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The structure and vascularization of the biceps brachii long head tendon
= = = = = = = = = ANNALS
Of ANATOMY
=========
The structure and vascularization of the biceps brachii long head tendon* I. Kolts, B. Tfllmann! and R. Lullmann-Rauch! Department of Anatomy, University Tartu/Estland, and 'Department of Anatomy, Christian-Albrechts-University, OlshausenstraBe 40, D-24098 Kiel, Germany
Summary. In the present study we examined the structure and the blood supply of the long biceps tendon as well as the surface of the intertubercular sulcus, using tissue samples from children and adults. The applied methods were light and electron microscopy, immunohistochemistry, and arterial injection techniques. The tendon represents a sliding tendon with the inter tubercular sulcus and humeral head as hypomochlion. The parts facing the humerus show some ultrastructural features of fibrous cartilage, the ovoid chondrocyte-like cells of the tendon lying within felt-like matrix. In the opposite part adjacent to the capsule , the tendon resembles a traction tendon. The intertubercular sulcus is covered by fibrous cartilage. The tendon is supplied with arteries from three different sources. The density of intratendinous vessels in the traction zone is comparable to that of other tendons, while in the sliding zone it is markably decreased . The immediate vicinity of the sliding surface is avascular. Our findings show that the long biceps tendon is structurally adapted to both its functions as sliding and traction tendon. The blood supply seems to be related to the metabolic requirements of the different parts of the tendon.
Key words: Biceps tendon - Vascularization - Sliding tendon
Introduction Due to a rising amount of sporting activities, nowadays lesions of the shoulder region occur even in younger persons with increasing frequency . In about 30 % of the population older than 40 years pathological alterations of the shoulder joint are found. The frequency of alterations increases with aging (Reichelt 1981; McKendry et al. 1982; Refior et al. 1987). As far as the long biceps tendon is concerned, subluxations and luxations as well as partial or complete ruptures are observed in addition to tendosynovitis (Jager and Wirth 1986). Ruptures of the tendon are thought to occur on the basis of preceding degenerative lesions. These could be related (a) to the position of the tendon within the intertubercular sulcus (Tillmann and Thomas 1982) and at the humeral head, as well as (b) to the pattern of vascularization (Lindblom 1939; Uhthoff et al. 1976; Rathbun and Macnab 1970; Macnab 1981; KeyI1989). The present study was undertaken to contribute to the elucidation of the pathogenesis of lesions affecting the long biceps tendon. For this purpose, the following investigations were performed: Light and electron microscopic examination of the intertubercular sulcus and the tendon at defined segments; visualization of the vascular pattern by means of arterial injections and immunohistochemical demonstration of the vascular basement membranes.
Materials and methods • Dedicated to Professor Dr. med. Wolfgang Kuhnel on the occasion of his 60th birthday. Correspondence to : B. Tillmann
~I
Ann Anat (1994) 176: 75 - 80 Gustav Fischer Verlag lena
Arterial injections were performed on 10 unfixed shoulder joints of 10 male cadavers (aged 61 - 67 years). For histological investigations 22 tendons were used (16 from male cadavers, ages 14days to 82 years, and 6 from female cadavers, ages 27 to
trois to exclude artefacts due to unspecific binding of the antibody. Cryostat sections of human skin and liver were taken to verify the specific appearance of vessels in well vascularized tissues.
66 years). In 5 cases the intertubercular sulcus was also examined. For immunohistochemical investigations, tendons of 3 male cadavers (ages 7,22,72 years) were obtained 12 hours post mortem . Ultrastructural investigations were performed on tendons of one femal (27 years) and one male (70 years). Two different mixtures were used for arterial injection: (a) 10 % aqueous dispersion of Natur-Kautschuk stabilized with 0.7 % ammonia; (b) 5010 gelatine containing 0.5 010 (v/v) indian ink (Pelikan, Hannover, Germany). 300ml were injected simultaneously via the subclavian and the brachial arteries (Korn and Schunke 1989). After polymerization of the injection mixture, the tendon was removed and processed according to the method of Spalteholz (1914) as modified by luskiewenski and Vaysse (1987). For light microscopy, the segments of the tendon (Fig. 1) were fixed in phosphate-buffered paraformaldehyde (4 %) for 6 hours and embedded in glycolmethacrylate. Semithin sections (3llm) were stained with toluidine blue (0.1 %) at pH 5.0 in 0.1 M acetate buffer. For ultrastructural examination, the tissue samples were fixed in 3.5 % glutaraldehyde and processed according to routine methods. For immunohistochemical investigations, the unfixed tissue samples were incubated with 10 % sucrose in phosphate-buffered saline and frozen with liquid nitrogen. Cryostat sections (8 - 161lm) were cut in a cryostat and mounted on gelatinecoated slides. Rabbit anti -laminin (MEDAC, Hamburg/FRG) served as a specific antibody for the immunofluorescence technique. Sections were washed in phosphate-buffered saline (PBS, pH 7.2 -7.4). After incubation with the antibody (diluted I : 20, 45 min at room temperature in a moist chamber), the sections were rinsed three times with PBS. They were then incubated for 30 min with fluorescein isothiocyanate (FITC)conjugated anti-rabbit IgG (1 : 30), diluted with human serum (1 : 20), rinsed again three times with PBS and mounted with PBS/Glycerine (9 : 1 in 2.5 0J0 NaN ), pH 8.6). Sections incubated with FITC-conjugated antibodies alone served as con-
I ,
Results Vasculature The long biceps tendon is supplied by arteries from three different sources: The distal portion by branches of the brachial and deep brachial artery, the proximal portion additionally by branches of the anterior circumflex humeral artery (Fig. 2). In the intertubercular sulcus a branch of this artery gives rise to two smaller branches running in cranial and caudal directions. The cranial branch provides small vessels which reach the proximal segment of the tendon and its synovial sheath.
Fig. 2. Latex-injection preparation. Right shoulder of a 63 year old man. The long biceps tendon (B) is visible after incision of the coraco-acromial ligament (LCA) and the joint capsule (C) in the rotator intervall (RI). The tendon was dislocated anteriorly to the intertubercular sulcus to demonstrate the mesotendon (M). The anterior circumflex humeral artery (CH) gives off an ascending (a) and a descending branch (b). The ascending branch passes through the intertubercular sulcus and supplies mesotendon (M) and long biceps tendon (arrows).
I
Fig. 1. Ventral aspect of a right humerus. Arrows mark the course of the long biceps tendon in the intertubercular sulcus and around the head of the humerus. This part of the tendon was examined by immunohistochemical and histological methods.
76
After injection of indian ink-gelatine, the samples showed complete filling of the small peri- and intratendinous vessels in the intraarticular part of the tendon. The portion of the tendon adjacent to the capsule exhibited a continuous vascular network extending from the distal segment up to the supraglenoidal tubercle (Fig. 3 a). In contrast, most of the portion adjacent to the humeral head was devoid of blood vessels (Fig. 3 b). Proximally to the avascular zone vessels were seen only in the insertion zone of the tendon. The intratendinous vasculature could be most clearly observed in samples prepared according to Spalteholz (1914) (Fig. 3 c). Within the distal segment, the vessels were evenly distributed and orientated in parallel with collagen fibre bundles. Further proximally, where the tendon is adjacent to the intertubercular sulcus and the caput humeri, a complete dense network of small vessels was seen within the region adjacent to the capsule (Fig. 4 b). An intermediate central region contained only a few intratendinous vessels. The region immediately adjacent to the humerus was devoid of blood vessels. In all immunohistochemical samples incubated with antibodies against laminin, a brillant fluorescence was seen in the walls of major and minor vessels (Fig. 4 a). The topographical distribution of the vessels was comparable to that seen in the injection samples described above: In the proximal segment, peritendinous vessels were observed only in the region adjacent to the capsule Fig. 3 a, c). The region directly adjacent to the humerus appeared avascular (Fig. 4a, b).
Fig. 3 a, b. Long biceps tendon injected with indian-ink gelatine. a) A continuous network of vesselsin the part of the tendon facing the joint capsule. b) The sliding area is free of vessels. Vessels descend from the origin at the supraglenoid tubercle and penetrate the tendon (arrows). Ascending vessels reach the tendon from the musculartendinous connection (arrow-heads). c) Proximal part of the long biceps tendon injected with indian-ink gelatine (Spalteholz technique). Numerous anastomoses are found between the proximal (p) and distal (d) vessels.
b Fig. 4 a, b. Longitudinal median cuts from the sliding area of the long biceps tendon (s. Fig. 1). a) Demonstration of the basement membrane of blood vessels with an antibody against laminin. Vesselsare visible only in the part of the tendon facing the joint capsule. The sliding area is free of vessels. b) Arteries injected with indian-ink gelatine. Complete network of blood vessels in the part of the tendon facing the joint capsule, no visible vessels in the sliding area (*).
c 77
Histological obsenations The osseous intertubercular sulcus was found to be covered by connective and cartilagineous tissue. At the lateral wall of the sulcus loose connective tissue was observed. The medial wall was covered by tissue reminiscent of fibrous cartilage. In the proximal portion of the sulcus, where the sliding surface is in contact with the tendon, the osseous tissue was covered with fibrous cartilage. The histological appearance of the tendon varied within the individual segments. In the distal segment a typical traction tendon was seen over the whole cross section. In the proximal segment (s. Fig. I), the histological appearance varied (Fig. 5): Adjacent to the capsule, slender tenocytes were the only cells embedded between parallel bundles of collagen fibres giving it the typical appearance of a traction tendon (Fig. 5 b). In the centre and in the internal region directly adjacent to the humerus, the bundles of collagen fibres were arranged more irregularly and interwoven . Also the peritendineum was more voluminous than in the external region. The central region contained slender tenocytes and ovoid cells (Fig. 5 d). In the internal region adjacent to the humerus, most cells were of ovoid shape and reminiscent of chondrocytes (Fig. 5 e, f).
b
----
Ultrastructural obsenations In the region adjacent to the capsule, typical tenocytes with numerous slender processes were found (Fig. 6 b). Occasionally, small bundles of microfibrils were seen near the cell surface. The sulcus part contained tenocytes and ovoid cells (Fig. 6 a). These were either devoid of processes as described below; or they showed a few processes on one front only, whereas the cell body was smooth at the other front, which was covered by felt-like matrix. The sliding area of the tendon of the 27 year old female showed mainly ovoid cells devoid of processes, the cell bodies of which were covered by felt-like matrix (Fig. 7). Occasionally, microfibrils were embedded in the matrix. In the tendon of the 70 year old male, basically the same pattern was observed, although most of the cells were not covered by felt-like matrix.
f Fig. 5 a - f. Histologically investigated longitudinal sections from the area marked in Fig. I (Toluidine-blue). a) The part of the tendon facing the joint capsule is covered by synovial tissue that contains numerous vessels (x 240). b) The part of the biceps tendon facing the joint capsule has the structure of a traction-tendon with typical tenocytes (x 370). c) Ovoid cells are found in the internal peritendineum of the tendon's central part (x 370). d) In the tendinous tissue of the central part both typical tenocytes and ovoid cells are visible (x 370). e) The tendon's sliding area shows mainly chondroid cells (x 370). f) Only chondroid cells are observed at the sliding area (arrowheads) (x 370).
Discussion
the portion adjacent to the capsule, the tissue resembles a traction tendon. Where it is adjacent to the hypomochlion, it resembles a sliding tendon. At the sliding surface the tissue shows features of fibrous cartilage. The same applies to the slide bearing surface of the intertubercular sulcus.
The long biceps tendon shows structural variations along its course from its origin to the distal end of the intertubercular sulcus. These variations are thought to be governed by the prevailing biomechanical conditions: In
78
Fig. 6. Ovoid cell from the sliding area of the tendon of a 27 year old woman. A felt-like matrix (arrows) lies between cell and collagen fibrils (x 2 600). Inset: Typical tenocyte with many cytoplasmic processes ( x225OO).
The ultrastructural observation of chondrocyte-like cells in the biceps tendon is similar to the one on the tendon of the flexor digitorum muscle of the rabbit as re-
ported by Merrilees and Flint (1980). These authors also describe a felt-like matrix surrounding the ovoid cells. At present the biochemical structure of this matrix is un-
Fig. 7. Ovoid cell of the sliding area (arrowheads). The cell is surrounded by a felt-like matri x (arrows) (x 11500).
79
known, and its functional significance remains to be elucidated. In immunohistochemical preparations incubated with an antibody against laminin for visualization of blood vessels, the chondrocyte-like cells regularly showed a halo of immunopositive material. Whether or not the pericellular matrix indeed contains laminin and possibly other basement membrane constituents needs to be further investigated. Ploetz (1938) was the first to experimentally demonstrate the correlation between the varying structures of traction and sliding tendons and their functional differences. Altmann (1964)performed a biomechanical analysis on the same subject. According to the hypothesis of Pauwels (1960) of "Kausale Histogenese" the occurrence of fibrous cartilage within a sliding tendon can be explained by the prevailing intermittent compressive stress and the superimposed shear stress. In addition to the structural differences, there are also biochemical differences between the tension and the pressure zone of a sliding tendon with regard to proteoglycans (Vogel and Koob 1989). The significance of the intermittent compressive stress for the fibrous cartilage-like biochemical features of a sliding tendon has also been demonstrated in vitro (Koob et al. 1992). The present light and electron microscopic findings are in accordance with the stress distribution within the tendon where it is adjacent to the hypomochlion: The sliding surface bears a high compressive stress which decreases with distance from the hypomochlion. The reverse is true for the tension stress, which has a maximum in the external protion of the tendon and decreases towards the hypomochlion. Intratendinous blood vessels initially were not found within the sliding zone of the tendon. It appeared avascular when examined macroscopically in injected preparations. Upon microscopic inspection of samples treated according to Spalteholz (1914), however, it became evident that the sliding zone is hypovascular rather than being avascular. Only the sliding surface proved to be devoid of blood vessels. These observations were confirmed by immunohistochemical results. The present findings are not compatible with the mechanistic concept that movements in the shoulder joint lead to compression of blood vessels and to ischemia of the tendinous tissues (Rathbun and Macnab 1970; Macnab 1981, Keyl 1989). The hypo- and avascularity of the sliding zone of the tendon are related to structure. Vascular architecture represents a functional adaption to the stress of a sliding tendon. These results go along well with previous findings on the tendon of the supraspinatus muscle (Tillmann et al. 1991; Tillmann and Kolts 1993). The clinical significance of the present observations is that fibrous cartilage-like tissue is located just in that region where ruptures of the tendon most frequently occur. With respect to the pathogenesis of the ruptures rheological factors have to be taken into account: The resistance to traction-strain of sliding tendons is significantly lower than that of traction tendons.
References Altmann K (1964) Zur kausalen Histogenese des Knorpels. W. Roux's Theorie und experimentelle Wirklichkeit. Ergeb Anat Entwickl-Gesch 37: 1- 171 Jager W, Wirth CJ (1986) Praxis der Orthopadie. Thieme , Stuttgart New York Juskiewenski S, Vaysse P (1987) Arterial vascularization of the testes and surgery for undescended testicles. Anatomia elinica 1: 127- 134 Keyl W (1989) Pathologisch-anatomische Grundlagen von Verletzungen und Erkrankungen der Rotatorenmanschette und der langen Bizepssehnen. In : Resch H, Speme E, Beck E (Hrsg). Verletzungen und Erkrankungen des Schultergelenks . Hft z Unfallheilkd 206: 12-18 Koob TJ, Clark PE, Hernandez DJ, Thurmond FA, Vogel KG (1992) Compression loading in vitro regulates proteoglycan synthesis by tendon fibrocartilage. Arch Biochem Biophysics 298: 303- 312 Korn S, Schunke M (1989) Darstellung der Gefalle in der Ursprungssehne des Caput longum m. bicipitis brachii. Anat Anz 168: 70 Lindblom K (1939) On pathogenesis of ruptures of the tendon aponeurosis of the shoulder joint. Acta Radiol 20: 563- 577 Macnab I (1981) Die pathologische Grundlage der sogenannten Rotatorenmanschetten-Tendinitis. Orthopadie 10: 1991-1995 McKendry RJR, Uhthoff HK , Sarkar K, Hyslo PSG (1982) Calcifying tendinitis of the shoulder: prognostic value of clinical, histologic, and radiologic features in 57 surgically treated cases. J Rheumatol 9: 75 - 80 Merrilees MJ, Flint MH (1980) Ultrastructural study of tension and pressure zones in a rabbit flexor tendon. Am J Anat 157: 87 -106 Pauwels F (1960) Eine neue Theorie tiber den Einfluf3 mechanischer Reize auf die Differenzierung der Stutzgewebe. Zehnter Beitrag zur funktionellen Anatomie und kausalen Morphologie des Stutzapparates, Z Anat Entwickl-Gesch 121: 478 - 515 Ploetz E (1938) Funktioneller Bau und funktionelle Anpassung der Gleitsehnen. Z Orthop 67: 212 - 234 Rathbun JB, Macnab I (1970) The microvascular pattern of the rotator cuff. J Bone Joint Surg 52-B: 540-553 Refior HJ, Kroedel A, Melzer C (1987) Examinations of the pathology of the rotator cuff. Arch Orthop Trauma Surg 106: 301- 306 Reichelt A (1981) Beitrag zur operativen Therapie der Tendinosis calcarea der Schulter . Z Orthop 119: 21- 24 Spalteholz KW (1914) Uber das Durchsichtigmachen von menschlichen und tierischen Praparaten. 2. A. Hirzel, Leipzig Tillmann B, Thomas W (1982) Anatomie typischer Sehnenansatze, -ursprunge und Engpasse. Orthop Praxis 12: 910- 917 Tillmann B, Schunke M, Roddecker (1991) Struktur der Supraspinatusansatzsehne. Anat Anz 172: 82 - 83 Tillmann B, Kolts I (1993)Ruptur der Ursprungssehne des Caput longum musculi bicipitis brachii. Struktur und Blutversorgung der Bizepssehne. Operat Orthop Traumatol 5 (2): 107- 111 Uhthoff HK, Sarkar K, Maynard JA (1976) Calcifying tendinitis. A new concept of its pathogenesis . Clin Orthop 118: 164-168 Vogel KG, Koob TJ (1989) Structural specialization in tendons under compression. Intern. Rev. Cytol. 115: 267 - 293 Accepted July 20, 1993
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Of ANATOMY
=========
The structure and vascularization of the biceps brachii long head tendon* I. Kolts, B. Tfllmann! and R. Lullmann-Rauch! Department of Anatomy, University Tartu/Estland, and 'Department of Anatomy, Christian-Albrechts-University, OlshausenstraBe 40, D-24098 Kiel, Germany
Summary. In the present study we examined the structure and the blood supply of the long biceps tendon as well as the surface of the intertubercular sulcus, using tissue samples from children and adults. The applied methods were light and electron microscopy, immunohistochemistry, and arterial injection techniques. The tendon represents a sliding tendon with the inter tubercular sulcus and humeral head as hypomochlion. The parts facing the humerus show some ultrastructural features of fibrous cartilage, the ovoid chondrocyte-like cells of the tendon lying within felt-like matrix. In the opposite part adjacent to the capsule , the tendon resembles a traction tendon. The intertubercular sulcus is covered by fibrous cartilage. The tendon is supplied with arteries from three different sources. The density of intratendinous vessels in the traction zone is comparable to that of other tendons, while in the sliding zone it is markably decreased . The immediate vicinity of the sliding surface is avascular. Our findings show that the long biceps tendon is structurally adapted to both its functions as sliding and traction tendon. The blood supply seems to be related to the metabolic requirements of the different parts of the tendon.
Key words: Biceps tendon - Vascularization - Sliding tendon
Introduction Due to a rising amount of sporting activities, nowadays lesions of the shoulder region occur even in younger persons with increasing frequency . In about 30 % of the population older than 40 years pathological alterations of the shoulder joint are found. The frequency of alterations increases with aging (Reichelt 1981; McKendry et al. 1982; Refior et al. 1987). As far as the long biceps tendon is concerned, subluxations and luxations as well as partial or complete ruptures are observed in addition to tendosynovitis (Jager and Wirth 1986). Ruptures of the tendon are thought to occur on the basis of preceding degenerative lesions. These could be related (a) to the position of the tendon within the intertubercular sulcus (Tillmann and Thomas 1982) and at the humeral head, as well as (b) to the pattern of vascularization (Lindblom 1939; Uhthoff et al. 1976; Rathbun and Macnab 1970; Macnab 1981; KeyI1989). The present study was undertaken to contribute to the elucidation of the pathogenesis of lesions affecting the long biceps tendon. For this purpose, the following investigations were performed: Light and electron microscopic examination of the intertubercular sulcus and the tendon at defined segments; visualization of the vascular pattern by means of arterial injections and immunohistochemical demonstration of the vascular basement membranes.
Materials and methods • Dedicated to Professor Dr. med. Wolfgang Kuhnel on the occasion of his 60th birthday. Correspondence to : B. Tillmann
~I
Ann Anat (1994) 176: 75 - 80 Gustav Fischer Verlag lena
Arterial injections were performed on 10 unfixed shoulder joints of 10 male cadavers (aged 61 - 67 years). For histological investigations 22 tendons were used (16 from male cadavers, ages 14days to 82 years, and 6 from female cadavers, ages 27 to
trois to exclude artefacts due to unspecific binding of the antibody. Cryostat sections of human skin and liver were taken to verify the specific appearance of vessels in well vascularized tissues.
66 years). In 5 cases the intertubercular sulcus was also examined. For immunohistochemical investigations, tendons of 3 male cadavers (ages 7,22,72 years) were obtained 12 hours post mortem . Ultrastructural investigations were performed on tendons of one femal (27 years) and one male (70 years). Two different mixtures were used for arterial injection: (a) 10 % aqueous dispersion of Natur-Kautschuk stabilized with 0.7 % ammonia; (b) 5010 gelatine containing 0.5 010 (v/v) indian ink (Pelikan, Hannover, Germany). 300ml were injected simultaneously via the subclavian and the brachial arteries (Korn and Schunke 1989). After polymerization of the injection mixture, the tendon was removed and processed according to the method of Spalteholz (1914) as modified by luskiewenski and Vaysse (1987). For light microscopy, the segments of the tendon (Fig. 1) were fixed in phosphate-buffered paraformaldehyde (4 %) for 6 hours and embedded in glycolmethacrylate. Semithin sections (3llm) were stained with toluidine blue (0.1 %) at pH 5.0 in 0.1 M acetate buffer. For ultrastructural examination, the tissue samples were fixed in 3.5 % glutaraldehyde and processed according to routine methods. For immunohistochemical investigations, the unfixed tissue samples were incubated with 10 % sucrose in phosphate-buffered saline and frozen with liquid nitrogen. Cryostat sections (8 - 161lm) were cut in a cryostat and mounted on gelatinecoated slides. Rabbit anti -laminin (MEDAC, Hamburg/FRG) served as a specific antibody for the immunofluorescence technique. Sections were washed in phosphate-buffered saline (PBS, pH 7.2 -7.4). After incubation with the antibody (diluted I : 20, 45 min at room temperature in a moist chamber), the sections were rinsed three times with PBS. They were then incubated for 30 min with fluorescein isothiocyanate (FITC)conjugated anti-rabbit IgG (1 : 30), diluted with human serum (1 : 20), rinsed again three times with PBS and mounted with PBS/Glycerine (9 : 1 in 2.5 0J0 NaN ), pH 8.6). Sections incubated with FITC-conjugated antibodies alone served as con-
I ,
Results Vasculature The long biceps tendon is supplied by arteries from three different sources: The distal portion by branches of the brachial and deep brachial artery, the proximal portion additionally by branches of the anterior circumflex humeral artery (Fig. 2). In the intertubercular sulcus a branch of this artery gives rise to two smaller branches running in cranial and caudal directions. The cranial branch provides small vessels which reach the proximal segment of the tendon and its synovial sheath.
Fig. 2. Latex-injection preparation. Right shoulder of a 63 year old man. The long biceps tendon (B) is visible after incision of the coraco-acromial ligament (LCA) and the joint capsule (C) in the rotator intervall (RI). The tendon was dislocated anteriorly to the intertubercular sulcus to demonstrate the mesotendon (M). The anterior circumflex humeral artery (CH) gives off an ascending (a) and a descending branch (b). The ascending branch passes through the intertubercular sulcus and supplies mesotendon (M) and long biceps tendon (arrows).
I
Fig. 1. Ventral aspect of a right humerus. Arrows mark the course of the long biceps tendon in the intertubercular sulcus and around the head of the humerus. This part of the tendon was examined by immunohistochemical and histological methods.
76
After injection of indian ink-gelatine, the samples showed complete filling of the small peri- and intratendinous vessels in the intraarticular part of the tendon. The portion of the tendon adjacent to the capsule exhibited a continuous vascular network extending from the distal segment up to the supraglenoidal tubercle (Fig. 3 a). In contrast, most of the portion adjacent to the humeral head was devoid of blood vessels (Fig. 3 b). Proximally to the avascular zone vessels were seen only in the insertion zone of the tendon. The intratendinous vasculature could be most clearly observed in samples prepared according to Spalteholz (1914) (Fig. 3 c). Within the distal segment, the vessels were evenly distributed and orientated in parallel with collagen fibre bundles. Further proximally, where the tendon is adjacent to the intertubercular sulcus and the caput humeri, a complete dense network of small vessels was seen within the region adjacent to the capsule (Fig. 4 b). An intermediate central region contained only a few intratendinous vessels. The region immediately adjacent to the humerus was devoid of blood vessels. In all immunohistochemical samples incubated with antibodies against laminin, a brillant fluorescence was seen in the walls of major and minor vessels (Fig. 4 a). The topographical distribution of the vessels was comparable to that seen in the injection samples described above: In the proximal segment, peritendinous vessels were observed only in the region adjacent to the capsule Fig. 3 a, c). The region directly adjacent to the humerus appeared avascular (Fig. 4a, b).
Fig. 3 a, b. Long biceps tendon injected with indian-ink gelatine. a) A continuous network of vesselsin the part of the tendon facing the joint capsule. b) The sliding area is free of vessels. Vessels descend from the origin at the supraglenoid tubercle and penetrate the tendon (arrows). Ascending vessels reach the tendon from the musculartendinous connection (arrow-heads). c) Proximal part of the long biceps tendon injected with indian-ink gelatine (Spalteholz technique). Numerous anastomoses are found between the proximal (p) and distal (d) vessels.
b Fig. 4 a, b. Longitudinal median cuts from the sliding area of the long biceps tendon (s. Fig. 1). a) Demonstration of the basement membrane of blood vessels with an antibody against laminin. Vesselsare visible only in the part of the tendon facing the joint capsule. The sliding area is free of vessels. b) Arteries injected with indian-ink gelatine. Complete network of blood vessels in the part of the tendon facing the joint capsule, no visible vessels in the sliding area (*).
c 77
Histological obsenations The osseous intertubercular sulcus was found to be covered by connective and cartilagineous tissue. At the lateral wall of the sulcus loose connective tissue was observed. The medial wall was covered by tissue reminiscent of fibrous cartilage. In the proximal portion of the sulcus, where the sliding surface is in contact with the tendon, the osseous tissue was covered with fibrous cartilage. The histological appearance of the tendon varied within the individual segments. In the distal segment a typical traction tendon was seen over the whole cross section. In the proximal segment (s. Fig. I), the histological appearance varied (Fig. 5): Adjacent to the capsule, slender tenocytes were the only cells embedded between parallel bundles of collagen fibres giving it the typical appearance of a traction tendon (Fig. 5 b). In the centre and in the internal region directly adjacent to the humerus, the bundles of collagen fibres were arranged more irregularly and interwoven . Also the peritendineum was more voluminous than in the external region. The central region contained slender tenocytes and ovoid cells (Fig. 5 d). In the internal region adjacent to the humerus, most cells were of ovoid shape and reminiscent of chondrocytes (Fig. 5 e, f).
b
----
Ultrastructural obsenations In the region adjacent to the capsule, typical tenocytes with numerous slender processes were found (Fig. 6 b). Occasionally, small bundles of microfibrils were seen near the cell surface. The sulcus part contained tenocytes and ovoid cells (Fig. 6 a). These were either devoid of processes as described below; or they showed a few processes on one front only, whereas the cell body was smooth at the other front, which was covered by felt-like matrix. The sliding area of the tendon of the 27 year old female showed mainly ovoid cells devoid of processes, the cell bodies of which were covered by felt-like matrix (Fig. 7). Occasionally, microfibrils were embedded in the matrix. In the tendon of the 70 year old male, basically the same pattern was observed, although most of the cells were not covered by felt-like matrix.
f Fig. 5 a - f. Histologically investigated longitudinal sections from the area marked in Fig. I (Toluidine-blue). a) The part of the tendon facing the joint capsule is covered by synovial tissue that contains numerous vessels (x 240). b) The part of the biceps tendon facing the joint capsule has the structure of a traction-tendon with typical tenocytes (x 370). c) Ovoid cells are found in the internal peritendineum of the tendon's central part (x 370). d) In the tendinous tissue of the central part both typical tenocytes and ovoid cells are visible (x 370). e) The tendon's sliding area shows mainly chondroid cells (x 370). f) Only chondroid cells are observed at the sliding area (arrowheads) (x 370).
Discussion
the portion adjacent to the capsule, the tissue resembles a traction tendon. Where it is adjacent to the hypomochlion, it resembles a sliding tendon. At the sliding surface the tissue shows features of fibrous cartilage. The same applies to the slide bearing surface of the intertubercular sulcus.
The long biceps tendon shows structural variations along its course from its origin to the distal end of the intertubercular sulcus. These variations are thought to be governed by the prevailing biomechanical conditions: In
78
Fig. 6. Ovoid cell from the sliding area of the tendon of a 27 year old woman. A felt-like matrix (arrows) lies between cell and collagen fibrils (x 2 600). Inset: Typical tenocyte with many cytoplasmic processes ( x225OO).
The ultrastructural observation of chondrocyte-like cells in the biceps tendon is similar to the one on the tendon of the flexor digitorum muscle of the rabbit as re-
ported by Merrilees and Flint (1980). These authors also describe a felt-like matrix surrounding the ovoid cells. At present the biochemical structure of this matrix is un-
Fig. 7. Ovoid cell of the sliding area (arrowheads). The cell is surrounded by a felt-like matri x (arrows) (x 11500).
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known, and its functional significance remains to be elucidated. In immunohistochemical preparations incubated with an antibody against laminin for visualization of blood vessels, the chondrocyte-like cells regularly showed a halo of immunopositive material. Whether or not the pericellular matrix indeed contains laminin and possibly other basement membrane constituents needs to be further investigated. Ploetz (1938) was the first to experimentally demonstrate the correlation between the varying structures of traction and sliding tendons and their functional differences. Altmann (1964)performed a biomechanical analysis on the same subject. According to the hypothesis of Pauwels (1960) of "Kausale Histogenese" the occurrence of fibrous cartilage within a sliding tendon can be explained by the prevailing intermittent compressive stress and the superimposed shear stress. In addition to the structural differences, there are also biochemical differences between the tension and the pressure zone of a sliding tendon with regard to proteoglycans (Vogel and Koob 1989). The significance of the intermittent compressive stress for the fibrous cartilage-like biochemical features of a sliding tendon has also been demonstrated in vitro (Koob et al. 1992). The present light and electron microscopic findings are in accordance with the stress distribution within the tendon where it is adjacent to the hypomochlion: The sliding surface bears a high compressive stress which decreases with distance from the hypomochlion. The reverse is true for the tension stress, which has a maximum in the external protion of the tendon and decreases towards the hypomochlion. Intratendinous blood vessels initially were not found within the sliding zone of the tendon. It appeared avascular when examined macroscopically in injected preparations. Upon microscopic inspection of samples treated according to Spalteholz (1914), however, it became evident that the sliding zone is hypovascular rather than being avascular. Only the sliding surface proved to be devoid of blood vessels. These observations were confirmed by immunohistochemical results. The present findings are not compatible with the mechanistic concept that movements in the shoulder joint lead to compression of blood vessels and to ischemia of the tendinous tissues (Rathbun and Macnab 1970; Macnab 1981, Keyl 1989). The hypo- and avascularity of the sliding zone of the tendon are related to structure. Vascular architecture represents a functional adaption to the stress of a sliding tendon. These results go along well with previous findings on the tendon of the supraspinatus muscle (Tillmann et al. 1991; Tillmann and Kolts 1993). The clinical significance of the present observations is that fibrous cartilage-like tissue is located just in that region where ruptures of the tendon most frequently occur. With respect to the pathogenesis of the ruptures rheological factors have to be taken into account: The resistance to traction-strain of sliding tendons is significantly lower than that of traction tendons.
References Altmann K (1964) Zur kausalen Histogenese des Knorpels. W. Roux's Theorie und experimentelle Wirklichkeit. Ergeb Anat Entwickl-Gesch 37: 1- 171 Jager W, Wirth CJ (1986) Praxis der Orthopadie. Thieme , Stuttgart New York Juskiewenski S, Vaysse P (1987) Arterial vascularization of the testes and surgery for undescended testicles. Anatomia elinica 1: 127- 134 Keyl W (1989) Pathologisch-anatomische Grundlagen von Verletzungen und Erkrankungen der Rotatorenmanschette und der langen Bizepssehnen. In : Resch H, Speme E, Beck E (Hrsg). Verletzungen und Erkrankungen des Schultergelenks . Hft z Unfallheilkd 206: 12-18 Koob TJ, Clark PE, Hernandez DJ, Thurmond FA, Vogel KG (1992) Compression loading in vitro regulates proteoglycan synthesis by tendon fibrocartilage. Arch Biochem Biophysics 298: 303- 312 Korn S, Schunke M (1989) Darstellung der Gefalle in der Ursprungssehne des Caput longum m. bicipitis brachii. Anat Anz 168: 70 Lindblom K (1939) On pathogenesis of ruptures of the tendon aponeurosis of the shoulder joint. Acta Radiol 20: 563- 577 Macnab I (1981) Die pathologische Grundlage der sogenannten Rotatorenmanschetten-Tendinitis. Orthopadie 10: 1991-1995 McKendry RJR, Uhthoff HK , Sarkar K, Hyslo PSG (1982) Calcifying tendinitis of the shoulder: prognostic value of clinical, histologic, and radiologic features in 57 surgically treated cases. J Rheumatol 9: 75 - 80 Merrilees MJ, Flint MH (1980) Ultrastructural study of tension and pressure zones in a rabbit flexor tendon. Am J Anat 157: 87 -106 Pauwels F (1960) Eine neue Theorie tiber den Einfluf3 mechanischer Reize auf die Differenzierung der Stutzgewebe. Zehnter Beitrag zur funktionellen Anatomie und kausalen Morphologie des Stutzapparates, Z Anat Entwickl-Gesch 121: 478 - 515 Ploetz E (1938) Funktioneller Bau und funktionelle Anpassung der Gleitsehnen. Z Orthop 67: 212 - 234 Rathbun JB, Macnab I (1970) The microvascular pattern of the rotator cuff. J Bone Joint Surg 52-B: 540-553 Refior HJ, Kroedel A, Melzer C (1987) Examinations of the pathology of the rotator cuff. Arch Orthop Trauma Surg 106: 301- 306 Reichelt A (1981) Beitrag zur operativen Therapie der Tendinosis calcarea der Schulter . Z Orthop 119: 21- 24 Spalteholz KW (1914) Uber das Durchsichtigmachen von menschlichen und tierischen Praparaten. 2. A. Hirzel, Leipzig Tillmann B, Thomas W (1982) Anatomie typischer Sehnenansatze, -ursprunge und Engpasse. Orthop Praxis 12: 910- 917 Tillmann B, Schunke M, Roddecker (1991) Struktur der Supraspinatusansatzsehne. Anat Anz 172: 82 - 83 Tillmann B, Kolts I (1993)Ruptur der Ursprungssehne des Caput longum musculi bicipitis brachii. Struktur und Blutversorgung der Bizepssehne. Operat Orthop Traumatol 5 (2): 107- 111 Uhthoff HK, Sarkar K, Maynard JA (1976) Calcifying tendinitis. A new concept of its pathogenesis . Clin Orthop 118: 164-168 Vogel KG, Koob TJ (1989) Structural specialization in tendons under compression. Intern. Rev. Cytol. 115: 267 - 293 Accepted July 20, 1993
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