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Tutorial Article Ultrasonographic examination of the proximal tendon of the brachii: Technique and reference images H. PASQUET*, V. COUDRY AND J.-M. DENOIX CIRALE – Ecole Nationale Vétérinaire de Maisons-Alfort, 14430 Goustranville, France. Keywords: ; ultrasonography; biceps brachii; reference images

Summary The purpose of this paper is to describe the ultrasonographic technique to image the PTBB completely and Ultrasonography of the shoulder is of interest in the the normal ultrasonographic appearance of this tendon in diagnosis of proximal forelimb lameness. The proximal order to improve the practitioner’s ability to detect lesions and tendon of the biceps brachii (PTBB) and its associated avoid misinterpretation of some anatomic features. structures are frequently injured and should be included in the routine ultrasonographic examination Indications of the shoulder. This paper describes a complete ultrasonographic Ultrasonography of the PTBB is indicated whenever an injury procedure for examining the bicipital apparatus, on of the cranial aspect of the shoulder is suspected because of: transverse and longitudinal scans, from the insertion of the PTBB on the supraglenoid tubercle to the muscle • trauma of the cranial aspect of the shoulder; body below the intertubercular sulcus. • local physical deformation: soft tissue swelling, asymmetry of the point of the shoulders, muscle atrophy; Introduction • forelimb lameness associated with an abnormal response to the mobilisation tests of the shoulder without any Shoulder lameness is often difficult to diagnose and document abnormal findings in the middle and distal parts of the in field practice. Soft tissue injuries have been considered as limb; the most frequent cause of shoulder lameness (Dyson 1986). • negative response to antebrachial and distal nerves Radiographs and diagnostic analgesia are often difficult to diagnostic analgesia; interpret and sometimes do not permit a precise diagnosis. • negative response to intra-articular analgesia performed in Ultrasonography was proven an adequate noninvasive the , carpus and distal limb; technique to examine equine soft tissues in the field (Denoix • positive intra-articular analgesia of the scapulohumeral joint or bicipital bursa; and 1996). Traumatic injuries of the proximal tendon of the biceps • abnormal radiographic and/or scintigraphic findings on the brachii (PTBB) have been described (Dyson 1985; McDiarmid shoulder. 1999) and the use of ultrasonography to diagnose bicipital apparatus injuries has been presented (Hamelin et al. 1994; Anatomical review of the area Denoix et al. 2001). More recently congenital hypoplasia of the minor tubercle of the with medial luxation of the The equine bicipital apparatus is composed of the biceps PTBB has been reported in 4 adult (Coudry et al. 2005). brachii muscle, the supraglenoid tubercle of the , the Because of its anatomic location, the PTBB cannot be imaged intertubercular sulcus of the humerus, the bicipital bursa and with the current magnetic resonance imaging equipment. The the proximal tuberosity of the (distal attachment of the normal ultrasonographic appearance of the PTBB has been biceps brachii). It contributes to the forelimb passive stay published previously (Crabill et al. 1995; Tnibar et al. 1999) apparatus and assists in forelimb protraction coupling the but little detail on the tendon architecture and echogenicity shoulder and elbow angles (Gyuru and Zajer 1982; was given and the technique to image the tendon on Hermanson and Hurley 1990; Barone 2000). In the horse, the longitudinal scans was not described in detail. biceps brachii is a simple, spindle-shaped muscle with 2 tendonous extremities. The proximal tendon originates on *Author to whom correspondence should be addressed. the supraglenoid tubercle of the scapula. It is very thick and 332 EQUINE VETERINARY EDUCATION / AE / June 2008

fits tightly the intertubercular groove of the humerus, which is and receives the attachment of the most proximal fibres of the covered with fibrocartilage and the bicipital bursa (Fig 1). The ascending pectoral muscle. The muscular body of the biceps cranial aspect of this tendon is covered by the distal brachii contains a high amount of fibrous lamellae from which aponeurosis of the supraspinatus muscle. This structure emanates distally the lacertus fibrosus that attaches over the extends between the medial and lateral supraspinatus tendons radial carpal extensor muscle (Barone 2000). The distal tendon of the biceps brachii is shorter than the proximal and inserts on the ; some fibres end on the medial collateral ligament of the elbow joint.

Equipment

Ultrasonographic examination of the proximal tendon of the biceps brachii is ideally performed with a 5–7.5 MHz convex probe. However, a 7.5 MHz linear probe can provide adequate diagnostic ultrasonographic images. To improve contact, a stand-off pad can be used. The cranial aspect of the shoulder is clipped, washed with warm water and a coupling gel is applied over the entire point of the shoulder.

Technique and reference images

The complete ultrasonographic evaluation of the bicipital apparatus is performed on the fully loaded limb in transverse and longitudinal (sagittal and parasagittal) sections. Reference transverse ultrasound scans are presented in the following 4 sites (Fig 1): Site 1 – at the level of the supraglenoid tubercle; Site 2 – between the supraglenoid tubercle and the intertubercular sulcus; Site 3 – at the level of the intertubercular sulcus; and Site 4 – just below the intertubercular sulcus.

Transverse sections Fig 1: Lateral view of a left dissected shoulder. S1 = site 1; S2 = site 2; S3 = site 3; S4 = site 4. 1 = neck of scapula; 2 = glenoid cavity; 3 = supraglenoid tubercle; 4 = major humeral tubercle: Site 1 (Fig 2) 4a = convexity (caudal portion), 4b = top (cranial portion), 4c = crest; 5 = humeral body; 6 = biceps brachii: 6a = proximal tendon, The surface of the supraglenoid tubercle appears as a regular, 6b = cranial muscle fibres, 6c = body; 7 = bicipital bursa (open). convex and hyperechogenic line. The PTBB is visualised as a

Fig 2: Transverse ultrasound scan (Site 1 on Fig 1) of the Fig 3: Transverse ultrasound scan (Site 2 on Fig 1) of the proximal proximal tendon of the biceps brachii at the level of the tendon of the biceps brachii (see Fig 1 and 6) (cranial is to the top supraglenoid tubercle (see Fig 1) (cranial is to the top and medial and medial is to the left). 1 = scapulohumeral fat pad; is to the left). 1 = supraglenoid tubercle; 2 = proximal tendon of 2 = proximal tendon of the biceps brachii: 2a = medial lobe, the biceps brachii; 3 = supraspinatus muscle: 3a = medial 2b = lateral lobe, 2c = cranial muscle fibres; 3 = supraspinatus tendon, 3b = lateral tendon; 4 = brachiocephalicus muscle; 5 = muscle: 3a = medial tendon, 3b = lateral tendon, skin. Arrows = cranial limit of the supraspinatus muscle. 3c = aponeurosis; 4 = brachiocephalicus muscle; 5 = skin. EQUINE VETERINARY EDUCATION / AE / June 2008 333

crescent-shaped homogeneously echogenic structure. It is body and tendons. The medial supraspinatus tendon is covered by the supraspinatus muscle, which has 2 echogenic echogenic and flat, medially to the PTBB; the lateral intramuscular tendonous branches laterally and medially. supraspinatus tendon is bigger than the medial tendon, echogenic and presents a triangular cross section. Between the Site 2 (Fig 3) PTBB and the lies the scapulohumeral fat pad, which is less echogenic than the tendon. The PTBB is irregularly elliptic in shape. At this level, it contains areas of fat connective tissue inducing a heterogeneous Site 3 (Fig 4) echogenicity. The PTBB divides progressively in 2 homogeneously echogenic lobes. The lateral lobe is thicker The 2 lobes of the PTBB are visualised over the intertubercular and oval; the medial lobe has a C shape. The cranial layer of the sulcus. The surface of this sulcus appears as a smooth, PTBB is made of hypoechogenic striated muscle fibres (Fig 1). hyperechogenic and W-shaped line. The PTBB is not The PTBB is completely surrounded by the supraspinatus muscle homogenously echogenic because of the different radii of curvature of the superficial and deep fibre layers over the intertubercular sulcus. Between the tendon and the intertubercular sulcus bone surface, the fibrocartilage appears as a thin interface with little echogenicity.

Site 4 (Fig 5)

The PTBB merges progressively with the hypoechogenic striated fibres of the muscle body. On transverse sections this junction has an oval shape and a heterogeneous echogenicity. It is separated from the humerus by a poorly echogenic space made of the distal recess of the bicipital bursa and fat. A small amount of fluid can be seen at the caudal and lateral aspect of the PTBB. In normal horses this distal recess never extends to the cranial aspect of the tendon and its width does not exceed 10 mm.

Fig 4: Transverse ultrasound scan (Site 3 on Fig 1) of the proximal tendon of the biceps brachii at the level of the intertubercular sulcus (see Fig 1) (cranial is to the top and medial is to the left). 1 = humerus (intertubercular sulcus): 1a = minor tubercle, 1b = intermediate tubercle, 1c = major tubercle, 1d = grooves of the intertubercular sulcus; 2 = proximal tendon of the biceps brachii: 2a = medial lobe, 2b = lateral lobe; 3 = supraspinatus muscle: 3a = supraspinatus aponeurosis; 4 = brachiocephalicus muscle; 5 = skin.

Fig 6: Transverse section of a right shoulder (Site 2 on Fig 1) (cranial is to the top and medial is to the left). Section A = sagittal section; section B = medial parasagittal section; section C = lateral parasagittal section. 1 = head of the Fig 5: Transverse ultrasound scan (Site 4) of the biceps brachii at humerus; 2 = scapula (glenoid margin); 3 = proximal tendon of the level of the proximal humerus (cranial is to the top and the biceps brachii: 3a = medial lobe, 3b = lateral lobe; 4 = fat; medial is to the left). 1 = humerus; 2 = biceps brachii; 5 = supraspinatus muscle: 5a = medial tendon, 5b = lateral 3 = brachiocephalicus muscle; 4 = skin. tendon; 6 = infraspinatus tendon; 7 = brachiocephalicus muscle. 334 EQUINE VETERINARY EDUCATION / AE / June 2008

Longitudinal sections Sites 3 and 4

The reference longitudinal scans are performed from the At this level, the PTBB curves over the intertubercular sulcus. supraglenoidal tubercle to the intertubercular sulcus in the The bone surface of this sulcus appears as a regular, 4 previously described locations. hyperechogenic and convex line covered by poorly echogenic fibrocartilage. Some anechogenic fluid can be visualised in the Site 1 bicipital bursa distally to the intertubercular sulcus, at the caudolateral aspect of the PTBB. The PTBB inserts on the supraglenoid tubercle and is imaged as a regular and hyperechogenic convex line. Tendon fibres are homogeneously echogenic and parallel. The tendon is covered cranially by the less echogenic supraspinatus muscle.

Site 2

The PTBB is divided in 2 parallel lobes, which must be imaged separately (Fig 6).

• When the probe is placed sagittally (Fig 7), the ultrasound beam passes between the medial and lateral lobes and only a thin part of the echogenic tendon is imaged covered by hypoechogenic muscle fibres. • A longitudinal section of the medial lobe is obtained by moving the probe medially (Fig 8). This lobe is covered by striated muscle fibres and shows parallel echogenic tendon fibres. It is completely surrounded by the medial part of the supraspinatus muscle body. Fig 8: Medial parasagittal ultrasound scan (section B) of the • A longitudinal section of the lateral lobe of the PTBB is proximal tendon of the biceps brachii (proximal is to the left). 1 = supraglenoid tubercle; 2 = intertubercular sulcus (medial obtained by moving the probe laterally with a proximodistal groove); 3 = medial lobe of the PTBB: 3a = muscle fibres; orientation (Fig 9). This tendon is made of parallel 4 = scapulohumeral fat pad and supraspinatus muscle body; echogenic tendon fibres covered by hypoechogenic muscle 5 = supraspinatus muscle; 6 = brachiocephalicus muscle; fibres. It is located between the supraspinatus aponeurosis 7 = skin. and the scapulohumeral fat pad.

Fig 7: Sagittal ultrasound scan (section A) of the proximal tendon of the biceps brachii (proximal is to the left). The tendon has an unclear deep limit because its fat merges with Fig 9: Lateral parasagittal ultrasound scan (section C) of the the scapulohumeral fat pad. 1 = supraglenoid tubercle; proximal tendon of the biceps brachii (proximal is to the left). 2 = intertubercular sulcus (sagittal ridge); 3 = proximal tendon 1 = supraglenoid tubercle; 2 = intertubercular sulcus (lateral of the biceps brachii: 3a = tendon fibres, 3b = muscle fibres, groove); 3 = lateral lobe of the proximal tendon of the biceps 3c = fat; 4 = fat and supraspinatus muscle body; brachii; 4 = scapulohumeral fat pad; 5 = supraspinatus muscle: 5 = supraspinatus muscle; 6 = brachiocephalicus muscle; 5a = body, 5b = aponeurosis; 6 = brachiocephalicus muscle; 7 = skin. 7 = skin. EQUINE VETERINARY EDUCATION / AE / June 2008 335

Discussion echogenicity between deep and superficial layers. In some horses a notch can be seen over the sagittal ridge of the All these images can be made with linear probes; but as the intertubercular sulcus; it results from incomplete ossification field is often narrower, repositioning of the probe is required between 2 separated centres (head and minor/major tubercle). to achieve complete imaging of the tendon in transverse and Radiography allows assessment of bone involvement such longitudinal planes. As the PTBB is covered by the as fracture of the supraglenoid tubercle, lysis or remodelling brachiocephalicus muscle, a stand-off pad is not required of the intertubercular sulcus, major tubercle fracture and especially with high frequency probes. On transverse sections, minor tubercle hypoplasia (Coudry et al. 2005). It can also be the supraspinatus muscle presents a strong triangular lateral useful to assess the degree of concomitant joint disease tendon and a thinner medial one; these 2 tendons can be (Cauvin 1998; Coudry et al. 2005). However, radiographs of followed down to their respective attachments on the major the shoulder can be difficult to perform in strong horses as and minor humeral tubercles. well as in painful horses when the injured forelimb is The PTBB is a complex structure made of 2 lobes, a cranial extended in protraction. layer of striated muscle fibres and fat. Therefore an adequate Nuclear scintigraphy may be useful to identify shoulder technique and interpretation of the images are required lameness and lesions of the glenoid cavity or humeral head during the ultrasound evaluation of this tendon. The data (Stashak 2002). At the cranial aspect of this area, it provides a presented in this paper are useful to detect lesions of the PTBB good assessment of early bone changes in the supraglenoid and avoid misinterpretation. In case of doubt about tubercle, intertubercular sulcus or tubercles of the humerus. interpretation, a comparison with the contralateral limb at the Abnormal uptake can also be detected in muscles of the same anatomical level and with the same position of the shoulder area during the bone phase (Dyson 2002). This probe is made. technique has the limitation that it can not detect tendon Many injuries involving this structure can be diagnosed injuries when not associated with bone abnormalities. using ultrasonography. Fracture of the supraglenoid tubercle is associated with Conclusion distal displacement of the origin of the PTBB. In recent cases, the fracture site is wide and often presents isolated fragments. Improvement in the knowledge of anatomy and technique is The hyperechogenic supraglenoid tubercle is displaced distally essential for the development of any diagnostic imaging and PTBB retraction induces thickening and hypoechogenic modality. Reference images described in this paper aid artefacts. Calcification of the PTBB is often observed casting recognition and documentation of lesions of the PTBB and acoustic shadows in chronic cases (Meagher et al. 1979; avoid misinterpretation of ultrasonographic images. Stashak 2002; Boys Smith and Singer 2007). Traumatic injuries Presently, ultrasonography is the technique of choice for the of the PTBB are more common in the lateral lobe; abnormal diagnosis and documentation of soft tissues injuries of the findings include thickening of the injured part of the tendon point of the shoulder. and hypoechogenic areas. Rupture and ossification of the PTBB have rarely been reported (Meagher et al. 1979; Seco Diaz References et al. 2003). Proximal enthesopathies, with bone remodelling and/or hyperechogenic enthesophytes of the supraglenoid Barone, R. (2000) Anatomie comparée de mammifères domestiques. Arthrologie et Myologie, Vol 2, 4th edn., Vigot, Paris. pp 735-756. tubercle, have been documented in sport horses (Dyson 2002). Traumatic or septic bicipital bursitis is another quite common Boys Smith, S.J. and Singer, E.R. (2007) Mineralisation of the biceps brachii tendon in 6-year-old Cob mare. Equine vet. Educ. 19, 74-79. condition of the point of the shoulder; the fluid cavity expands Cauvin, E.R.J. (1998) Soft tissues injuries in the equine shoulder between the PTBB and the supraspinatus muscle making the region: a systematic approach to differential diagnosis. Equine vet. mesotendon visible (Cauvin 1998; Gough et al. 1998; Stashak Educ. 10, 70-74. 2002). The echogenicity of the fluid depends on the amount of Coudry, V., Allen, A.K. and Denoix, J-M. (2005) Congenital fibrin and debris. 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