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Morphology of the dorsal phalangeal connective tissue body.

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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. The special architecture and cellular differentiation of the connective tissue lamellae in the dorsal
metacarpo-phalangeal transitional region are the results of differences in mobility of the connective tissue
above and below the extensor apparatus of the finger.
Saving or reconstructing these specific topographical
relationships may be important in preventing for adhesion caused disorders in finger motion following surgical treatment in the dorsal phalangeal region.
MORPHOLOGY OF CONNECTIVE TISSUE BODY
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sehnenscheidenfreien Strecke der Extensorensehnen des 11. bis V.
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233-238.
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human finger and its functional significance. Anat. Rec., 104:3144.
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Schmidt, H.-M., and U. Lam 1992 Chirurgische Anatomie der Hand.
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