447
J. Anat. (1992) 181, pp. 447-453, with 11 figures Printed in Great Britain
Blood supply of the articular disc of the antebrachiocarpal joint in dogs Z. Dj. MIKIC Orthopaedic and Traumatology Clinic, Faculty of Medicine, Novi Sad, Yugoslavia (Accepted 11 September 1992)
ABSTRACT
The normal vascular anatomy of the articular disc of 48 antebrachiocarpal joints was studied in 24 dogs (12 puppies and 12 adult animals) using an India ink vascular injection technique. It was found that the articular disc receives its blood supply mainly from the palmar and dorsal branches of the palmar interosseous artery. Branches of these 2 arteries arborise and give direct peridiscal vessels to the dorsal, proximal and palmar sides of the articular disc. The peridiscal vessels ramify and anastomose with one another to form a cup-shaped terminal peridiscal capillary plexus around the disc which ends at the peripheral parts of the disc in a series of terminal capillary loops. This leaves the major central segment of the disc without blood vessels. The proportion of vascularised to nonvascularised areas of the disc depends upon the age of the animals. In young puppies, the degree of vascular penetration into the disc is quite extensive, while in adult animals it ranges from 15 to 25 % of the discal width; the considerably larger central area of the articular disc is thus avascular.
INTRODUCTION
Knowledge concerning the articular disc of the antebrachiocarpal joint (AC joint) in dogs is at present limited (Corner, 1898; Henschel, 1973; Mikic et al. 1992). Little information is available as to its vascularity and only some general information on the origin of the blood supply can be found in standard textbooks of veterinary anatomy (Kadletz, 1932; Evans & Christensen, 1979; Nickel et al. 1986). The vascular anatomy of the intra-articular discs and menisci in general was reviewed by Davies & Edwards (1948) and Barnett et al. (1961). Several studies on the vascularity of the knee menisci were also undertaken both in man (Scapinelli, 1968; Sick & Koritke, 1969; Danzig et al. 1981; Arnoczky & Waren, 1982) and in dogs (Bengin et al. 1978; Tirgari, 1978; Arnoczky et al. 1981; Mikic et al. 1987). Recently, 2 reports on the microvasculature of the articular disc of the human distal radioulnar joint have been published (ThiruPathi et al. 1986; Mikic, 1992). As the vascular anatomy of the articular disc of the AC joint in dogs has not yet been investigated and as dogs are frequently used in experimental orthopaedic
surgery, the present study was undertaken to explore and describe the pattern of the blood supply to this structure and to compare it with the microvasculature of the articular disc of the human distal radioulnar joint. MATERIAL AND METHODS
Twenty-four mongrel dogs of both sexes (12 puppies aged 7-30 d and 12 young adult animals) with 48 joints were examined. The animals were killed by an overdose of barbiturate. Both forelimbs were amputated through the shoulder joint and the brachial artery was exposed. A polyethylene catheter with an inner diameter of 0.5 mm in puppies and 1-2 mm in adult animals was inserted into the artery which was then injected with an India ink suspension in 10 % formalin (equal parts India ink and 10 % formalin) using a large syringe under constant manual pressure. The injection was terminated when blackening of the outflow occurred at an incision made over the palmar aspect of the distal phalanx of the third digit. The injected limbs were fixed in 10% formalin for at least 5 d. The arterial origins and then the vascular
Correspondence to Professor Zelimir Dj. Mikic, Medicinski fakultet, Hajduk Veljkova 1, 21000 Novi Sad, Yugoslavia.
448
Z. Dj. Mikic'
-;'
*
*!@D
,.1 ....,
i;.*
Fig. 1. Macroscopic appearance of an injected specimen of the ulnar part of the antebrachial articular surface of the AC joint in a dog. The articular disc (AD) with its radial extension (RE) is situated between the radius (R) and ulna (U), and the palmar ulnocarpal ligament (UCL) is situated beneath the disc. The subsynovial plexus injected with the India ink can be seen on the dorsal edge of the radial extension.
supply to the articular disc itself were studied first by gross dissection. The forearm arteries were isolated and dissected down to the level of the wrist; the AC joints were opened and the vascularity of the disc was examined. Subsequently, the distal portions of the radius and ulna together with the disc were decalcified in 10% formic acid at room temperature. The specimens were divided into 3 groups, half being taken from puppies and half from adult animals. In 20 specimens, the discs and the adjacent ulna and radius were cleared as a whole using the Spalteholz technique (Crock, 1967). Twenty other specimens were sectioned serially into radioulnar and dorsopalmar planes at 50 and 100 gm and processed for tissue clearing. All cleared specimens were studied by a dissecting microscope. Eight discs were embedded in paraffin wax and 5-7 gm sections were cut in radioulnar and dorsopalmar planes, stained with haematoxylin and eosin and examined by light microscopy. RESULTS
For orientation purposes the articular disc of the antebrachiocarpal joint in dogs is interposed between the most inferior parts of the radius and ulna and, when viewed from the carpal side, has a triangular shape (Fig. 1). The base of the triangle is situated on the dorsal edge of the antebrachial surface, and the apex on the palmar side of the joint. There is a radial extension of the disc at its dorsal base. Proximally, the disc tissue fills the gap between the radius and ulna up to the distal radioulnar joint. The dorsal edge of the
disc is covered by the capsule of the joint which is slightly thickened by the dorsal radioulnar ligament, while the palmar apex, although covered by the synovium, is relatively free. No volar radioulnar ligament could be found (Mikic et al. 1992). The arterial supply to the articular disc of the AC joint in dogs originates predominantly from the palmar interosseous artery, a branch of the common interosseous artery. The palmar interosseous artery, just proximal to the distal radioulnar joint, bifurcates into a larger palmar and a smaller dorsal branch (Fig. 2), running over the palmar and dorsal aspects of the AC joint and its articular disc and terminating in the rete carpi palmare et dorsale. Branches of these 2 arteries arborise on the palmar, proximal and dorsal sides of the articular disc and then penetrate the capsule to supply the disc directly (Fig. 3). These socalled peridiscal vessels ramify and form an anastomotic capillary network around the disc which ends at the peripheral parts of the disc in a series of small terminal capillary loops oriented towards the centre of the disc (Fig. 3). Two types of terminal capillary plexus could be differentiated. First, a subsynovial plexus extending within the synovial membrane which covers both the dorsal peripheral border of the disc and its radial extension where it has an elongated comb-like appearance (Fig. 4). The other type is located on the palmar corner of the disc where it has a triangular shape (Fig. 5). These networks are superficial and clearly visible on the carpal surface of the disc of an injected specimen prior to clearing. Secondly, centrodiscal or intradiscal plexi penetrate
Blood supply of articular disc in dogs
449
Fig. 2. Bifurcation of the palmar interosseous artery (IA) into dorsal (D) and palmar (P) branches viewed from the ulnar side. The vessels injected with India ink are on the distal end of the radius (R). x 3.
Fig. 3. Distal end of the radius of an adult animal with the articular disc (AD) and blood vessels injected with India ink sectioned in a dorsopalmar plane. The dorsal branch (D) of the palmar interosseous artery ramifies on the dorsal and proximal sides of the articular disc forming a terminal vascular network around it. Note that only the peripheral part of the disc is vascularised while the major central part is avascular. The arrows indicate the carpal surface of the disc which is also avascular. Spalteholz, x 5.
AD Fig. 4. Carpal surface of the articular disc (AD) of a specimen perfused with India ink showing the at the dorsal margin which ends with a series of terminal capillary loops. S, synovium. x 20.
subsynovial terminal capillary plexus
450
Z. Dj. Mikic'
/
Fig. 5. Carpal aspect of the palmar corner of the same articular disc as in Figure 3 showing a triangular-shaped subsynovial terminal plexus and its looped capillaries (arrows). S, synovium; U, ulnar articular cartilage; R, radial articular cartilage. x 20.
4
Fig. 6. Dorsopalmar sagittal section of an articular disc (AD) showing the centrodiscal terminal capillary plexus injected with India ink at its proximal side. The looped capillaries penetrate into the discal stroma. Detail from Figure 3. Spalteholz, x 12.
the deeper parts of the discal stroma on its dorsal, proximal and palmar sides (Figs 3, 6). These vessels arborise for a short distance and terminate as looped capillaries between the bundles of the collagen fibres at the peripheral area of the disc (Figs 6, 7, 8), which
Fig. 7. Transverse section of the peripheral part of an articular disc demonstrating the presence of the vessels (black spots) injected with India ink within the synovial membrane (S) and within the peripheral area of the discal stroma (arrows). More central parts of the disc are avascular. Haematoxylin and eosin, x 40.
was confirmed both by tissue clearing and by histological studies (Figs 6, 7, 8). The terminal capillary loops were found to be of differing appearance and calibre (Figs 4, 5, 6, 8), although their basic pattern was always similar. However, a number of loops with an arteriovenous (AV) shunt was also observed (Fig. 8b). In general, the major central portion of the disc was found to be avascular (Fig. 3). The free carpal surface except for its dorsal margin and palmar corner (Figs 4, 5) and all the attachments of the disc to bones were also found to be avascular. Only the peripheral parts on the dorsal, proximal and palmar sides were vascular, this consisting of an anastomotic, cupshaped vascular network (Fig. 3), ending inwardly with a series of looped capillaries. The width of the vascularised zone depended on the age of the animals. In very young puppies the degree of vascular penetration into the disc was quite extensive and sometimes the discs appeared to be completely vascularised (Fig. 9), although the plexi from dorsal and palmar sides were never found to anastomose between themselves and a central avascular zone could always be observed (Fig. 10). In adult animals
Blood supply of articular disc in dogs
451
4;.
.
Fig. 8. Terminal capillary loops found in the articular disc stroma of a puppy aged 2 months. (a) Typical looped capillary located between the wavelike bundles of collagen fibres of the disc fibrocartilaginous tissue; (b) terminal capillary loop with an arteriovenous shunt (arrows) surrounded by the fibrocartilaginous tissue. Haematoxylin and eosin, x 400.
Fig. 9. Section in the radioulnar plane of the ulna (U), articular disc (AD) and radius (R) of a puppy aged 7 days. The disc appears to be completely vascularised. Note the sinusoidal vessels of the cartilaginous radius and ulna and also the difference between the vasculature of the palmar ulnocarpal ligament (PUL) and the disc. Spalteholz, x 5.
the degree of vascular penetration ranged from 15 to 25 % of the discal width, so that the considerably larger central area of the disc was found always to be avascular (Figs 3, 11). DISCUSSION
The results of this study clearly demonstrate that the vascular supply to the articular disc of the AC joint in dogs is very similar to that seen in other intra-articular fibrocartilaginous structures both in man (Davies & Edwards, 1948; Barnett et al. 1961; Scapinelli, 1968; Sick & Koritke, 1969; Danzig et al. 1981; Arnoczky & Waren, 1982; Thiru-Pathi et al. 1986; Mikic, 1992)
and in dogs (Bengin et al. 1978; Tirgari, 1978; Arnoczky et al. 1981; Mikic et al. 1987). As in man (Mikic, 1992), the articular disc of the AC joint in dogs mainly receives its blood supply from the palmar and dorsal branches of the palmar interosseous artery, and the contribution of the radial and ulnar arteries through the rete carpi palmare et dorsale is considerably less important. Smaller branches of these 2 arteries, the peridiscal vessels, which resemble very clearly the perimeniscal vessels of Policard (1936), form an anastomotic capillary network around the disc. This network is obviously terminal since it gives rise to smaller branches which penetrate the periphery of the disc where they end in
452
Z. Dj. Mikic
Fig. 10. Detail from the central part of the disc of the same specimen as in Figure 9. The vascular network from the dorsal (D) and palmar (P) sides, although very close, does not anastomose and the central part of the disc, indicated by arrows, is avascular. x 20.
;'
*
x4
.L
Fig. I11. Section in the radioulnar plane of the radius (R), articular disc (AD) and ulna (U) of an adult animal. The most avascular articular disc is located between the well vascularised osseous parts of the radius and ulna. The dorsal margin and palmar corner of the disc are also vascularised. Note the typical ligamentous type of vasculature of the palmar ulnocarpal ligament (PUL).
a series of terminal looped capillaries. This pattern of vascularity, which is very similar to that found in man (Thiru-Pathi et al. 1986; Mikic, 1992) is comparable with the arrangement of the 'circulus articuli vasculosus' described by Hunter (1743) and Toynbee (1841). An interesting finding in this study was the occasional appearance of a particular type of the terminal capillary loop with an AV shunt (Fig. 8b) which has also been observed in dog knee menisci (Mikic et al. 1987). This specialised vessel which permits extracapillary circulation was described by Kupriianov (1965) and Sorokin (1973) as characteristic of the terminal plexus at the border between the vascular and avascular zones in various tissues. The exact role and significance of this arrangement is not clear. The apparent age-related variations in disc vascularity between the puppies and the adult animals observed in this study were in accordance with findings in other studies of intra-articular fibrocartilaginous structures (Davies & Edwards, 1948; Bengin et al. 1978; Thiru-Pathi et al. 1986; Mikic et al. 1987; Mikic, 1992). While the vascularity of the disc in newborn animals is very extensive during the postnatal period of growth of the disc, a progressive regression of vascularity seems to occur with age, and in adult animals a definite large central avascular zone is formed. There seems to be no further regression of vascularity beyond this point. No degenerative changes in the avascular zone of the adult dogs have been noted macroscopically, possibly because only young adult animals were investigated. The microvascular anatomy of the articular disc of the AC joint in dogs in this study seems to be typical of intra-articular fibrocartilaginous discs and menisci in general (Davies & Edwards, 1948; Barnett et al. 1961) and is quite different from the vascular arrangement in ligaments (Barnett et al. 1961; Mikic et al. 1987). This is a further reason to consider the articular disc of the AC joint in dogs as an intraarticular fibrocartilaginous disc and as a homologue to the articular disc of the human distal radioulnar joint (Mikic et al. 1992), even though this contradicts the opinion of some authors who regard it as a radioulnar ligament (Henschel, 1973). REFERENCES
ARNOCZKY SP, TARvIN GP, WAREN RF (1981) The microvasculature of the meniscus and its response to injury. An experimental study in the dog. Transactions of the Orthopaedic Research Society 6, 177. ARNOCZKY SP, WAREN RF (1982) Microvasculature of the human meniscus. American Journal of Sports Medicine 10, 90-95.
Blood supply of articular disc in dogs BARNETT CH, DAVIES DV, MACCONAILL MA (1961) Synovial Joints. Their Structure and Mechanics. London: Longmans, Green. BENGIN B, OBRADOVIC D, MIKIC Z (1978) Blood supply of the knee menisci in dogs. Folia Anatomica lugoslavica 7, 159-166. CORNER EM (1898) The morphology of the triangular cartilage. Journal of Anatomy and Physiology 12, 272-277. CROCK HW (1967) The Blood Supply of the Lower Limb Bones in Man. Edinburgh: Livingstone. DANZIG L, GoNSALVES MR, RESNICK D (1981) Human meniscal blood supply. Transactions of the Orthopaedic Research Society 6, 338. DAVIES DV, EDWARDS DAW (1948) The blood supply of the synovial membrane and intraarticular structures. Annals of the Royal College of Surgeons of England 2, 142-156. EVANS H, CHRISTENSEN G (1979) Miller's Anatomy of the Dog. Philadelphia: W. B. Saunders. HENSCHEL E (1973) Funktion und vergleichend-anatomische Bedeutung des Lig. radioulnare des Karnivoren. Anatomischer Anzeiger 133, 445-449. HUNTER W (1743) Of the structure and diseases of articulating cartilages. Philosophical Transactions of the Royal Society of London 42, 514-521. KADLETZ M (1932) Anatomischer Atlas der Extremitdtengelenke von Pferd und Hund. Berlin, Vienna: Urban-Schwarzenberg. KUPRIIANOV W (1965) Morfologiceskie osnovi Mikrocirkuljacii. Moscow: Vtoroi Moskovskii gosudarstvenii medicinskii institut imeni M. N. Pirogova. MIKIC ZDi (1992) The blood supply of the human distal radioulnar
453 joint and the microvasculature of its articular disc. Clinical Orthopaedics and Related Research 275, 19-28. MIKIC Z, ERCEGAN G, SOMER LJ, SOMER T, VUKADINOVId S (1987) Experimental Surgery of the Knee Joint in the Dog. Novi Sad: Drustvo lekara Vojvodine. MIKIC ZDJ, ERCEGAN G, SOMER T (1992) Detailed anatomy of the antebrachiocarpal joint in dogs. Anatomical Record 233, 329-334. NICKEL R, SCHUMMER A, SEIFERLE E (1986) Lehrbuch der Anatomie der Haustiere. Berlin, Hamburg: Paul Parey. POLICARD A (1936) Physiologie Geinerale des Articulations az rEtat Normal et Pathologique. Paris: Masson. SCAPINELLI R (1968) Studies on the vasculature of the human knee joint. Acta Anatomica 70, 305-331. SICK H, KORITKE JG (1969) La vascularisation des menisques de I'articulation du genou. Zeitschrift fur Anatomie und Entwicklungsgeschichte 129, 359-379. SOROKIN AP (1973) Obscie Zakonomernosti Stroienia Opornogo Aparata Celoveka. Moscow: Medicina. THIRU-PATHI RG, FERLIC DC, CLAYTON ML, MCCLURE DC (1986) Arterial anatomy of the triangular fibrocartilage of the wrist and its surgical significance. Journal of Hand Surgery 11A, 258-263. TIRGARI M (1978) The surgical significance of the blood supply of the canine stifle joint. Journal of Small Animal Practice 19, 451-462. TOYNBEE J (1841) Researches tending to prove the non-vascularity and the peculiar uniform mode of organisation and nutrition of certain animal tissues. Philosophical Transactions of the Royal Society of London 131, 159-192.
J. Anat. (1992) 181, pp. 447-453, with 11 figures Printed in Great Britain
Blood supply of the articular disc of the antebrachiocarpal joint in dogs Z. Dj. MIKIC Orthopaedic and Traumatology Clinic, Faculty of Medicine, Novi Sad, Yugoslavia (Accepted 11 September 1992)
ABSTRACT
The normal vascular anatomy of the articular disc of 48 antebrachiocarpal joints was studied in 24 dogs (12 puppies and 12 adult animals) using an India ink vascular injection technique. It was found that the articular disc receives its blood supply mainly from the palmar and dorsal branches of the palmar interosseous artery. Branches of these 2 arteries arborise and give direct peridiscal vessels to the dorsal, proximal and palmar sides of the articular disc. The peridiscal vessels ramify and anastomose with one another to form a cup-shaped terminal peridiscal capillary plexus around the disc which ends at the peripheral parts of the disc in a series of terminal capillary loops. This leaves the major central segment of the disc without blood vessels. The proportion of vascularised to nonvascularised areas of the disc depends upon the age of the animals. In young puppies, the degree of vascular penetration into the disc is quite extensive, while in adult animals it ranges from 15 to 25 % of the discal width; the considerably larger central area of the articular disc is thus avascular.
INTRODUCTION
Knowledge concerning the articular disc of the antebrachiocarpal joint (AC joint) in dogs is at present limited (Corner, 1898; Henschel, 1973; Mikic et al. 1992). Little information is available as to its vascularity and only some general information on the origin of the blood supply can be found in standard textbooks of veterinary anatomy (Kadletz, 1932; Evans & Christensen, 1979; Nickel et al. 1986). The vascular anatomy of the intra-articular discs and menisci in general was reviewed by Davies & Edwards (1948) and Barnett et al. (1961). Several studies on the vascularity of the knee menisci were also undertaken both in man (Scapinelli, 1968; Sick & Koritke, 1969; Danzig et al. 1981; Arnoczky & Waren, 1982) and in dogs (Bengin et al. 1978; Tirgari, 1978; Arnoczky et al. 1981; Mikic et al. 1987). Recently, 2 reports on the microvasculature of the articular disc of the human distal radioulnar joint have been published (ThiruPathi et al. 1986; Mikic, 1992). As the vascular anatomy of the articular disc of the AC joint in dogs has not yet been investigated and as dogs are frequently used in experimental orthopaedic
surgery, the present study was undertaken to explore and describe the pattern of the blood supply to this structure and to compare it with the microvasculature of the articular disc of the human distal radioulnar joint. MATERIAL AND METHODS
Twenty-four mongrel dogs of both sexes (12 puppies aged 7-30 d and 12 young adult animals) with 48 joints were examined. The animals were killed by an overdose of barbiturate. Both forelimbs were amputated through the shoulder joint and the brachial artery was exposed. A polyethylene catheter with an inner diameter of 0.5 mm in puppies and 1-2 mm in adult animals was inserted into the artery which was then injected with an India ink suspension in 10 % formalin (equal parts India ink and 10 % formalin) using a large syringe under constant manual pressure. The injection was terminated when blackening of the outflow occurred at an incision made over the palmar aspect of the distal phalanx of the third digit. The injected limbs were fixed in 10% formalin for at least 5 d. The arterial origins and then the vascular
Correspondence to Professor Zelimir Dj. Mikic, Medicinski fakultet, Hajduk Veljkova 1, 21000 Novi Sad, Yugoslavia.
448
Z. Dj. Mikic'
-;'
*
*!@D
,.1 ....,
i;.*
Fig. 1. Macroscopic appearance of an injected specimen of the ulnar part of the antebrachial articular surface of the AC joint in a dog. The articular disc (AD) with its radial extension (RE) is situated between the radius (R) and ulna (U), and the palmar ulnocarpal ligament (UCL) is situated beneath the disc. The subsynovial plexus injected with the India ink can be seen on the dorsal edge of the radial extension.
supply to the articular disc itself were studied first by gross dissection. The forearm arteries were isolated and dissected down to the level of the wrist; the AC joints were opened and the vascularity of the disc was examined. Subsequently, the distal portions of the radius and ulna together with the disc were decalcified in 10% formic acid at room temperature. The specimens were divided into 3 groups, half being taken from puppies and half from adult animals. In 20 specimens, the discs and the adjacent ulna and radius were cleared as a whole using the Spalteholz technique (Crock, 1967). Twenty other specimens were sectioned serially into radioulnar and dorsopalmar planes at 50 and 100 gm and processed for tissue clearing. All cleared specimens were studied by a dissecting microscope. Eight discs were embedded in paraffin wax and 5-7 gm sections were cut in radioulnar and dorsopalmar planes, stained with haematoxylin and eosin and examined by light microscopy. RESULTS
For orientation purposes the articular disc of the antebrachiocarpal joint in dogs is interposed between the most inferior parts of the radius and ulna and, when viewed from the carpal side, has a triangular shape (Fig. 1). The base of the triangle is situated on the dorsal edge of the antebrachial surface, and the apex on the palmar side of the joint. There is a radial extension of the disc at its dorsal base. Proximally, the disc tissue fills the gap between the radius and ulna up to the distal radioulnar joint. The dorsal edge of the
disc is covered by the capsule of the joint which is slightly thickened by the dorsal radioulnar ligament, while the palmar apex, although covered by the synovium, is relatively free. No volar radioulnar ligament could be found (Mikic et al. 1992). The arterial supply to the articular disc of the AC joint in dogs originates predominantly from the palmar interosseous artery, a branch of the common interosseous artery. The palmar interosseous artery, just proximal to the distal radioulnar joint, bifurcates into a larger palmar and a smaller dorsal branch (Fig. 2), running over the palmar and dorsal aspects of the AC joint and its articular disc and terminating in the rete carpi palmare et dorsale. Branches of these 2 arteries arborise on the palmar, proximal and dorsal sides of the articular disc and then penetrate the capsule to supply the disc directly (Fig. 3). These socalled peridiscal vessels ramify and form an anastomotic capillary network around the disc which ends at the peripheral parts of the disc in a series of small terminal capillary loops oriented towards the centre of the disc (Fig. 3). Two types of terminal capillary plexus could be differentiated. First, a subsynovial plexus extending within the synovial membrane which covers both the dorsal peripheral border of the disc and its radial extension where it has an elongated comb-like appearance (Fig. 4). The other type is located on the palmar corner of the disc where it has a triangular shape (Fig. 5). These networks are superficial and clearly visible on the carpal surface of the disc of an injected specimen prior to clearing. Secondly, centrodiscal or intradiscal plexi penetrate
Blood supply of articular disc in dogs
449
Fig. 2. Bifurcation of the palmar interosseous artery (IA) into dorsal (D) and palmar (P) branches viewed from the ulnar side. The vessels injected with India ink are on the distal end of the radius (R). x 3.
Fig. 3. Distal end of the radius of an adult animal with the articular disc (AD) and blood vessels injected with India ink sectioned in a dorsopalmar plane. The dorsal branch (D) of the palmar interosseous artery ramifies on the dorsal and proximal sides of the articular disc forming a terminal vascular network around it. Note that only the peripheral part of the disc is vascularised while the major central part is avascular. The arrows indicate the carpal surface of the disc which is also avascular. Spalteholz, x 5.
AD Fig. 4. Carpal surface of the articular disc (AD) of a specimen perfused with India ink showing the at the dorsal margin which ends with a series of terminal capillary loops. S, synovium. x 20.
subsynovial terminal capillary plexus
450
Z. Dj. Mikic'
/
Fig. 5. Carpal aspect of the palmar corner of the same articular disc as in Figure 3 showing a triangular-shaped subsynovial terminal plexus and its looped capillaries (arrows). S, synovium; U, ulnar articular cartilage; R, radial articular cartilage. x 20.
4
Fig. 6. Dorsopalmar sagittal section of an articular disc (AD) showing the centrodiscal terminal capillary plexus injected with India ink at its proximal side. The looped capillaries penetrate into the discal stroma. Detail from Figure 3. Spalteholz, x 12.
the deeper parts of the discal stroma on its dorsal, proximal and palmar sides (Figs 3, 6). These vessels arborise for a short distance and terminate as looped capillaries between the bundles of the collagen fibres at the peripheral area of the disc (Figs 6, 7, 8), which
Fig. 7. Transverse section of the peripheral part of an articular disc demonstrating the presence of the vessels (black spots) injected with India ink within the synovial membrane (S) and within the peripheral area of the discal stroma (arrows). More central parts of the disc are avascular. Haematoxylin and eosin, x 40.
was confirmed both by tissue clearing and by histological studies (Figs 6, 7, 8). The terminal capillary loops were found to be of differing appearance and calibre (Figs 4, 5, 6, 8), although their basic pattern was always similar. However, a number of loops with an arteriovenous (AV) shunt was also observed (Fig. 8b). In general, the major central portion of the disc was found to be avascular (Fig. 3). The free carpal surface except for its dorsal margin and palmar corner (Figs 4, 5) and all the attachments of the disc to bones were also found to be avascular. Only the peripheral parts on the dorsal, proximal and palmar sides were vascular, this consisting of an anastomotic, cupshaped vascular network (Fig. 3), ending inwardly with a series of looped capillaries. The width of the vascularised zone depended on the age of the animals. In very young puppies the degree of vascular penetration into the disc was quite extensive and sometimes the discs appeared to be completely vascularised (Fig. 9), although the plexi from dorsal and palmar sides were never found to anastomose between themselves and a central avascular zone could always be observed (Fig. 10). In adult animals
Blood supply of articular disc in dogs
451
4;.
.
Fig. 8. Terminal capillary loops found in the articular disc stroma of a puppy aged 2 months. (a) Typical looped capillary located between the wavelike bundles of collagen fibres of the disc fibrocartilaginous tissue; (b) terminal capillary loop with an arteriovenous shunt (arrows) surrounded by the fibrocartilaginous tissue. Haematoxylin and eosin, x 400.
Fig. 9. Section in the radioulnar plane of the ulna (U), articular disc (AD) and radius (R) of a puppy aged 7 days. The disc appears to be completely vascularised. Note the sinusoidal vessels of the cartilaginous radius and ulna and also the difference between the vasculature of the palmar ulnocarpal ligament (PUL) and the disc. Spalteholz, x 5.
the degree of vascular penetration ranged from 15 to 25 % of the discal width, so that the considerably larger central area of the disc was found always to be avascular (Figs 3, 11). DISCUSSION
The results of this study clearly demonstrate that the vascular supply to the articular disc of the AC joint in dogs is very similar to that seen in other intra-articular fibrocartilaginous structures both in man (Davies & Edwards, 1948; Barnett et al. 1961; Scapinelli, 1968; Sick & Koritke, 1969; Danzig et al. 1981; Arnoczky & Waren, 1982; Thiru-Pathi et al. 1986; Mikic, 1992)
and in dogs (Bengin et al. 1978; Tirgari, 1978; Arnoczky et al. 1981; Mikic et al. 1987). As in man (Mikic, 1992), the articular disc of the AC joint in dogs mainly receives its blood supply from the palmar and dorsal branches of the palmar interosseous artery, and the contribution of the radial and ulnar arteries through the rete carpi palmare et dorsale is considerably less important. Smaller branches of these 2 arteries, the peridiscal vessels, which resemble very clearly the perimeniscal vessels of Policard (1936), form an anastomotic capillary network around the disc. This network is obviously terminal since it gives rise to smaller branches which penetrate the periphery of the disc where they end in
452
Z. Dj. Mikic
Fig. 10. Detail from the central part of the disc of the same specimen as in Figure 9. The vascular network from the dorsal (D) and palmar (P) sides, although very close, does not anastomose and the central part of the disc, indicated by arrows, is avascular. x 20.
;'
*
x4
.L
Fig. I11. Section in the radioulnar plane of the radius (R), articular disc (AD) and ulna (U) of an adult animal. The most avascular articular disc is located between the well vascularised osseous parts of the radius and ulna. The dorsal margin and palmar corner of the disc are also vascularised. Note the typical ligamentous type of vasculature of the palmar ulnocarpal ligament (PUL).
a series of terminal looped capillaries. This pattern of vascularity, which is very similar to that found in man (Thiru-Pathi et al. 1986; Mikic, 1992) is comparable with the arrangement of the 'circulus articuli vasculosus' described by Hunter (1743) and Toynbee (1841). An interesting finding in this study was the occasional appearance of a particular type of the terminal capillary loop with an AV shunt (Fig. 8b) which has also been observed in dog knee menisci (Mikic et al. 1987). This specialised vessel which permits extracapillary circulation was described by Kupriianov (1965) and Sorokin (1973) as characteristic of the terminal plexus at the border between the vascular and avascular zones in various tissues. The exact role and significance of this arrangement is not clear. The apparent age-related variations in disc vascularity between the puppies and the adult animals observed in this study were in accordance with findings in other studies of intra-articular fibrocartilaginous structures (Davies & Edwards, 1948; Bengin et al. 1978; Thiru-Pathi et al. 1986; Mikic et al. 1987; Mikic, 1992). While the vascularity of the disc in newborn animals is very extensive during the postnatal period of growth of the disc, a progressive regression of vascularity seems to occur with age, and in adult animals a definite large central avascular zone is formed. There seems to be no further regression of vascularity beyond this point. No degenerative changes in the avascular zone of the adult dogs have been noted macroscopically, possibly because only young adult animals were investigated. The microvascular anatomy of the articular disc of the AC joint in dogs in this study seems to be typical of intra-articular fibrocartilaginous discs and menisci in general (Davies & Edwards, 1948; Barnett et al. 1961) and is quite different from the vascular arrangement in ligaments (Barnett et al. 1961; Mikic et al. 1987). This is a further reason to consider the articular disc of the AC joint in dogs as an intraarticular fibrocartilaginous disc and as a homologue to the articular disc of the human distal radioulnar joint (Mikic et al. 1992), even though this contradicts the opinion of some authors who regard it as a radioulnar ligament (Henschel, 1973). REFERENCES
ARNOCZKY SP, TARvIN GP, WAREN RF (1981) The microvasculature of the meniscus and its response to injury. An experimental study in the dog. Transactions of the Orthopaedic Research Society 6, 177. ARNOCZKY SP, WAREN RF (1982) Microvasculature of the human meniscus. American Journal of Sports Medicine 10, 90-95.
Blood supply of articular disc in dogs BARNETT CH, DAVIES DV, MACCONAILL MA (1961) Synovial Joints. Their Structure and Mechanics. London: Longmans, Green. BENGIN B, OBRADOVIC D, MIKIC Z (1978) Blood supply of the knee menisci in dogs. Folia Anatomica lugoslavica 7, 159-166. CORNER EM (1898) The morphology of the triangular cartilage. Journal of Anatomy and Physiology 12, 272-277. CROCK HW (1967) The Blood Supply of the Lower Limb Bones in Man. Edinburgh: Livingstone. DANZIG L, GoNSALVES MR, RESNICK D (1981) Human meniscal blood supply. Transactions of the Orthopaedic Research Society 6, 338. DAVIES DV, EDWARDS DAW (1948) The blood supply of the synovial membrane and intraarticular structures. Annals of the Royal College of Surgeons of England 2, 142-156. EVANS H, CHRISTENSEN G (1979) Miller's Anatomy of the Dog. Philadelphia: W. B. Saunders. HENSCHEL E (1973) Funktion und vergleichend-anatomische Bedeutung des Lig. radioulnare des Karnivoren. Anatomischer Anzeiger 133, 445-449. HUNTER W (1743) Of the structure and diseases of articulating cartilages. Philosophical Transactions of the Royal Society of London 42, 514-521. KADLETZ M (1932) Anatomischer Atlas der Extremitdtengelenke von Pferd und Hund. Berlin, Vienna: Urban-Schwarzenberg. KUPRIIANOV W (1965) Morfologiceskie osnovi Mikrocirkuljacii. Moscow: Vtoroi Moskovskii gosudarstvenii medicinskii institut imeni M. N. Pirogova. MIKIC ZDi (1992) The blood supply of the human distal radioulnar
453 joint and the microvasculature of its articular disc. Clinical Orthopaedics and Related Research 275, 19-28. MIKIC Z, ERCEGAN G, SOMER LJ, SOMER T, VUKADINOVId S (1987) Experimental Surgery of the Knee Joint in the Dog. Novi Sad: Drustvo lekara Vojvodine. MIKIC ZDJ, ERCEGAN G, SOMER T (1992) Detailed anatomy of the antebrachiocarpal joint in dogs. Anatomical Record 233, 329-334. NICKEL R, SCHUMMER A, SEIFERLE E (1986) Lehrbuch der Anatomie der Haustiere. Berlin, Hamburg: Paul Parey. POLICARD A (1936) Physiologie Geinerale des Articulations az rEtat Normal et Pathologique. Paris: Masson. SCAPINELLI R (1968) Studies on the vasculature of the human knee joint. Acta Anatomica 70, 305-331. SICK H, KORITKE JG (1969) La vascularisation des menisques de I'articulation du genou. Zeitschrift fur Anatomie und Entwicklungsgeschichte 129, 359-379. SOROKIN AP (1973) Obscie Zakonomernosti Stroienia Opornogo Aparata Celoveka. Moscow: Medicina. THIRU-PATHI RG, FERLIC DC, CLAYTON ML, MCCLURE DC (1986) Arterial anatomy of the triangular fibrocartilage of the wrist and its surgical significance. Journal of Hand Surgery 11A, 258-263. TIRGARI M (1978) The surgical significance of the blood supply of the canine stifle joint. Journal of Small Animal Practice 19, 451-462. TOYNBEE J (1841) Researches tending to prove the non-vascularity and the peculiar uniform mode of organisation and nutrition of certain animal tissues. Philosophical Transactions of the Royal Society of London 131, 159-192.
