The ossification centre of the talus

ANNALS Of ANATOMY = = = = = = = = =

The ossification centre of the talus Helga Fritsch, Oliver Schmitt and Reinhard Eggers lnstitut flir Anaromie del !Vledizinischen Universitiit zu LUbeck, Ratzeburger Allee 150, D-23538 LUbeck, Germany ------ -- - - - - - - - - - - - - - - - - -

Summary. The ossification of the talus was studied in plastinated and histological preparations of normal feet of eight newborn children. Quantitative data on the newborn talus were obtained with the IBAS image analysis system and by point counting methods. In the newborn talus up to 24 percent ot the talar anlage already consists of bony tissue. The ossification centre is situated in the neck, which includes the non-articulating surfaces of the talus. Periosteal bone joins lhe endochondral centre below and, in well-differentiated specimens also above. The basal periosteal collar forms the surfaces of the sinus and canalis tarsi, whereas the cranial bony collar is included in the tibiotalar joint. The histological architecture of these periosteal collars differs. Four arteries contribute to the blood supply of the talar ossification centre Key words: Human development - Short bone tion - Topography - Vascularization

Ossifica-

Introduction The cartilage of the talus is the first of the tarsals to show vascular invasion in early fetal life, but its ossification does not start before late fetal life (Gardner et al. 1959). Knowledge about the regular ossification of the talus is very limited, but such knowledge is necessary for the diagnosis (Howard and Benson 1992) and understanding of malformations of the talus, especially in cases of clubfoot. A number of details regarding the topography. histology and vascularization of the talar ossification centre therefore require further clarification. It is not clear exactly where the talar ossification first occurs, or just where the talar ossification is situated within the cartilaginous anlage at birth and what the relationship of the ossification centre to extraosseous structures is. Furthermore, quantitative data on the talal ossification centre Correspondence to: H. Fritsch

~I

Ann Anat (1996) 178: 455

-4~9

Gustav Fischer Verlag .lena

at birth do not exist. Therefore, the topology of the ossification has been studied in histological preparations of the newborn foot. The vascularization of the talus has been comprehensively studied in the adult (Wildenauer 1950; Muifinger and Trueta 1970; Gelberman and Mortensen 1983) where the major blood supply originates from the artery of the sinus tarsi and from the artery of the tarsal canal. The vascularization of the talar ossification centre has only been described in a comparative study of a normal and a clubfoot talus in a nine-day old boy (Shapiro and Glimcher 1979). In this study, it was pointed out that the major blood supply of the ossification centre entered from the dorsocranial surface of the talar neck. These results need to be confirmed with respect to the normal vascularization pattern of the developing talus. The ossification of short or irregular bones such as the talus mainly proceeds as endochondral ossification. Sometimes small additional regions of periosteal bone have also been described in short bones (Tondury and Theiler 1990). With respect to the normal talus, regions of periosteal bone have only been mentioned by some authors (Hasselwander 1903; Gardner et al. 1959), but the existence of cortical bone has been pointed out for the clubfoot talus (Shapiro and Glimcher 1979). Recently periosteal bone formation and two grooves of Ranvier (1873) have been shown for the developing human talus in a histological-radiological investigation (Cheng et al. 1995). In commonly used textbooks of anatomy (Williams 1995: Gray's Anatomy) and foot anatomy (Sarrafian 1993), the endochondral ossification is the only kind of bone development described for the talus. The purpose of the following study was therefore to re-examine the status of bone formation in the newborn talus.

Material and methods The ossification centre of the talus was studied in the feet of eight newborn or stillborn babies. Six of them were full term infants, two were between 34 and 35 weeks old. They showed no signs of

periosteal bone situated below, i. e. at the infero-Iateral surface of the talar neck (Fig. 3). In all newborn specimens studied the superior surface of the basal periosteal collar was joined with the endochondral bone. Medially and laterally the borders between endochondral and periosteal bone are clearly demarcated and the periosteal bone overlaps the endochondral centre. The surface of the basal periosteal bone is regular and smooth and covered by a periosteum. In some places it is invaded by large vessels that derive from the artery of the sinus tarsi and ascend and branch within the endochondral ossification centre (Fig. 7). In the neighbourhood of the periosteal bone the ligaments of the sinus tarsi insert into the thick perichondrium (Fig. 3 and Fig. 7) of the fetal cartilage. When the ossification centre also reaches the superior surface of the talar neck (Fig. 2), an additional area of adjoining periosteal bone is found cranially (Fig. 4). The layers covering this periosteal bone differ from that in the region of the basal periosteal collar. At the outside the cranial bony collar is covered by the synovial membrane of the tibiotalar capsule by a thick periosteum and by a layer of fibrocartilage-like tissue (Fig. 4) that irregularly merges with the periosteal bone. The cranial bony collar of the talus corresponds to the segment of the talar neck that is located within the tibiotalar joint. The fibrous capsule of the tibiotalar joint and the talonavicular ligament are inserted distal to the periosteal bone.

maceration or foot deformities. The newborn feet were fixed by immersion and stored in 4070 formaldehyde solution for at least three months. Plastination histology: Six entire feet were taken for plastination histology (v. Hagens et al. 1987). They were dehydrated with acetone, defatted with methylenechloride and then impregnated with the epoxy resin BIODUR E 12 (Fritsch 1988). After polymerization the epoxy blocks were sectioned with a diamondwire saw (Well®) either in the transverse, coronal or sagittal planes. The thickness of the sections ranged between 300 - 500 ~m. After mounting and polishing, the sections were stained with azure III methylene blue and counterstained with basic fuchSin. The stained sections were examined and photographed with a macroscope (Wild, Heerbrugg) at magnifications of 4 80 , Histology: The tali of two newborn feet were processed in accordance with the normal paraffin technique. They were decalcified in EDTA. The 10 ~m thick coronal sections werc alternatively stained with hematoxylin-eosin and azan. Quantification: In the five plastinated series from the full term infants, three-dimensional reconstructions of the talus, the calcaneus and their ossification centres wcre made with the IBAS 25 image analysis system (Kontron, Germany). Determination of surfaces and volumes was obtained With the help of this system. In addition, the volumes of the talm ,ind Its ossification centre were determined by using point counting methods (Cavalieri principle, Gundersen and Jensen 1987).

Results Vascularization

Topography, shape and size of the talar ossification centre The ossification centre of the talus is detectable in all specimens. In the two younger specimens it is situated in the central part of the neck and does not touch any surface of the talar anlage. In the six full term infants, the talar ossification centre nearly fills out the entire region of the neck (Fig. 1 and Fig. 2). It extends 10 the antero-medial region of the talar body and borders the posterior and central regions of the talar head (Fig. 5 - Fig. 7) . In these specimens the ossification centre has developed as far as the inferior and the infero-lateral surfaces of the talar neck (Fig. 1, Fig. 2 and Fig. 7), i. e. to the root' of the sinus tarsi. In two of these specimens the ossification centre is rather large and has already extended to the superior surface of the talar neck (Fig. 2). The entire talar neck is covered by a thick perichondrium or periosteum into which ligaments and joint capsules are inserted. As shown in figure 5, the volumes of the talar anlagen range between 1199 mm 3 and 1345 mm' and the volumes of their ossification centres range between 161 mm] and 316mm3 • Thus in full term newborn children II 24 percent of the talar anlage consists of bone. The volumes of the talar perichondrium range between 60 mm and 78.8 mm'.

The blood supply of the talar ossification centre arises from several arteries entering the talus from all directions. The sides of vascularization are indepent of the size and differentiation of the ossification centre. Branches of the deltoid vessels deriving from the posterior tibial atery enter the talus dorso-medially (Fig. 5). These vessels derive from the posterior tibial artery and reach that part of the ossification centre that extends to the anteror-medial region of the talar body. The artery of the tarsal canal (Fig. 1) enters the basal part of the ossification centre and branches within its infero-medial part. At the roof of the sinus tarsi its artery invades the small periosteal bony collar (Fig. 7). This vessel ramifies within the inferior and lateral parts of the ossification centre. The superior surface of the talar neck is invaded by superior neck vessels (Fig. 8). They derive from the dorsalis pedis artery, enter the talar head and branch retrogradely within the ventral tip of the ossification centre. The branching pattern of all arteries that supply the talar anlage is similar. They have straight branches (Fig. 6 and Fig. 7) that run from the outside of the cartilage to the marrow spaces of its ossification centre.

Discussion Histology The ossification of the talus mainly derives from one large ossification centre that shows the endochondral sequence (Fig. 2 - Fig. 4 and Fig. 7). This centre is covered by a small

The present study is the first to summarize qualitative and quantitative data on the talar ossification centre in full term delivered newborn infants. Our findings show that ossification is always detectable in the newborn thus. This is in

456

Fig. 1. Ossification centres in a plastinated foot of a newborn child. Lateral view. x 1.5. Fig. 2. Ossification centre of the talus in a sagittal section (500

~m)

of a left foot. x 4.5.

Fig. 3. Periosteal bone at the roof of the sinus tarsi in a coronal sect ion (500 E, endochondral ossification centre; BP, basa l periosteal bone

~m)

of a right talus. x 40.

Fig . 4. Periosteal bone at the superior surface of the talus in a sagittal section (500 ~m) of a left foot. Enlargement of the cranial part of the ossification centre shown in Fig. 2. x .' 0 . S, synovial membrane of the tibiotalar joint c'a psule. Po, periosteum; F, fibrocartilage-like tissue; CP, cranial periosteal bone

457

Talus in full term infants

mm 3

XLVI

o

CIXV

CXXV

PERI CHONDRIUM

0

CARTILAGE

CXVIII

53ll

BONE

C2

ANLAGE

Fig. 5. Volumes of the ossifying talus.

agreement with Christie (1949), who in a study correlating roentgenographic findings with body weight in the newborn showed that the talus is always ossified in children of more than 2000 g. We have found that in full term newborn children 11 - 24 percent of the talus is already bony. The observed differences in the amount of ossification may be due to the interindividual variation or to different degrees of maturity among our specimens. Our data constitute an important basis for the diagnosis of postnatal talar development. Magnetic resonance imaging (MRl) offers the possibility of achieving similar data from three-dimensional reconstructions of the living individual. In a clinical study by Hubbard et a1. (1993), the first data on the developing talar ossification centre were presented from children aged between three months and seven year~. 11 is a pity, however, that these data were not obtained by defined morphometric methods. They were based on length measurements in selected, single MRIs and therefore do not constitute a reliable foundation. In the adult, it has been shown that the talus is well vascularized from four sides. The main vessels derive from the artery of the sinus and canalis tarsI (Gelberman and Mortensen 1983; Mulfinger and Trueta 1970; Wildenauer 1950). We were able to show that even in the newborn the talar ossification centre is supplied by vessels from four sides. Compared to the situation in the adult, it. becomes evident that in the newborn the main blood supply derives from the vessels of the sinus tarsi, and al,o from the dorsal neck vessels. The branches of rhe,e • essds reach the ossification centre through cartilage ,'anal, that have already been described by Agrawal et al (19K4), It is generally accepted that talar ossification mainly proceeds according to the endochondral mnilallislll In addition, two periosteal collars have beeil r..llllll III our specimens. This is in agreement with 'ecen! findings of Cheng et al. (1995) and with the prcllous hn lings of Hasselwander (1903), whose work ha, becn ncglected in the literature. We have shown that one periosteal bark IS situated below the ossification centre and thU', forllls tbe mof of the sinus tarsi. In all our specimem the perioqeal barh is directly connected with the endochondral <)s'ilhcatlon centre. As

Fig. 6. Deltoid branches (arrows) invading the talus and its ossification centre. Coronal section (300 ~m) of a left foot. x4. Fig. 7. Branches of the artery of the tarsal sinus (arrows) invading the periosteal bone and the talar ossification centre. Coronal section (300 ~m) of a left foot. x4. Fig. 8. Superior neck vessels (arrows) ramifying within the talar ossification centre. Coronal section (300 ~m) of a left foot. x4.

we only studied newborn specimens, i. e. one developmental stage, we are not able to decide whether the periosteal collar develops from the fibrovascular periosteum or from the endochondral centre. The second periosteal collar of the talus

458

is situated at the roof of the well differentiated talar ossification centre and is covered by a layer of fibrocartilage-like tissue, by a layer of dense connective tissue and by the synovial membrane of the tibiotalar joint. It is identical with that part of the talar neck that is situated within the joint capsule. The architecture within the region of the cranial periosteal bone of the talus resembles the structure of specific parts of long bones: on the one hand it may be compared with the regions of insertion of some tendons, as described by Knese and Biermann (1958). On the other hand it may be compared with the region of the ossification groove of Ranvier (Ranvier 1873; Shapiro et al. 1977). which has also been suggested by Cheng et al. (1995), who even described two ossification grooves in the developing talus of the newborn child. The layering in the insertion regions of tendons or in the groove of Ranvier (1873) is similar to that found in the cranial periosteal collar of the talus. Knese and Biermann (1958) have already stated that the insertion organs of tendons possess their own growth plates and are identical with the ossification groove of Ranvier (1873). We therefore suppose that there is a growth plate within the region of the cranial bony collar of the talus. This theory needs to be confirmed in a further 51 udy by refined histological and histochemical means. and at a wide range of pre- and postnatal developmental stage,. Acknowledgements: The technical assistance of Mrs. M.-L. Leppin, Mrs. C. von Lingelsheim, Mrs. S. Markmann and Mrs. H. Strauchmann is gratefully acknowledged. This work was supported by the Deutsche Forschungsgemeinschaft Fr 829/3-1.

Literature Agrawal P, Atre PR, Kulkawi OS (1984) The role of the cartilage canals in the ossification of the talus. Acta Anatl19: 238 - 240 Cheng X, Wang Y, Qu H, Yebin J (1995) Ossification processes and perichondral ossification groove of Ranvier. A morphological study in developing human calcaneus and talus. Foot Ankle lnt 16: 7-10 Christie A (1949) Prevalence and distributlOn of ossification centers in the newborn. Am J Dis Child 7~ ~55

Fritsch H (1988) Developmental changes in the retrorectal region of the human fetus. Anat Embryol 177: 513 - 522 Gardner E, Gray OJ, O'Rahilly R (1959) The prenatal development of the skeleton and joints of the human foot. J Bone Joint Surg 41A: 847-876 Gelberman RH, Mortensen WW (1983) The arterial anatomy of the talus. Foot Ankle lnt 4: 64-72 Gundersen HJG, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147: 229-263 Hagens G von, Tiedemann K, Kriz W (1987) The current potential of plastination. Anat Embryol 175: 411 - 421 Hasselwander A (1903) Untersuchungen tiber die Ossification des menschlichen Fussskelets. Z Morphol Anthropol 5: 438 - 508 Howard CB, Benson MKD'A (1992) The ossific nuclei and the cartilaginous anlage of the talus and calcaneum. J Bone Joint Surg 74B: 620 - 623 Hubbard AM, Meyer JS, Davidson RS, Mahboubi S, Harty MP (1993) Relationship between the ossification centre and cartilaginous anlage in the normal hindfoot in children. AJR 161: 849 - 853 Knese K-H, Biermann H (1958) Die Knochenbildung an Sehnenund Bandansatzen im Bereich ursprtinglich chondraler Apophysen. Z Zellforsch Mikrosk Anat 49: 142 - 187 Mulfinger GL, Trueta J (1970) The blood supply of the talus. J Bone Joint Surg 52B: 160-167 Ranvier L (1873) Quelques faits relatifs au developpement du tissu osseux. Comptes rend Acad Sciences 77: 1105 - 1109 Sarrafian S (1993) Anatomy of the foot and ankle: descriptive, topographic, functional. 2nd ed. Lippincott Company, Philadelphia Shapiro F, Glimcher MJ (1979) Gross and histological abnormalities of the talus in congenital club foot. J Bone Joint Surg 61 A: 522 - 530 Shapiro F, Holtrop ME, Glimcher MJ (1977) Organization and cellular biology of the perichondral ossification groove of Ranvier. J Bone Joint Surg 59A: 703 -723 Tondury G, Theiler K (1990) Entwicklungsgeschichte und Fehlbildungen der Wirbelsaule. 2. tiberarb. u. erw. Aufl., Hippokrates, Stuttgart Wildenauer E (1950) Die Blutversorgung des Talus. Z Anat Entwicklungsgesch 115: 32 - 36 Williams PL (1995): Gray's Anatomy. 38th edition, Churchill Livingstone, New York Edinburgh London Tokyo Madrid Melbourne Accepted June 20, 1996

459