The development of synovial plicae in human knee joints: An embryologic study

The development of synovial plicae in human knee joints: An embryologic study

Arthroscopy: The Journal of Arthroscopic and Related Surgery Published by Raven Press, Ltd. 0 1990 Arthroscopy 6(4):315-321 Association of North...

5MB Sizes 14 Downloads 18 Views

Arthroscopy:

The Journal

of Arthroscopic

and Related Surgery

Published by Raven Press, Ltd. 0 1990 Arthroscopy

6(4):315-321

Association of North America

The Development of Synovial Plicae in Human Knee Joints: An Embryologic Study Satoshi Ogata, M.D., and *Hans K. Uhthoff, M.D., F.R.C.S.(C)

Summary: An embryologic study about the development of the human knee joint cavity was carried out with special attention to the formation of synovial plicae, using a total of 116 knees of embryos and fetuses. The incidence of synovial plicae in the fetal stage was also investigated. Formation of joint space starts at the middle of the interzone at around 8 weeks of gestation. Multiple small cavitations around the femoral condyle and patella coalesce to form larger cavitations. At around 1OY;weeks, the knee joint consists of a single cavity with synovial lining. At certain sites, such as at the medial part of patello-femoral and the infrapatellar regions, mesenchymal tissue strands remain. They may become plica. In the fetal stage from 11 to 20 weeks, an infrapatellar plica was found in 50% of specimens, a suprapatellar plica in 33%, and a mediopatellar plica in 37%. Only the infrapatellar plica showed a decrease in incidence. Key Words: Knee-Synovial plica-Embryology.

reported that the incidence of suprapatellar plica amounts to 78%. The development of the knee joint has been the subject of many investigations (6-8). Although there is no consensus about the way the joint cavity forms, it has been widely believed that the knee joint is originally composed of three compartments: medial and lateral synovial compartments and suprapatellar bursa. Synovial plicae are regarded as remnants of the divisions between these compartments that were present in the knee during embryologic development (5). Although that theory may explain the way of formation of the suprapatellar and infrapatellar plicae, that of the mediopatellar plica remains uncertain. This embryologic study had two goals: to elucidate the process of formation of the joint cavity with special reference to the formation of synovial plicae in the knee, and to determine the incidence of synovial plica during the fetal stage.

The synovial fold, or plica, of the knee may be a cause of knee symptoms. There are three predominant plicae in the knee: infrapatellar plica (ligamen-

turn mucosum), suprapatellar plica, and mediopatellar plica (shelf). The clinical significance of the infrapatellar plica and suprapatellar plica is said to be minimal. On the other hand, recent arthroscopic reports indicate that the mediopatellar plica may give rise to symptoms. Although a lateral patellar plica has been described, it is believed to be exceedingly rare (1). Mayeda (2) reported that 21% of knees have supra-, infra-, or mediopatellar plicae. Iino (3) studied 67 adult cadaver knees and reported that more than half of specimens had a mediopatellar plica, and an obvious mediopatellar plica was seen in nine instances. Sakakibara (4) reported that 45% of knees have a mediopatellar plica. Pipkin (5) From the Department of Orthopaedic Surgery, Cbiba University, Cbiba-city, Cbiba, Japan; and the *Division of Orthopaedic Surgery, University of Ottawa, and the Ottawa General Hospital, Ottawa, Ontario, Canada. Address correspondence and reprint requests to Dr. Hans K.

MATERIALS AND METHODS

Uhthoff at Division of Orthopaedic Surgery, 501 Smyth Road, Ottawa, Ontario, KlH 8L6 Canada. This study was done in the Bone and Joint Research Laboratory at the University of Ottawa.

One hundred and sixteen knees from 112 embryos and fetuses ranging in crown-rump (C-R) 315

S. OGATA AND H. K. UHTHOFF

316

length from 14 to 195 mm (age of gestation from 6 to 20 weeks) form the basis of this study. After fixation in 10% neutral formalin, all specimens were decalcified in ethylenediaminetetraacetic acid (EDTA) and embedded in paraffin. Serial or nonserial sections were made according to the size of the specimen. Sixty specimens were cut in sagittal, 54 were in frontal, and 2 were cut in a transverse plane. The sections were stained with Goldner’s trichrome, haematoxylin-phloxine-saffron (HPS), or azan. The distribution according to Streeter’s staging or as to age was as follows. Stage 17 (n = I), stage 21 (n = l), stage 22 (n = 2), stage 23 (n = 4), 8 weeks (n = 3), 8% weeks (n = 7), 9 weeks (n = 4), 9ti weeks (n = 7), 10 weeks (n = lo), lOi/2 weeks (n = 5), 11 weeks (n = 6), 12 weeks (n = 5), 13 weeks (n = 13), 14 weeks (n = 7), 15 weeks (n = 4), 16 weeks (n = 9), 17 weeks (n = 7), 18 weeks (n = 4), 19 weeks (n = lo), 20 weeks (n = 7). A possible decrease in incidence with age in supra- , medio- , and infrapatellar plicae were analyzed using Spareman’s ranking correlation coefficient. RESULTS Six weeks (stage 17) Femur and tibia were already chondrified. However, the interzone between the femur and the tibia was homogeneous. No intraarticular structures could be identified. Stage 21 A chondrifying patella was found. The interzone between cartilaginous anlages developed into three

ET AL.

layers, but no cruciate identified.

ligament or meniscus

was

Stage 23 The shapes of skeletal elements were already similar to those in adults. Mesenchymal condensations for menisci and cruciate ligaments could be identified. One specimen showed no sign of formation of joint cavitation. Loosely arranged tissue under the quadriceps tendon was found in two specimens. Another specimen showed a cavitation between the patella and the femur that already extended between the quadriceps tendon and the femur. Eight weeks Two specimens had small cavitations at the periphery of the patello-femoral region near the proximal and distal end of the patella. In this specimen, no cavitation was seen between the patella and the femur. The other one showed a space like a slit at this level. All three specimens showed cavitation at the periphery of the femoro-meniscal region. Although the mesenchymal tissue was loose at the menisco-tibia1 region, no obvious cavitation was seen in any specimen. Eight and a half weeks One transversely cut specimen showed an early stage of cavitation at the medial part of the patellofemoral region. Cavitation appeared at the middle part of the patello-femoral interval (Fig. 1). The patella appeared to be shifted laterally, so that the

FIG. 1. Frontal section of an W&week-old fetus. Small cavitations (s) at the medial part of the patello-femoral interval can be seen. r, Medial patellar retinaculum. HPS, x29.

Arthroscopy,

Vol. 6, No. 4, 1990

DEVELOPMENT

OF SYNOVIAL

PLICAE IN THE KNEE

317

FIG. 2. Sagittal section of an W-week-old fetus. Cavitations can be seen under the quadriceps tendon, the proximal and the distal parts of the patello-femoral region. A mesenchymal band (b) separates the two cavitations near the proximal pole of the patella. HPS, x29.

medial patello-femoral interval was wider than that of the lateral one. In three sagittally cut specimens, peripheral cavitation at the patello-femoral region was found. In these specimens, mesenchymal tissue separating two cavitations was seen between the proximal end of the patella and the anterior part of the femur. This appeared to represent an early stage of a suprapatellar plica (Fig. 2). At the femoro-

meniscal region, two specimens showed loosely arranged mesenchymal tissue. Peripheral cavitations were found in four specimens. One specimen showed a space like a slit. At the menisco-tibia1 region, five specimens showed no sign of cavitation. Peripheral cavitations were seen in only two specimens. The intercondylar area was still fully occupied by mesenchymal tissue.

FIG. 3. Frontal section of a 9Yz-week-old fetus at the proximal part of the patello-femoral region showing a slit-like cavitation. Mesenchymal tissue (t) is rich at the medial side of the region, whereas the cavitation (c) is located more at the lateral side. Anterior part of the medial femoral condyle is covered by mesenchymal tissue. Villi can be seen at the medial side of the cavitation. HPS, x29.

Arthroscopy,

Vol. 6, No. 4, 1990

318

S. OGATA AND H. K. UHTHOFF ET AL.

FIG. 4. Sagittal section of a lo-week-old fetus showing a mesenchymal band (b) running between the patella and the medial femoral condyle. Goldner, x29.

Nine weeks Two specimens showed peripheral cavitations at the patello-femoral region. Two other specimens showed a slit like space between patella and femur. In one specimen, there was a cavitation posterior to the anterior cruciate ligament in the intercondylar notch, but it was not continuous with the cavitation in the patello-femoral region. A mesenchymal band connecting the proximal end of the patella and the anterior surface of the femur was found in two specimens, Another specimen showed a synovial band between the patella and the lateral femoral condyle. All specimens showed peripheral cavitation at the femoro-men&al and the menisco-tibia1 region. 9 and a half weeks At the patello-femoral region, peripheral cavitation was found in two specimens. A slit-like cavitation was seen in five specimens. In a frontal section, a cavitation between patella and femur was mainly found in the lateral part of the patello-femoral region; the medial part was still filled by mesenchyma1 tissue (Fig. 3). At the femoro-meniscal region, peripheral cavitation was found in two specimens and a slit-like cavitation was seen in five specimens. At the menisco-tibial region, one specimen showed loosely arranged mesenchymal tissue. Two specimens showed peripheral cavitation and four showed a slit-like cavitation. In one specimen whose caviArthroscopy,

Vol. 6. No. 4, 1990

tation near the distal end of the patello-femoral region extended distally, synovial mesenchyme in front of the anterior cruciate ligament appeared to form a band between the anteroinferior part of the femoral condyle and the infrapatellar region. Ten weeks Two specimens showed multiple independent small cavitations, including the menisco-tibia1 space. Another specimen showed a single cavity. The remaining specimens showed an intermediate developmental stage of joint formation. A mesenchymal suprapatellar band was found in one knee, a mediopatellar band in another (Fig. 4), and two showed an infrapatellar band. The bands at all three sites could constitute a forerunner of a plica. 10 and a half weeks Since from this moment on the knee joint seemed to consist of a single cavity with synovial lining, we TABLE

1. Numbers of specimens

suprapatellar, Weeks: No. of specimens: SupraMedialInfra-

that showed mediopatellar, or infrapatellar plicae, by week of gestation 11 6

12 5

3 4 4

1 0 3

13 13

14 7

15 4

16 9

17 7

18 4

52264011 3 1 1 a 4 1

4 6

2 6

3 1

19 20 10 7 6 2

3 1

DEVELOPMENT

OF SYNOVIAL

considered mesenchymal tissues at the suprapatellar, mediopatellar, and infrapatellar region as plicae. A suprapatellar plica was seen in one knee and a mediopatellar plica was found in another knee. An infrapatellar plica was found in two knees. After this stage of development, changes were mainly found in terms of the extent of the joint cavity. However, there were two exceptions seen in an 1lweek-old specimen that showed no cavitation between menisci and tibia1 articular surface. The incidence of the suprapatellar, mediopatellar, or infrapatellar plicae can be seen in Table 1. From 11 to 20 weeks of age, a suprapatellar plica (Fig. 5) was found in 33.3% of specimens, a mediopatellar plica (Fig. 6) was seen in 36.8%, and an infrapatellar plica (Fig. 7) was seen in 50%. Progressive decrease in incidence between 11 and 20 weeks was shown only for the infrapatellar region (p < 0.05). DISCUSSION McDermott (6) believed that the formation of the joint cavity starts at 8-9 weeks in the form of four compartments, two femoromeniscal and two meniscotibial. Gray and Gardner (7) found the early joint space

319

PLICAE IN THE KNEE

at the femoro-patellar and the femoro-meniscal regions. Also, Gardner (9) described small cavitations that appeared in the interzone, then gradually coalesced to form a large cavity. Anderson (8) believed that the joint cavity developed as three separate cavities: one femoro-patellar and two femoro-tibia1 at 8 weeks. Then at 9r/2 weeks, the three cavities became confluent. Synovial plicae in the knee joint are considered a remaining portion of the synovial septum from the fetal stage (5). Sakakibara (4) showed a knee joint of a cadaver horse having synovial septa between the patello-femoral joint and the medial and lateral femoro-tibia1 joints. Our observation confirmed the results of Gray and Gardner (7) and of Gardner (9) that the formation of joint space started as multiple small cavitations at the middle of interzone around 8 weeks. These small cavitations appeared at the patellofemoral and femoro-meniscal regions. Approximately 1 week later, cavitation started at the menisco-tibia1 region. At first, small cavitations appeared at the peripheral part of each region, then a slit-like cavitation between the articular surfaces appeared. After the coalescence of small cavitations, a small amount of mesenchymal tissue sepa-

FIG. 5. Sagittal section of a 17-week-old fetus showing a suprapatellar plica (s). Goldner, x8.

Arthroscopy,

Vol. 6, No. 4, 1990

320

S. OGATA AND H. K. UHTHOFF ET AL.

FIG. 6. Sag&al section of a 17-week-old fetus showing a mediopatellar plica (M). Goldner, ~5%.

Arthroscopy

DEVELOPMENT

OF SYNOVIAL

rating cavitations sometimes remained unresolved, especially in three regions: supra-, infra-, and mediopatellar regions. In the frontal section, the relation between patella and femur could be well observed. The shape of the patella already resembled that of a mature one; it showed an asymmetry in cross-sections. The patella and femur articulated mostly at the lateral side of the articular facets. The interval between the patella and the femur was wide at the medial side and was narrow at the lateral side. Thus, the amount of mesenchymal tissue was larger at the medial side of the patello-femoral region. We found only one lateral patellar plica in a 9-week specimen. After 10 weeks, no lateral patellar plica was found. Also, the amount of mesenchymal tissue was bigger medially at the proximal end of the patella because of the lateral shift of the quadriceps tendon and suprapatellar bursa. The intercondylar fossa was also rich in mesenchymal tissue. The suprapatellar plica can be explained as a septum between the suprapatellar bursa and the patello-femoral cavitation. The infrapatellar plica may be also considered as a septum of the medial and lateral femoro-tibia1 cavitations. On the other hand, we believe that the mediopatellar plica is not a remnant of a septum of a distinct compartment during the developmental stage, but constitutes a remnant of mesenchymal tissue due to developmental circumstances. Our results in regard to the incidence confirmed that the infrapatellar plica is the most frequent one. There was a progressive decrease in its incidence

321

PLICAE IN THE KNEE

from 11 to 20 weeks of gestation, indicating that the development of the joint cavity is still ongoing at the intercondylar notch. The incidence of the suprapatellar (33.3%) and the mediopatellar plica (36.8%) was similar to that of Iino (35%). There was no progressive decrease in incidence of these plicae. Therefore, it seems that the supra- and the mediopatellar plicae are not likely to disappear once they are formed. Acknowledgment: We thank Mrs. Brigitte Eiselt for her technical assistance. REFERENCES 1. Sisk TD. Arthroscopy of the knee and ankle. In: Crenshaw AH, ed. Campbell’s operative orrhopaedics. 7th ed. St. Louis: C.V. Mosby Company, 1987:2547-2608. 2. Mayeda T. Uber das strangartige Gebilde in der Kniegelenkhohle (chorda cavi articularis genu). Mitt Med Fak Kaiser Univ Tokyo 1918;21:507-53. 3. Iino S. Normal arthroscopic findings in the knee joint in adult cadavers. J Jpn Orthop Assoc 1939;14:467-523. 4. Sakakibara J. Arthroscopic study on Iino’s band-plica synovialis mediopatellaris. J Jpn Orthop Assoc 1976;50: 513-22. 5. Pipkin G. Knee Injuries: the role of the suprapatellar plica and suprapatellar bursa in simulating internal derangements. C/in Orthop 1971;74:161-76. 6. McDermott LJ. Development of the human knee joint. Arch Surg 1943;46:705-19. 7. Gray DJ, Gardner E. Prenatal development of the human knee and superior tibiofibular joints. Am J Anar 1950;86: 235-87. a. Andersen H. Histochemical studies on the histogenesis of the knee joint and superior tibiotibular joints. Am J Anar 1950;86:235-87. 9. Gardner E. The anatomy of the joints. Number 1. Development of joints. In: The American Academy of Orthopaedic Surgeons instructional course lectures, Vol. IX. Ann Arbor: JE Edwards, 1952:14%155.

Arthroscopy, Vol. 6, No. 4, 1990