THE ANATOMICAL RECORD 243:l-9 (1995) Morphology of the Dorsal Phalangeal Connective Tissue Body HOLGER BADE, MARKUS SCHUBERT, AND JURGEN KOEBKE Department of Anatomy of the University of Cologne, Germany ABSTRACT Background: The connective tissue body of the dorsal finger is partitioned by multiple horizontal lamellae derived from expansions of intercellular spaces. These connective fibres are involved in providing gliding spaces for the extensor apparatus, and they formed spreading rooms of infection processes. Methods: In order to describe the topographical histological and histochemical behavior of cellular and intercellular elements of the border lamellae of the dorsal aponeurosis of the fingers, a modified method of Epoxid resin embedding technique without pre-infiltration is used. Results: The bordering elements of the connective tissue lamellae described in this investigation are especially well defined in the region of the dorsal aponeurosis. The morphological examinations show that both the expansions of the intercellular space as well as defined fibrocytic cellular elements function in a manner equivalent to a synovial membrane of tendon sheaths. Conclusions: Saving or reconstructing these structures appears to be of importance in preventing for adhesive disorders of finger motion following surgical intervention in this region. o 1995 Wiley-Liss, Inc. Key words: Anatomy, Extensor apparatus, Dorsal aponeurosis, Tendon sheath In view of its connective tissue architecture, the dorsal hand can be distinguished from the palm. The collagenous connective tissue around the extensory apparatus forms normally loosely structured connective tissue layers providing the dorsal skin with a high degree of mobility (Schmidt and Lanz, 1992). In contrast to the palm, the extensory tendons in the metacarpophalangeal transitional region do not form tendon sheaths, rather they course between the multiple layers of connective tissue lamellae which also serve the preservation of circulation for those portions of tendons not surrounded by tendon sheaths (Bade et al., 1992). The absence of a dorsal digital tendon sheath (Koebke, 1988) and the formation of the dorsal aponeurosis as the mean part of the extensor apparatus lead to a special orientation of the peritendinous tissue as a bordering and connecting instrument between extensory apparatus and the dorsal connective tissue lamellae of the finger. Connective tissue fiber bundles adjacent t o the interphalangeal joints stray away from the upper layer of the dorsal aponeurosis and insert on the internal surface of the dorsal folds in the skin t o curtail their mobility and solidly fix them to the connective tissue layers below (Milford, 1968). The mobility of the skin and the subcutaneous connective tissue above the basal and interphalangeal joints of the finger often lead to the formation of subcutaneous bursae above the interphalangeal joint capsules. They compensate for the pressure induced by the tensed skin during flexion of the finger. In the domain about the dorsal aponeurosis of the fingers, the laminary organization of colla0 1995 WILEY-LISS, INC. gen fibers leads to independently mobile fiber systems which often include extensive bordering layers. Spaces similar to those found amidst the diagonal fibers can also be identified between the sagittal ligamentous strands of the dorsal aponeurosis (Landsmeer, 1949). Pathologic processes often spreading by route of the periosseous and periarticular connective tissue spaces include inflammatory and degenerative alterations of the tendons and musculo-tendinous gliding loges and bursae (Mann, 1988). In addition, intercellular spaces of the subcutaneous connective tissue and intermuscular septa also permit pyogenic, phlegmonic, inflammatory processes and hemorrhages to develop and expand (Kanavel, 1939; Grodinsky and Holyoke, 1941). Insufficient post-traumatic and post-operative regenerative processes or adhesions between the bordering layers of such connective tissue spaces often lead to secondary functional disturbances of neighboring tendinous elements of the phalangeal extensory apparatus (Geldmacher and Kockerling, 1991). The cellular architecture of the covering elements characterizes the physiological and pathological behaviour of the bordering structures of the connective tissue gliding spaces and cavities. The first attempts to obtain a macroscopic representation of such connective tissue Received August 16, 1994; accepted March 15, 1995. Address reprint requests to Holger Bade, M.D., Department of Anatomy of the University of Cologne, Joseph-Stelzmann-Strape 9, D-50931 Cologne, FRG. 2 H. BADE ET AL. cavities and their morphological description were performed by Mason and Koch as early as 1930 (Mason and Koch, 1930). The authors investigated the expansive pathways of post-traumatic infections following biting injuries on the backs of the hand or finger by injecting radiologically dense contrast dies. For the first time several parallel oriented dorsal “fascias” were defined as bordering structures of epitendinous “fascia1 spaces” on the extensory side of the dorsal aponeurosis of the metacarpo-phalangeal transition. Faciszewski and Coleman (1989) only delivered sparse indications toward the morphology of the epifascial connective tissue spaces of the back of the hand, whereas no closer description of the histological architecture or a histomorphological characterization of such connective tissue spaces was provided. The goal of the following examination is to describe the topographic relations of macroscopically visible connective tissue spaces or cavities of the back of the finger with regards to their histomorphologic pattern. To get a n explanation of their interactions with the elements of the dorsal aponeurosis, this study focusses the histomorphology of the cellular elements bordering this intercellular spaces. This may offer a morphological explanation for post-traumatic and inflammatory functional disturbances i n the sheathless region of the phalangeal extensor tendons. In addition the histochemical characterization of the intercellular matrix will clarify whether the intercellular substance produced by the neighboring cells gets a synovia-like function or both the cellular elements and the intercellular matrix border limit the connective tissue body covering the phalangeal extensory apparatus. MATERIALS AND METHODS Both the topographical as well as the histological examinations were performed on fixed fingers of male and female individuals between 65 and 72 years of age. The specimens were dehydrated and then decalcified using EDTA. In order to deal with such large specimens, the resin embedding technique (Technovit 7100@,Kulzer GmbH, Wehrheim, Germany) had to be modified. The pre-infiltration of the specimens in a preparatory solution was eliminated. Following a n acetone bath, the specimens were placed directly in a resin embedding medium. The reaction-heat as well as the duration of the entire process was easily controlled when the basic resin solution was cooled to -8°C. During acetone-extraction and resin infiltration, the specimens were kept in a vacuum environment for 3 hours. While hardening, the specimens were kept at -25°C in order to decrease both the polymerization speed and the reaction-heat involved with such large objects. The hard microtome sections (5-3 pm) were stained with Toluidine-blue, Alcian-blue, basic Fuchsin, Giemsa, and a trichromatic stain according to Sevier and Munger (1968). In addition, the resin sections were pretreated with potassium-peroxymonosulfate (Oxone, Sigma Chemical Co., Deisenhofen, Germany) as a mild oxidant. The Toluidin-blue staining of non-deplastinated sections in the semi-thin slicing technique provided distinct orthochromatic representations of cells and their intercellular substance. In turn, the metachromatic reaction of acidic glycosaminoglycans allowed for a differentiation of cellular elements. Dem- ineralized solid tissue matrix, cells, and histiocytic cellular elements stained in different intensities of blue, whereas cartilagenous matrices and mast cell granules appeared blue-violet. A semi-thin slicing procedure (3 pm) coupled with a PAS-reaction and histochemical proof of acidic phosphatase was used to obtain a valid characterization of intercellular glucose and enzyme dispersions. The advantages of the present modification of the Technovit 7100@method lay quantitatively in the utilization of a much greater number of specimens to perform topographical and histological examinations a t the same time and qualitatively in a more even penetration of the specimens, eliminating disturbing bubbles. At the same time, the use of resin was reduced by omitting the pre-infiltration (Fig. 1). RESULTS Topography of the Dorsal Phalangeal Connective Tissue Apparatus of the Finger Sagittal sections of the dorsum of the fingers displayed a visible separation of the dorsal connective tissue above the phalangeal bone into separate lamellary systems. These ran parallel to the extensory apparatus and were separated in the median and paramedian regions into two systems-below and above the dorsal aponeurosis. The below of these systems was separated in two laminae, first (palmar) lamina of these was attached to the phalangeal bone while the second (dorsal) lamina was associated with the dorsal aponeurosis (Fig. 2). This separation of the dorsal connective tissue became more apparent proximally towards the basal finger joint. Here the palmar system connected the adventitia of the phalangeal periosteum with the palmar surface of the dorsal aponeurosis. The loosely structured intercellular substance of this region concealed the various calibers of vessels and nerves and was comparable with the vincula tendineum of the flexory side which has phalangeal tendon sheaths. While the transition to the adventitia of the periosteum was continuous, the palmar system bore a bordering lamella to the stiff collagen fiber system of the dorsal aponeurosis, whose fibrous composition displayed a distinct proximal-distal differentiation. A spacial separation of the connective tissue body of the periosteum from the palmar side of the dorsal aponeurosis, which was best to be observed between the interphalangeal joints, took place without the formation of a bordering layer of cells. Nevertheless, blood vessels came into close contact with the extensor tendon in regular intervals and occasionally passed between the palmar collagen fiber bundles of the flexory apparatus. The stiff collagenous connective tissue of the dorsal aponeurosis itself displayed regional divisions and horizontal septa formed by delicate vascular guiding connective tissue strands which guided delicate vessels and were equivalent to a peritendineum. About the lateral strands of the dorsal aponeurosis, larger vessels protected by loose connective tissue entered the tendinous body dorsally and dispersed in the peritendinous connective tissue. Towards the bony insertion at the distal phalanx, the vascular cross sections and the peritendinous septa became more sparse. In contrast to the palmar side of the dorsal rw Specimen: ' '-------.fixed, 85 x 60 x 40 24 h EDTA without pre-infiltration Technovit 7100 (-8°C) Hard microtome: 3i-W 5iJm Alcohol Aceton 2x12h Cooling 7Vacuum '-------- A Staining: Toluidin-Blue Trichrom Fig. 1. Schematic representation of the technical processes used in order to investigate the histological features of the connective tissue laminae and its spaces. The advantages of our modification of the Technovit 7100' method lie quantitatively in the utilization of a much greater amount of specimens and qualitatively in a more even penetration of the specimens, eliminating disturbing bubbles. At the same time, the use of resin is reduced via elimination of the pre-infiltration. Fig.2.Paramedian sagittal section through the proximal phalanx of a plastinated right thumb (Biodur epoxide resin, Toluidine-blue, x 5). Above the phalanx, a visible gap in the dorsal connective tissue body is present in different lamellary systems, running parallel to the extensory apparatus and separated by the dorsal aponeurosis (A) into a palmar system (PI associated with periostal layer of the phalangeal bone (arrow 1)but detached to the palmar layer of the dorsal aponeurosis (arrow 2) and a dorsal system (D) situated atop the extensory apparatus. The separation of the dorsal connective tissue body becomes more apparent toward the middle of the phalangeal bone. 4 H. BADE ET AL. Fig. 3. Palmar side of the dorsal aponeurosis of a n index finger in the region of the middle phalanx ( x 400 and x 600, Toluidine-blue, 3 km). The connective tissue beneighboring the dorsal aponeurosis presents as a loosely structured transitional zone to the adventitia of the periosteum and possesses a concentrated fibrocytic zone at the dorsal border to the subtendinous space (arrowheads) opposite the areas of the dorsal aponeurosis more highly populated with cells (a). The fibrocytes of the subtendinous connective tissue are located in the perivascular cell populations as well as immediately below or in the superficial collagen fiber lamella. Their cytoplasm often displays metachromatic granules (arrowheads) in the Toluidine-blue stain as a sign of increased activity (b). MORPHOLOGY OF CONNECTIVE TISSUE BODY 5 Fig. 4. Epitendinous space of the dorsal aponeurosis of a n index finger ( x 600, Toluidine-blue, 3 km). The cavity is bordered by a fibrous condensed zone (arrowhead) and cellular elements, which display qualities of active fibrocytes as well as monocytic or phagocytic qualities. Cell populations can be observed in view of their different orientations to the connective tissue bordering layer of the epitendinous cavity, located either beneath the surface, in the perivascular space, or in deeper connective tissue layers. aponeurosis, the dorsal side displayed a clear division separating the tendinous body from the connective tissue system of the dorsal finger. Both the superficial fiber strands of the dorsal aponeurosis and the opposing loose connective tissue displayed clear zones of greater concentration at the border to the separating space. Only at the insertion zones did lateral strands of loose connective tissue bundles traverse this space as vascular guiding tissue and thereby passed between the collagen fiber bundles of the dorsal aponeurosis. The dorsal connective tissue body of the extensory apparatus formed a fibrous bordering layer towards the opposing dorsal aponeurosis which was clearly depicted in the trichromatic stain with Fast green and Safranin and complemented by cellular elements. Beneath a more concentrated fibrous zone, a loose vessel directing connective tissue formed horizontal fiber strands or plates which were organized by zones of lesser compact collagen fiber bundles, but did not appear separated. Such loose connective tissue layers carrying vascular and nervous bundles of varying regional differentiation continued into the loose subcutaneous connective tissue and were penetrated by the sagittally oriented cutaneous retinacula of the subcutaneous connective tissue. Histology of the Dorsal Phalangeal Connective Tissue Compartments The cellular and intercellular architecture of the bordering surfaces of the phalangeal connective tissue compartments was easily differentiated among the sagittal semi-thin sections of this region. Differences between the cellular elements and their orientation in the bordering region between the dorsal extensory apparatus and the neighboring fields of connective tissue became especially clear here. The subtendinous space of the dorsal aponeurosis was bordered by a connective tissue layer, which, in contrast to the epitendinous space, displayed no marked cellular surface architecture. The neighboring connective tissue of the palmar side of the dorsal aponeurosis displayed a loosely structured transitional zone to the adventitia of the periosteum and had a concentrated zone of fibrocytes on its dorsal border which was opposed to the more highly populated areas of the dorsal aponeurosis (Fig. 3a). The fibrocytes of the subtendinous connective tissue were arranged in perivascular cell conglomerations and also scattered beneath or within the superficial collagen fiber lamellae. Their cytoplasm displayed defined metachromatic granules in the Toluidine-blue stain, which is a sign of increased activity (Fig. 3b). 6 H. BADE ET AL. Fig. 5. Epitendinous cavity of the dorsal aponeurosis of an index finger ( x 600, Toluidine-blue, 3 km). Fibrocytes are located in the superficial lamellae of the dorsal aponeurosis, and especially in different relation to the superficial condensed zone of the epitendinous connective tissue sheet (arrowhead). Their granulated cytoplasm and light colored nuclei indicate different cellular stages of activity. Their cell bodies protrude into the cavity and form a partially interrupted cell layer. The epitendinous space was incompletely bordered by a layer of cells displaying both qualities of active fibrocytes and of monocytic or phagocytic cells. Topographically, three groups of cells were observed, each demonstrating specific characteristics with regard to their different orientations to the connective tissue lamella (Fig. 4).Fibrocytes were situated upon the superficial lamella of the dorsal aponeurosis and especially on the safranin-positive concentrated zone of the epitendinous connective tissue layer. The acidophilic cytoplasm of these cells and their light colored nuclei gave evidence of a special secretoric activity. The cell bodies protruded into the cavity and obviously formed a n interrupted cell layer (Fig. 5). Underlying this layer of cells was a loose epitendinous connective tissue seen, which displayed collections of fibrocytes. In regions of increased vascularity, cell populations were augmented by cells which were classified as mast cells based on their metachromatic, basophilic cytoplasm. They were situated in groups in the perivascular connective tissue, however, isolated cells were also found beneath the superficial safraninpositive bordering lamella (Fig. 6). In the space above the dorsal aponeurosis, remnants of cells and detritus-varying in preservation-were seen. Isolated structures were found whose size and form were reminiscent of cell conglomerates or aggregated components of structured intercellular sub- stance. The regions of the cavity which contained connective tissue vessel-guiding bridges also showed a n increased density of fibrocytic and leukocytic cellular elements. The opposing safranin-positive bordering lamellae of the dorsal aponeurosis and the above connective tissue body were well formed here. These reddish-brown imposing, safranin-positive, i.e., acidophilic reacting bordering lamellae were only observed at the border to the epitendinous space, where they were most numerous and frequently visible in the central region of the middle phalanx. Collagen fiber bundles or nets which formed a bordering layer were also found between the other connective tissue lamellae of the dorsal finger, however, the superficial bordering connective tissue layers displayed no histochemical alterations in their intercellular matrix. They should be differentiated due to their alternating fiber density and orientation. The subtendinous connective tissue body between the adventitia of the periosteum and the dorsal aponeurosis is bordered against the extensory apparatus by condensed collagen fiber lamellae. There is no evidence of a n altered intercellular milieu and of safranin-positive lamellae. DISCUSSION The intercellular spaces of the dorsal phalangeal connective tissue body between the basal finger joint and the proximal interphalangeal joint are bordered by MORPHOLOGY OF CONNECTIVE TISSUE BODY 7 Fig. 6. Epitendinous cavity of the dorsal aponeurosis of a n index finger ( x 600, Toluidine-blue, 3km). Loose connective tissue underlies the border layer of the cavity, which displays a higher population of fibrocytes. Cell populations are increased most of all in regions of increased vascularization. These additional cells can be identified as mast cells based on their metachromatic and basophilic cytoplasm (arrowheads). They are situated in cell conglomerates in the perivascular connective tissue, and can also be displayed isolatedly beneath the safranin-positive border lamella. more dense connective tissue lamellae. They can be viewed as expansions of the loose connective tissue of the intercellular space according to their histological architecture (Webster, 1988; Geldmacher and Kockerling, 1991). Their expanse is determined by the pressure of moving tendons of the extensor muscles but by spreading pathological processes too. Therefore they are not clearly bordered in an unloaded finger. The more profound space between the deep lamellar system of the dorsal connective tissue and the dorsal aponeurosis forms gliding surfaces between the elements of the extensory apparatus and the covering soft tissue layer of the dorsal finger. In order to describe the function of such connective tissue spaces, it is therefore necessary to take into consideration the passive expansion following physiological and above all pathological processes as well as position alterations of the connective tissue layers, which lie in a closed relation to the phalangeal joints. A synovia-like or epithelial structure of the lining cells of such spaces determines the function of those spaces as gliding spaces. An uninterrupted cell layer atop the described connective tissue could not be demonstrated, but the presence of secretory fibroblasts in the connective tissue lamellae of the margins and a condensed glucosaminoglycane consisting zone a t the border of these compartments are morphological signs of an adaptation of the cellular function to the mechan- ical strain of the various collagen fiber lamellae during finger movement. These cells display a morphological similarity to type F (fibroblastic) synoviocytes of the tendon sheaths. The glycosaminoglycans within the fibroblasts allow assumptions about the enhanced activity of these cells. The intercellular glucosaminoglycanes of the gliding spaces form the medium for extracellular collagen fiber synthesis and increase the lubrication of th neighboring connective tissue lamellae. The building of more concentrated bordering zones between the dorsal surface of the extensory apparatus and the opposing connective tissue layer appears to be of special importance. These parts differ in their staining behavior from their respective connective tissue layer. The trichromatic stain, with which the bordering layers react more intensely acidophilic as reddishbrown concentrated zones, especially documents an alteration in the composition of the intercellular matrix. They quite clearly differ from the opposing and differently mobile fluorescent green collagen connective tissue body of the dorsal aponeurosis and the underlying connective tissue jacket. The acidophilic stain reaction of these bordering lamellae indicates an increased content of acidic mucopolysaccharides in the intercellular substance and can be viewed in direct connection with the increased activity of the fibroblasts thereupon. These fibroblasts do not only secrete a “lubricatory” 8 H. BADE ET AL. midd I swerficial lamellar svstem I deep lamellar system I digital vessels Aponeurosis dorsalis I Periosteum / Bone Fig. 7. Schematic representation of the dorsal connective tissue body of a finger. The subcutaneous connective tissue is separated in two lamellar systems (superficial and deep) around the subcutaneous veins. The deep lamella of this subcutaneous tissue body bordered a space above the dorsal aponeurosis (D). Below the dorsal aponeurosis a second space (PI is formed out, which bears two laminar systems: one closed to the periosteum and one closed to the palmar side of the dorsal aponeurosis. The last is bordered by the lateral strands of the extensor apparatus. mucus, but they are also obviously sloughed off into the gliding space in order to form a surface coating typical for synovial membranes. If one compares the palmar, subtendinous area of the dorsal aponeurosis with the dorsal epitendinous area, it becomes clear that the latter can be considered as a genuine gliding space with surface structures which form bordering surfaces. The dorsal epitendineal tissue shows histomorphological signs which can also be found in the synovial sheaths of the triceps surae tendon or in the vincula of the phalangeal flexor tendons (Lang, 1963; Geldmacher and Kockerling, 1991). The subtendinous intercellular substances form a network of a loose connective tissue which can be seen as paratendineum in the sheathless parts of many tendons. Those multi-laminar apparatuses are able to follow the excursion of the tendon elastically. Therefore the differences in morphology between the areas of a superficial and a deep lamellar system must be explained by the difference in mobility between the overlaying connective tissue and the extensory apparatus related to the mobility between the extensory apparatus and the underlying periostal tissue (Fig. 7). The extensory apparatus inserts through the periostal layer in the phalangeal bone with different fiber systems and thus enjoys an especially intense fixation to the skeletal elements. During flexion and extension of the finger the relative movements between osseous surface and dorsal aponeurosis are therefore limited and lead to only a slight difference of mobility between both structures. Another situation is found above the dorsal aponeurosis. Here the cutis, in conjunction with the subcutaneous connective tissue body, forms a connective tissue body with elastic and rigid properties independent of the dorsal aponeurosis, which experiences an intense concentration about the finger joints and which above the cutaneous retinacula remains fixed in transverse reserve folds opposed to the extensory apparatus. The high mobility of this “cutaneous jacket” related to the underlying dorsal aponeurosis causes a greater longitudinal dislocation between both structures and thus causes the necessity for the formation of a gliding space, which allows an independent moving of the extensory apparatus and without overstretching the phalangeal cutaneous jacket fixing by its retinacular system. This also becomes apparent in the studies of Kaplan and Milford (19841, wherein the movements of the cutaneous and subcutaneous connective tissue above the phalangeal extensory apparatus are described as independent from the underlying tendon apparatus. Moreover, both peritendineous tissue systems may be viewed as secondary reactive areas for pathological joint alterations, arthritis or joint infection, due to their spatial vicinity and incomplete separation from the neighboring cavities of the phalangeal joints. In this manner, cellular elements dominate in the epitendinous connective tissue body on the extensory side of the dorsal aponeurosis as a signal of defensive mechanisms of the perivascular connective tissue. Mast cells and phagocytic cells found below the bordering zones are the histomorphological sign for age-related transpired inflammatory and regenerative processes in the peritendineous connective tissue. But many of them are responsible for forming bordering surfaces like the synoviocytes. Thus, this would indicate pathological alterations of the intercellular milieu (Wojciak and Crossan, 1993) or reparative processes (Eguchi et al., 1992; Spector et al., 1992) including the epitendineous tissue. 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