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THE ANATOMICAL RECORD 248:269–278 (1997)

Development of the Human Knee Joint


JUAN A. MÉRIDA-VELASCO,1* INDALECIO SÁNCHEZ-MONTESINOS,1
JOAQUÍN ESPÍN-FERRA,1 JOSÉ F. RODRÍGUEZ-VÁZQUEZ,2
JOSÉ R. MÉRIDA-VELASCO,2 AND JUAN JIMÉNEZ-COLLADO2
1Human and Experimental Embryology Research Group, Department of Morphological

Sciences, University of Granada, E-18071 Granada, Spain


2Department of Morphological Sciences II, University Complutense of Madrid,

Madrid, Spain

ABSTRACT Background: Many studies have been published on the


development of the human knee joint, but different investigators disagree
on its morphogenetic time table. Most discrepancies center on the cavita-
tion of the knee joint and the participation of the superior tibiofibular
joint in the joint knee system.
Methods: We summarize our observations of the development of the knee
joint in 50 serially sectioned human embryonic and fetal lower limbs (26
embryos and 24 fetuses).
Results: The epiphysis of the femur and tibia become condryfied from
O’Rahilly stage 18, and ossification begins during the 13th week of
development. The patella appears as a dense blastema during O’Rahilly
stage 19, becomes condryfied during O’Rahilly stage 22, and begins its
ossification during the 14th week of development. The knee joint cavity
appears during O’Rahilly stage 22, initially as the femoropatellar joint.
This process begins at the periphery of the articular interzone. The
superior tibiofibular joint communicates with the lateral meniscotibial
joint between 10 and 11 weeks of development and becomes separated
from the 13 week on. The menisci arise from the eccentric portions of the
articular interzone during O’Rahilly stage 22; however, until week 9 of
development, they are not easily distinguishable.
Conclusions: We establish the morphogenetic time table of the human
knee joint. Anat. Rec. 248:269–278, 1997. r 1997 Wiley-Liss, Inc.

Key words: articular interzone; superior tibiofibular joint; meniscus; de-


velopment; human

During recent decades, a wealth of information about appears immediately thereafter in the femoromeniscal
the development of bones and joints has been published interzone.
(Bernays, 1878; Hagen-Torn, 1882; Bardeen, 1907; The role of the head of the fibula in the formation of
Walmsley, 1940; Whillis, 1940; Haines, 1947, 1953; the knee joint has been widely debated. The superior
Gray and Gardner, 1950; Gardner and O’Rahilly, 1968; tibiofibular interzone appears during O’Rahilly stage
among others). More attention has been given to the 22 (Gray and Gardner, 1950; Haines, 1952, 1953;
development of the knee joint than to any other joint. Andersen, 1961; Palacios and Rhode, 1980); neverthe-
This intense interest must be seen in the light of the less, McDermott (1943) reported that the superior
size of this joint and of its complexity and clinical tibiofibular interzone is not yet clearly established
importance. The elements that have received the most during weeks 8 and 9. The cavitation of the superior
attention are the cavitation of the knee joint and the tibiofibular joint becomes evident during week 10
role of the head of the fibula in the formation of the knee (Andersen, 1961), in 60-mm specimens (Gray and Gard-
joint system. The first signs of cavitation of the knee ner, 1950), or during week 15 of development (Palacios
joint are seen in peripheral areas (Gray and Gardner, and Rhode, 1980). A clear communication forms be-
1950; O’Rahilly, 1952; Palacios and Rhode, 1980; Cáce- tween the superior tibiofibular and lateral menisco-
res and Caja, 1980) or near the center (Andersen, 1961; tibial articular cavities during weeks 9.5 (Keith, 1933;
Andersen and Bro-Rasmussen, 1961) of the medial Gray and Gardner, 1950) or 10 and 11 of development
layer of the articular interzone; however, Mitrovic
(1978) believed the process to take play simultaneously
in central and peripheral areas. This process is initially *Correspondence to: Juan A. Mérida-Velasco, Departamento de
Ciencias Morfológicas, Facultad de Medicina, Avda. de Madrid 11,
detectable in the femoropatellar interzone (Lucien, E-18071 Granada, España.
1904; Walmsley, 1940; Gray and Gardner, 1950) and Received 23 July 1996; accepted 11 December 1996.

r 1997 WILEY-LISS, INC.


270 J.A. MÉRIDA-VELASCO ET AL.

TABLE 1. Features of the specimens used


Embryos’
C-R length Plane of O’Rahilly Fetuses’ C-R Plane of Weeks of
(mm) section stage length (mm) section development
X-12 15 Transverse 18 CA-1 35 Transverse 9
GG-1 17 Transverse 18 RI-1 38 Transverse 9
BE-1 17 Transverse 19 H-19 39 Transverse 9
BB-5 18 Transverse 19 BB-1 39 Transverse 9
E-19 19 Transverse 20 GV-3 41 Transverse 10
JD-7 19 Transverse 20 AM-1 41 Transverse 10
PT-9 20 Transverse 20 PE-7 41 Transverse 10
JD-2 20 Transverse 20 ZO-1 42 Transverse 10
R-1 21 Transverse 21 SA-1 44 Transverse 10
MA-7 22 Transverse 21 GV-1 45 Transverse 10
X-6 22.5 Transverse 21 MA-3 46 Transverse 10
PE-8 23 Transverse 22 SA-3 48 Transverse 10
HA-2 23 Transverse 22 X-8 50 Sagittal 11
CH-1 24 Transverse 22 MA-2 50 Transverse 11
X-14 24 Transverse 22 MA-1 52 Transverse 11
EA-3 24.5 Sagittal 22 X-11 53 Transverse 11
BB-4 26 Transverse 22 BB-3 53 Transverse 11
GV-4 27 Transverse 22 H-4 62 Transverse 12
HE-1 28 Transverse 23 SA-4 63 Transverse 12
FA-5 28 Transverse 23 PE-3 70.5 Transverse 12
NA-1 29 Transverse 23 JM-1 80 Transverse 13
RI-4 29 Transverse 23 OL-1 83 Transverse 13
X-18 30 Transverse 23 ZO-2 102 Sagittal 14
BB-2 30 Transverse 23 BU 113 Transverse 14
H-23 31 Transverse 23
X-4 31 Transverse 23

(McDermott, 1943; O’Rahilly, 1951; Olivier, 1965). How- sections, which were stained with hematoxylin–eosin
ever, Gray and Gardner (1950), Haines (1953), Andersen (McManus and Mowry, 1968) for light microscopic
(1961), Palacios and Rhode (1980), Cáceres and Caja study.
(1980) found no evidence that the head of the fibula is
involved in the formation of the knee joint during RESULTS
development. These studies are now especially perti- O’Rahilly Stages 18 and 19
nent because of the increasing interest in congenital During O’Rahilly stage 18, chondrification began at
anomalies of the skeleton. The purpose of this study the lower portion of the femur and upper part of the
was to analyze the development and establish the tibia (Fig. 1A). An articular interzone, consisting of a
morphogenetic time table of the knee joint. single band of mesenchymal tissue, formed between
MATERIALS AND METHODS these two areas (Fig. 1A).
At the end of O’Rahilly stage 19, a condensation of
Fifty human embryos and fetuses from the embryo mesenchyme representing the future patella became
collections of the Department of Morphological Sciences visible ventral and cranial to the condyles of the femur
of the universities of Granada and Madrid (Universi- (Fig. 1B).
dad Complutense) were used in the present study.
Crown–rump (C-R) length, plane of section, and stage O’Rahilly Stages 20 and 21
of development (O’Rahilly and Müller, 1987) are shown Chondrification continued at the lower end of the
in Table 1. The usual laboratory procedures were used femur and upper part of the tibia. The femoral condyles
to prepare 10–15-µm-thick transverse or sagittal serial

Abbreviations Fig. 1. A: Human embryo GG-1. The epiphysis of the femur (F) and
tibia (T) begin their condryfication. Between them is the articular
F lower epiphysis of the femur interzone of the knee (1). Note that the interzone consists of an
L cruciate ligaments unlayered dense mesenchyme. B: Human embryo BB-5. The articular
P patella interzone of the knee (1), as an unlayered dense mesenchyme, is
T upper epiphysis of the tibia located between the epiphysis of the femur (F) and tibia (T). Ventrally
= cartilage canal to the femur, the organization of the patella (P) begins as a dense
1 interzone of the knee joint blastema. C: Human embryo MA-7. Condryfication of the epiphysis of
2 interzone of the superior tibiofibular joint the femur (F) and tibia (T) continue, and the first signs of organization
3 menisci of the femoral and tibial condyles are observed. Between these, the
4 articular capsule articular interzone of the knee (1) begins to form as a three-layered
5 condylopatellar ligaments structure. D: Human embryo CH-1. The articular interzone of the
6 femoropatellar joint cavity knee (1) appears as a three-layered structure. Two dense eccentric
7 femoromeniscal joint cavity layers lean against the condyles of the femur (F) and tibia (T) and
8 meniscotibial joint cavity represent the future articular cartilage. Between these layers is a lax
9 superior tibiofibular joint cavity medial layer. Bars 100 µm in A,B, 200 µm in C, 50 µm in D.
Fig. 1.
272 J.A. MÉRIDA-VELASCO ET AL.

and upper surface of the tibia began to be distinguish- The superior tibiofibular joint cavity first appeared,
able (Fig. 1C). and a connection between this cavity and the lateral
The articular interzone of the knee was formed of two meniscotibial cavity was visible (Fig. 4A).
eccentric bands of mesenchymal tissue that covered the Development of the medial meniscus continued and
condyles of the femur and upper surface of the tibia brought about the organization of the internal femoro-
(Fig. 1C) and a medial band that began to appear more meniscal and meniscotibial joints (Fig. 4B). The ante-
lax in comparison with the eccentric layers (Fig. 1C). rior horn of the medial meniscus was attached to the
anterior aspect of the upper surface of the tibia (Fig. 4B).
O’Rahilly Stage 22 The lateral meniscus was clearly evident, and its
formation brought about the organization of the lateral
The eccentric bands of the interzone followed the
femoromeniscal and meniscotibial joints (Fig. 4C).
shape of the femoral and tibial condyles, forming a
dense band of perichondrial connective tissue (Fig. 1D) Weeks 12 and 13
that marked the first sign of organization of the articu-
lar cartilage. At the same time, the medial layer of the The knee joint cavity attained its adult appearance
interzone appeared more lax than the eccentric layers during this time, when the communication between the
(Fig. 1D). The lateral parts of the interzone became lateral meniscotibial and superior tibiofibular cavities
densified and began to form the menisci (Fig. 2A). The disappeared.
joint capsule began to attach peripherally to the me- During week 13, ossification began in the epiphyses
nisci (Fig. 2A & 2B). of the elements comprising the knee joint and first
The medial layer of the interzone appeared lax. became apparent in the lower epiphysis of the femur
Laterally, at the level of the medial layer, small cavities and upper epiphysis of the tibia (Fig. 5A & 5B).
began to appear between the meniscus and the lateral Cartilage canals invaded the perichondrial zone of the
condyles of the femur and tibia. These cavities were condyles and penetrated from superficial to deep areas
crossed by conjunctive tissue septae (Fig. 2B). (Fig. 5A & 5B). In the femur, these canals penetrated
Chondrification of the patella began, as did cavitation preferentially from the margins and deep portion of the
of the femoropatellar interzone (Fig. 2C). intercondylar notch of the femur (Fig. 5A). In the tibia,
On the upper surface of the tibia, the intercondylar they penetrated preferentially from the anterior and
eminence began to form, and immediately dorsal to superior margins (Fig. 5B). The invading vessels came
this, the tibial insertion of the posterior cruciate liga- from the pericapsular arterial network, which in turn
ment appeared (Fig. 2C). was dependent on the genus arteries.
In the superior tibiofibular interzone, no sign of
cavitation was apparent (Fig. 2D). Week 14
Ossification of the patella began, with cartilage ca-
O’Rahilly Stage 23 nals penetrating from the anterior and superior surface
The articular capsule was visible, and densification of (Fig. 5C).
the condylopatellar ligaments was evident (Fig. 3A).
From the lateral margins of the patella, the articular DISCUSSION
capsule surrounded the femoral condyles (Fig. 3A) and The elements that constitute the knee joint begin to
became attached to the eccentric surface of the menisci chondrify during O’Rahilly stage 18 (Gardner and
(Fig. 3B). O’Rahilly, 1968; Cáceres and Caja, 1980; Palacios and
The femoropatellar (Fig. 3A), femoromeniscal, and Rhode, 1980; Clark and Odgen, 1983), when the ap-
meniscotibial joint cavities (Fig. 3A & 3B) were distin- posed ends of the femur and tibia are covered with a
guishable. The interzone of the superior tibiofibular dense layer of perichondrium. However, Andersen (1961)
joint was visible but showed no signs of cavitation (Fig. noted that in 20-mm embryos, ‘‘the distal end of the
3C). femur as well as the proximal end of the tibia and fibula
still persist as a dense blastemal precartilage.’’ McDer-
Week 9 mott (1943) reported that chondrification of the femur
Development of the menisci proceeded, giving rise to and the tibia began on days 47–51 of development, and
the femoromeniscal and meniscotibial joint cavities O’Rahilly (1952) first observed chondrification during
(Fig. 3D & 3E), in which a few tracts of connective stage 27. O’Rahilly et al. (1956) reported chondrifica-
tissue were still visible. tion of the femur and tibia in a few O’Rahilly stage-17
The patella lay opposite of, and was articulated embryos, whereas Haines (1953) found that this pro-
mainly with, the lateral condyle. The triangular space cess was first evident in the knees of 13-mm embryos.
with an anterior base that formed below the patella was The patella first becomes visible at the end of
occupied by mesenchymal tissue, which may represent O’Rahilly stage 19 (Bardeen, 1907; Gardner and
the first sign of formation of the fat pad (Fig. 3D). O’Rahilly, 1968). Some investigators have reported that
Peripherally, the menisci were attached by the coro- it makes its first appearance later, when the embryo
nary ligaments to the capsule (Fig. 3E). has reached 20 mm (Walmsley, 1940; Haines, 1947), 23
mm (Andersen, 1961), 24.5 mm (Caja and Cáceres
1980), 42 mm (Eberl-Rothe and Sonnenschein, 1950), or
Weeks 10 and 11 7.5 weeks of development (Gray and Gardner, 1950).
The degree of development of the knee joint at this According to Gardner and O’Rahilly (1968), the patella
time was similar to that seen during week 9, with slight begins to undergo chondrification during O’Rahilly
modifications. stage 22, although they also noted that in four of the
HUMAN KNEE JOINT 273

Fig. 2. A: Human embryo PE-8. The lateral portions of the articular eccentric margin of the menisci. C: Human embryo PE-8. condryfica-
interzone of the knee form the menisci (3) that are located between the tion of the patella (P) and the organization of the femoropatellar cavity
condyles of the femur (F) and tibia (T). The knee joint capsule (4) is (6) have begun. The posterior cruciate ligament (L) is observed in the
attached to the eccentric margin of the menisci. B: Human embryo medial layer of the knee joint interzone (1). D: Human embryo EA-3.
PE-8. Formation of the meniscofemoral (7) and meniscotibial (8) knee The articular interzone of the superior tibiofibular joint (2) is ob-
joint cavities has begun. Both cavities are crossed, at this time, by served. At this time, no sign of cavitation is evident. Bars 200 µm in
mesenchymal trabeculae. Knee joint capsule (4) is attached to the A,C,D, 100 µm in B.
274 J.A. MÉRIDA-VELASCO ET AL.

Fig. 3.
HUMAN KNEE JOINT 275
specimens they examined, signs of chondrification were in central and peripheral areas, although this author
evident during O’Rahilly stage 21. Walmsley (1940) noted that cavitation was more advanced at the periph-
reported the earliest signs of chondrification in 30-mm ery.
embryos, whereas McDermott (1943) distinguished this The role of the head of the fibula in the formation of
phenomenon during fetal development at 9 and 10 the knee joint has been widely debated. In our material,
weeks. we observed the appearance of a superior tibiofibular
The epiphysis of the femur and tibia begin to ossify interzone during O’Rahilly stage 22 (Gray and Gardner,
during week 13, and in the patella, ossification begins 1950; Haines, 1952, 1953; Andersen, 1961; Palacios and
during week 14. However, Gray and Gardner (1950) Rhode, 1980). Nevertheless, McDermott (1943) re-
and Palacios and Rhode (1980) found signs of the ported that the superior tibiofibular interzone was not
formation of cartilage canals in the knee in 12-week-old yet clearly established in weeks 8 and 9. We also found
fetuses. The vessels penetrated from superficial to deep that cavitation of the superior tibiofibular joint became
levels after invading the perichondrial zone of the evident during week 10 (Andersen, 1961) and not in
condyle. In the lower epiphysis of the femur, vessels 60-mm specimens (Gray and Gardner, 1950) or during
invaded from the margins and the deep portion of the week 15 of development (Palacios and Rhode, 1980). A
intercondylar notch, and in the upper epiphysis of the clear communication forms between the superior tibio-
tibia, invasion proceeded from its anterior and superior fibular and lateral meniscotibial joint cavities during
part surfaces (Palacios and Rhode, 1980). In the pa- weeks 10 and 11 (McDermott, 1943; O’Rahilly, 1951;
tella, vessels penetrated from the superior and anterior Olivier, 1965). This space was also seen by Keith (1933)
margins (Kreutz and Kreutz, 1981; Doskocil, 1985) and and Gray and Gardner (1950) in a 9.5-week fetus.
not from the inferomedial margin of the kneecap, as However, Gray and Gardner (1950), Haines (1953),
noted by Palacios and Rhode (1980). Andersen (1961), Palacios and Rhode (1980), and Cáce-
Formation of the capsule of the knee joint begins res and Caja (1980) found no evidence that the head of
during O’Rahilly stage 22. According to Archer et al. the fibula was involved in the formation of the knee
(1994), hyaluronan appears to play a central role in this joint during development, and Gray and Gardner (1950)
process. However, in one of the O’Rahilly stage-23 reported that in most cases the knee joint cavity was
embryos studied by Gardner and O’Rahilly (1968), separated from the superior tibiofibular joint cavity by
there was no evidence of the joint capsule in the knee; either a small amount of very loose tissue or very thin
and in another stage-23 embryo, one of the knees strands of somewhat denser tissue. O’Rahilly (1951)
showed signs of incipient cavitation near the femur and described a femorofibular interzone in embryos of 16–20
patella. In material studied by Bardeen (1907), Gray mm, although in our material no such interzone was
and Gardner (1950), and O’Rahilly and Gardner (1975), visible.
cavitation began during O’Rahilly stage 23; however, Discrepancies also exist with regard to the final
Walmsley (1940), Haines (1947), Moll (1948), and Pala- organization of joint cavity, considered to arise from the
cios and Rhode (1980) first observed this process at 9 confluence of five initially separate cavities: the femoro-
weeks of development, and Dubinkin and Motnenko patellar, two femoromeniscal, and two meniscotibial
(1931) noted this process in 11.8-cm fetuses. cavities (McDermott, 1943; Gray and Gardner, 1950;
The first signs of cavitation of the knee joint are seen Palacios and Rhode, 1980). However, one investigator
in peripheral areas of the medial layer of the articular considered only three cavities to be involved, i.e., the
interzone (Gray and Gardner, 1950; O’Rahilly, 1952; femoropatellar and two femorotibial cavities (Andersen,
Cáceres and Caja, 1980; Palacios and Rhode, 1980). 1961), and another investigator (Doskocil, 1985) re-
This process is initially detectable in the femoropatellar ported that only two symmetrical cavities initially
interzone (Lucien, 1904; Walmsley, 1940; Gray and separated by a medial mediastinum were involved. Our
Gardner, 1950) and appears immediately thereafter in observations show that initially a femoropatellar cavity
the femoromeniscal interzone. However, Andersen and and two femoromeniscal cavities exist and that subse-
Bro-Rasmussen (1961) and Andersen (1961) reported quently two meniscotibial cavities are formed. Nonethe-
that cavitation began near the center of the interzone less, a sixth space, the superior tibiofibular cavity, is in
and spread toward the periphery, whereas (Mitrovic, communication with the meniscotibial cavity during
1978) believed the process to take play simultaneously weeks 10 and 11 of development and thus forms part, at
least temporarily, of the developing knee joint cavity.
The formation of a single cavity, with the disappearance
Fig. 3. A: Human embryo X-4. The femoropatellar (6) and menisco- of communication with the superior tibiofibular cavity,
femoral (7) cavities are observed. The knee joint capsule (4), attached takes place during weeks 12 and 13 of development
to the eccentric margin of the menisci (3), is strengtened by the according to Palacios and Rhode (1980) and during the
condylopatellar ligaments (5). B: Human embryo NA-1. The menisco-
femoral (7) and meniscotibial (8) cavities are clearly distinguishable. eighth week according to Keith (1933).
In the middle of the knee joint, organization of the cruciate ligaments Organization of the menisci begins during O’Rahilly
(L) continues. Knee joint capsule (4). C: Human embryo HE-1. At the stage 22 (Haines, 1947; Andersen, 1961; Gardner and
level of the superior tibiofibular joint (2), a three-layered interzone is O’Rahilly, 1968; Cáceres and Caja, 1980; Clark and
present; hence, no sign of articular cavitation is evident. D: Human
fetus RI-1. The patella (P) is basically articulated with the lateral Odgen, 1983), although Gardner and O’Rahilly (1968)
condyle of the femur (F). Below the patella, a triangular space forms. observed the lateral meniscus in one of the nine
This space is occupied by a mesenchymal tissue that gives rise to the O’Rahilly stage-20 specimens they studied. The menisci
intraarticular pad of fat. Lateral meniscus (3). E: Human fetus RI-1. cannot be distinguished clearly until week 9 (Gray and
Enlargement of D. Observe the knee joint capsule (4) attached to the
eccentric margin of the menisci (3), which organize the coronary Gardner, 1950; Palacios and Rhode, 1980); however,
ligament. The femoromeniscal (7) and meniscotibial (8) cavities are some investigators have reported that they form at
clearly distinguishable. Bars 200 µm in A–D, 100 µm in E. later stages, i.e., week 8 (Palacios and Rhode (1980),
276 J.A. MÉRIDA-VELASCO ET AL.

Fig. 4. A: Human fetus GV-1. The superior tibiofibular


joint cavity (9) shows its communication with the lateral
meniscotibial joint cavity (8). Lateral meniscus (3).
Posterior cruciate ligament (L). B: Human fetus GV-1.
The medial meniscus (3) is completely formed, and the
medial meniscofemoral (7) and meniscotibial (8) joint
cavities are established. The anterior horn of the medial
meniscus is attached to the anterior aspect of the upper
surface of the tibia. Anterior cruciate ligament (L). C:
Human fetus BB-3. The lateral meniscus (3) is com-
pletely organized, and the lateral meniscofemoral (7)
and meniscotibial (8) joint cavities are established.
Observe the communication between the superior tibio-
fibular (9) and the lateral meniscotibial (8) joint cavities.
Bars 5 200 µm.
HUMAN KNEE JOINT 277

Fig. 5. A: Human fetus OL-1. Cartilage canal (arrow)


penetrates the lower end of the femur at the level of its
posterior surface. B: Human fetus OL-1. Cartilage ca-
nals (arrow) penetrate the upper end of the tibia.
Ossification begins on the superior and anterior surfaces
of the tibia. The anterior horn of the lateral meniscus (3)
is also distinguishable. C: Human fetus ZO-2. Cartilage
canals (arrow) penetrate the superior and anterior sur-
face of the patella (P). Bars 100 µm in A,B, 200 µm in C.
278 J.A. MÉRIDA-VELASCO ET AL.

weeks 9 and 10 (McDermott, 1943), or even as late as in Eberl-Rothe, G., and A. Sonnenschein 1950 Die ontogenetische Ausbil-
dung des Kniegelenkes beim Menschen. Zschr. Anat. Entwgsch.,
the 3.5-month fetus (Dubinkin and Motnenko, 1931). 115:251–272.
The joint capsule is attached to the anterior margin Gardner, E., and R. O’Rahilly 1968 The early development of the knee
of the external meniscus during O’Rahilly stage 22 and joint in staged human embryos. J. Anat., 102:289–299.
to the eccentric surface of both menisci during O’Rahilly Gray, D.J., and E. Gardner 1950 Prenatal development of the human
knee and superior tibiofibular joints. Am. J. Anat., 86:235–287.
stage 23. According to McDermott (1943) and Gray and Hagen-Torn, O. 1882 Entwickelung und Bau der Synovialmembranen.
Gardner (1950), this final attachment does not take Arch. Mikr. Anat., 21:591–663.
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upper surface of the tibia. Haines, R.W. 1953 The early development of the femoro-tibial and
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