Cartilage-Free Areas in the Elbow Joint of Young Golden Retrievers

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1 THE ANATOMICAL RECORD PART A 275A: (2003) Cartilage-Free Areas in the Elbow Joint of Young Golden Retrievers CLAUDIA F. WOLSCHRIJN, 1 * MARJA J. L. KIK, 2 AND WIM A. WEIJS 1 1 Department of Pathobiology, Division of Anatomy, Utrecht University, Utrecht, The Netherlands 2 Department of Pathobiology, Division of Pathology, Utrecht University, Utrecht, The Netherlands ABSTRACT The present study describes cartilage-free areas on the ulnar trochlear notch and the humeral condyle of eight very young golden retrievers with otherwise healthy elbow joints. Remarkably, the youngest dog with fullthickness cartilage-free areas was only 8 weeks old. The younger dogs showed no macroscopic abnormalities on the locations that were affected in the older dogs. Two kinds of cartilage modifications were found. Cartilagefree areas at the edges of the articular cartilage layer were present on the humeral capitulum and on two locations of the ulna, (the medial and lateral at the base of the anconeal process, and the trochlear notch near the lateral coronoid process, which was fractured in two cases). Histological examination showed that these cartilage-free areas were filled with dense supportive tissue. Synovial cells covered this tissue as well as the surrounding hyaline cartilage. The synovial membrane covering the areas was macroscopically enlarged, but histological examination revealed no signs of inflammation. The second type of modification consisted of discoloration of the articular surface at the humeral trochlea. Histological examination revealed that in this area the articular surface was composed of fibrocartilage instead of hyaline cartilage. Apparently, there are locations within the elbow joint in which articular cartilage is not necessary for normal joint functioning. The presence of fibrocartilage on the articular surface of the humeral condyle is a surprising finding, for which no explanation has yet been found. Anat Rec Part A 275A: , Wiley-Liss, Inc. Key words: dogs; elbow; articular cartilage; synovial fossae; fibrocartilage Although anatomy textbooks usually depict joint surfaces as being completely covered by articular cartilage, interruptions in the cartilage lining have been described for several joints and in various animal species (Doige and Horowitz, 1975; Nickel et al., 1986). These cartilage-free areas have also been observed in humans. For instance, a cartilage-free zone across the trochlear notch was found in human elbow joints without concomitant pathology or symptoms of disease (Tillmann and Bartz, 1989; Soames, 1995). A cartilage-free area, or synovial fossa, can best be characterized as a macroscopically visible interruption of the articular cartilage. The exposed bone in this shallow depression of the articular surface is largely covered by an extension of the synovial membrane. A few previous reports described these cartilage-free areas in dogs, in joints without (Loeffler and Branscheid, 1976; Van Ryssen et al., 1993) and with (Grondalen and Grondalen, 1981) concomitant pathology. The alteration was also found in dogs with elbow dysplasia, and was termed cartilage atrophy (Wind, 1986). Recent studies (Kuenzel et al., 2002; Probst et al., 2002) reported cartilage-free areas on the trochlear notch in almost two-thirds of non-lame dogs of various breeds examined in those *Correspondence to: Claudia F. Wolschrijn, DVM, Department of Pathobiology, Division of Anatomy, PO Box , 3508 TD Utrecht, The Netherlands. Fax: (31) C.F.Wolschrijn@vet.uu.nl Received 12 June 2003; Accepted 29 July 2003 DOI /ar.a WILEY-LISS, INC.

2 studies. Since new arthroscopic techniques allow inspection of a larger part of the elbow joint surfaces compared to conventional medial arthrotomy (Van Ryssen et al., 1993; Van Ryssen and van Bree, 1997), additional knowledge of the normal anatomy and appearance of the joint is required. Relatively little is known about the origin of these cartilage-free areas, although the present evidence suggests that they develop progressively. In young animals, the complete elbow joint surface is covered with articular cartilage. During maturation, this cartilage becomes thinner and finally results in full-thickness defects (Loeffler and Bidier, 1984; Tillmann and Bartz, 1989). In this study we examined the development of articular cartilage-free areas by investigating the proximal articular surfaces of the ulna and radius, and the distal articular surface of the humerus in a series of healthy dogs (golden retrievers, 4 24 weeks old). The youngest dogs in this study had completely covered articular surfaces, while the older dogs all showed defects on the trochlear notch of the ulna, and some showed defects on the humeral condyle. The positions and extensions of the cartilage depressions are shown, and histological details regarding the cartilage, defects, and covering synovial membrane are provided. The possible functional significance of these cartilage modifications is discussed. MATERIALS AND METHODS The right elbows of 11 golden retrievers (4, 5, 6, 8, 10, 13, 16, 18, 20, 22, and 24 weeks old, respectively) were dissected. The dogs were obtained from a commercial breeder. They were not lame, and they showed no other signs of elbow dysplasia on physical examination. They had been bought for a different study, which was approved by the committee for animal experimentation (DEC) of the Faculty of Veterinary Medicine, University of Utrecht, The Netherlands. After the dogs were killed, they were intravenously perfused with a 4% buffered formaldehyde solution. The joint surfaces were inspected and all abnormalities of the articular cartilage on the proximal parts of the radius and ulna, or the humeral condyle were photographed, and representative samples were removed for histological evaluation. Without prior decalcification, the bony parts were embedded in methylmetacrylate (MMA) (ethylenediaminetetraacetic acid; Sigma Chemical, St. Louis, MO). The extension of the synovial membrane that covered the cartilage alterations was also collected for histology and embedded in MMA. Sections (5 m thick) were cut and stained with hematoxylin and eosin (H&E) or Masson Goldner trichrome, using standard techniques. RESULTS All dogs of 8 weeks and older showed full-thickness cartilage-free areas in their elbows. The three dogs younger than 8 weeks did not display any macroscopic cartilage disorders. Figures 1 3 show the cartilage-free areas, which are indicated with a white arrow. Figure 1a f shows cartilage-free areas on the lateral side of the trochlear notch. The elongated area of the 8-week-old dog was situated on the lateral side of the trochlear notch, including the base of the anconeal process (Fig. 1a), while the 13- and 20-week-old dogs had a defect more distal at the base of the lateral coronoid process (Fig. 1b and e). In the ARTICULAR CARTILAGE-FREE AREAS IN CANINE ELBOWS week-old dog, a cartilage-free area was observed between the medial and lateral coronoid processes, to which the synovial membrane did not extend. In addition, it was found that the lateral coronoid process was fractured (Fig. 1c). A fractured lateral coronoid process was also found in the 24-week-old dog (Fig. 1f). The large cartilage-free area in the 18-week-old dog was situated at the base of the lateral coronoid process and extended toward the sagittal crest (Fig. 1d). Figure 2a e shows articular cartilage-free areas on the medial side of the trochlear notch. The 10-week-old dog had an elongated defect along the edge of the trochlear incisure from the base of the anconeal process halfway to the trochlear notch (Fig. 2a). The 13-week-old dog showed the same modification, as well as a second one in the caudal part of the anconeal process (Fig. 2b). The anconeal processes of the 18-, 20-, and 22-week-old dogs showed cartilage-free areas at their base (Fig. 2c e). Figure 3a d shows articular cartilage alterations on the humeral condyle of the dogs. In the 16-week-old dog, there was a reddish discoloration on the lateral side of the humeral trochlea (Fig. 3a). The 18-week-old dog had a cartilage-free area on the capitulum humeri, with an ingrowing synovial membrane (Fig. 3b), as did the 22- and 24-week-old dogs (Fig. 3c and d). Furthermore, a large red discoloration was observed on the medial side of the trochlea of the 18-week-old dog (Fig. 3b, black arrow, and Fig. 4). The cartilage modifications on the trochlear notch can thus be divided into two groups. Some are situated medially and/or laterally, surrounding the base of the anconeal process, while others are located at the base of the lateral coronoid process (the latter were fractured in some cases). The modifications observed on the humeral condyle can be divided into two types: cartilage-free areas at the edge of the articular cartilage of the capitulum humeri, and discolored areas of the articular cartilage of the trochlea humeri. Furthermore, the following changes take place as part of normal anatomical development in the canine elbow. First, the synovial membrane attaches to the border of the cartilage of the anconeal process. This attachment shifts toward the tip of the anconeal process during ossification (see Fig. 2b (13 weeks) and c (18 weeks), black arrowheads). Second, the slope of the articular surface of the medial coronoid process (MCP) becomes larger, leading in some cases (Fig. 2d (20 weeks) and e (22 weeks)) to a position at the apex of the MCP below the surface of the articular cartilage of the radial head. Third, the anular ligament develops from a thin single band (Fig. 2b (13 weeks), black arrow) to a more massive, broadly attached structure (Fig. 2e (22 weeks), black arrow). Histological analysis of the cartilage-free areas showed that the articular cartilage surrounding the area is covered with tissue, two to four cell layers thick. The cells of this tissue have a plump nucleus and are most likely synovial cells. The same cells are spread over the top of the area, which itself is filled with dense supportive tissue. Figure 5a and b demonstrates a sudden change from articular cartilage to this type of dense supportive tissue, with many blood vessels present in the transition zone. Directly below the gap, the subchondral bone is visible. No signs of inflammatory infiltration are present. Histological examination of the discolored articular cartilage revealed that the lining was not composed of hya-

3 992 WOLSCHRIJN ET AL. Fig. 1. Articular cartilage-free areas on the lateral side of the trochlear notch. a: An 8-week-old dog, elongated area on the trochlear notch. b: A 13-week-old dog, area at the base of the lateral coronoid process. c: A 16-week-old dog, area between both coronoid processes, and a fractured lateral coronoid process. d: An 18-week-old dog, area at the base of the lateral coronoid process, extending toward the sagittal crest. e: A 20-week-old dog, area at the base of the lateral coronoid process. f: A 24-week-old dog, fractured coronoid process.

4 ARTICULAR CARTILAGE-FREE AREAS IN CANINE ELBOWS 993 Fig. 2. Articular cartilage-free areas on the medial side of the trochlear notch. a: A 10-week-old dog, elongated area at the edge of the trochlear notch. b: A 13-week-old dog, elongated area at the edge of the trochlear notch and in the caudal part of the anconeal process. c: An 18-week-old dog, area at the base of the anconeal process. d: A 20-week-old dog, same location. e: A 22-week-old dog, same location.

5 994 WOLSCHRIJN ET AL. Fig. 3. Articular cartilage defects on the humeral condyle. a: A 16-week-old dog, reddish discoloration on the lateral side of the humeral trochlea. b: An 18-week-old dog, area on the capitulum humeri with an ingrowing synovial membrane and a large reddish discoloration on the medial side of the trochlea humeri. c: A 22-week-old dog, same location. d: A 24-week-old dog, same location. line cartilage. Layers of cartilage matrix alternated with layers of collagen fibers, which is characteristic of fibrocartilage (Fig. 5c). The synovial membrane was macroscopically extended to cover the defects, but histological examination revealed no signs of inflammation. DISCUSSION Although cartilage modifications are widespread in several mammalian joints, they normally develop during puberty. This study is the first to show their appearance at a very young age, i.e., at weaning time (8 weeks). In humans, the articular cartilage covers the trochlear notch completely during childhood, but at years of age the lining starts to thin (Tillmann and Bartz, 1989). The younger dogs in this study showed no cartilage-free areas, cartilage depressions, or any other possible preliminary stage of these defects, which is in contrast to the developmental stages described in pigs (Loeffler and Bidier, 1984). Wind (1986) observed thinning of the articular cartilage at the lateral side of the trochlear notch in healthy Reddish discoloration of the trochlea humeri of an 18-week- Fig. 4. old dog.

6 ARTICULAR CARTILAGE-FREE AREAS IN CANINE ELBOWS 995 Fig. 5. Histology of the full thickness defects (a and b) and the discolored articular cartilage (c; fibrocartilage). a and b: The black arrows indicate the blood vessels in the transitional zone, the crosses indicate the dense supportive tissue, the black arrowheads show the hyaline cartilage, and the open arrowhead indicates the subchondral bone. c: The discolored articular cartilage is fibrocartilage; the white arrowhead is pointing at the collagen fibers, and the open arrowhead indicates the cartilage matrix. elbows of adult dogs. It is possible that the defects found in our study only occur in this form in golden retrievers and related breeds, which are particularly susceptible to hereditary elbow diseases. In these disorders, articular cartilage is frequently involved. Early development of defects in these breeds may cause or accompany elbow disorders in the first year of life. In older dogs of many breeds, cartilage disorders have been found (Kuenzel et al., 2002; Probst et al., 2002). It is possible that the defects described here persist into adulthood; alternatively, the gaps may fill in and develop again at another location. For example, the disappearance of cartilage defects has been described in foals (van Weeren and Barneveld, 1999). Defects on the trochlear notch were found at two major locations. The defects of the lateral and medial sides did not fuse, nor did they extend into the radial notch, as reported by others (Loeffler and Branscheid, 1976; Grondalen and Grondalen, 1981; Kuenzel et al., 2002; Probst et al., 2002). It is possible that the defects observed in our dogs would have persisted into later life. However, the cartilage surrounding the defects appeared normal, apart from being covered by synovial cells, and normal enchondral bone formation was observed in this area. No indications for aggravation of the defects were found. Furthermore, a cartilage-free area was found between both coronoid processes (Fig. 1c), which, as far as we know, is a new finding in the dog, but is common in ungulates (Nickel et al., 1986). The macroscopic and histologic descriptions of the fullthickness defects correlate with those in humans (Tillmann and Bartz, 1989). In our small sample of specimens we were unable to find early stages of formation of cartilage-free areas macroscopically and/or microscopically. This is due, first, to the fact that the lesions appear at locations that cannot be fully predicted and, secondly, that not all possible locations are sectioned in the right plane to allow examination. Therefore, we were unable to verify whether a cartilage depression preceded the formation of a cartilage-free area. Opinions vary as to the cause of full-thickness cartilage defects, and their effect on joint function. Some investigators believe that hyaline articular cartilage exists only at those locations where the exerted pressures are within a specific range: if the pressure is below a certain threshold,

7 996 WOLSCHRIJN ET AL. the cartilage will disappear (Tillmann and Bartz, 1989), or will not be formed (Hamrick, 1999). On the other hand, abnormally high pressures may result in the development of nutritional deficits, eventually leading to the formation of synovial fossae (Buerki, 1904; Hamrick, 1999). Both hypotheses assume that pressure distribution over the articular surface is heterogeneous. Such an uneven pressure distribution could be caused by joint incongruity. For instance, it is known that the trochlear notch in humans is not fully congruent with the trochlea humeri (Soames, 1995), and this has also been morphologically substantiated in dogs (Preston et al., 2000, 2001; Collins et al., 2001). However, no measurements or mechanical models to estimate pressures are available. Given the normal canine posture, it seems most likely that major pressures arise on the radial head and the medial coronoid process, but not on the trochlear notch. The lesions are generally located in areas away from these pressure concentrations. Furthermore, they are positioned in such a way that they will not seriously impair the weight-bearing function. The absence of inflammatory reactions suggests that cartilage alterations at these specific locations do not interfere with joint function. It is possible, however, that defects appearing at more critical locations impair joint function. It is therefore important to know the locations on which the defects can appear without giving rise to clinical problems. The appearance of fibrocartilage on the trochlea humeri has (to our knowledge) not been described before, and the meaning of this finding remains unclear. This type of cartilage is usually found in the mandibular condyle and intervertebral disks. Fibrocartilage can also be formed when the original hyaline cartilage is damaged, but no (other) secondary joint changes indicative of this process were found in our material. LITERATURE CITED Buerki E Die Synovialgruben des Rindes. Thesis, University of Zurich, Zurich, Switzerland. Collins KE, Cross AR, Lewis DD, Zapata JL, Goett SD, Newell SM, Rapoff AJ Comparison of the radius of curvature of the ulnar trochlear notch of rottweilers and greyhounds. Am J Vet Res 62: Doige C, Horowitz A A study of articular surfaces and synovial fossae of the pectoral limb of swine. Can J Comp Med 39:7 16. Grondalen J, Grondalen T Arthrosis in the elbow joint of young rapidly growing dogs. V. A pathoanatomical investigation. Nord Vet Med 33:1 16. Hamrick MW A chondral modeling theory revisited. J Theor Biol 201: Kuenzel W, Breit S, Probst A Morphologische Besonderheiten am Olekranon des Hundes und deren funktionelle Bedeutung. Wien Tieraertzl Mschr 89: Loeffler K, Branscheid W Synovialausschnitte im Ellbogengelenk des Hundes. Kleintier-praxis 21: Loeffler K, Bidier I Zur Frage der Umdifferenzierung der Knorpelzellen der Gelenkoberflaeche am Beispiel der Synovialgrubenbildung. Zbl Vet Med C Anat Histol Embryol 13: Nickel R, Schummer A, Seiferle E, Frewein J, Wilkens H, Wilke K-H The anatomy of the domestic animals. Vol. I. In: Nickel R, Schummer A, Seiferle E, editors. The locomotor system of the domestic animals. Berlin, Hamburg: Verlag Paul Parey. p Preston CA, Schulz KS, Kass PH In vitro determination of contact areas in the normal elbow joint of dogs. Am J Vet Res 61: Preston CA, Schulz KS, Taylor KT, Kass PH, Hagan CE, Stover SM In vitro experimental study of the effect of radial shortening and ulnar ostectomy on contact patterns in the elbow joint of dogs. Am J Vet Res 62: Probst A, Kuenzel W, Breit S The canine olecranon are variations in shape of the articular surface incidental findings or expressions of different loading capacities? In: 24th Congress of the European Association of Veterinary Anatomists, Brno., Czechoslovakia p 53. Soames RW Gray s anatomy. 38th ed. Edinburgh: Churchill Livingstone. p Tillmann B, Bartz B Funktionelle Anatomie des Ellbogengelenks. Aktuelle Probl Chir Orthop 37: Van Ryssen B, van Bree H, Simoens P Elbow arthroscopy in clinically normal dogs. Am J Vet Res 54: Van Ryssen B, van Bree H Arthroscopic findings in 100 dogs with elbow lameness. Vet Rec 140: van Weeren PR, Barneveld A The effect of exercise on the distribution and manifestation of osteochondrotic lesions in the warmblood foal. Equine Vet J Suppl: Wind AP Elbow incongruity and developmental elbow diseases in the dog: part I. J Am Anim Hosp Assoc 22: