Three-dimensional anatomy of the ostrich (Struthio camelus) knee joint

Osteology

The knee joint of an adult ostrich has five component bones: the distal femur, the proximal tibia and fibula, and the proximal and distal patella (Fig. 2B). The femur has asymmetric condyles, the lateral being appreciably larger than the medial. While we observed general asymmetry in other ratites, the differential size between lateral and medial condyle appears to be greatest in the ostrich. There is also a large lateral femoral epicondyle lateral to the lateral femoral condyle, forming a fibular trochlea. The tibiotarsus has lateral and cranial tibial crests extending from those two aspects of the proximal tibia.

The proximal patella lies high on the lateral femoral condyle, dipping slightly into the large sulcus in the position the specimen was scanned in (similar to that in three other specimens scanned). The proximal patella therefore topologically corresponds to the single patella of other birds, which occupies a position within or slightly above the sulcus (Shufeldt, 1884; Haines, 1942; Cracraft, 1971), and its flattened morphology likewise is similar.

The distal patella, which has only been briefly mentioned in literature (Macalister, 1864; De Vriese, 1909; Thompson, 1890; Bezuidenhout, 1999; Gangl et al., 2004; Wagner, 2004), is 75.7 mm long in our subject (ossified portion; Table 1) and sits in front of the lateral femoral condyle. There was considerable variability in the distal patella lengths we observed in our dissected and museum specimens, however, the length does roughly correlate with femur length (Table 1), which suggests a correlation with age. The distal patella extends down to just above the tip of the tibial crest, where it is connected by a short band of connective tissue (∼3 mm), apparently corresponding to a distal remnant of the patellar tendon. This distal-most sesamoid, much like the patella observed in some diving species (Shufeldt, 1883; Shufeldt, 1884; Thompson, 1890), appears like a proximal extension of the tibial crest, observed in other species such as Colymbus glacialis (Thompson, 1890; Vickaryous & Olson, 2007). Both patellae are enveloped by a thick, fibrous facial sheet to which many tendons contribute. While neither patella articulates directly with any other bone in the knee (through an articular cartilage interface), the layer of fibrous tissue between the femur and proximal patella is thin and may allow transmission of contact forces in some poses or loading regimes.

Ligaments and menisci

There are four primary ligaments which provide stability and alignment in the knee joint of ostriches, as in many other tetrapods (Fig. 2A; Fuss, 1989; Fuss, 1991; Fuss, 1996). A wide, flat collateral ligament spans the femorotibial joint space on either side, laterally and medially. The medial collateral ligament (MedCL) connects the medial femoral condyle to the tibiotarsus. It originates within a small fossa on the distal medial side of the medial femoral condyle and inserts distally to the tibial plateau on the medial edge of the proximal tibia. The lateral collateral ligament (LatCL) originates on the distal part of the lateral femoral epicondyle, and inserts onto the fibula, on the posterior-distal corner of the lateral side of the bulbous epiphysis, as well as the lateral meniscus, on the lateral side of the large, pointed cranial extension of the meniscus. There is additionally a larger lateral collateral ligament (LatCL_2) which originates at the very top of the lateral femoral condyle, inserts on the shaft of the fibula, and also connects cranially to the meniscus. The cranial cruciate ligament (CranCL) is round in cross-section, originates caudally (in the popliteal fossa) between the femoral condyles and inserts cranially on the tibial plateau (Fig. 3A). The caudal cruciate ligament (CaudCL) is thicker and flatter. It originates from a small impression on the medial side of the lateral femoral condyle, crosses over the top of the CranCL, and inserts on the caudomedial corner of the tibial plateau (Fig. 3A). We found slight differences in the size and shape of attachments, particularly on the tibial head, from previous descriptions (Fuss & Gasser, 1992); however, the general location agreed (Fig. 3B).

The medial meniscus sits between the medial femoral condyle and the tibial plateau. It is circular, thickest on its outermost aspect and thinner towards the incomplete centre, so that it forms a triangular wedge in cross section. Cranially, the medial meniscus connects to the lateral meniscus. The lateral meniscus is smaller than the medial meniscus and is longer (craniocaudally) than it is wide (mediolaterally). It sits primarily in the gap between the tibiotarsus and the fibula and extends cranially up the lateral femoral condyle. The femoral meniscal ligament attachments match well with Fuss & Gasser’s (1992) descriptions, however, the tibial attachments differ in size and two meniscal attachments on the fibula were found, which were not previously noted (Fig. 3B).

Myology

From our MRI scan and dissections of the knee region, we identified 12 distinct muscles that cross the knee joint near the patellae (see Hutchinson et al., 2014 for details on anatomical nomenclature): M. ambiens part 1 (AMB1), M. femorotibialis intermedius (FMTIM), M. femorotibialis lateralis pars distalis (FMTLD), M. femorotibialis lateralis pars proximalis (FMTLP), M. femorotibialis medialis (FMTM), M. fibularis longus (FL), M. gastrocnemius intermedius (GIM), M. gastrocnemius lateralis (GL), M. gastrocnemius medialis (GM), M. iliotibialis cranialis (IC), M. tibialis cranialis- femoral head (TCfem), and M. tibialis cranialis- tibial head (TCtib). Seven of these muscles are directly connected by tendons to the patellae: the IC, GL, FL, GM, FMTIM, FMTLD, and FMTLP (Fig. 4). The IC, FMTIM, FMTLD, and FMTLP muscle bellies lie proximal to the patellae, whereas the GL, FL and GM muscle bellies lie distally.

The knee extensors have major insertions around the patella. The IC originates on the cranial end of the ilium and inserts into the superficial tendofascial sheet as well as the medial side of the tibial head. The origin of the FMTLD is along the entire lateral femoral shaft and it inserts onto the deep tendofascial sheet above the lateral femoral condyle. The FMTLP origin occurs laterally on the trochanteric crest of the femur, and laterally on the proximal femoral shaft (Gangl et al., 2004), and inserts into the deep tendofascial sheet near the proximal patella. The FMTIM arises from the trochanteric crest and proximal three-quarters of the cranial femoral shaft (Gangl et al., 2004), and inserts on the deep tendofascial sheet, near the proximal patella and directly above the medial femoral condyle. A third femorotibial muscle, M. femorotibialis medialis, crosses the knee joint from the medial femoral shaft to the medial surface of the proximal tibia but does not interact with the patellar tissues and thus is not further described here (but see Zinoviev, 2006 for an accurate account and Hutchinson et al., 2014 for some explanation of confusion surrounding these femorotibial muscles’ identities in other literature).

The thin, round tendon of the AMB1, which originates from the pectineal (preacetabular) process of the pubis, runs through the tendofascial sheet and directly behind the distal patella in a distolateral direction, toward its fusion with the tendinous origin of M. flexor perforates digiti III, distal to the fibular head (Gangl et al., 2004). We observed that there were no direct tissue connections between the AMB1 tendon and the patellae. The tendon was free to slip and move independently within the tendofascial sheet, behind the distal patella, unlike in many other (neognath) birds in which the AMB1 tendon perforates or grooves the front of the patella (e.g., Shufeldt, 1884). However, we describe it here as it does run close to the patellae. The second head of M. ambiens, which is unique to ostriches, originates dorsal to the other from the cranioventral iliac rim and inserts on the medial surface of the proximal tibia (Hutchinson et al., 2014). However, it does not come near the patellae and so we do not further describe it.

The lower limb muscles of ostriches also have associations with the patella. The GL originates on the proximolateral side of the distal patella and superficial tendofascial sheet, joining with the GM and GIM into a single gastrocnemius end-tendon distally, and inserting onto the tarsometatarsus after wrapping around the intertarsal joint. The FL attaches to the distolateral side of the distal patella and splits into two tendons of insertion proximal to the intertarsal joint, Tendo lateralis and Tendo caudalis. Tendo lateralis inserts on the tendon of the M. flexor perforates digiti III, distal to the intertarsal joint, and the Tendo caudalis inserts on the lateral tibial condyle (Gangl et al., 2004). The GM takes its origin from the superficial tendofascial sheet and the medial side of the distal patella, and joins the gastrocnemius end-tendon before the intertarsal joint. Other lower limb muscles such as M. tibialis cranialis, M. popliteus and the many digital flexors do not originate near the patellae and are well described in the literature (Gangl et al., 2004; Zinoviev, 2006), so we do not discuss them here.

Functional attachments

To understand the loading across the knee joint of ostriches, identification and description of the tissues which directly interact with the two sesamoid bones is essential (Figs. 2–4). The two sesamoids are embedded in sheets of tendofascial tissue that bond together at the proximal edge of the distal patella. The sheets are the origins and insertions of various leg muscles. The proximal sesamoid constitutes the insertion of the FMTIM tendon proximal-medially and the FMTLP tendon proximal-laterally. Distally, the sheath attaches to the distal sesamoid. The distal sesamoid forms the insertion for the FMTLD tendon proximal-laterally and the IC tendon proximally. The distal sesamoid also is part of the muscle origins of the GL proximal-laterally, the FL distal-laterally, and the GM medially.

Based on our anatomical observations, we hypothesize that all seven of the muscles attached to the patellae would induce a compressive (into the joint) stress on the patellae. The GL, FL, and GM would also induce a tensile force component in the distal direction while the IC, FTIM, FMTLP, and FMTLD would exert a tensile force component in the proximal direction. This could create areas of large compressive and shear loading near the joint as the tissues wrap around the femoral condyles. In addition to the proximal-distal loading, additional mediolateral loads may occur as a result of the tissues wrapping around the distal femur where there is a complex surface between the large lateral condyle and deep sulcus. This variegated surface may induce higher stress concentrations in areas where the surface geometry is most irregular.

Patellar anatomy, connections and evolution

The first two (in 1894) mentions of ostriches having a second patella described it not as a true patella, but as an “ossified ligamentum patellae” (Macalister, 1864; Haughton, 1864). Since then there have been several other descriptions. Thompson (1890) mentioned a small double patella in ostrich while De Vriese (1909) described the patellae as large, consisting of two successive parts which connected to the tibia by a short ligament. Fowler (1991) claimed that ostriches only had a single ossified bone in the tendon which inserted onto the cnemial crest. We found this to be untrue of our adult subjects. In a juvenile ostrich hindlimb we observed joints which were not fully ossified and no patellae were detected, but it is still unclear when in ontogeny each patella ossifies.

In more modern literature, there have been two primary papers providing thorough descriptions of the patellae and related ostrich knee anatomy (Bezuidenhout, 1999; Gangl et al., 2004). Bezuidenhout (1999) describes a primary patella with medial and lateral articular surfaces, and a “second patella” distal to the patella. The “second patella” is described as a long bony column extending from the medial bottom edge of the patella to the tibial crest. This account was also the first to detail muscle attachments to the two patellae. Muscles described in association with the patellae were the M. femorotibialis medius (inserts laterally on the patella), the M. femorotibialis accessorius (inserts proximally on the patella), the M. femorotibialis internus (inserts medially on the patella), and the M. gastrocnemius (one of four heads originates from the patella). We consider the three M. femorotibialis to be what we describe as FMTLP and FMTIM (two muscle bellies, vide Zinoviev, 2006; Hutchinson et al., 2014). Gangl et al. (2004) first described what we consider another very important aspect of the double patellae, which is the tendofascial sheet in which they are embedded, connecting multiple muscles and inserting on the Crista cnemialis cranialis. The authors also detailed additional muscles which surround and attach to this tendofascial sheet. The muscles which Gangl et al. (2004) described as inserting onto the tendofascial sheet are the M. iliotibialis cranialis and the M. femorotibialis accessorius—caput mediale (what we describe as FMTIM). The tendon of the M. ambiens (here AMB1) was described as running medially to the proximal patella and caudally to the distial patella through the tendofascial sheet of the knee within its own channel. The M. fibularis longus and the M. gastrocnemius pars medialis were both described as having their origins on the distal patella.

Additional modern studies have also shed light on the patellae through both osteological (Wagner, 2004) and myological (Zinoviev, 2006; Smith et al., 2006) descriptions. Wagner (2004) added a description of the occurrence and shape of the proximal and distal patella of ostriches at various ages, as well as describing the fascia formed by the ends of multiple tendons which the two patellae are embedded. Zinoviev (2006) described the proximal patella as being embedded within the distal extension of the tendon of the M. femorotibialis medius pars distalis (what we describe as FMTIM), whereas Smith et al. (2006) described the patella to be within the flat tendon of insertion of the M. femorotibialis medius, externus, and accessorius (what we describe as FMTLP, FMTLD, and FMTIM, respectively).

The tibial crest (specifically, the cranial crest or crista cnemialis cranialis; see Regnault, Pitsillides & Hutchinson, 2014 for more discussion) in birds has been termed a traction epiphysis, or a projection from the end of a bone shaft with a separate centre of ossification to which a tendon inserts (Barnett & Lewis, 1958; Parsons, 1904; Vickaryous & Olson, 2007). Traction epiphyses derive, in an evolutionary sense, from sesamoid bones that have fused to the main bone of tendon/ligament insertion. The concurrent existence of a distinct patella and tibial crest does not falsify the hypothesis that the tibial crest is a traction epiphysis in birds, because the patella could be independent from whatever ancestral sesamoid fused with the tibia to form a traction epiphysis (Hutchinson, 2002). However, to our knowledge the ostrich is the only case among birds of a tibial crest and two patellae appearing concurrently (Barnett & Lewis, 1958). The most plausible hypothesis is that the distal patella in ostriches is a neomorphic ossification unique to that lineage, rather than an atavistic or plesiomorphic case of a lack of fusion of the traction epiphysis, because the evolutionary sequence of traits in birds is (1) appearance of a cranial cnemial crest in stem (ornithothoracine) birds (Hutchinson, 2002), (2) evolution of a patellar sesamoid in ornithurine birds (Regnault, Pitsillides & Hutchinson, 2014), and (3) origin of a second (distal) patella in ostriches (this study).

However, some birds have a proximally elongate tibial crest that has been proposed to be a patella fused to the proximal tibia (Shufeldt, 1883; Shufeldt, 1884; Thompson, 1890). The extreme proximity of the distal patella to the tibial crest in ostriches, while autapomorphic, presents an example of an intermediate condition between the ancestral lack of ossification in the distal patellar tendon and the derived state of a proximally extended tibial crest. Such evolutionary trajectories, however, have barely been studied in the lineages in which they may have occurred. Our study shows the need for careful re-examinations, using modern techniques such as 3D imaging, of phylogenetic patterns in the knee joint morphology of birds.