Cartilage Erosion and Patellar Luxation

Patellar luxation is a developmental or traumatic disease, and occurs when the patella becomes dislocated, either medially or laterally, from its normal position within the femoral trochlea (Figure 1) (Bevan and Taylor, 2004, Harasen, 2006b, O’Neill et al., 2016, Lavrijsen et al., 2014, Phetkaew et al., 2018). Medial patellar luxation is considered to be more common than lateral luxation and often occurs concurrently with cranial cruciate ligament rupture (Bound et al., 2009, Mostafa et al., 2008, Langenbach and Marcellin-Little, 2010, Lavrijsen et al., 2014).

The patella is normally held within the femoral trochlea by fascia lata, femoral fascia, medial and lateral patellofemoral ligaments, medial and lateral trochlear ridges, joint capsule; and supported by the medial and lateral parapatellar fibrocartilages (Bevan and Taylor, 2004, Evans and de Lahunta, 2013, Ferguson, 1997, Roush, 1993). It works as a lever arm to control the direction of the pull by the quadriceps muscles, which essentially reduces the amount of force required to extend the stifle joint (Bevan and Taylor, 2004, Ferguson, 1997, Roush, 1993). The patellofemoral joint is innately unstable and its stability relies on the normal morphology of bones and musculotendinous structures within the stifle joint (Fonseca et al., 2017). Additionally, the collateral patellofemoral ligaments are relatively weak, which may contribute to the instability of the patellofemoral joint (Dyce et al., 2010).

Any abnormality in the extensor components of the stifle joint – patella, patellar ligament, quadriceps muscles, tibial tuberosity and the femoral trochlea – can lead to malalignment of the extensor mechanism of the stifle, which will place abnormal forces on the patella, ultimately increasing the potential for luxation (Bevan and Taylor, 2004, Harasen, 2006b, Mostafa et al., 2008, Ferguson, 1997). This is because all of these components are directly or indirectly interconnected one way or another and ultimately function together as an extensor mechanism for the stifle (Dyce et al., 2010). The patella is joined to the tibial tuberosity by the patellar ligament; the patellar ligament itself acts as the tendon of insertion for the quadriceps muscles; and the patella sits within the femoral trochlear groove (Dyce et al., 2010, Evans and de Lahunta, 2013). The normal function and morphology of these components are therefore essential for proper functioning of the stifle joint.

The size, weight, and age of animals also influence the aetiology and prognosis of patellar luxation (Wangdee et al., 2015). In terms of size – toy breeds, miniature and smaller dogs are more at risk of developing patellar luxation, especially medial patellar luxation (Langenbach and Marcellin-Little, 2010, Harasen, 2006a, Roush, 1993, Bound et al., 2009, Bevan and Taylor, 2004, O’Neill et al., 2016). This may be due to the fact that certain toy breeds are more prone to genu varum, a risk factor associated with the abnormal pull of the quadriceps muscles and medial luxation of the patella (Dyce et al., 2010). In young animals with immature skeletons, patellar luxation tends to lead to the development of angular and torsional malformations, placing abnormal forces on open growth plates (Roush, 1993, Ferguson, 1997). This ultimately leads to the improper growth of the distal femoral physes and subsequent abnormal growth in the proximal tibia resulting in tibial bowing (Ferguson, 1997). Furthermore, the rectus femoris muscle (part of the quadriceps musculature) in some young animals may exhibit congenital atrophic changes causing a “bowstring” effect which pulls the patella medially, and can potentially lead to the dislocation or luxation of the patella due to abnormal force exerted by the extensor mechanism (Harasen, 2006b). Older animals, however, tend to develop degenerative joint disease due to the lack of proper patellofemoral contact (such as through cartilage erosion) as a result of patellar luxation (Roush, 1993, Boonsri et al., 2016).

With regards to the weight of animals, dogs that weigh below their breed’s average bodyweight had a higher risk of patellar luxation than dogs that weighed above their breed’s average bodyweight (O’Neill et al., 2016, Lavrijsen et al., 2014). This correlation may be due to the fact that lighter dogs have less overall muscle mass, including the mass of the quadriceps muscles, which can increase the risk of patellar laxity (O’Neill et al., 2016). Conversely, the patellar luxation itself could lead to reduced overall muscle mass due to muscle atrophy due to prolonged limb disuse (O’Neill et al., 2016). However, heavier dogs do suffer greater cartilage erosion during the course of patellar luxation due to the impact that their higher body weight has on the loading of the patellar cartilage (Daems et al., 2009). As lighter dogs have less weight, this most likely reduces stresses on the stifle joint in comparison to heavier dogs (Dona et al., 2016).

Patellar luxation varies in its severity and the different changes that can be observed in an animal with this disease are used to grade the severity (Bevan and Taylor, 2004, Harasen, 2006a, Ferguson, 1997). A grade 1 patellar luxation is given when the patella can be luxated with manual pressure but will return to its normal position within the trochlear groove when released, and this is usually associated with a minor laxity in the lateral retinacular structures (Bevan and Taylor, 2004, Harasen, 2006a, Ferguson, 1997). If the animal’s patella luxates with flexion of the stifle or due to manual pressure and remains luxated until stifle extension or manual reduction, this usually indicates that mild torsional and angular abnormalities with the femur/tibia have occurred causing mild lameness (Ferguson, 1997, Harasen, 2006a). This is a grade 2 patellar luxation (Bevan and Taylor, 2004). If the animal’s patella becomes permanently luxated and will spontaneously luxate after manual reduction, this indicates a shallow trochlear groove, abnormalities of the tibial tuberosity, or bowing of the tibia and/or femur – a grade 3 patellar luxation, causing persistent lameness (Ferguson, 1997, Harasen, 2006a). The most severe form of luxation occurs when the patella is luxated permanently and cannot be manually reduced, usually associated with a wide range of skeletal and muscular abnormalities, and results in a complete failure to extend the stifle joint, lameness and the dog walking in a crouched position – a grade 4 patellar luxation (Harasen, 2006a, Ferguson, 1997).

It was previously hypothesised that hip deformities such as coxa valga and coxa vara predisposed the patella to luxation, as these deformities affected the angles of inclination between the femoral head and neck and may displace the extensor muscles of the hindlimb, such as the quadriceps muscles (Mostafa et al., 2008, Bevan and Taylor, 2004, Harasen, 2006b). However, it has also been suggested that medial patellar luxation arises only due to abnormalities in the stifle components and are unrelated to the hip deformities (Bound et al., 2009, Ferguson, 1997). These abnormalities arise due to congenital malformations in the components of the extensor mechanism of the stifle and can include hereditary disorders such as bowing and torsion of the femur; displacement of the quadriceps muscles; a shallow femoral trochlear groove (Figure 2); abnormal angulations or torsions of the femur or tibia; or irregular development of the femoral condyles or tibia (Ferguson, 1997, Harasen, 2006a, Roush, 1993, Phetkaew et al., 2018, Zilincik et al., 2018). Rather than patellar luxation being a congenital disease in itself, the disorder develops as a result of these congenital skeletal or muscle malformations which alters the normal structure of the stifle joint, increasing the likelihood that the patella is either pulled out, or slips out of its position in the femoral trochlea (Bevan and Taylor, 2004, Harasen, 2006b, Harasen, 2006a, O’Neill et al., 2016, Phetkaew et al., 2018). Patellar luxation can also lead to morphological and anatomical abnormalities in the pelvic limb, especially in younger animals (Phetkaew et al., 2018, Zilincik et al., 2018).

Patellar luxation can also occur as a result of a traumatic injury, however, this is not as common as congenital luxation (Harasen, 2006a, Ferguson, 1997). This occurs when a traumatic injury inflicts damage to the retinacular structures in the stifle joint, particularly those on the lateral side (Ferguson, 1997, Harasen, 2006a). The medial and lateral retinacula both provide stability to the stifle joint during movement, and its fibres insert into the patella and the patellar ligament (Starok et al., 1997, Fonseca et al., 2017). If a traumatic injury causes a tear in the retinacular attachments which are located close to, or at, the attachment to the patella – this is a common cause of traumatic patellar luxation, as the patella becomes destabilised due to the loss of function of one of its supporting structures (Starok et al., 1997). Traumatic patellar luxation may also inflict other intra-articular damages to the stifle joint, such as a tear in the joint capsule or rupture of the cranial cruciate ligament (Roush, 1993).

Normally, the extensor components of the stifle will exert a straight line of force which is essential for proper function of the stifle joint, but any abnormal developments of the extensor components can pull or drag the patella out of its proper position within the trochlear groove as the stifle attempts to maintain the straight line of force during movement (Roush, 1993, Ferguson, 1997). In the case of smaller toy breed dogs, genu varum is a common congenital disorder and when the pull of the quadriceps muscles fails to correspond with the axis of the femoral trochlea, this can lead to patellar luxation (Dyce et al., 2010). As the patella becomes luxated, the medial bowing of the femur, and potentially, the bowing or rotation of the tibia begins to occur (Harasen, 2006b, Bound et al., 2009, Bevan and Taylor, 2004). Furthermore, the forces exerted on the femoral trochlear sulcus by the patella begins to reduce as the patella no longer sits properly within the groove, ultimately resulting in the development of a shallow femoral trochlea (Figure 2) (Ferguson, 1997, Roush, 1993). A shallow femoral trochlea exacerbates the luxation, as the groove which is meant to hold the patella can no longer do so. As a result of this, the patella is forced to sit outside of the femoral trochlear groove, unable to retain its original position within the trochlea (Figure 2). These skeletal malformations can occur quickly, caused by these new abnormal forces acting on the femur and tibia (Ferguson, 1997).

The cranial cruciate ligament is often ruptured concurrently with patellar luxation, with approximately 15% to 25% of dogs rupturing their cranial cruciate ligament whilst suffering from patellar luxation at the same time (Piermattei et al., 2006, Harasen, 2006a, Bound et al., 2009, Langenbach and Marcellin-Little, 2010). This can be attributed to the internal rotation of the tibia as a result of the luxation, which puts additional stress on the cranial cruciate ligament (Harasen, 2006a). Furthermore, due to malalignment of the extensor components of the stifle – in particular the quadriceps muscles, patella and the patellar ligament – this provides less cranial stability to the stifle joint, resulting in less resistance to forces that have the ability to subluxate the tibia cranially which again, puts additional stress on the cranial cruciate ligament (Harasen, 2006a).

Stability of the stifle joint, notably the femorotibial articulation, depends quite significantly on the cruciate ligaments (Dyce et al., 2010). Both the medial femorotibial and patellofemoral joint cavities communicate with each other constantly (Dyce et al., 2010). Rupture of the cranial cruciate ligament allows irregular free forward displacement of the tibia with relation to the femur (Dyce et al., 2010). When patellar luxation and rupturing of the cranial cruciate ligament occurs concurrently, this is a common cause for lameness in dogs and needs to be addressed through surgery such as tibial plateau levelling osteotomy (TPLO) in order to rectify the stifle joint (Langenbach and Marcellin-Little, 2010). Histologically, a ruptured cranial cruciate ligament can lead to decreased cell density and metaplasia of ligament fibroblasts in the surrounding tissue, which potentially can result in a reduced ability to produce more extracellular matrix as fibroblasts actively produce this (Hayashi et al., 2003, Eurell et al., 2013). It also leads to a significant disruption to the hierarchy and organisation of the collagenous extracellular matrix within the surrounding tissue itself (Hayashi et al., 2003).

In addition to this, patellar luxation may further erode cartilage within the stifle joint due to joint instability from the movement of the patella in and out of the femoral trochlear groove (Boonsri et al., 2016, Daems et al., 2009, Zilincik et al., 2018). More severe cases of patellar luxation lead to higher degrees of cartilage erosion, especially on the articular surface of the patella due to greater abnormal forces affecting the articulation between the patella and femoral trochlea (Daems et al., 2009). The erosion of cartilage at the patellofemoral articulation leads to severe friction as the articular surfaces of the joint rub together without cartilage protection (O’Neill et al., 2016). This has the potential to lead to osteoarthritis and rupture of the cranial cruciate ligament as a consequence of the resulting degenerative joint disease (Boonsri et al., 2016, Harasen, 2006a, O’Neill et al., 2016, Lavrijsen et al., 2014, Zilincik et al., 2018).

Cartilage erosion and patellar luxation has also been associated with increased expression of the enzyme MMP-3, which promotes the degradation process in the stifle joint by cleaving collagen, proteins of the extracellular matrix, aggrecan and link proteins (found in the ground substance of the cartilage matrix); contributing to the subsequent development of osteoarthritis (Boonsri et al., 2016, Eurell et al., 2013). The activity of MMP-3 is regulated by another enzyme: TIMP-1, which is also upregulated during patellar luxation and cartilage erosion (Boonsri et al., 2016). However, MMP-3 was upregulated in greater amounts in comparison to TIMP-1 in both the articular cartilage and synovial membrane during patellar luxation with cartilage erosion (Boonsri et al., 2016). This upregulation of MMP-3 may also potentially exacerbate problems involving the patellar ligament, cruciate ligaments or retinacular structures, as they are composed primarily of collagenous connective tissue (Sjaastad et al., 2003, Eurell et al., 2013). The synovial membrane also consists majorly of collagen, which is a major site of MMP-3 upregulation and is also damaged during the onset of osteoarthritis (Updike and Diesem, 1983, Boonsri et al., 2016, Zilincik et al., 2018). Indeed, rupture of the cranial cruciate ligament is associated with the degradation of the hierarchical architecture of the collagenous extracellular matrix in the surrounding tissue (Hayashi et al., 2003). However, even if cartilage erosion does not occur or is limited, patellar luxation increases the expression of the pro-inflammatory cytokines: IL-1 and TNF- which contributes to the development of osteoarthritis (Boonsri et al., 2016). Additionally, if osteoarthritis begins to become established as a result of the patellar luxation, this can lead to synovial effusion of the stifle joint, osteophytosis, synovial hypertrophy, articular mineralisation, enthesopathy of supporting tendons or ligaments within the stifle, cyst formation within bones of the stifle, and sclerosis of the subchondral bone (Ferguson, 1997, Pownder et al., 2018, Innes et al., 2004).

Illustrations

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