Growth Plate Injuries

Growth plates, or physes, are composed of several merged layers that produce longitudinal growth of the long bones by the method of endochondral ossification. Physeal damage is not uncommon in the small animal and can result from trauma, genetic disorders, nutritional imbalances, or other medical disturbances. The physis can be either completely or partially damaged and injuries can vary in their subsequent extensiveness from total growth arrest to retardation. Common sequelae of physeal injury include shortened limbs, angular limb deformation, and adjacent joint subluxation. Angulations can occur in multiple planes depending on the location of the growth plate damage and whether the affected bone is anatomically paired with another long bone, as with the radius and ulna. Malalignment can be in the frontal plane, resulting in varus and/or valgus deformities, or in the sagittal plane, causing pro- or recurvatum and rotationally causing internal or external bone torsion. A thorough understanding of the resulting pathology from physeal injury necessitates a discussion of the anatomy and physiology of the growth plate.

Growth Plate Anatomy

Although the physiology of the individual layers of the growth plate is unique, the functional unit of the physis can be summarized as a column of chondrocytes that proliferate, hypertrophy, and synthesize matrix before ultimately undergoing apoptosis [1]. These functions are intimately regulated intrinsically by growth factors and mechanical forces and extrinsically both hormonally and mechanically. The growth plate can be divided into its various layers both morphologically and functionally. As such, a standard set of descriptive terms for the layers does not exist and will vary widely depending on the author.

For purposes of this discussion, a functional scheme of evaluation is presented including the 1) germinal zone; 2) columnar zone with upper proliferating area and lower maturation area; 3) hypertrophic zone with an upper four fifths possessing nonmineralized matrix and lower one fifth with mineralized matrix; and 4) outer metaphysis (Fig. 109-1). The cells within the germinal zone are also frequently referred to as resting cells because they do not proliferate [2]. The small, irregularly spaced cells in the germinal zone contain a high concentration of lipid within their vacuolar contents, suggesting their important role in nutrient storage [3].

Figure 109-1. Photomicrograph of a normal canine growth plate stained with hematoxylin and eosin and labeled for the four primary functional zones: germinal zone, columnar zone, hypertrophic zone, and outer metaphyseal zone. The proximal aspect of the bone is at the top of the photograph. (Courtesy of Dr. Keiichi Kuroki.)

The upper portion of the columnar zone represents the only aspect of the growth plate in which chondrocytes undergo division. The active division in this area results in the stacking of flattened cells into columns that are separated from each other by large conglomerations of type II collagen. This proliferating portion of the columnar zone is high in oxygen content and undergoes active glycogen storage by the chondrocytes [4,5]. The high concentration of rough endoplasmic reticulum within chondrocytes in the lower half of the columnar zone dictates their role in extensive matrix synthesis [1].

The hypertrophic zone of the physis is the driving force of longitudinal bone growth through cell expansion. The chondrocytes of this zone increase their intracellular volume anywhere from 5- to 10-fold. Variation in the rate of chondrocyte hypertrophy is now thought to be the main reason for different anatomically located physes to grow at different rates [6]. Like the lower half of the columnar zone, the cells of the hypertrophic zone also possess a highly active metabolism that is responsible for large quantities of matrix synthesis. In addition to abundant type II collagen, both type X collagen and vascular endothelial growth factor (VEGF) are produced in the hypertrophic zone. The production of these elements is a hallmark for cellular differentiation and the ceasing of cellular division. These processes occur in an environment that is lower in oxygen tension and in which glycogen is consumed by the chondrocytes until depleted [4,5]. In the lower one fifth of this zone, the matrix is modified for calcification and vascularization. Whereas recruitment for vessel ingrowth is signaled by the release of VEGF, matrix mineralization is mediated by budding vesicles formed from the chondrocyte plasma membrane [7]. The vesicles contain calcium and enzymes, including both alkaline phosphatase and matrix metalloproteinase (MMP) [1]. Newly deposited matrix then forms in longitudinal septa between the columns of chondrocytes and primarily consists of crystalline hydroxyapatite. The septa eventually become primary trabeculae as the upper two thirds are resorbed by chondroclasts and the distal third acts as a scaffolding for osteoid deposition from osteoblasts [7]. Within the mineralized cartilage, matrix forms a transverse septum that is invaded by capillary loops from the metaphysis as they penetrate the distal hypertrophic chondrocyte lacunae. The differentiated chondrocytes then undergo caspase-mediated programmed apoptosis [8].

Finally, the zone of the outer metaphysis is the area where the endochondral ossification process yields true bone tissue through remodeling of the primary trabeculae into trabeculae of lamellar bone, or secondary trabeculae [7]. This remodeling is mediated by a variety of cells, including undifferentiated mesenchymal cells, preosteoblasts, and osteoblasts in addition to the metaphyseal vascular system [1]. The combined areas of the distal hypertrophic zone and proximal metaphysis are also often referred to as the zone of provisional calcification.

Whereas the layers described above provide for longitudinal growth, they do not account for the necessary increasing width of the physis during bone development. The growth plate zones are thus circumscribed by a wedge-shaped area of chondrocyte progenitor cells known as the perichondrial ossification groove of Ranvier, which contributes germinal cells to allow expansion of the bone’s width at the physis. Within this groove is the fibrous ring of LaCroix, which contains fibers arranged vertically, circumferentially, and obliquely to provide mechanical support in response to compression, tension, and shear loads on the physis [1,7].

During the late embryonic phase of development, the epiphyseal cartilages of the long bones are well vascularized, with vessels frequently crossing the physes either partially or completely [1]. Following birth, the transphyseal vascular bridging is eliminated resulting in the physeal vasculature arising from two separate sources. Epiphyseal vessels supply the germinating, proliferating, and upper hypertrophic zones through diffusion, and separate metaphyseal vessels permeate to the level of the distal hypertrophic zone. The epiphyseal and metaphyseal vessels normally only anastomose once the physis has closed, marking the onset of skeletal maturity [9]. Premature vascular anastomosis across the physis results in pathologic closure of the growth plate. Alteration in this specific vascular pattern can result in aberrant long-bone development at the level of the physis. Disruption of the epiphyseal blood supply is the most devastating injury to the physeal growth plate vasculature. Epiphyseal vessel damage can cause avascular necrosis of both the germinal chondrocytes and secondary ossification center of the epiphysis, resulting in ossification of the growth plate and premature cessation of growth. To the contrary, injury of the metaphyseal vasculature can result in transitory increases in physeal growth [1,7].

Growth Plate Physiology

A complex and multifactorial array of factors regulate control over a variety of growth-plate functions including cell proliferation, maturation, hypertrophy and apoptosis, matrix synthesis and mineralization, vascular infiltration, and ultimately physeal closure. Ongoing studies elucidating many of these processes are shedding new light on the disease processes that result in growth-plate dysfunction. Major regulating factors are hormones, growth factors, vitamins, and biomechanical forces.

Chondrocyte proliferation within the growth plate is believed to be under the primary control of a local negative feedback loop involving three signaling molecules synthesized by growth-plate chondrocytes: parathyroid hormone-related peptide (PTHrP), Indian hedgehog (Ihh), and transforming growth factor-beta (TGF-β) [5,7,10]. The release of Ihh by cells newly undergoing hypertrophic differentiation triggers the release of TGF-β by the perichondrium, which in turn stimulates perichondrial and juxtaarticular cells to increase synthesis of PTHrP, thus slowing the progression of proliferating cells expressing the PTHrP receptor from advancing into the hypertrophic stage [10]. This feedback loop is not exclusive in its control of cell proliferation within the growth plate and is greatly modulated by a number of other systemic and local signaling molecules including the fibroblast growth factor (FGF) family and its receptors [11]. In addition, growth hormone (GH) produced in the anterior pituitary, and its mediator, insulin-like growth factor (IGF), play important roles in physeal chondrocyte proliferation. Chondrocyte maturation and hypertrophy appear to occur spontaneously largely through the actions of the bone morphogenic proteins (BMPs) and their receptors [12]. The peptide hormone thyroxine (T4) can only induce chondrocyte maturation and production of type X collagen through induction of BMP-2 [13]. Because hypertrophy can occur spontaneously, negative inhibitors are likely to be crucially important in the regulation of growth-plate kinetics. Once the chondrocytes have terminally differentiated, their purpose is to foster matrix calcification in preparation for osteoblastic bone formation [7]. Subsequent death and removal of the chondrocyte then allows space for infiltrating vasculature and bone marrow stromal cells [14]. It is now accepted that the death of terminally differentiated chondrocytes occurs through highly regulated apoptosis, or programmed cell death. Alteration in the normal caspase-mediated apoptotic process through mutation of regulating FGF receptors is now suspected to be the cause of achondroplasia, or dwarfism [15]. The administration of both glucocorticoids and radiation to juvenile animals has been shown to increase the rates of hypertrophic chondrocyte apoptosis, and can alter the shape and normal activity of the growth plate [16-18].

Matrix synthesis in the growth plate is thought to be regulated by many of the same factors that direct the development and differentiation of physeal chondrocytes. One transcription factor in particular, Sox 9, binds with various related proteins to specific enhancer regions in the promoter regions of genes expressing types II, IX, and XI collagen and aggrecan [19]. Mineralization of the secreted matrix is an essential precursor to the conversion of the chondroid nature of the growth plate to bone. As previously stated, matrix vesicles serve as the principal site for matrix mineralization within the lower hypertrophic zone largely through their accumulation of calcium and alkaline phosphatase. The accretion of calcium is dependent on the calcium channel molecule family of annexins [20]. An interesting relationship exists between type X collagen and annexin V. Type X collagen, present exclusively within the hypertrophic zone of the physis, is able to bind to matrix vesicles with the assistance of annexin V and subsequently stimulates its activity, thus facilitating calcium deposition [7,21]. Although still incompletely characterized, the likely function of the vesicular alkaline phosphatase is the hydrolysis of pyrophosphate, an inhibitor of hydroxyapatite crystal formation, into two molecules of orthophosphate [22]. Vitamin D is well known for its critical influence on increasing both alkaline phosphatase and MMPs within the chondrocyte. In particular, MMP-13, present within matrix vesicles, is important for the cleavage of type II collagen and the activation of latent TGF-β, both of which are associated with the onset of matrix mineralization [23,24].

Following matrix mineralization, vascular invasion from the metaphyseal side of the physis is an essential precursor to ossification. The process of vascularization is multifactorial but is largely mediated through the actions of VEGF expressed by hypertrophic chondrocytes and targeting vascular endothelial cells, stimulating their proliferation and migration [25]. Another growth factor that has been shown to possess pro-angiogenic characteristics is basic FGF [26]. Failure of appropriate vascularization results in disruption of normal physeal architecture and widening of the hypertrophic zone with diminished trabecular bone formation [7]. Physeal closure is associated with a decrease in chondrocyte proliferation, resulting in a diminished height of both proliferative and hypertrophic zones. In most mammals, the epiphysis and metaphysis become fused with resorption of the growth plate following sexual maturity. Some evidence suggests that physeal closure is estrogen-mediated through promotion of chondrocyte-replicative senescence and not through vascular invasion or ossification [27].

Fractures of the Growth Plate

A thorough understanding of the mechanical properties of the growth plate has yet to be achieved. Large variation exists among studies, attributable to differences in animal models and their respective ages, test parameters, and the anatomic locations tested. Because the physes represent both the sole source of skeletal longitudinal growth as well as the weakest point of the juvenile skeleton, an understanding of growth-plate biomechanics and modes of failure is essential. Growth-plate fractures are common and can result in significant alteration of physiologic growth function. A close relationship exists between the ultrastructural properties of the physeal extracellular matrix and its mechanical behavior. In cadaveric testing, the germinal and proliferating portion of the columnar zones are somewhat protected from excessive external force owing to a more random organization of collagen fibers and overall higher concentration of collagen [28]. Experimentally, the hypertrophic zone may represent the weakest region within the growth plate during tensile loading owing to the lower concentration and more regular organization of collagen in addition to the parallel chondrocyte orientation with respect to the longitudinal axis of the bone [5]. The clinical situation may differ greatly, however, with differences in anatomic sites and complexity of offending forces.

A commonly used classification system of growth-plate fractures intended to correlate the characteristics and prognoses of each fracture configuration was proposed by Salter and Harris [29]. Salter-Harris fractures have been covered in more detail previously within this text but are briefly discussed here in the context of physeal injuries. Using this classification system, physeal fractures can be categorized into one of five types. Type I fractures represent a displacement of the epiphysis from the metaphysis with no associated bone fracture as a result of shearing and tensile forces. Type I fractures are more common in younger animals (<6 months of age) and were classically thought to carry more favorable prognoses owing to the larger thickness of the physis at this age and limitations of the fractures to the hypertrophic zone [30]. Several clinical reports now contradict this, however, and important exceptions should be noted. A high incidence of damage to the proliferating portion of the columnar physeal zone has been reported in naturally occurring type I fractures in the dog, explaining the common clinical observation of growth retardation [31]. Additional exceptions occur with specific anatomic sites including the femoral capital physis, which may see direct disruption of ascending epiphyseal vasculature along the femoral neck, resulting in secondary femoral neck resorption. This has been documented to occur in as many as 70% of affected patients following surgery and ultimately necessitated femoral head and neck excision in 20% of cases in one report [32,33].

Salter-Harris type II fractures occur along the length of the growth plate but extend into the metaphysis, resulting in a wedge-shaped metaphyseal fragment that remains attached to the epiphysis. The side on which the metaphyseal fragment occurs is related to the direction of the impacting force and subsequent bending of the bone. Most metaphyseal fragments remain adhered to the epiphyseal component on the concave aspect of the deformed bone during impact.

Type III fractures are intra-articular in that an epiphyseal fracture communicates with the fissure extending along the growth plate. With disruption of the articular cartilage and subchondral bone, a higher likelihood exists for postoperative osteoarthritis. Goals for surgical treatment include accurate reduction and fixation of the articular components to reestablish the joint surface.

Type IV fractures consist of type III fractures with the addition of a metaphyseal extension of the epiphyseal injury. Like type III fractures, type IV fractures are intraarticular and thus require perfect anatomic reduction to reduce the risk of secondary osteoarthritis. Displaced type IV fractures must also be accurately reduced to minimize the risk of formation of a bone bridge along the fracture line that extends from the joint across the physis and into metaphysis, resulting in subsequent growth retardation [5].

Type V Salter-Harris fractures are classically described as compression fractures of the growth plate. The offending compression is theorized to result in necrosis of proliferating chondrocytes of the growth plate, resulting in overall growth arrest of the bone if the entire physis is affected or angular limb deformities if only a portion of the physis is involved. The most commonly affected location in the dog is the distal ulnar physis because of its unique conical shape. In cases in which the distal ulna is affected without concomitant involvement of the distal radius, antebrachial deformation ensues in the form of excessive procurvatum, external rotation, and carpal valgus.

Again, caution should be used in extrapolating prognosis based on radiographic interpretations of fracture configurations. Numerous other factors that are difficult or impossible to assess radiographically have a tremendous impact on the response of the bone as it heals, including the post-traumatic status of epiphyseal vasculature, the physeal zone affected, and the nature of insulting forces creating the fracture.

Pathologic States Affecting the Growth Plate

Irradiation

Although much more frequently diagnosed in people, juvenile osteosarcoma has been reported in dogs [34]. Palliative treatment of bone tumors with various forms of radiation has been investigated in several juvenile animal models, elucidating the negative impact radiation has on growth-plate physiology. It has been determined that the proliferating cells of the upper portion of the columnar zone and epithelial cells of the metaphyseal vasculature are the most radiosensitive cellular populations of the growth plate [35,36]. Studies investigating the effects of a β-particle-emitting radionuclide on physeal growth and development in skeletally immature rabbits revealed decreased production of type X collagen and MMP-13 in hypertrophic chondrocytes with subsequent limb shortening in treated animals.18

Bacterial

Bacteria are capable of invading the metaphyseal portion of the growth plate causing microabcessation through vascular sinusoids. Although it is not clearly understood why these infections occur, theories include reduced blood velocity through the torturous vascular system, low oxygen tension, and deficiencies in the reticuloendothelial system [5]. Likely to be more common in the horse and human, bacterial physitis has been reported to occur in the dog most frequently in the lumbar vertebra, where it causes lucent widening of the growth plate and loss of definition of the physeal margins [37]. Although collapse of the physis and subsequent sclerosis typically ensues, secondary sequestration has been reported requiring sequestrectomy and long-term antimicrobial therapy [38].

Endocrine

As previously described, the physes function under intimate guidance by the various components of the endocrine system. Endocrine diseases, therefore, can result in alteration of normal growth-plate physiology and secondary skeletal deformities. It is important to note that some features typical of endocrine disorders are often accepted as breed characteristics in the dog [39]. Increases (gigantism) or decreases (dwarfism) in body size can be considered normal and classified as constitutional, as the result of complex genetic effects, or abnormal, as the result of endocrinopathies or other complex disorders. Each condition can exist either proportionately or disproportionately, depending on whether the appendicular and axial skeletal components are altered in synchrony.

The anterior pituitary gland, under the stimulation of the hypothalamus, releases growth hormone, which plays an important role in chondrocyte proliferation, physeal development, and bone growth. Alterations in available concentrations of growth hormone result in developmental skeletal disorders. Reduction in levels of growth hormone production by the anterior pituitary gland typically results in proportionate dwarfism, which is a rare but well documented disorder in the dog, most frequently affecting the German shepherd dog (Fig. 109-2). In this breed, hypopituitary dwarfism is known to be an autosomal inherited disorder [40]. In most of these cases, intrapituitary cysts exist and enlarge with age; suprapituitary stimulation does not increase the release of GH or thyroid stimulating hormone (TSH) [41]. Hypopituitary dwarfs demonstrate retarded bone development and delayed epiphyseal fusion [42]. The growth plates may remain open for years, and possess architectural derangement of the proliferating chondrocyte arrangement and intercellular matrix [42].

Figure 109-2. Photograph of three German Shepherd dog littermates, aged 6.5 weeks. The two puppies on the left represent proportional hypopituitary dwarfs. (Courtesy of Ms. Susie Zeiner and Mr. John Walker.)

True hyperpituitary gigantism (acromegaly) is rare in small animals. Normal giant breeds of dogs represent proportional constitutional gigantism, and may possess the features frequently associated with acromegaly in humans, including bone thickening of the supraoribtal frontal bones and enlarged paws manus and pedes. Interestingly, GH levels are normal in these dogs, but concentrations of IGF-1 may be elevated [43]. An acromegalic syndrome in cats is documented, which occurs in middle-aged to older animals, associated with GH-secreting tumors of the pituitary gland with many clinical sequelae; however, the age of onset obviates growth-plate involvement.

Congenital or juvenile-onset hypothyroidism has been frequently documented in the dog. The skeletal manifestations of this disorder include delay in time of ossification of the epiphyseal centers (epiphyseal dysgenesis) and physeal closure, stunted growth, and disproportionate dwarfism (Fig. 109-3) [42,44]. Familial congenital hypothyroidism has been documented in Scottish deerhounds [45], giant Schnauzers [46], boxers [47], and toy fox terriers [48]. Some evidence suggests that, if a diagnosis can be made at an early age (<4 months), appropriate treatment can result in remission [46].

Figure 109-3. Orthogonal radiographs of the pelvis of a 5-month-old intact female miniature Schnauzer puppy that was presented with a nonspecific history of chronic lethargy. The animal was diagnosed with congenital hypothyroidism. Note the complete lack of ossification of the epiphyseal centers (epiphyseal dysgenesis). (Courtesy of Dr. Valerie Samii.)

A close association exists between the sex steroids, estrogen and testosterone, and the onset of skeletal maturity. Whereas androgen alone does not affect growth-plate closure, estrogen accelerates physeal fusion and terminates linear growth [49]. Androgens are converted to estrogens via aromatization in the male, such that estrogen mediates growth termination in both genders. Thus, prepubertal surgical gonadectomy can affect bone development. Salmeri et al determined that radial and ulnar growth-plate closure was delayed in dogs by 4 months if surgical gonadectomy was completed at 7 weeks of age, and by 3 months if gonadectomy was completed at 7 months of age [50]. Although not examined in this study, it was suspected that animals neutered prior to skeletal maturity might be more susceptible to sustaining traumatic Salter-Harris fractures for a longer time [50]. Subsequently, spontaneous, atraumatic fractures of the capital physis in male cats have now been shown to be linked with prepubertal gonadectomy [51]. This population of cats still possessed open growth plates at a mean age of 94.5 weeks, suggesting that the diminished presence of androgens could have resulted in delayed growth-plate closure and thus posed a higher risk for fractures [51].

Chondrodysplasias

Chondrodysplasia is a general term referring to any number of disturbances in the development of the cartilaginous growth plates, primarily of the long bones. It frequently results in achondroplasia, which is disproportionate dwarfism, where the long bones of the appendicular skeleton are shortened but the axial components, including skull and vertebral column, are of normal size. Many types of chondrodysplasia have been documented and are cited as specific entities particular to certain breeds. Again, these disorders are distinguished from constitutional dwarfism owing to chondrodystrophy, which is accepted as a nonpathologic breed standard in many types of dog (e.g., Basset hounds, Welsh corgis, and beagles). Brief descriptions of various reported chondrodysplasias are discussed; however the reader is referred to pathology texts and listed references for more detailed descriptions of each.

Pseudoachondroplastic dysplasia has been documented in both miniature poodles and Scottish deerhounds, although the disease has characteristics unique to each breed [52,53]. However, the condition is likely to be autosomal recessive in both breeds and is first recognized when the animals are several weeks old. Although histologic changes of the physeal derangements are specific and well described for the different breeds, linear growth of the long bones only reaches approximately 65% of that of normal dogs of like breed [52-54]. By the time the animals achieve skeletal maturity, severe angular limb deformities are noted, with subsequent marked joint laxity.

A condition has been documented to affect young beagle dogs called multiple epiphyseal dysplasia, in which stippled mineralizations can be radiographically detected in the epiphyses of the femur, humerus, and carpal and tarsal bones [55,56]. Clinical and radiographic signs are first detected at 3 to 4 weeks of age; however, they typically resolve with development and are no longer apparent by 5 months of age [42]. Affected dogs may possess osteoarthritis as adults, attributable to the abnormal epiphyseal development.

Specific chondrodysplasias have now been documented for several canine breeds. The condition is well documented in the Alaskan malamute, in which a disproportionate dwarfism with concurrent macrocytic hemolytic anemia results from the autosomal recessive disorder. Among other clinical sequelae, hallmarks of the disease include derangement of the proliferative zone of the physes and abnormal endochondral ossification that is radiographically most apparent as flattened distal ulnar physes and retarded ossification of cuboid bones detected between 4 and 12 weeks [42,57]. A similar chondrodysplasia causing disproportionate dwarfism in Norwegian elkhounds has been documented, with a distinguishing characteristic being shortened vertebral bodies [58]. Chondrodysplastic dwarfism with vertebral malformation has been described in great Pyrenees, which also exhibit concurrent deafness [59]. Dwarfism has also been reported as autosomal recessive traits owing to chondrodysplasia in the English pointer and Irish setter breeds [42,60].

Oculo-skeletal dysplasia has been reported in both the Labrador retriever and Samoyed breeds [61,62]. Aside from the ocular pathology, which includes cataracts and retinal dysplasia, affected animals may also be chondrodysplastic dwarfs with more severely affected forelimbs. Secondary changes can include fragmented coronoid processes, ununited anconeal processes, and hip dysplasia. In the Labrador, the severity of dwarfism is positively correlated with the extent of microscopic degeneration of the physeal chondrocytes, detected in part by the presence of cytoplasmic inclusions [63].

Nutritional

Many nutritional disorders can affect bone physiology, and with respect to the growth plate specifically, it is well documented that certain dietary alterations can cause pathologic changes to physeal architecture and development. Diets low in vitamin D and phosphorus can result in rickets, causing derangement of the normal chondrocyte columns within the physes, an inability to appropriately calcify the matrix surrounding the hypertrophied cells, and diminished vascular invasion from the metaphysis necessary for physeal closure [39]. Large projections of uncalcified cartilage subsequently protrude into the metaphysis and are occasionally bypassed by the irregular ingrowth of vascularized, ossifying tissue, resulting in a tortuous metaphyseal junction [42]. Angular limb deformities can occur secondary to the growth-plate disturbances. Hypervitaminosis A has been reported to cause exuberant and premature calcification of growth-plate cartilage, resulting in early physeal closure [64].

Idiopathic

Retardation of endochondral ossification and the formation of apparent retained cartilage cores have been reported to affect most frequently the distal canine ulnar growth plate (Fig. 109-4) [65]. These lesions consist of a cone of unmineralized hypertrophic cartilage projecting from the growth plate into the metaphysis. Although the etiology is unknown, it is speculated that they arise either from a process similar to osteochondrosis or an interruption to the metaphyseal blood supply [42]. They typically occur bilaterally and can be associated with premature closure of the distal ulnar physis with secondary antebrachial angular limb deformities.

Figure 109-4. Lateral radiograph of a distal canine radius and ulna exhibiting a retained cartilage core apparent as a longitudinal radiolucent projection extending from the open physis proximally into the metaphysis.