HISTOGENESIS AND MORPHOLOGY OF THE FLEXOR TENDON PULLEY SYSTEM IN THE HUMAN EMBRYONIC HAND M. C. SBERNARDORI, G. FENU, A. PIRINO, C. FABBRICIANI and A. MONTELLA From the Department of Orthopaedics and the Department of Biomedical Sciences, Division of Human Anatomy, University School of Medicine, Sassari, Italy
The number, position, structural and ultrastructural features of the ¯exor tendon pulley system in six human embryonic hands, aged from 6 to 12 weeks, were studied by light and electron microscope. The pulley system can be recognized from the ninth week; later, at 12 weeks, the structures are easily identi®ed around the ¯exor tendon in positions closely correlated to those found during post-natal growth and in the adult hand. Structurally and ultrastructurally the pulleys are not simply thickened portions of the sheath. They are formed by three layers: an inner layer, one or two cells thick, probably representing a parietal synovial tendon sheath; a middle layer formed by collagen bundles and ®broblasts whose direction is mainly perpendicular to the underlying phalanx; and an outermost layer consisting of mesenchymal tissue with numerous vessels which extends dorsally in an identical layer, forming a ring that includes ¯exor and extensor tendons and the cartilaginous model of the phalanx. The pulley does not have a semicircular shape but a much more complicated one, owing to the middle layer which in part runs dorsally and in part ventrally, under the ¯exor tendons. Journal of Hand Surgery (British and European Volume, 2000) 25B: 2: 175±179 There have been numerous studies to delineate the number, position, function and histomorphology of the ¯exor tendon sheath and its related pulley system in the human adult hand in the last 20 years (Brand et al., 1975; Cohen and Kaplan, 1987; Ochiai et al., 1979). At the present time it is accepted that ®ve annular (A1±A5) and three cruciform pulleys (C1±C3) can be identi®ed (Doyle, 1988, 1989, 1990; Hoving and Hillen, 1989; Jones and Amis, 1988; Lin et al., 1989) as localized ®brous reinforcements of the tendon sheath. However, their structural and ultrastructural aspects are the subject of greater controversy. Katzman et al. (1998), in a study on the A5 pulley, reported that there were three layers, as described by Ellis et al. (1995) in the A2 pulley. Only two layers were described by Cohen and Kaplan (1987), Sampson et al. (1991) and Lundborg and Myrhage (1977). The last authors denied the existence of a continuous cellular layer (the synovial parietal layer) in the deepest part of the pulley and they called this region the ``friction surface''. Doyle (1990) also did not mention a synovial layer on the inner layer of the pulley. During post-natal development, Bogumill (1983) and Flake et al. (1990) have reported that the appearance of the pulley system is closely related to that seen in the adult hand. The present study was carried out to analyse the structural and ultrastructural features of the ¯exor tendon sheath and pulley system at dierent ages in human embryonic and fetal hands and to ®nd out at which week of gestation it is possible to identify these structures.
and fetal hands of 6, 9, 11,12 weeks of gestation, derived from voluntary abortions. The age of each embryo was exactly determined both on the basis of echographic standards and the crown-rump length. The specimens obtained were prepared for light and electron microscope examination. For histological examination the specimens were ®xed in 10% buered formalin, dehydrated in alcohol and embedded in paran. The serial transverse sections (from the tip to the base of the ®nger) 5 m thick were stained with haematoxyline-eosin and then observed in a light microscope. For ultrastructural studies the specimens were ®xed in 2.5% glutaraldehyde in 0.1 M phosphate buer (pH 7.4) and post-®xed in 1% osmium tetroxide. Ultrathin sections of 500 A were stained sequentially in a saturated solution of uranyl acetate in 50% ethanol, for 25 min, and lead citrate for 8 min. The specimens were then examined in a Zeiss E.M 902 transmission electron microscope. RESULTS Histology The ¯exor tendon sheath and its related annular pulley system were identi®able in the hands 9 weeks post gestation. Before this only an undierentiated embryonic mesenchymal tissue was present around the cartilaginous models of the phalanges. At 9 weeks of pregnancy the mesenchymal tissue of the palmar region of the ®ngers began to show a morphological dierentiation into ¯exor tendons and there was the ®rst appearance of the annular pulley system (Fig 1).
MATERIALS AND METHODS The ¯exor tendon sheaths and related pulley systems were studied in 30 ®ngers from six human embryonic 175
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Fig 1 Transverse section of the cartilage model of the proximal phalanx at 9 weeks of pregnancy: the mesenchymal tissue shows morphological dierentiation into the ¯exor tendon (T), ¯exor tendon sheath and annular pulley system (P). (Paran embedding. Haematoxylin-eosin stain. Original magni®cation650.)
At 12 weeks of gestation ®ve annular pulleys were recognizable along the axis of the digit and their positions in serial transverse sections closely correlated to those in post-natal and adult hands. Structurally, the pulleys seemed to be thickenings of the ¯exor tendon sheath, semicircular in shape (Fig 2), inserted in the perichondrium with the A2 and A4 being the thickest pulleys. On the basis of the structural organization of the elements of the pulleys it was possible to distinguish three distinct layers: an inner, middle and outer (Fig 3). The inner one was composed of a layer of one or two cells; these cells, ¯attened in shape, with large nuclei show morphological features similar to those which were seen in the most super®cial part of the ¯exor tendon. A semicircular cavity (the future synovial cavity) separated this part of the pulley from the super®cial layer of the ¯exor tendon which was identi®able along the length of the digital axis. The middle layer showed a high grade of cellularity: the spindle-shape ®broblasts were lying along the collagen ®bres. The small bundles of collagen ®bres apparently perpendicular to the digital axis surrounded
THE JOURNAL OF HAND SURGERY VOL. 25B No. 2 APRIL 2000
Fig 2 Transverse section of A2 pulley at 12 weeks. The pulley (P) is structurally similar to a thickening of the ¯exor tendon sheet (T). (Semithin section. Toluidine blue stain. Original magni®cation650.)
the ¯exor tendon, inserting in the perichondrium. Careful inspection showed that some ®bres, instead of penetrating into the perichondrium, changed their direction and ran under the ¯exor tendons, giving an important element of stability to this system (Fig 4), whereas others ran dorsally into the perichondrium in the direction of the extensor tendons. It was possible to recognize a ``®gure-of-8'' arrangement which stabilized the ¯exor tendons on the underlying skeletal element (Fig 5). The outermost layer was formed by a loose mesenchymal tissue, rich in vessels (sometimes it was possible to see some ``lacunae vasculares''), whose ®bres run dorsally constituting an oval-shaped structure surrounding the ¯exor and extensor tendons and the cartilaginous bone model (Figs 3±5). Ultrastructure The ultrastructural examination con®rmed the histological data. In the inner layer of the pulley ¯attened cells were evident with few collagen ®bres lying in an irregular
PULLEY SYSTEM IN THE EMBRYONIC HAND
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Fig 3 Transverse section of A2 pulley at 12 weeks. The pulley is constituted by three layers: I=inner layer, II=middle layer, III=outer layer. (* synovial cavity) (Semithin section. Toluidine blue stain. Original magni®cation6250.)
Fig 4 Transverse section of A2 pulley at 12 weeks. Some ®bres of the pulley penetrate into the perichondrium; others change direction and run between the ¯exor tendon and the cartilaginous bone model (arrows). (Semithin section. Toluidine blue stain. Original magni®cation6100.)
fashion with some of them adjacent to the cavity (Fig 6). They were similar to those present in the outer layer of the tendon in terms of their ultrastructural features. The outer layer showed a few ®broblasts, irregular in shape, surrounded by an amorphous matrix and small bundles of collagen ®bres, mainly running perpendicular to the ¯exor tendon (Fig 7). In the middle layer the bundles of collagen ®bres were larger and rather disarranged, although the main direction was perpendicular to the axis of the digit (Fig 8). In this layer the cells, which were uniform in shape and size, had a well developed system of granular endoplasmic reticulum and prominent nucleoli, like active ®broblasts. No chondroblasts or chondrocytes were detected.
described by Doyle (1988; 1989) in every digit, excluding the thumb, there are ®ve annular pulleys of which the A2 and A4 are the thickest, by the twelfth week. In every pulley there are three layers as previously described in post-natal life by Ellis et al. (1995) in the A2 pulley and by Katzman et al. (1998) in the A5 pulley. Contrary to the description of Doyle (1989) and Sampson (1991), who deny the presence of parietal synovial tissue on the inner surface of the pulley, we found an inner layer of the pulley that we think constitutes the parietal stratum of the synovial membrane. There was no dierence in the structural and ultrastructural features in this layer and the most super®cial part of the ¯exor tendon which was separated from it by the future synovial cavity. We agree with Cohen and Kaplan (1987) who considered that:
DISCUSSION This study has shown that the ¯exor annular pulley system starts to dierentiate together with the ¯exor tendons around the ninth week of intrauterine life, reaching a high grade of dierentiation at the twelfth week (the end of the ®rst trimester of pregnancy). As
the retinacular pulley system is external to the synovial sheath and there are no dierences structurally and ultrastructurally between the parietal synovial layer in the inner layer of the pulley, the membranous portion of the sheath and the visceral synovium forming the epitenon.
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Fig 7 Ultrastructural appearance of the cells in the outer layer of the pulley. (Ultrathin section. Original magni®cation63000.)
Fig 5 The pulley system ®bres constitute a ``®gure-of-8'' structure that also stabilizes the ¯exor tendon. P: pulley; FT: ¯exor tendon; ET: extensor tendon. (Semithin section. Toluidine blue stain. Original magni®cation625.)
Fig 6 Ultrastructural appearance of the cells in the inner layer of the pulley. (* synovial cavity) (Ultrathin section. Original magni®cation67000.)
In the middle layer there is, at the end of the ®rst trimester, no evidence of ovoid cells with ultrastructural characteristics of chondrocytes as described in the control and trigger A1 pulley by Sampson et al. (1991). In this layer the most interesting aspects concern the bundles of collagen ®bres that are still quite disarranged and which run into the perichondrium towards the dorsal aspect of the ®nger but also beneath the ¯exor tendons, to stabilize the system eciently. To summarize, the pulley does not have a semicircular shape but a much more complicated one, owing to its middle layer which in part runs dorsally and in part ventrally, under the ¯exor tendons like a ®gure-of-8. The outmost layer running to the dorsal aspect of the ®nger forms a ring which encloses not only the inner portions of the pulley system, but also the ¯exor and the extensor tendons and the cartilaginous model of the bone.
Fig 8 Ultrastructural appearance of the cells in the middle layer of the pulley. (Ultrathin section. Original magni®cation67000.)
PULLEY SYSTEM IN THE EMBRYONIC HAND
It might be necessary to reconsider the annular pulley system as a component of a more extensive system involving not only the ¯exor tendons but also the extensor mechanism. References Bogumil GP (1983). Relationship of collateral ligaments to growth plate. Journal of Hand Surgery, 8: 74±79. Brand PW, Cranor CK, Rouge B, Ellis JC (1975). Tendon and pulleys at the metacarpophalangeal joint of a ®nger. Journal of Bone and Joint Surgery, 57A: 779±784. Cohen MJ, Kaplan L (1987). Histology and ultrastructure of the human ¯exor tendon sheath. Journal of Hand Surgery, 12A: 25±29. Doyle JR (1988). Anatomy of the ®nger ¯exor tendon sheath and pulley system. Journal of Hand Surgery, 13A: 473±484. Doyle JR (1989). Anatomy of the ¯exor tendon sheath and pulley system: A current review. Journal of Hand Surgery, 14A: 349±351. Doyle JR (1990). Anatomy and function of the palmar aponeurosis pulley. Journal of Hand Surgery, 15A: 78±82. Ellis FD, Seiler JG, Sewell CW (1995). The second annular pulley: A histologic examination. Journal of Hand Surgery, 20A: 632±635. Flake J, Light TR, Ogden JA (1990). Postnatal growth and development of the ¯exor tendon pulley system. Journal of Pediatric Orthopaedics, 10: 612±617. Hoving EW, Hillen B (1989). Functional anatomy of the vagina ®brosa of the ¯exors of the ®ngers. Journal of Hand Surgery, 14B: 99±101.
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Received: 16 August 1999 Accepted after revision: 25 October 1999 Dr C. Sbernardori, Via Abozzi 28, 07100 Sassari, Italy. E-mail:
[email protected] # 2000 The British Society for Surgery of the Hand DOI: 10.1054/jhsb.1999.0341, available online at http://www.idealibrary.com on