, is associated with lower risk of postoperative shoulder dysfunction. The average DASH score in postlumpectomy patients is 9.88 (0–100, where the higher the number the greater the disability) and around 8% of the patients report shoulder stiffness. However, the incidence of shoulder pain ranges between 8% and 31%, even 5 year after the surgery. Breast cancer survivors tend to report lower levels of shoulder dysfunction (31% of survivors) compared to objective findings of 20 degrees or more of decreased range of motion (49% of survivors). These findings suggest that patients may not notice smaller decreases in shoulder motion and/or develop compensatory strategies that allow them to continue to carry their prior level of activity.
Women who undergo breast-conserving surgery are not exempt from developing dysfunction of the shoulder girdle or shoulder pain. Shoulder impairments associated to breast-conserving surgery, although less frequent, can still have an impact in breast cancer survivors’ function and quality of life. Therefore a thorough evaluation of the shoulder function by health-care providers is highly recommended.
Mastectomy
Breast cancer survivors who undergo mastectomy are known to be at a higher risk of developing shoulder dysfunction, especially in the acute postoperative period. The average DASH score in postmastectomy patients is 24.4 (>20 is associated with major disability) 4 months after the surgery and 12.9 at the year mark. Similarly, 6 months postmastectomy, breast cancer survivors have a 20% prevalence of decreased shoulder range of motion, and 50% prevalence of difficulties with overhead activities, versus 10% and 47% 12 months after the surgery. Controversially, patients have higher levels of neck–shoulder pain at 12 months (40.6%) than at 6 months (38.5%) were observed.
The perceived disability changes are associated with changes in the biomechanics of the shoulder function. Patients who undergo mastectomy have greater upward rotation of the scapula. This change could be a compensatory mechanism secondary to glenohumeral joint dysfunction, such as in cases of adhesive capsulitis. Decrease in muscle activity observed in pectoralis major, upper trapezius, and rhomboid muscles are likely responsible for some of the biomechanical deviations.
When evaluating shoulder range of motion, postmastectomy patients present limitations in all planes. However, abduction and flexion are affected the most. Impaired flexion and abduction of more than 25 degrees has been reported in 24% and 38% of postmastectomy patients, respectively. Limitations are greater in women with involvement of the nondominant side. Furthermore, patients who develop surgical seromas have reduced external rotation. Tightness of the anterior chest wall muscles has been reported in 16% of breast cancer survivors who undergo mastectomy.
Mastectomy is the strongest risk factor for the development of adhesive capsulitis. Its incidence has been reported between 7.7% and 10.3% of the cases. Moreover, patients who undergo reconstruction after mastectomy are at a bigger risk as well as those who receive adjuvant radiation therapy. The onset of adhesive capsulitis is insidious. However, an onset as early as 4 months has been suggested.
Lymph Node Dissection
Axillary lymph node dissection is another risk factor for the development of shoulder dysfunction. Patients that undergo axillary lymph node dissection have a significant reduction in internal rotation strength with a mean loss of 2.2 kg. Range of motion in all planes has also been described, with shoulder abduction and flexion being affected the most. A reduction of 3.2 to 21 degrees of abduction and 5 to 6.3 degrees of flexion has been described at the 12-month mark. Shoulder impairments associated with lymph node dissection are typically seen early in the postoperative period. However, other studies suggest that patients that undergo sentinel lymph node biopsy or axillary node dissection report shoulder pain (9%–25%) and stiffness (14%–24%) 6 years after the surgery. In addition, a correlation of the number of lymph nodes removed with the degree of the shoulder impairments has been described. Women with positive lymph nodes required more aggressive treatment, which could also result in greater deficits.
Breast cancer survivors who undergo axillary lymph node dissection are at a higher risk of developing axillary web syndrome (71%) compared to patients that undergo single lymph node biopsy (6%–41%). A higher number of lymph nodes resected along with lower body mass index and younger age are risk factors for the development of axillary web syndrome. In the early postoperative period, axillary web syndrome is more frequent, and it is associated with reduced shoulder abduction. However, it is believed that the presence of chronic cords can result in worsening mobility of the shoulder.
Breast Reconstructive Surgery
As the flap options for breast reconstructive surgery increase, changes in shoulder biomechanics bring different challenges. Myung et al. evaluated the effects of implant insertion, latissimus dorsalis flap and transverse rectus abdominis musculocutaneous flap on the shoulder muscle strength. Three months after the surgery there were no significant differences observed within groups. However, at the 6-month mark, the patients who underwent latissimus dorsalis flap had greater shoulder deficits. These findings are similar to other studies that showed shoulder weakness 6 month after a latissimus dorsalis flap reconstruction, especially during abduction, internal rotation, and adduction. Breast cancer survivors who undergo transverse rectus abdominis musculocutaneous flap show a faster recovery rate.
Decrease in shoulder muscle strength translates into functional impairments that interfere with breast cancer survivor daily activities. Unilateral latissimus dorsi reconstruction is associated with functional impairment during the first 3 months after the surgery. Furthermore, bilateral extended autologous latissimus dorsi reconstruction has been associated with an increase in DASH scores of 25 points at 3 months and 18 points at 6 months (minimal clinically significant change=12.7 points). Although the tendency is to recover over time, due to the heterogenicity of the procedures and studies as well as potential confounding factors (i.e., access to therapy, lymph node involvement, age, body mass index), there is no consensus in the literature as per the long-term effects of latissimus dorsi reconstruction on shoulder function.
The type of breast reconstruction after mastectomy has a significant impact on the shoulder associated morbidity. Survivors who undergo a reconstruction that involves the use of the latissimus dorsi have a higher risk of developing shoulder pathology. However, the use of expander–implants has also been associated with shoulder dysfunction. Around 23.8% of women who undergo expander–implants reconstruction develop shoulder impairments. The implants inserted under the subpectoral space are thought to cause increased tension of the pectoralis muscle and tendon resulting in pectoralis tightness. During the procedure the muscle is also detached from the lower ribs and the sternum causing further injury to the muscle fibers. Pain associated to this intervention is exacerbated during the expansion period. As mentioned before, pain and pectoralis muscle tightness often result in changes in the biomechanics of the scapula and shoulder movement resulting in shoulder dysfunction. The use of expander–implants for breast cancer survivors has an odds ratio of 2.15 ( p +0.010) of developing shoulder dysfunction. Most of the shoulder morbidity is secondary to decrease in the shoulder range of motion during abduction and flexion.
