A Review of Lameness Attributable to the Shoulder in the Dog: Part Two
The scapulohumeral joint is a common site of forelimb lameness in the dog. Establishing a definitive diagnosis may be difficult because of the limitations of orthopedic examination and radiographs and the inherent elusiveness of the associated conditions.
The intent of this review is to present, in a single reference, the pathophysiology, diagnosis, and treatment of reported causes of lameness intrinsically associated with the shoulder. Part One of this series discusses conditions associated with cartilage and bone maturation disorders and joint instability, while Part Two reviews tendon diseases, muscle disorders, synovial diseases, and soft-tissue mineralization disorders.
Introduction
Thoracic limb lameness resulting from disorders of the shoulder has been attributed in the past to a small number of well-described conditions. Nevertheless, cases of thoracic limb lameness that are often associated with shoulder pain but have no discernible cause are common. As diagnostic imaging and arthroscopic capabilities have improved, the clinician’s ability to identify other causes of shoulder pain and dysfunction has improved. In Part One of this series, cartilage and bone disorders and joint instability were examined. Part Two reviews the current understanding of tendon diseases, muscle disorders, synovial diseases, and soft-tissue mineralization disorders of the shoulder.
Tendon Diseases
Biceps Brachii Tendinopathy
Bicipital tenosynovitis is a relatively common cause of shoulder lameness in dogs.1–7 The true incidence is unknown and may be less than previously thought.7 Lameness previously attributed to bicipital tenosynovitis is now being identified as originating from other soft-tissue structures associated with the shoulder. This refinement is due largely in part to the capabilities of other imaging modalities such as ultrasonography and magnetic resonance imaging (MRI).1,2,8–10
Bicipital tenosynovitis in dogs has been classified as either primary or secondary.3 Primary bicipital tenosynovitis is thought to result from inflammation of the tendon of origin of the biceps brachii as a result of overuse or chronic repetitive injury. Secondary bicipital tenosynovitis may occur as a response to intraarticular disease or loose body entrapment beneath the tendon, or it may be the result of acute trauma causing rupture and strain of tendons.3,4 In either case, bicipital tenosynovitis historically has been assumed to occur as a result of the inflammatory process that follows repetitive overuse. Recent studies in humans have shown that many cases of tendinopathy as a result of overuse may not be inflammatory.3 Similarly, several reports in the veterinary literature document the lack of inflammatory changes in some instances of bicipital tenosynovitis. One theory proposed to explain these findings is impairment of the vascular supply to the tendon and subsequent degeneration as a result of aging and sedentary lifestyle, disease, or trauma.3 Therefore, while the histopathological lesions of tenosynovitis in dogs and an arthroscopic classification of biceps tendon lesions have been described,2,3,5 the exact pathophysiological mechanisms responsible for these changes remain unknown.
Affected dogs are usually middle-aged to older, medium to large breeds with no apparent breed or sex predilection. Clinical signs are variable but often include a chronic intermittent or progressive weight-bearing forelimb lameness that becomes worse with exercise.6 These dogs are often refractory to oral administration of nonsteroidal anti-inflammatory drugs (NSAIDs).
Diagnosis of bicipital tenosynovitis may involve direct palpation of the biceps tendon, radiography, contrast arthrography, tendon ultrasonography, synovial cytology, MRI, and arthroscopy. Palpation of the biceps tendon in the intertubercular groove during flexion of the shoulder (i.e., biceps tendon test) [Figures 1A, 1B] has been found to be highly suggestive of bicipital tenosynovitis, although it has been countered that this may be more indicative of generalized shoulder pain than related specifically to the biceps tendon.4,7 Because radiographic changes may be subtle, a flexed cra-niodistal-cranioproximal view should be performed (in addition to the standard caudocranial and mediolateral views) to identify irregularities in the intertubercular groove and mineralization of the biceps tendon.4 Contrast arthrography has been shown to be valuable for identifying irregularities associated with the biceps tendon and the surrounding synovium, and it may be more sensitive than ultrasonography for diagnosis [Figures 2A, 2B].4,8,9 Shoulder arthroscopy is recognized as superior to other diagnostic procedures for diagnosis of bicipital tenosynovitis.2,5,6
Medical treatment of bicipital tenosynovitis is appropriate if the injury is acute. Treatment involves one to two intraarticular injections of a long-acting steroid, methyl-prednisolone acetate, followed initially by strict cage rest and then a gradual return to activity.11 To lessen the risk of iatrogenic joint infection, it is imperative that aseptic technique be used when injecting the steroid. Intraarticular use of steroids has been associated with tendon weakening and rupture in humans and rabbits,12 but, to the authors’ knowledge, no clinical reports of tendon rupture in dogs following intraarticular steroid injection have been described. Whether rupture of the biceps brachii tendon following steroid injection is truly a rare occurrence in dogs, or biceps brachii tendon rupture occurs following steroid injection but fails to produce clinical signs in dogs is unknown. In either case, concern for biceps tendon rupture following intraarticular steroid injection seems unwarranted.
Surgical treatment is recommended for cases in which a mechanical problem is found or those cases that do not respond to medical therapy.6 Surgical treatment traditionally has consisted of tenodesis of the biceps brachii tendon to the proximal portion of the humerus through a cranial arthrotomy. Although good long-term outcomes have been reported in dogs and people,4,13 complications such as tissue irritation and drainage associated with the implanted hardware and seroma, prolonged lameness, and other surgical-associated morbidity may occur. More recently, arthroscopic procedures including biceps brachii tenotomy [Figures 3A, 3B] and arthroscopic tenodesis have been shown to be as effective as open procedures.6,42
Other conditions of the biceps tendon that have been reported include medial displacement of the biceps tendon as a result of rupture of the transverse humeral ligament and rupture of the tendon sheath.15–17 Rupture of the transverse humeral ligament allows the biceps brachii tendon to displace medially from the intertubercular groove when the joint is extended and supinated. Radiographs are normal, but arthrography reveals poor delineation of the tendon within the intertubercular groove. Reconstruction of the transverse humeral ligament, with or without screw and suture augmentation, followed by controlled gradual return to normal activity is usually successful.15,16
Rupture of the biceps brachii tendon sheath has been reported in two dogs, a male and a female Labrador retriever. 17 The lameness appeared acutely following exercise in one dog, and it was a more chronic and ill-defined disorder in the other. In both cases, moderate lameness and variable degrees of pain and muscle atrophy were observed. Radiographs, ultrasonographic examination of the biceps brachii tendon, and electromyographic evaluation of the shoulder muscles were normal. Positive-contrast arthrography revealed leakage of contrast from the distal end of the biceps brachii tendon sheath. Arthroscopic examination of the shoulder revealed subtle and nonspecific synovial hyperemia and hyperplasia associated with the biceps tendon. Instillation of intraarticular corticosteroids was of variable benefit. Tenodesis of the biceps brachii tendon to the proximal humerus, followed by rest and gradual return to function resulted in improvement of the lameness; however, some degree of lameness persisted. Histological examination of excised tendon revealed moderate degenerative tendinopathy and cartilaginous metaplasia.
The pathogenesis of biceps tendon sheath rupture is not completely understood, but it may represent a subset of bicipital tenosynovitis or be a consequence of hyperflexion of the shoulder that leads to tearing of the sheath at its distal insertion on the proximal humerus.17
Dystrophic calcification of the tendon of origin of the biceps brachii occurs infrequently.20 The pathogenesis of calcifying tendinopathy is unknown. One theory suggests that tendon trauma or rupture results in a disturbance of tendon blood supply, leading to hypoxia. Hypoxia may trigger remodeling of tendon collagen into fibrocartilage, followed by chondrocyte-mediated osteogenesis.18,19 Because the biceps tendon is intraarticular, the pathogenesis of biceps tendon calcification may be different and may represent a subset of bicipital tenosynovitis or acute partial disruption of the tendon as a result of trauma.20 Concurrent displacement of the biceps brachii and signs of bicipital tenosynovitis have been recently reported to occur as a result of tendinosis of the supraspinatus tendon. The diagnosis was made by use of MRI, and surgical excision of the excess tissue in the supraspinatus tendon resulted in resolution of the lameness.21
Calcification of the biceps brachii tendon most commonly affects large, middle-aged, active dogs; Labrador retrievers and rottweilers are overrepresented.20,22 Affected dogs usually have a unilateral chronic lameness that can be intermittent or persistent. Pain on palpation or manipulation of the joint may or may not be present.20 Lesions are often bilateral, but only one leg may be clinically affected. Radiographs reveal a mineral density in the cranial aspect of the shoulder, but a flexed cranioproximal-craniodistal (sky-line) view is usually necessary to identify the mineralization as originating in the biceps brachii tendon or the supraspinatus tendon [Figures 4A, 4B].23 Positive-contrast arthrography, arthroscopy, and computed tomography (CT) are other modalities for further delineation of the conditions. Nonsurgical management of calcifying tendinopathy should include rest and administration of NSAIDs. Corticosteroid treatment provides relief in humans, but use of such drugs is controversial and may predispose the tendon to weakening and rupture.9 Mineralization of the biceps brachii tendon can be addressed surgically by tenotomy or tenodesis of the tendon.23,24
Calcifying Tendinopathy of the Supraspinatus Tendons
Dystrophic calcification of the tendon of insertion of the supraspinatus is an infrequent occurrence and may be an incidental finding if no clinical signs are associated with the mineralization. The pathogenesis is unknown.18,19 Signalment, history, and physical examination findings are similar to those of biceps brachii calcification, although pain on palpation or manipulation of the joint appears to be more significant with supraspinatus calcification.20,21,23
Standard radiographic views may demonstrate a mineralization consistent with supraspinatus calcification, but a flexed cranioproximal-craniodistal (skyline) view, CT, or MRI may be necessary to confirm the diagnosis and differentiate supraspinatus from biceps brachii calcification. Nonsurgical management includes rest and administration of NSAIDs. Surgical treatment of supraspinatus mineralization by excision of calcified tissue from the supraspinatus tendon and adjacent muscle has been reported to yield generally poor results.23,24
Muscle Disorders
Musculotendinous disorders of the shoulder comprise a group of relatively uncommon conditions that include muscle strains and muscle contractures. While muscle injuries are the most common types of musculoskeletal disorders in people, a survey of veterinary teaching hospitals reported only 5% of musculoskeletal cases as muscle disorders, with traumatic muscle injuries accounting for only 1% of cases.25–27 This low incidence rate may not be a true low rate of occurrence, but rather a reflection of the difficulty in diagnosing these conditions before the advent of ultrasonography and MRI.
Muscle strains usually occur in mature, athletic dogs and result from overstretching or overuse. Disruption of muscle fibers, most commonly near the musculotendinous junction, results in inflammation followed by healing with fibrosis. 26,28 The strength of muscle contraction is affected by strain injury. The ability to contract decreases by 30% immediately after injury, 50% after 24 hours, 25% after 48 hours, and recovers to 90% original function after 1 week in muscle that is strained to 80% of failure.29 Muscles at risk of strain include those that cross two or more joints, and in the forelimb they include the biceps, triceps, pectorals, serratus ventralis, rhomboideus, and flexor carpi ulnaris.26
Spontaneous muscle ruptures resulting from corticosteroid injection and parasite migration have been reported.28 Dogs with muscle strains may be presented with lameness, focal swelling of the affected muscle, subcutaneous hemorrhage, muscle displacement, and pain. Definitive diagnosis of muscle strains is often difficult and may require ultrasonography, MRI, or surgical exploration.28 Reported treatments for muscle strains include ice packs for the first 24 hours followed by warm compresses after 24 hours, compressive wraps, NSAIDs, analgesics, muscle relaxants, rest, controlled physical therapy, and surgery.28
Muscle contracture is an uncommon condition described as a state of shortening of a muscle not caused by active contraction of the muscle fibers.30 Contracture is thought to result from fibrous connective tissue replacement of muscle secondary to degenerative changes, most commonly as a result of trauma to muscle fibers, nerves, or blood vessels.31 Since severely damaged muscle has little regenerative ability, fibrosis and contracture ensues secondary to necrosis.30 Congenital contractures, as well as those secondary to infection or autoimmune reactions, have been reported.32 Contracture of both the infraspinatus and supraspinatus muscles can occur, with the infraspinatus being more commonly affected.30
Dogs presented for infraspinatus contracture are usually medium to large, active, middle aged, and with no apparent sex predilection. Abiphasic history may be reported with an acute painful lameness that improves over 2 to 6 weeks, followed by a chronic, static, nonpainful gait abnormality.31 The chronic phase is characterized by a prominent scapular spine due to muscle atrophy. The elbow is held in adduction while the shoulder is abducted with outward rotation of the antebrachium. The elbow may be maintained in adduction throughout the stride, with circumduction of the limb and a carpal flip.31 Infraspinatus tenotomy is the treatment of choice and restores the gait to nearly normal.28,31
A case of teres minor myopathy causing chronic lameness has been described.33 The lameness in this case differed from supraspinatus and infraspinatus contractures, in that pain was a prominent feature while forelimb circumduction was not observed. Reduced shoulder flexion was present. Ultrasonography was used to localize the lesion to the teres minor muscle, and histopathology confirmed the diagnosis. The etiology of the condition is unknown, but bacterial, parasitic, or immune-mediated diseases or trauma should be considered. Treatment in this case consisted of removing the entire muscle, and no appreciable decrease occurred in stability of the shoulder.33
Synovial Diseases
Synovial Chondrometaplasia
Synovial chondrometaplasia or synovial osteochondromatosis is a proliferative disorder of undifferentiated stem cells of the synovium, in which cartilage formation occurs through a different process than normal chondrogenesis. Formation of chondral or osteochondral nodules occurs in the synovial tissue of the joint, tendon sheath, or bursa. The nodules often break off, and the resulting loose bodies are nourished by synovial fluid, allowing their growth.34
Primary and secondary synovial osteochondromatoses have been described in humans. Primary synovial osteochondromatosis is the spontaneous formation of intrasynovial nodules in an otherwise normal joint, while secondary synovial osteochondromatosis is a similar proliferative synovial disorder that follows traumatic, degenerative, or inflammatory joint diseases.34–36 Synovial osteochondromatosis has been reported in the scapulohumeral, coxofemoral, talocrural, and stifle joints in medium- to large-breed dogs with no sex predeliction.34,35 Historically, a chronic, low-grade lameness is reported, and pain is present with manipulation of the joint. Arthrocentesis yields either normal synovial fluid characteristics or those typical of osteoarthritis. Radiographs reveal intraarticular nodules of varying radiodensity and signs of degenerative joint disease. Arthrography and arthroscopy may more clearly define the disease [Figures 5A, 5B]. Good outcomes have been reported with debridement of nodules, loose body removal, and synovial stripping.34 Arthrodesis may be necessary in severe cases.35
Villonodular Synovitis
Villonodular synovitis has been rarely reported in the dog.37 Middle aged to older, large breeds are usually affected by this disorder, although a recent report describes villonodular synovitis in two dachshunds.37 No gender predilection is apparent.
The lameness associated with villonodular synovitis is often severe and can be acute or chronic in nature. Examination of the shoulder reveals muscle atrophy, marked pain with manipulation, and capsular distention. The joint is stable. Synovial fluid is orange to red and composed of moderate numbers of neutrophils or macrophages. Radiographs reveal varying degrees of osteoarthritis. Yellowish discoloration of the synovium, capsular hemorrhages, hemorrhagic nodules, and prominent tissue masses protruding into the joint may be observed diffusely or focally via arthroscopy. Synovectomy alone or in conjunction with radiation or cryotherapy has been reported in humans and horses with variable success.37 A good outcome in one human case was obtained by administration of antitumor necrosis factor alpha monoclonal antibody.38 The effectiveness of these modalities in dogs has not been investigated. Treatment with NSAIDs may result in short-term improvement. Intraarticular corticosteroid injection appears to be ineffective.37
Soft-Tissue Mineralization Disorders
Soft-Tissue Mineralization
Ectopic or heterotropic ossification of soft tissues (other than the synovium, supraspinatus muscle, biceps brachii tendon, and infraspinatus bursa) can occur in the canine shoulder.39 Calcium deposition in soft tissues is usually described as metastatic or dystrophic, and the histological appearance is one of amorphous calcification. Metastatic calcification can occur if the calcium-phosphate product is increased due to a sustained elevation in serum levels of either calcium or phosphate, while dystrophic calcification occurs in areas of damaged soft tissues with normal levels of serum calcium and phosphate.39 When trabecular bone is formed in soft tissues, other etiologies should be considered, such as trauma, tumor, and fibrodysplasia ossificans progressiva (FOP).
Neurologically induced ossification has not been reported in the dog. In the report of Aron et al., an FOP-like syndrome was suggested, because the features of the disorder present in that dog shared some similarities with FOP in humans. However, significant characteristics of FOP as described in humans, such as changes in the great toe and thumb, fever, cervical exostoses, scoliosis, hearing impairment, alopecia, and restrictive lung disease were not described in the dog of that report.40 Nevertheless, soft-tissue mineralization can occur in the soft tissues of the shoulder, and FOP-like syndrome should be considered when diagnosing shoulder lameness.
Soft-tissue mineralization, if not associated with trauma, tumor, or other specifically described shoulder disorder, often is presented as a progressive, multifocal, and nonsymmetric disorder. Soft-tissue swelling in or around muscles, tendons, and ligaments is initially present, but it progresses to diffuse calcification and eventually organized trabecular bone. Nuclear scintigraphy will identify areas of mineralization before the mineralization is radiographically evident. Although clinical and radiographic signs can suggest the presence of an ectopic mineralization syndrome, definitive diagnosis is made by biopsy. Biopsy may exacerbate the condition. Surgical excision of the calcified masses generally is unrewarding and may worsen the condition.39,40 Other mechanisms that can produce soft-tissue injury, such as intramuscular injections or overstretching of joints, may result in mineral deposition and should be avoided if possible. The administration of corticosteroids and disodium etidronate in combination is reportedly of limited benefit, but such treatment appears to be more effective than other medical therapies.40
Infraspinatus Bursal Ossification
Infraspinatus bursal ossification has been recently reported. 41 Radiographic examination may show single or multiple mineralizations within the infraspinatus bursa, especially in the craniocaudal view. The mineralizations may not be clinically significant if no pain over the tendon can be elicited. Treatment options include intralesional glucocorticoids, NSAIDs, or surgical therapy.42
Discussion
Although much research is still needed to fully elucidate the pathophysiology and clinical importance of the conditions described, awareness of these conditions is vital to developing a diagnostic plan and providing a prognosis for owners. Comprehensive knowledge of the anatomy of the shoulder and adherence to a thorough and systematic orthopedic examination, appropriate radiographic views, and timely referral for advanced diagnostics will generally allow for a positive outcome for the animal.
Diagnostic algorithms for shoulder diseases are available and can be useful if the clinician is able to isolate the pain to a particular structure.43 However, due to the often chronic nature of many of the described conditions and inability to localize the lesion to a specific structure, many of these conditions cannot be categorized into a diagnostic algorithm and are treated empirically, often to the detriment of the animal.
Recent data would suggest that many of the conditions of the shoulder, especially shoulder instability, are much more common than previously thought. Veterinary medicine lags well behind human medicine in diagnosis and treatment of shoulder diseases, and further research is needed in nearly all aspects of shoulder lameness. As advanced diagnostics become increasingly available, these conditions and their clinical importance will continue to be assessed.
Conclusion
Shoulder conditions resulting in forelimb lameness are common in the dog but can present a diagnostic challenge. Fortunately, the increasing availability of advanced diagnostic techniques such as ultrasonography, CT, MRI, and arthroscopy can allow definitive diagnosis for many of these conditions.
Citation: Journal of the American Animal Hospital Association 44, 4; 10.5326/0440163
Citation: Journal of the American Animal Hospital Association 44, 4; 10.5326/0440163
Citation: Journal of the American Animal Hospital Association 44, 4; 10.5326/0440163
Citation: Journal of the American Animal Hospital Association 44, 4; 10.5326/0440163
Citation: Journal of the American Animal Hospital Association 44, 4; 10.5326/0440163
Citation: Journal of the American Animal Hospital Association 44, 4; 10.5326/0440163
Citation: Journal of the American Animal Hospital Association 44, 4; 10.5326/0440163
Citation: Journal of the American Animal Hospital Association 44, 4; 10.5326/0440163
Citation: Journal of the American Animal Hospital Association 44, 4; 10.5326/0440163
Demonstration of proper placement of the examiner’s thumb for performing the biceps tendon test (A). Direct pressure against the tendon while flexing the shoulder should elicit a pain response if bicipital tenosynovitis is present (B).
Positive-contrast arthrogram of a normal shoulder of a dog. Observe the smooth and well-defined outline of the biceps brachii tendon.
Positive-contrast arthrogram of the shoulder of a dog with bicipital tenosynovitis. Observe the irregular and poorly defined outline of the biceps brachii tendon, especially at its origin on the supraglenoid tuberosity.
Inflamed bicipital tendon as viewed through a lateral arthroscopic portal.
Survey lateral radiograph of a shoulder of a dog. A mineralized body is seen immediately proximal to the greater tubercle.
Skyline view of the intertubercular groove of the same dog as in Figure 4A, demonstrating the utility of this view for separating mineralization of the biceps brachii tendon from mineralization of the supraspinatus tendon or muscle. The mineralized body is not seen in the bicipital tendon groove, suggesting the mineralization is within the supraspinatus muscle.
Survey lateral radiograph of the shoulder of a dog with synovial chondrometaplasia. A few slightly mineralized, loose bodies can be seen in the caudal joint pouch.
Positive-contrast arthrogram of the shoulder of a dog with synovial chondrometaplasia. Contrast demonstrates numerous, nonmineralized, loose bodies within the joint and bicipital tendon sheath. Exploratory surgery revealed numerous, cartilaginous, loose bodies that were typical of synovial chondrometaplasia.
