Magnetic resonance imaging of the normal dromedary camel tarsus

Background Magnetic resonance imaging (MRI) is the most versatile and informative imaging modality for the diagnosis of locomotor injuries in many animal species; however, veterinary literature describing the MRI of the dromedary camel tarsus is lacking. Our purpose was to describe and compare the MRI images of twelve cadaveric tarsi, examined in a 1.5 Tesla MRI scanner, with their corresponding anatomical gross sections. Turbo spin-echo (TSE) T1-weighted (T1), T2-weighted (T2), proton density-weighted (PD), and short tau inversion recovery (STIR) sequences were obtained in 3 planes. Tarsi were sectioned in sagittal, dorsal, and transverse planes. MRI images from different sequences and planes were described and compared with the anatomical sections. Results The soft and osseous tissues of the dromedary camel tarsus could be clearly defined on MRI images and corresponded extensively with the gross anatomic sections. The obtained MRI images enabled comprehensive assessment of the anatomic relationships among the osseous and soft tissues of the camel tarsus. Several structure were evaluated that cannot be imaged using radiography or ultrasonography, including the transverse inter-tarsal ligaments, the talocalcaneal ligament, the short dorsal ligament, branches of the short medial and lateral collateral ligaments and the tarsometatarsal ligaments. Specific anatomical features regarding the dromedary camel tarsus were identified, including the fused second and third tarsal bone, an additional bundle of the short medial collateral ligament connecting the talus and metatarsus and the medial and lateral limbs of the long plantar ligament. Conclusions MRI images provided a thorough evaluation of the normal dromedary camel tarsus. Information provided in the current study is expected to serve as a basis for interpretation in clinical situations.


Background
The camel tarsus is an anatomically complex region comprising numerous osseous and soft tissue structures [1]. The biomechanics of the tarsal region and the influence of loading on those structures are also complex [2]. Imaging of the tarsus with the commonly used diagnostic methods (radiography and ultrasonography) is technically a challenge due to the increased possibility of structural superimposition [3]. Indecisive outcomes, in complicated cases, with radiography and/or ultrasonography necessitate the use of advanced imaging techniques. Fortunately, Magnetic resonance imaging (MRI) allows for volumetric imaging of thin section views into multiple customizable planes, which enable the assessment of joint structures without superimposition [4]. MRI is the most sensitive noninvasive imaging method currently available for imaging of soft tissue structures [5], due to the superior contrast among different soft tissues without the use of ionizing radiation [6]. In horses, MRI can demonstrate lesions that are underestimated or undetected by radiography and/or ultrasonography [7] and enables the assessment of various tissues in greater anatomical and physiological details than do radiography and ultrasonography [8].
Hind limb lameness due to tarsal lesions is common and affects many breeds and disciplines [9]. MRI of the tarsus in horses has been shown to be specific and sensitive for detection of all types of conditions concerning soft tissues [9,10] and osseous lesions [5] as well as detection of articular surface alterations through quantitative assessment of the osteochondral tissue and subchondral bone thickness [11]. However, MRI interpretation and lesion identification require experience with cross-sectional imaging and signal variations in normal animals in order to properly evaluate clinical cases and reach a definitive diagnosis and prognosis [9]. The normal MRI of the tarsus in the horse, cattle, cat, and the dog has been reported [3,[12][13][14][15][16] and computed tomography of the dromedary camel tarsus has been described [17]; however, no available data elucidating the normal MRI of the dromedary camel tarsus exist. Accordingly, the objective of the present study was to describe the normal MRI appearance of the dromedary camel tarsus with the aid of anatomical cryosections.

Results
None of the limbs showed tarsal abnormalities on the preliminary radiographic and ultrasonographic examinations. The osseous and soft tissue structures of the dromedary camel tarsus were illustrated (Figs. 1 and 2), and labeled in the MRI images and gross sections (Figs. 3, 4, 5, 6, 7, 8, 9 and 10). The level of each figure was indicated in Fig. 11. The use of high field MRI resulted into high quality images and various anatomical structures in the MRI images were identified and verified thanks to the gross anatomic sections. The overall time of the imaging protocol was around 40 minutes. T1 and PDweighted images provided high anatomic details and allowed a thorough evaluation of articular cartilage and the peri-articular structures. T2-weighted and STIR sequences provided better visualization of synovial fluid.
The relevant soft tissue structures evaluated in the MRI images included the tendons of fibularis tertius, long digital extensor and cranial tibial muscles dorsally; the fibularis longus and lateral digital extensor muscles laterally; the caudal tibial and the lateral and medial digital flexor muscles medio-plantarly; and the long plantar ligament, the superficial (SDFT) and deep digital flexor tendons (DDFT) on the plantar aspect of the joint. Tendons were best evaluated in the transverse plane and had homogenous low signal intensity on all sequences (Figs. The tarsal collateral ligaments consisted of short and long bundles on the medial and lateral aspects of the joint (Fig. 2). The long medial collateral ligament originated from the medial tibial malleolus, attached to the medial tarsal bones, and inserted into the medial proximal end of the metatarsus. The short medial collateral ligament consisted of three parts: a part connecting tibia and talus (tibiotalar branch); a part connecting tibia and calcaneus (tibiocalcaneal branch); and a wide part connecting talus and metatarsal bone. The long lateral collateral ligament originated from the malleolar bone, attached to the lateral tarsal bones, and inserted into the proximal metatarsus. The short lateral collateral ligament consisted of two parts: a part connecting the tibia and calcaneus (tibiocalcaneal branch) and a part between the base of calcaneus and metatarsal bone (calcaneometatarsal branch). The collateral ligaments were best evaluated in dorsal plane and had homogeneous low signal intensity in all sequences (Figs. 5, 6, 7, 8 and 9, and 10). The inter-tarsal ligaments connecting the talus and calcaneus and connecting tarsal bones had heterogeneous signal intensity (Figs. 5 and 6).

Discussion
To the authors' knowledge, this is the first published report providing description of the high field MRI appearance of the normal dromedary camel tarsus. The signal intensity of the clinically relevant osseous and soft tissue structures of the dromedary camel tarsus was described and the MRI images corresponded well with the gross anatomic sections. The obtained information in the current study appointed that MRI enabled assessment of structures inside the tarsus (soft and bony tissues) that otherwise cannot be imaged by other means and offers the opportunity to diagnose lesions within the tarsus that cannot be investigated through other imaging modalities [18]. MRI permitted viewing of the camel tarsus in three planes and obtaining information of cartilage, cortical bone, subchondral bone, trabecular bone, cancellous bone, ligaments, and tendons which is not all possible with other available diagnostic imaging tools. This enables the clinicians to interpret the tarsus in different angles and accurately detect the problem. The obtained results are in agreement with the conclusions reported earlier, that MRI offers the best evaluation technique of all anatomical structures, particularly soft tissues, of the tarsal joint in horse, cattle, dog and cat [3,[12][13][14][15][16].
The camel tarsus (hock) is a composite joint made up of four articulations: the tarsocrural, proximal intertarsal, distal inter-tarsal, and the tarsometatarsal joints. The tarsal joints in horses, cattle and camels share some similarities; however, numerous intra-articular and periarticular anatomical variations exist among those species. The hock joint consists of six tarsal bones in camel and horse and five tarsal bones in cattle. However, the pattern of tarsal bone arrangement is variable: in camels, the second and third tarsal bones are fused; in horses, the first and second tarsal bones are fused; and in cattle, the central and fourth and the second and third tarsal bones are fused. Moreover, the distal part of fibula in camels and cattle persists as an isolated bone (malleolar bone), which articulates with the distal extremity of the tibia, while in horses, it is completely fused to the tibia and forms the lateral malleolus. Furthermore, the talus in camels and cattle: bears a trochlea at either end; the proximal trochlear ridges are directed sagittaly; and the distal trochlea is well defined and articulates with the fused central and fourth tarsal bones in cattle and with the central and fourth tarsal bones in camel. In horses, the talus bears one proximal trochlea and the trochlear ridges are orientated obliquely in a mediolateral direction. The calcaneus in camels and cattle articulates with the distal tibia, while in horses, it has no articular surface for the tibia and covers less of the lateral aspect of the talus than in cattle and camels. Regarding the periarticular soft tissues, the tarsus of cattle and camels have more tendons and ligaments than horses: the fibularis longus tendon; an additional bundle of the short medial collateral ligament connecting the talus and the medial metatarsal bone; and the split of the long digital extensor tendon to the common extensor of digits III and IV and the medial digital extensor. In camels also, the long plantar ligament consists of a medial and lateral limbs, unlike cattle and horses in which the ligament is undivided [1,[19][20][21]. The anatomical differences among camels, cattle and horses are likely to direct the attention towards demonstration of the magnetic resonance appearance of various intra-articular and peri-articular structures of the dromedary camel tarsus.
Magnetic resonance imaging is frequently used in horses owing to its ability to produce high-contrast and anatomically detailed tomographic images [9,22]. The use of MRI in camels is still in its infancy and was limited to cadaveric studies. Cadaver limbs are commonly used for evaluation of MRI anatomy and the signal intensity recorded in cadavers was similar to that reported in live animals [12] and findings would be generalizable for live animals. The present study provided the first ever conducted detailed description of the normal anatomy of the dromedary camel tarsus on MRI  images. By knowing the variation in MRI images in the normal camel, it would be possible to understand the importance of signal intensity changes in the clinical patients. Additionally, description of the high field MRI appearance of the tarsal joint structures can also be useful in the interpretation of radiographs, ultrasound, and computed tomography of the camel tarsus [22].
Currently, the use of MRI in camels is overburdened by cost, necessity for general anesthesia, and limited availability of equipment. High field MRI scanners are now available at a small number of equine clinics in the Middle East (where camels exist in high populations) and are increasingly available and developing fast for veterinary use. We do believe that the use of MRI in camels is still a new and developing field and would be a useful diagnostic imaging modality in the future for evaluation of various dromedary orthopedic problems, besides that it is currently a valuable imaging modality for investigational purposes. As clinical availability of this modality increases in the future, it is expected that new orthopedic disorders concerning dromedary camels will be identified that have not previously been reported with other imaging modalities. In the present study, the camel tarsus was a good candidate for the high field MRI. Its narrow linear profile and minimal soft tissue coverage allowed the use of the human extremity coil and enabled close apposition of the magnetic field to the tarsus resulting into good signal intensity as reported for the tarsus of horses and cattle [12,14]. General anesthesia in camels obligates particular approach due to the different anatomical and physiological features of this species [23]. Tracheal intubation is necessary whenever general anesthesia is selected; however, endotracheal intubation in camels is a challenge [24], especially in males, due to the presence of a diverticulum of the ventral aspect of the soft palate [1]. Hence, a guiding tube and a long laryngoscope are needed to accomplish successful endotracheal intubation [25]. Accordingly, understanding of the anatomical and physiological dissimilarities of camels is indispensable to ensure a successful outcome of anesthesia and MRI examination in this species.
Knowledge of the normal anatomy and signal intensity of various tissues are crucial for correct interpretation of MRI scans obtained from lame patients. In the present study, synovial fluid had high signal intensity in STIR, PD and T2 images and intermediate signal intensity in the T1-weighted images and it was not possible to define a clear limit between the subchondral and cortical bones as both had low signal intensity. Similar findings were reported in the horse [3,13]. The corticocancellous junction was regular and clearly defined, as mentioned for the bovine tarsus [14]. Cancellous bone had heterogeneous intermediate to high signal intensity where the bone of the trabeculae had low signal intensity and fat in the bone marrow filling the trabecular spaces had high signal intensity. This agreed with those reported in the horse [13]. Articular cartilage had homogenous intermediate signal intensity, on T1 images, adjacent to the low signal of subchondral bone at articular interfaces. Similar findings were reported in the horse [26]. The tarsocrural joint capsule, synovial tissue and synovial fluid had low to intermediate signal intensity similar to those reported in the bovine tarsus [14]. Tendons, collateral ligaments and the long plantar ligament of the dromedary camel had low signal intensity and the inter-tarsal ligaments had heterogeneous signal intensity. Similar findings were reported in horse [10,27].
Diagnostic imaging continues to play an important role in the assessment of joint injuries and assists investigators to understand the risk factors associated with the onset and progression of the disease condition. Conventional radiography is the simplest, least expensive and most commonly deployed imaging modality over the last decades because of its reproducibility and feasibility to detect structural damage; however, radiography can provide only indirect information on soft tissues and insensitive to early inflammatory bone involvement and bone damage. [8]. Ultrasonography enables real-time imaging of synovial pathology, articular cartilage and cortical erosive changes at relatively low cost but it is an operator-dependent and the physical properties of sound limit its ability to assess deeper structures [28]. Diagnostic arthroscopy is a crucial skill for diagnosing intraarticular disorders as it enables a direct magnified view of the cartilage surface. However, it is an invasive method, diagnosis is based only on subjective visual evaluation and manual mechanical palpation and deeper joint structure are inaccessible due to anatomic limitations [29]. MRI has become a key imaging tool for evaluation of joint pathology thanks to its ability to assess pathologic and biochemical changes within the joint before morphologic changes become evident with conventional imaging tools. In addition, the multi-plane and multi-slice capability of MRI enables visualization of the area of interest in three orthogonal planes. Therefore, MRI has the advantage of providing details concerning bone, articular cartilage and peri-articular structures, which is not shared by any other imaging modalities [4].
High field MRI provided comprehensive assessment of the dromedary camel tarsus. Results of the present study indicated that signal intensity varied according to the used sequence and investigated structure in the normal dromedary camel tarsus. Interpretation of MRI images is a challenge and obliges a good knowledge of anatomic details and familiarization to the normal MRI appearance of the region of interest in order to diagnose the problem with confidence. Further studies are warranted to determine the clinical application of high field MRI in the dromedary camel tarsus.

Conclusions
This study demonstrates and supports the use of high field MRI to evaluate various components of the dromedary camel tarsus and have the potential to become a useful reference for interpretation in clinical situations.

Animals
Six adult dromedary camels (four males and two females) were referred to the Veterinary Teaching Hospital, College of Veterinary Medicine, King Faisal University. The age of animals ranged from 6 to 14 years (mean ± SD, 8 ± 2.5) and weight from 480 to 700 kg (mean ± SD, 594 ± 93). Camels were euthanized for reasons unrelated to the study or orthopedic problems. Immediately after euthanasia, the right and left hind limbs of each camel were disarticulated at the stifle joint, to maintain normal soft tissue tension, and examined within two hours. Prior to MRI, Tarsi were examined radiographically in the four standard planes followed by a thorough ultrasonographic examination in both horizontal and longitudinal planes, with the purpose of screening for potential abnormalities.
The study was a prospective cadaveric study. A sample size of 12 was determined based on this being a novel study concept, as this value represents the first significant increase in power in a sample size for a study where no previous datasets were available as a reference on which to base calculations [22].

MRI protocol
Immediately after the preliminary imaging investigations, limbs were positioned with the lateral aspect contacting the MRI table and foot entered the magnet first to replicate clinical positioning. MRI images were acquired using a human extremity coil and a high field 1.5 Tesla magnetic resonance scanner (Philips Ingenia 1.5T MRI; Philips GmbH, Hamburg, Germany).
Three-plane scout images (transverse, sagittal and dorsal planes) were obtained to ensure correct positioning of the specimen and proper orientation of the following sequences. The transverse plane was oriented perpendicular to the long axis of the calcaneus. The sagittal plane was defined parallel to the sagittal plane of the calcaneus. The dorsal plane was perpendicular to the sagittal and transverse planes, aligned with the plane of the metatarsal bone. Tarsi were scanned via Turbo Spinecho (TSE) sequences in T1-weighted (T1), T2weighted (T2), proton density-weighted (PD), and short tau inversion recovery (STIR) sequences in the transverse, sagittal and dorsal planes. The acquisition settings used for the MRI scanning of the camel tarsus are displayed in Table 1.

Subjective evaluation of the MRI and gross images
After MRI, limbs were frozen at -18˚C for one week. Each 4 tarsi were randomly selected, sectioned (thickness, 1 cm) and photographed. The slice number per tarsus was 35, 18 and 14 slices in the transverse, dorsal and sagittal planes, respectively. A total number of 140 (transverse), 72 (dorsal) and 56 (sagittal) slices were enrolled in the study. MRI images were assessed to establish and record the normal high field MRI appearance and signal intensity for each structure. MRI images were then compared to their corresponding cryosections. The most representative MRI images at various levels that were best correlated with the macroscopic slices were selected.