Cross-sectional anatomy , magnetic resonance imaging and computed tomography of fetlock joint in camel

ARTICLE INFO The current study aimed to describe the normal cross sectional anatomy, magnetic resonance imaging and computed tomography of fetlock joint in adult camel from both sexes. The study was carried out on twelve fetlock joints of fresh cadavers from three camels. The case history of these camels indicated that they were grossly normal with no orthopedic disorders. The cadaveric fetlock joints (n=12) were scanned using CT scanner and a 1 Tesla MRI scanner, injected with colored latex and sectioned into transverse, dorsal and sagittal slices. Cross anatomical sections were correlated with their corresponding CT and MR images for evaluation of the normal relevant anatomical structures which appeared with different signal intensities on CT and MRI scans. The current study revealed that all major soft tissues in fetlock joint of camel were clearly visualized on both CT and MR images, except the short and cruciate sesamoidean ligaments which could not be identified on both CT and MR images. The anatomical sections with the corresponding CT and MR images obtained in this study could be used as a reference for diagnosis and interpretation of clinical diseases in fetlock joint of camel. Article history:


Introduction
Camel is adapted to the hard climatic conditions of the desert and has the capability to survive and produce under hard environmental conditions (Sadegh et al. 2007). Concurrently, it is used as an important source of milk, meat and hide especially in the developing countries (Ahmad et al. 2010). Moreover, the camel is considered an essential economy source in the Gulf region through the camel racing sports and tourism (Farah and Fischer 2004).
Lameness is a serious worldwide problem due to its negative economic impact on the dairy farms (Solano et al. 2015). Moreover, the camel has a different pattern of lameness when compared to the bovine and equine, because of its peculiar anatomy and biomechanics (Al-Juboori 2013). These instances require awareness of the normal anatomical structures and developing of the modern diagnostic imaging techniques for the identification and evaluation of the orthopedic problems.
Recently, there is a growing awareness for the use of the computed tomography (CT) and magnetic resonance imaging (MRI) as valuable diagnostic imaging modalities in veterinary practices (Bienert and Stadler 2006;Nuss et al. 2011). However, their limited accessibility, high costs and the need for animal general anesthesia diminish the use of these techniques in veterinary practices (Arencibia et al. 2000). Nevertheless, improvement in availability and accessibility of these tools increases the demand for their use in animals (Pollard and Puchalski 2011). These techniques are not only used for diagnostic purposes, but also can be used in several biometric researches and measurements (Onar et al. 2002). Even though many CT and MRI studies had been done on different joints of the animal digits The present study aimed to provide a comprehensive detailed anatomic reference on the cross-sectional anatomy, CT and MRI of the fetlock joint in dromedary camel to be used as a helpful reference for the interpretation and evaluation of the musculoskeletal disorders of the fetlock joint in camels.

Materials and methods 2.1. Animals
CT and MRI examination were performed on twelve fetlock joints (right and left) of the fresh cadavers from three dromedary camels (age 2-4 years, weighed about 350-500 kg). These cadaveric limbs (fore and hind limbs) were obtained from the local slaughter-house at Beni-Suef Governorate. The camels were grossly normal with no fetlock joint disorders.

Magnetic Resonance Imaging (MRI)
Distal limbs (n=12) were positioned with their palmar/plantar aspects as the dependent portion and their long axis perpendicular to the examination table. T1-weighted MR images (TR = 1900 ms, TE = 2.74 ms, slice thickness = 2mm) were acquired in transverse, sagittal, and dorsal planes using a 1 Tesla MR scanner (Philips Medical system Intera, 1T MRI; Philips GmbH, Hamburg, Germany). This examination was done within three hours after slaughtering.

Computed Tomography Imaging (CT)
Distal limbs were placed on the examination table as done in the MRI study. Toshiba Alexion CT scanner was used for obtaining the bone and soft tissue windows CT scans in transverse, dorsal, and sagittal planes. The acquisition settings were 120 KV and 250 MA with 2mm slice thickness.

Preparation of the cross-anatomical sections
The scanned specimens (n=12) were injected with a colored gum-milk latex. The needle was introduced into the dorsal pouches of the fetlock joint abaxial to the tendinous portions of the digital extensor tendons. The limbs were frozen at -18ᵒC for one week. Then sectioned into transverse (forelimbs=2, hind limbs=2), dorsal (forelimbs=2, hind limb=2) and sagittal (forelimbs=2, hind limbs=2) slices starting about 10 cm dorsal to the fetlock joint till the middle of the first phalanx in 1cm slice thickness using an electric band saw. All anatomic sections were gently cleaned using tap water and then photographed. The anatomical sections were inspected, identified and selected in correlation to their corresponding CT and MR images.

Comparison of the cross-anatomical sections with CT and MR images
The cross-anatomical sections of the fetlock joint were compared to their corresponding CT and MR images on the basis of the shape, location and tissue density properties. For evaluation of the most clinically relevant anatomical structures of the fetlock joint in dromedary camel of the same specimens, six CT and MR images were selected to be representative for the anatomical structures ( Fig. 1) in their matched anatomical sections, one in the sagittal plane, two in the dorsal planes and three in the transverse planes.

Results
The obtained anatomical cross sections were selected and compared with their corresponding CT and MR images in a sagittal plane (Fig. 2), dorsal planes (Figs. 3, 4) and transverse planes (Figs. 5-7). No significant morphological or topographical variations were observed between the fetlock joints of the fore and hind limbs, or between the right and left contralateral limbs.

Magnetic Resonance Imaging (MRI)
Articular cartilages were clearly recognized from the surrounding bony structures as a thin layer of high signal intensity (Figs. 2, 4). Subchondral bone appeared as a thin plate of a low signal intensity and could be easily differentiated from the articular cartilage at the proximal extremity of each bone (Figs. 2, 4). Cancellous bone could be visualized at the extremities of each bone with a heterogeneous high signal intensity (Figs. 2, 4). Cortical bone had a low signal intensity, while the medulla had a high signal intensity (Figs. 2, 4). However, the trabecular pattern of the bones could not be differentiated on the obtained MR images. Proximal sesamoid bones were best recognized on the transverse MR images (Fig. 6).
Soft tissue structures were clearly visualized in all MR images with variable signal intensities. Extensor tendons could be recognized on the MR images included; the lateral and common digital extensor tendons. These tendons had homogenous low signal intensities. Margins of these tendons were well-defined by the surrounding fascia that appeared as an intermediate signal intensity. Extensor tendons were best evaluated on the transverse MR images as three narrow strips on the dorsal aspect of the distal end of the metacarpus/metatarsus (Figs. 5-6).
At the level of the proximal phalanges, the extensors appeared as four structures indicated the division of the lateral limb of the common digital extensor tendon into two branches which could be visualized as small oval structures on the dorsomedial aspect of each digit (Fig. 7).
On the palmar/plantar aspect of the distal end of the metacarpus/metatarsus, the inter-osseous muscle (suspensory ligament) could be clearly visualized as an elongated structure with had a low signal intensity deep to the digital flexor tendons at a level about 4cm proximal to the fetlock joint, this muscle appeared as four oval structures representing the axial and abaxial proximal sesamoidean ligaments on the transverse MR images (Fig. 5). However, the inter-osseous muscle and its branches were best evaluated on the dorsal MR images at the level of the sesamoid bones (Fig.  2). Moreover, the branches of the inter-osseous muscle could be depicted on the sagittal MR images (Fig. 2).
Digital flexor tendons appeared with homogenous low signal intensity structures surrounded by digital tendon sheath which had a low signal intensity. On the transverse MR images, superficial digital flexor tendon (SDFT) appeared as an incomplete ring around the oval-shaped deep digital flexor tendon (DDFT) till the level of the proximal extremity of the first phalanx (Figs. 5-7). On the dorsal MR images, the SDFT appeared as two branches on both sides of the DDFT, and then it changed its position to be deep to DDFT (Fig. 3). This reposition of the flexor tendons could be also recognized on the sagittal MR images (Fig. 2). Moreover, the manica flexoria of the SDFT had a high signal intensity that was best recognized on the transverse and dorsal MR images (Figs. 3, 5).
Joint capsules of the fetlock joint appeared as low signal intensities and the margins of these capsules were clearly outlined as a thin line of intermediate signal intensity on the sagittal, dorsal, and transverse MR images (Figs. 2, 4, 6, 7). However, the ligaments of this joint were well-defined and clearly outlined on the transverse and dorsal MR images as heterogeneous intermediate signal intensities (Figs. 3-7). While the straight sesamoidean ligament and the annular ligament could be identified on the sagittal MR images (Fig.  2). Ligaments of the fetlock joint that could be clearly identified on the obtained MR images included; the suspensory, collateral, collateral sesamoidean, palmar/plantar and straight sesamoidean ligaments. While the short and cruciate sesamoidean ligaments could not be defined.

Computed Tomography Imaging
The bone window provided an excellent delineation between the cortical and subcortical tissues as well as the bone medulla with a clear differentiation of the trabecular patterns. This medulla appeared as hypo dense black colored area. Diaphysis, condyles, sagittal ridges, proximal sesamoid bones, and phalanges appeared as hyper dense with smooth margins on the transverse, dorsal, and sagittal CT images (Figs. 2-7).
In soft tissue window, bones appeared as hyper dense structures, while the soft tissues were depicted with variable densities. On the dorsal aspect of the fetlock joint, extensor tendons; lateral digital extensor as well as the medial and lateral limbs of the common digital extensor were visualized as hyper dense structures compared with the surrounded hypodense connective tissues. These tendons were best recognized on the transverse CT images as three narrow strips on the dorsal aspect of the metacarpus/metatarsus (Fig. 5). At the level of the proximal phalanx, these extensors appeared as four structures indicating the division of the lateral limb of the common digital extensor tendon into two branches that appeared as small oval structures on the dorsomedial aspect of the limb (Figs. 6-7). On the palmar/plantar aspect of the distal end of the metacarpus/metatarsus, the inter-osseous muscle (suspensory ligament) could be clearly visualized at a level about 4cm proximal to the fetlock joint as four oval structures representing the axial and abaxial proximal sesamoidean ligaments on the transverse CT images (Fig. 5). However, the inter-osseous muscle and its branches were best evaluated on the dorsal CT images at the level of the sesamoid bones (Fig.  3). Moreover, the branches of the inter-osseous muscle could be depicted on the sagittal CT images (Fig. 2).
Digital flexor tendons could be recognized as hyper dense structures surrounded by hypodense connective tissues on the palmar/plantar aspects of the fetlock joint on the transverse, dorsal, and sagittal CT images. On the transverse CT images, SDFT appeared as an incomplete ring around ovalshaped DDFT till the level of the proximal extremity of the first phalanx (Figs. 5-7). On the dorsal CT images, SDFT appeared as two branches on both sides of the DDFT, and then it changed its position to be deep to the DDFT (Fig. 3). This reposition of the flexor tendons could be also recognized on the sagittal CT images. Manica flexoria appeared as a well-defined hypodense structure on the transverse and dorsal CT images (Figs. 2, 3, 5).
Joint capsule of the fetlock joint appeared as a hypodense structure on the sagittal (Fig. 2), dorsal (Fig. 4) and transverse (Figs. 5-7) CT images. However, the ligaments of this joint were welldefined on the transverse and dorsal CT images as hyper dense structures with surrounding hypodense connective tissues (Figs. 4-7). While the straight sesamoidean and annular ligaments could be identified on the sagittal CT images (Fig. 2). On CT images, the ligaments of the fetlock joint could be clearly identified included; the suspensory, collateral, collateral sesamoidean, palmar/plantar, and the straight sesamoidean ligaments. While the short and cruciate sesamoidean ligaments could not be recognized.

Discussion
The compared anatomical cross sections with their corresponding CT and MR images provided detailed views for the normal relevant structures of the fetlock joint in dromedary camel. These images could be used as a normal anatomic reference during the diagnosis of the musculoskeletal disorders in this particular region. CT and MRI were excellent imaging modalities used for scanning of the fetlock joint in camel. These modalities permitted visualization of the clinically relevant structures in three planes and serial slices allowing evaluation of these structures at several angles. Moreover, using latex injected joint cavities allowed a precise description of the anatomical features of this joint, and gave a standard clinical reference for the position and shape of the normal anatomical structures. CT images were acquired with minimal slice thickness and interstice space providing an accurate spatial resolution and decrease partial volume artifacts, as well as a T1weighted MRI sequence was adjusted with minimal slice thickness at a high acquisition speed; these acquisitions allowed more detailed anatomical structures to be feasible for practical clinical imaging (Smith et al. 2011).
Due to the peculiar anatomy of the distal limb in dromedary camel and high risk of lameness which may affect the draft ability (Al-Juboori 2013). Using a high definitive diagnostic technique is very important. However, radiography is the main technique for evaluation of the musculoskeletal disorders due to its entire differentiation of the bony structures, ready accessibility and low cost Using the MRI scanning in the current study for evaluation of the articular cartilages, cortical bone, subchondral bone, cancellous bone and these structures were clearly outlined. Articular cartilages were evaluated on the MRI not on the CT images, where they were recognized from the surrounding bony structures as thin layers of high signal intensities. Similar findings were reported by Hagag and Tawfiek (2018) in cattle. On the other hand, the articular cartilage could be observed using the CT in horse (Vanderperren et al. 2008). Cohen et al. (1999) attributed this difficult imaging to the markedly curved articular surfaces of the distal limb and the too thin cartilages for the spatial resolution in clinical MRI.
Using MRI in this study, the subchondral bone appeared as a thin plate of low signal intensity and could be easily differentiated from the articular cartilage at the proximal extremity of each bone. Moreover, the cancellous bone could be visualized at the extremity of the first phalanx with a heterogeneous high signal intensity and the cortical bone had a low signal intensity. Similar findings were observed by Hagag and Tawfiek (2018) in cattle.
The present study showed that the medulla of the distal end of the metacarpus/metatarsus and the proximal end of the first phalanx had high signal intensities on the MRI and it appeared as hypodense and black colored structures on the CT images. On contrary to that it appeared with a low signal intensity in camel (El-Shafey and AbdAl-Galil 2012) and in cattle ( The current study revealed that all the major soft tissue structures in the distal limb of the dromedary camel were clearly visualized on both CT and MR images. However, it was difficult to identify the cruciate and the short sesamoidean ligaments on the CT and MR images, similar to the finding by  The extensor and flexor tendons were clearly outlined in cross anatomical sections and their corresponding MR and CT images in the current study. However, these tendons could be demonstrated in the cross anatomical sections only after dissection of the intervening fascia (El-Shafey and Abdel Al-Galil 2012 in camel and El-Shafey and Sayed-Ahmed 2012 in camel and buffalo). In agreement with Hagag and Tawfiek (2018) in cattle, these tendons appeared as hyper dense structures with the surrounding hypodense connective tissue on the CT images, while they were visualized on the MR images as homogenous low signal intensities. Moreover, the deep digital flexor tendon was depicted on the CT images by El-Nahas et al. (2015) in camel as a hyper dense structure. In addition to that on the MR images, the SDFT appeared as rounded structure with a low signal intensity, and the DDFT appeared as oval shaped structure with a low signal intensity and clear outlines (El-Shafey and Abd Al-Galil 2012 in camel). Moreover, the present study and Hagag and Tawfiek (2018) in cattle depicted the digital sheath as a thin layer of a low signal intensity on the MR images. Moreover, this sheath was visualized on the CT images as a hypodense connective tissue surrounding the digital flexor tendons, similar to the results of Puchalski et al. (2007) in horse. Moreover, the current study permitted a detailed visualization of the manica flexoria in gross anatomical sections, CT, and MR images. This structure was depicted, in this study, with a high signal intensity that was best recognized on the transverse and dorsal MR images, while it appeared as a well-defined hypodense structure on the transverse and dorsal CT images. This manica flexoria is clearly visible on the CT images surrounding the deep digital flexor tendon proximal to the fetlock joint of the horse (Vanderperren et al. 2008). On the other hand, it is demonstrated only in cross sectional anatomy of the buffalo, while in camel it could not be visualized either in cross anatomical sections or on the CT images (El-Shafey and Kassab 2012 and El-Shafey and Sayed-Ahmed 2012).
The inter-osseous muscle was clearly recognized in this study in gross anatomical sections, CT, and MR images, where it appeared as a hyper dense structure on the CT images and it had a low signal intensity on the MR images. Moreover, this muscle appeared as an elongated structure deep to the digital flexor tendons, while, at about 4cm proximal to the fetlock joint, this muscle appeared as four oval structures representing the axial and abaxial proximal sesamoidean ligaments. While Al-Akraa et al. (2014) reported that the interosseous muscle appears on the palmar aspect of the metacarpal bone in both CT images and cross sections as an elongated or flattened structure in cattle and elliptical in buffalo. However, El-Shafey and Sayed-Ahmed (2012) in buffalo and camel observed this muscle more distinctly in cross sections than in the CT images.
The joint capsule of the fetlock appeared in this study with a low signal intensity, the margins of this capsule were clearly outlined as thin lines of intermediate signal intensities on the transverse, dorsal, and sagittal MR images. Similar findings were observed in the fetlock joint of cattle (Hagag and Tawfiek 2018). Moreover, this capsule appeared as a hypodense structure on the transverse, dorsal, and sagittal CT images, similar to the findings of El-Nahas et al. (2015) in camel. On contrary, this joint capsule cannot be observed using the CT or MR images, due to they are potential cavities appear only in linear cross sections

Conclusion
The current study provided definite anatomical cross sections with their corresponding CT and MR images of the most clinically relevant structures of the fetlock joint in dromedary camel. These images could be used as a normal anatomic reference during the diagnosis of the musculoskeletal disorders in this region.