Dysplasia Epiphysealis Hemimelica in a Boxer Puppy

DYSPLASIA EPIPHYSEALIS HEMIMELICA IN A BOXER PUPPY MASSIMO VIGNOLI, DMV, SRV, GIUSEPPE SARLI, DMV, FEDERICA Rossi, DMV, SRV, ROSSELLA TERRAGNI, DMV, SPCAA, LUEIPozzr, DMV

A Boxer puppy had an unusual dysplastic lesion of the distal epiphysis of the left femur. Biopsy and CT examination were performed. A diagnosis of dysplasia epiphysealis hemimelica (DEH) was made. To the investigators knowledge, this condition has not been described before in animals. DEH is a growth disorder involving preferentially the medial compartment of the lower limbs, and it is associated with epiphyseal hypertrophy and delayed mineralization. Veterinary Radiology & Ultrasound, Vol. 43, No. 6, 2002, pp 528-533. Key words: bone, dysplasia, dog, CT-guided biopsy.

Introduction

History

T

HE PURPOSE OF this article is to describe the clinical, radiographic, and CT findings in a Boxer puppy with dysplasia epiphysealis hemimelica (DEH) and correlate them with similar findings in humans.

A 2-month-old female Boxer puppy underwent clinical evaluation before routine vaccination. A moderate, not painful enlargement of the distal epiphysis of the left femur was noticed. The left femur was shorter than the right one. The puppy was lame while walking or running. No other abnormal clinical signs were noticed. There was no history of trauma. Blood and urine examinations were norma]. In standard radiographs (Fig. l ) of the pelvis and both femurs, the left femur was shorter than the right. In addition,

Address correspondence and reprint requests to Dr. Massimo Vignoli, Clinica Veterinaria dell’Orologio, Via dell’orologio 38,40037 Sasso Marconi, Bologna, Italy. Received October 30, 2001; accepted for publication March 21, 2002.

FIG. I. Lateral radiograph (a) of the left femur made at 2 months of age. Note the small ossification center of the condyle, caudal folding of the metaphysis and soft tissue swelling. Ventrodorsal (b) view of the pelvis. There is shortening of the left femur, an increase in transverse diameter of the femoral metaphysis, and a lack of radiopacity distal to the physis.

528

VOL. 43, No. 6

DYSPLASIA EPIPHYSEALIS HEMIMELICA

Frti. 2. Histologic samples from the lateral (a) and medial (b) condyles of the left femur. There is apparent cartilagineous tissue with scant mature (white arrowheads) and hypertrophic (black arrowheads) chondrocytes close to the trabecular bone (arrows) i n the lateral condyle, whereas in the medial condyle there is a primary center of ossification, with vascular (v) invasion of the cartilage (c).

IN A

BOXERPUPPY

529

an increase in transverse diameter of the left femoral metaphysis and a lack of radiopacity of the medial femoral condyle were seen. A small radiopaque area was identified as the ossification center of the lateral femoral condyle. The patella appeared normal. A caudal folding of the metaphysis and soft tissue swelling of the distal third of the femur were also present. No abnormalities were detected in other parts of the skeleton. Twenty days after the evaluation neither the clinical nor radiogsaphic signs had changed. A bone biopsy through the distal left femoral epiphysis was performed with a 13-gauge needle. In a sample from the lateral side, there was cartilagineous tissue with a few mature hypertrophic chondrocytes close to the trabecular bone (Fig. 2a). Medially there was a primary center of ossification, with vascular invasion of the cartilage (Fig. 2b). Twenty days after the biopsy there was progressive ossification of the lateral femoral condyle, but no evidence of ossification medially (Fig. 3). Ten days later there was mild irregular radiopacity in medial condyle (Fig. 4). Twenty days later, there was progressive opacification of the medial femoral condyle, and the femoral epiphysis appeared very irregular (Fig. 5 ) . At 6 months of age, the left femur appeared short and irregular, with randomized foci of mineralization in the medial condyle (Fig. 6). At this time the dog was improved clinically. When the dog was 18 months old, a few radiographic changes were detected: the physis appeared closed, there was remodeling of the tibia1 plateau with an osteophyte on the lateral side, and a mild opacity increase in the subcondral bone of the lateral condyle and an osteophyte (Fig. 7). A CT was performed at this time, and a CT-guided biopsy of the condyle was performed. In the CT images, both the medial and lateral condyles were ir-

Flti. 3. Twenty days after biopsy (3.5 months old). There is complete radiopacity of the lateral condyle and enlargement of the surrounding soft tissue.

530

2002

VICNOLI ET AL.

FIG.4. Thirty days after biopsy (10 days before 4 months old) there is evidence of mild irregular radiopacity in medial condyle.

regular in shape with incomplete ossification medially (Fig. 8). Histologically, the medullary spaces were fat filled with some myeloid tissue and appeared interrupted by fibrous bands, which contained clusters of condrocytes. At the center of the fibrous bands, trabecular bone appeared close to the condrocyte clusters. This latter appeared both as a metaplastic change of fibrous bands as well as an expression of endochondral ossification (Figs. 9 and 10) and, therefore, was only partly interpreted as a cartilaginous metaplasia of fibrous tissue bordering several ununited ossification centers.

Discussion The delayed and irregular ossification of the medial condyle of the femur suggests epiphyseal dysplasia. The angulation of the femoral metaphysis is also characteristic of epiphyseal dysplasia. However, epiphyseal dysplasia (stippled epiphysis) is described in miniature Poodles and beagle^'^^,^ not in the Boxer breed. The radiographic pattern of dysplasia epiphysealis punctata is characterized by focal epiphyseal opacities. They disappear when the animal is an

'

FIG.5. Radiography made 2 months after biopsy (10 days after 4 months old). There is progression in radiopacity of the medial femoral condyle, and the condyle is very irregular.

VOL. 43, No. 6

DYSPLASIA EPlPHYSEALlS HEMIMELICA IN A BOXER PUPPY

53 1

FIG. 6. Six months of age; there is deformity of the left femur and randomized foci of mineralization in the medial condyle

adult. There is also shortening and widening of long bones and delayed ossification. This condition usually involves more than one epiphysis, whereas in this dog only one epiphysis was affected. Comparing radiographic findings with similar ones in humans, we considered some diseases that are rare or not described in animals. DEH is a rare condition described in children.‘-’ I It is a nonfamilial growth disorder involving preferentially the medial compartment of the lower limbs,‘-* and it is associated with epiphyseal h y p e r t r ~ p h y . ~ The physis and methaphysis can be involved.8 Radiographic findings are lack of radiopacity and ossification of the cartilage with secondary joint dege~ieration.~,’ Once a diagnosis of DEH is made, a skeletal survey needs

to be performed to evaluate for other sites of involvement.’ In this dog there was no involvement at other sites. In humans, three forms of DEH are described: 1) localized, affecting the bones of the hindfoot or ankle. but also possibly affecting an epiphysis; 2) classical, seen in a single lower extremity, particularly the talus, distal femur, and distal tibia1 epiphyses; 3) generalized or severe, involving the whole of a lower extremity from the pelvis to the foot or ankle. It can also be seen in more than one area of a single bone.8 When an epiphysis is involved, usually the medial compartment is most severely affected.’.I2 In our dog, only the medial aspect of one epiphysis was involved as described previously.* Surgery is indicated to correct a deformity or to restore function. In severe forms, surgery may

FIG.7. Eighteen months of age. The physes are closed, some bony foci appear united. and others appear separated from radiolucent tissue.

532

VIGNOLI ET AL.

2002

Frc. 8. CT examination at 18 months of age. The medial condyle (arrowhead) is irregular in shape with incompletely united bony foci.

actually stimulate hyperemia and abnormal bone growth.8 Histology, unlike radiology, is not conclusive for diagnosis of DEH.*.’ Actually, DEH, by histology alone, could not be differentiated from articular chondromatosis, exostosis, ost e o c h o n d r ~ m a s , ~or~ ~ from ” physiologic endochondral ossification, which takes place in the bone. Moreover, DEH can appear as a cap of disorganized cartilage with an underlying zone of normal endochondral ossification.6 Histologic features of DEH are characterized by an alternation of bone, cartilage, and fibrous tissue, including phases of normal endochondral ossification.’” Often chondrocytes are reported as h y p e r p l a s t i ~ .The ~ . ~ histologic findings in our dog are reminiscent of endochondral ossification taking place in several centers of ossification that do not unite, remaining joined together by fibrous bands. Gorham-Stout’s syndrome (“phantom bone” disease) was also considered. This condition of unknown pathogenesis is described in humans.13-15 It can be asymptomatic or painful with swelling. It involves long bones in children and young adults and facial bones in a d ~ 1 t s . ISevere ~ osteolysis usually involves the epiphysis and sometimes the diaphysis.’”Is This condition is clinically and radiographically similar to

findings in our dog, but histologically it is characterized by replacement of the bone by hemangiomatous tissue.’”’5 Another consideration is an arteriovenous fistula. These fistulas may be congenital or acquired as a result of trauma. They can be painful and ulcerative with radiographic signs of loss of bone opacity in the region of the fistula, along with mild periosteal reaction. Angiography is needed for diagn~sis.~ Trauma and infection were not considered as possible causes because the history, clinical signs, radiographic findings, and histopathology were not suggestive of these conditions. In our dog, the radiographic examination was useful to follow the changes of the lesion during growth and to evaluate the dysplastic origin of the disease. The CT images allowed confirmation of radiographic features and did not add important information about the condition, but CT was useful for guiding biopsy the bone.

FIG.9. Bone biopsy. There is an ossification center (0) surrounded by nests of chondrocytes (arrows) and a fibrous band (0that interposes with the adjacent trabecular hone (tb).

FIG.10. Biopsy. There are cartilagineous (c) and osseus (0) components of endochondral ossification in an ossification Center and CartilagineOUS metaplasia (arrows) of the surrounding fibrous hand (0.

VOL. 43, No. 6

DYSPLASIA EPIPHYSEALIS HEMIMELICA IN A BOXERPUPPY

533

REFERENCES 1. Konde LJ. Diseases of immature skeleton. In Thrall DE (Ed). Textbook of veterinary diagnostic radiology. 3rd ed. Philadelphia: WB Saun-

ders, 1998. 2 . Micheletto B. Patologia chirurgica e podologia. Torino: UTET, l97X

3. Kealy K, McAllister H. Diagnostic radiology and ultrasonography of the dog and cat. 3rd edition. New York: Harcourt, 2000. 4. Morgan JP. Radiology of veterinary orthopedics. Features of diagnosis. Napa, CA: Venture Press, 1999. 5. Burk RL, Ackerman N. Radiologia diagnoatica ed ecografia del cane e del gatto. 1st Italian edition on the 2nd USA edition. Torino: UTET,

.IYYI. ,.,~.

6. B ~ l l o ~ gPG. h Orthopaedic pathology. 3rd edition. St. Louis: Mosby-Wolfe, 1997. 7. Finidori G, Rigault P, Padovani JP, Naouri A. Hemimelica epiphysialis dysplasia. Rev Chir Orthop Reparatrice Appar Mot 1978 JuIAug;64(5):367-374. 8. A z o u ~EM. Slomic AM, Marton D, Rigault P, Finidori G. The

variable manifestations of dysplasia epiphysealis hemimelica. Pediatr Radiol l985;1S( 1):44-49. 9. Angeletti P, Lo Monte G. Sulla “dysplasia epifisaria emimelica” (iperostosi encondrale monomelica). Arch Putti Chir Organi Mov I971 ; 26344-356. 10. Martens M, Tanghe W, Mulier JC. Hemimelic epiphyjeal dysplasia. Acta Orthop Belg 1968;34(4):625-644. 11. Fontaine P, Maroteatix P, Fai-riaux JP, Saint-Auhert P. Heiniinelic epiphyseal dysplasia. Study of a case in a 10-month-old infant. Sem des Hop 197 1;47(14):861-865. 12. Campanacci M, Giunti A. Displasia epifisaria emimelica. Chir Or-gani Mov 1970;58(4):330-341. 13. Giraudet JS, Quintec JS, Peyrache MD, Courgod JP, Menkes CJ, Kerhou]l M, osteolyse massive idiopathique du femur,syndrome dit de Gorham-Stout. La Presse MCdicaIe 1995;24(15-22, Apr.):719-721. 14. Murphy JP, Doku HC, Carter BL. Massive osteolysis: phantom bone disease. J oralsurg]978;36(Aprjl):3]8-322. 15. Cadenat H, Bonnefont J , Barthelemy R, Fahe M, Courhelles R. La mandibule fantbme. Revue de Stomatologie 1976:77(7):X77-X89.