Anatomical study on the stifle (knee) joint in local breed of Awassi sheep

Abstract


Introduction
Sheep are an important source of livestock in the country, where they are raised primarily for producing meat, milk, wool, and leather. There are three breeds of sheep in Iraq: Al-Awassi, Al-Karadi, and Al-Arabi, and Al-Awassi is the most prevalent breed in Iraq and some parts of the Arab world, Turkey, and others (1). Musculoskeletal studies frequently employ adult sheep bones as large animal models (2,3). Animal paws have great importance as they help animals to move and graze, and the bones and joints injuries should be considered the complex stifle joint (4). This joint is often prone to many complications that may require surgical intervention, for instance, patellar dislocation, synovitis, joint destruction, meniscal tear, and cruciate ligament damage (4)(5)(6).
As a result of the injuries mentioned above, the stifle joint is exposed to injury in sheep and knowing the exact structure of this joint gave us the incentive to do this research on the local Awassi sheep in Nineveh Governorate, which aims to study the morphological characteristics of stifle joint in Awassi sheep by using macroscopic anatomy.

Materials and methods
Ten hind limbs of apparently healthy adult Awassi sheep of both sexes aged 2.5 -3.5 years old were purchased from Mosul slaughterhouse and dissected to expose the stifle joint. The samples were divided into two groups. Group one four joints were placed after removing the soft tissues from them as much as possible in a solution of sodium hydroxide NaOH at a concentration of 10% for 48 hours at room temperature to perform the maceration process for these joints in order to study the joint surfaces (7,8). Group two six joints were dissected to study the ligaments and cartilage and describe the joint capsule.

Ethical approve
Ethical approval was not required for this study because data were collected from slaughterhouse.

Results
In Awassi sheep, our results presented that the knee joint is one of the complex joints, where further than one articular surface participates in its formation, and it consist of articular surface of femur and patella as articular surfaces of femur and tibia.

femoral-patellar articular surface
It formed between the femural and patellar articular surfaces ( Figure 1). The femur's trochlea included two oblique and parallel ridges with a broad, deep groove between them. The medial edge is lower than lateral ridge and larger, especially in its distal part, where it continues with the medial condyle of the femur. The extensor fossa demarcates the lateral ridge from the lateral condyle ( Figure  2).
Compared to articular surface of trochlea, the patella is significantly smaller than supplemented medially with a plate of parapatellar fibro-cartilage, which bends over a medial margin of the trochlea, a simple middle ridge dividing the surface of the articulation of the patella that extends from the base proximally to apex distally into a small lateral part and a large medial part ( Figure 3).

Articulated capsule
The articular capsule of the patellofemoral articular surface in Awassi sheep was thin and broad, and it is a fibrous layer that connects and surrounds the edges of the articular surfaces. This capsule was strengthened laterally by the lateral patellar ligament, which is partially fused with it, while it is attached medially to the fibrous layer of the medial patellar femoral ligament from which it separated (Figures 4  and 5). The capsule is located under the quadriceps femoris muscle for about 1.5 cm, separated from this muscle by a piece of fat. A thick layer of adipose tissue separates the capsule from the patellar ligaments.

The medial and lateral femoral-patellar ligaments
Fibrous bands that strengthen the articular capsule from both sides. The medial femoral-patellar ligament ( Figure 4) appeared somewhat distinct and was fan-shaped, with its wide part located anteriorly to the patella. It comes from the eminence on medial epicondyle of femur proximal and posterior to the medial collateral ligament. The ligament diverges in the proximal and anterior direction to terminate at the patellar medial border, the parapatellar fibro-cartilage connected to the medial part of the patella's anterior surface, and the distal to medial tuberosity. The lateral femoralpatellar ligament ( Figure 5) appeared thin and indistinguishable from fibrous layer of articular capsule. It is represented by a narrow band arising from an eminence located on the lateral femoral epicondyle proximal and posteriorly from lateral collateral ligament of stifle joint. The ligament passes in an oblique anteriority direction to be attached in the middle of lateral border of patella.

Patellar ligaments
are three ligaments in the form of bands that attach patella to the tibial tuberosity. They are insertion tendons of the quadriceps femoris muscle and the femoralis biceps muscle. The medial ligament of the patella ( Figure 6) comes from the medial part of the anterior patellar surface, ventrally to the medial femoral-patellar ligament, which is partially covered by this ligament and then passes distally to attached in the medial surface from the proximal end of the tibia and posteriorly to the tibial tuberosity. The middle patellar ligament ( Figure 7) is long, strong, thick, and broadband that extends from the anterior patellar surface and passes straight distally to the tibial tuberosity. The lateral ligament of patella ( Figure 8) appeared indistinct and completely fused with insertion tendon of the biceps femoris muscle that comes from the distal half of the lateral border of patella toward the lateral surface of the tibial tuberosity.

femoral-tibial articular surface
The femoral-tibial articulation in Awassi sheep is created between the two femoral condyles, the proximal extremity of tibia, and menisci between them ( Figure 9). The femoral condyles appeared slightly oblique in direction ( Figure 10).
Compared to the medial condyle, the lateral one was wider and larger, and its articular surface was more curved than that of the medial condyle. The medial condyle is confluent distally with the trochlear medial ridge, while the lateral one is separated from the lateral ridge by extensor fossa. In addition, the articular surface of lateral condyle presents the popliteal fossa from which the oblique tendon of the popliteal muscle arises. Two articular eminences, the medial and lateral condyles, are located on the proximal end of the tibia. (Figure 11), Each has an articular surface that resembles a saddle to allow for articulation with the appropriate femoral condyle and meniscus. Medial condyle was more extended and larger than lateral condyle on caudal surface of the proximal extremity of the tibia. The lateral condyle's lateral surface contains the articular facet of the head of the fibula. The inter-condylar eminence or spine of the tibia is slightly oblique and consists of two parts, a large and high medial part, while the lateral part is small and low, and these two parts are separated from each other by a deep and narrow nonarticular fossa from which the cranial cruciate ligament arises. There were intercondyloid fossae cranially as well as caudally to inter-condyloid eminence. The caudal one is larger and deep and to which attaches the caudal ligament of medial meiscus. At the same time, the cranial fossa is represented by a small shallow nonarticular depression separated cranially by the lateral part of the intercondyloid spine of the tibia where the lateral meniscus's cranial ligament was attached ( Figure 11). Cranial to the medial part of the tibia's intercondyloid spine, the medial meniscus's cranial ligament is attached to a small prominence. The popliteal notch separates the two condyles of the tibia caudally, from which, in the medial part, there was a prominent tubercle to attach the caudal cruciate ligament. The tuberosity of the tibia has an oblique surface directed craniodistally. The middle patellar ligament covers it entirely ( Figure 11).
The medial and lateral menisci ( Figure 12) are crescentic plates of fibrocartilage that correspond to the femoral as well as the tibial articular surface. The lateral meniscus ( Figure  13) does not cover caudal part of the lateral-tibial condyle, which was the site of attachment of the origin tendon of the popliteal muscle. Each meniscus has a proximal deep concave surface corresponding to the femoral condyle and a convex distal surface corresponding to the tibial condyle. The lateral border of each meniscus is very thick and convex, while the medial border is very thin and concave. Meniscal ligaments connected the cranial and caudal extremities of meniscal cartilage to the tibia at cranial and caudal to the tibial spine.

Meniscal ligaments
The cranial meniscotibial ligament connects each meniscus cranially to the tibia. The lateral one is longer and wider than the medial one. It runs from the lateral meniscus's cranial extremity to attach to the intercondyloid spine's cranial fossa, while the medial one is shorter and thinner than the lateral one. It runs from cranial extremity of the medial meniscus to attach the eminence to cranial fossa and the cranial part of the tibial spine. In addition, the medial meniscal cartilage is connected to the tibia by the caudal meniscotibial ligament, which extends from the caudal extremity of the meniscus to caudal fossa caudal to the spine of the tibia. The lateral meniscus is attached to the femur by the meniscofemoral ligament ( Figure 13). This ligament is represented by a thick, short, and flat band extended in an oblique path from the lateral meniscus' caudal extremity toward a facet in the caudomedial part of femoral intercondyloid fossa proximal to medial condyle ( Figure 10).

Articular capsule
The fibrous layer was connected to the femur and tibia's condyle edges. The meniscus's and cruciate ligaments' convex borders are thin cranially and are represented only by the synovial layer, while they are much stronger caudally where the oblique tendon of the popliteal muscle strengthens them. The articular capsule is related to the medial and lateral femurotibial ligaments. There are two synovial sacs with minimal communication observed between them in between the cruciate ligaments.

Ligaments
There are four ligaments, two collateral, and two cruciate. The medial collateral ligament ( Figure 14) is a long, narrow, and thick band that extends from a depression on the femoral medial epicondyle distal to the attachment of the medial femur patella ligament. It passes straightly to be attached on the most caudal part of the inner surface of the tibia about 4 cm distal to the tibial inner condyle's edge.

Discussion
Two major joints comprise the stifle joint anatomically, the femurotibial and femuropatellar joints. Condyles of femur,tibia as well as medial and lateral meniscie come together to create the femur-tibial articulation. The femur's trochlea and the patella's articular surface come together to construct the femuropatellar articulation (8,9). This result agreed with our observation in Awassi sheep that the knee joint is one of the complex joints, where more than one particular surface participates in its formation, and it consists of the articular surfaces of the femoral-patellar and femoraltibial bones.
The external fibrous capsul as well as the inner synovial joint capsules comprised articular capsule, whereas outer one surrounded the femuropatellar and femurotibial joint sacs (10); our results agreed with the results mentioned above about the articular joint capsule. The articular surface of the patellofemoral capsule in Awassi sheep was thin and broad, where its fibrous sheet connects to the edge of the articular surfaces. It is strengthened laterally by a lateral patellar ligament partially fused with it, while medially, it is connected to a fibrous layer of the medial patella-femoral ligament. Medial and lateral femoro-patellar ligament existed skinny bands, as components of the fibrous joint capsule, running from the patellar medial and lateral borders to the medial and lateral sesamoid bones, respectively, at gastrocnemius muscle insertions (11).
Our results partially agree with what the researcher mentioned in the fact that there is a medial patellofemoral ligament and a lateral patellofemoral ligament, as the two ligaments connect to the patella. However, the difference is in the connection of the other end, where El-Bably and Noor (11) found the connection in the sesamoid bones at gastrocnemius muscle insertions. The difference is due to the difference in the type of animal under study. The Patellar ligaments are three bands that associate the patella with the tibia's tuberosity. Our findings approved those mentioned by Shigue et al. (12) in deer. Elbably and Noor (8), in their study on a red fox, said that the medial and lateral seasamoid bone, the medial and lateral femoral condyls located between the inter-condyloid fossa, the medial and lateral menescii, in addition to lateral and medial tibial condyles disconnected by the inter-condyloid eminance construct the femorotibial articulation, the observation of researcher like our results except there is no sesamoid bone in the stifle joint in sheep. Findings of current study were similar to that cited by Fathi et al. (13), who cited that the femoral medial condyle was inferior and lesser than the lateral one. Also, it was oblique in direction. The extensor fossa was situated between the lateral ridge of the femur's trochlea and the lateral condyle. The condyles of the tibia also were medial as well as lateral. These condyles have minimal contact with the femur's condyles since they were not designed to fit there. The existence of the menisci offset this adaption. The intercondylar eminence separates the two tibial condyles into medial and lateral parts. The medial part appeared higher than lateral part. Lateral condyle appeared greater than medial one. The inter-condyloid eminence has two fossae that were cranial and caudal to it (14).
This result agreed with our findings, where proxiemal extremity of the tibia presents medial as well as lateral condyles. Each has to some degree, a saddle-shaped articular surface used for articulation with the compatible femoral condyle and meniscus. The menisci, which recompense for the incongruence of the articular surfaces, are each semilunar and wedge-shaped in section with concave proximal and slightly convex distal surfaces. Each is protected by ligaments that run between its cranial and caudal extremities and the central nonarticular area of the proximal extremity of the tibia. The lateral meniscus was also attached caudally to the femoral intercondylar fossa (15). This result agreed with our results. The cranial and caudal cruciate ligaments are fundamental in the femoral intercondyloid fossa between the two synovial sacs of the femorotibial joint.
The anterior cruciate ligament is oriented to the caudal direction and dismisses in the lateral wall of the femur's intercondyloid fossa. The caudal cruciate ligament runs proximally and is cranially medially to cranial cruciate ligament to terminate in the anterior part of the femur's intercondyloid fossa (16). This result is agreed with our observation. The cruciate ligaments are two strong bands which are existed fundamentally in the femoral intercondyloid fossa between the paired synovial sacs. During the last decade, Numerous animals were admitted to hospital for various clinical reasons, and among these clinical cases, a sizable percentage had knee joint fractures (17,18). The caudally cruciate ligament is longer and lies medially to the cranial one. It arises from a prominent tubercle on the medial surface of the tibial popliteal notch. From its origin, the caudal cruciate ligament was directed proximally and cranially to be inserted in a depression situated in most cranial part of the femoral intercondyloid fossa. The cranial cruciate ligament was shorter than the posterior one. It arises from the intercondyloid fossa (central fossa) on the tibial spine and extends proximo-caudally to be attached to the horizontal wall of the femoral inter-condyloid fossa, these findings came in agreement with Hifny et al. (16).
This work concluded that fibrous sheet of articular capsule is connected around the edges of condyles of femur and tibia, and the articular capsule is attached to the medial and lateral tibiofemoral ligaments. There are two vesicular sacs with a simple connection between the cruciate ligaments. Severe joint lesions led to a high frequency of leg weakness, but this relationship was not absolute, indicating the joint lesions are not the only cause of leg weakness (19). Etterlin et al. (20) hypothesized that the increased magnitude and diversity of biomechanical stress experienced by freerange pigs promotes the development of osteochondrosis. Large animal models of osteoarthritis are a necessary testing ground for FDA approval of human medicine applications. Sheep models have advantages over other available large animals, but development and progression of osteoarthritis in sheep is exceedingly slow, which handicaps progress in development of potential treatments (21,22).

Conclusion
This study concluded that the fibrous sheet of the articular capsule is connected around the edge's condyles of femur and tibia, and the articular capsule is attached to the medial and lateral tibiofemoral ligaments. There are two vesicular sacs with a simple connection between the cruciate ligaments.