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ORIGINAL RESEARCH

Veterinary Surgery
23:475-487, 1994

Incomplete Ossification of the Humeral Condyle in Spaniels

DENIS J. MARCELLIN-LITTLE, DrMedVet, DAVID J . DEYOUNG, DVM, Diplomate ACVS, Diplomate ACVA,
KELLl K. FERRIS, BS, and CLIFFORD M. BERRY, DVM, Diplomate ACVR

An evaluation of 157 dogs with humeral fractures was performed. Cocker spaniels were more
likely to have humeral condylar fractures (HCFs) than other breeds ( P < .0001). Male cocker
spaniels were at increased risk ( P < .00 I ). Cocker spaniels had more bilateral HCFs than other
breeds of dogs ( P < .OOI). Eighteen dogs (17 purebred spaniels and 1 crossbred spaniel) with
HCFs of unknown cause or occurring with normal activity were further studied, using radiography
of their humeral condyle bilaterally (n = 18), computed tomography (n = 3), biopsy (n = 2),
bone scintigraphy (n = 2), and genetic evaluation (n = 8). Fourteen of these 18 dogs had a
nonfractured contralateral condyle. Twelve (86%)of the 14 nonfractured humeral condyles had
a radiolucent line within the center of the condyle, 13 (93%)had radiographic signs of degenerative
joint disease and an abnormal medial coronoid process, and six (43%)had periosteal proliferation
involving the lateral epicondyle. Examination of biopsy samples from the fracture sites of two
cocker spaniels showed fibrous tissue present at the fracture surfaces. The results of this study
suggest an association between incomplete ossification of the humeral condyle in cocker spaniels
and Brittany spaniels and a high prevalence of HCFs. Eight affected cocker spaniels with available
pedigree information were found to be genetically related, suggesting that incomplete ossification
of the humeral condyle may be a genetic disease with a recessive mode of inheritance.
OCopjvYglif I994 by Thc. American COIILJ~~P of' rf'rtcw'narySzirgeons

H UMERAL CONDYLAR fractures (HCFs) are


common in dogs.'-4 Major trauma, such as
motor vehicle accidents, is the leading cause of HCF
or intense
posing factors.
have been suggested as predis-

Skeletally mature dogs that had humeral fractures


in dogs. HCFs can occur in association with normal and were brought to our hospital between 1983 and
activities such as running, climbing stairs, or jumping 1993 were evaluated to determine the risk factors
from a height of one meter or less. Compared with associated with these injuries. Based on the breed
other breeds, spaniels have a higher incidence of distribution of these animal patients, we hypothe-
HCF occurring with such a c t i ~ i t i e s . ~The
,~'~
history, sized that a heritable condition resulting in incom-
signalment, and fracture type suggest that a patho- plete ossification of the distal humeral condyle pre-
logical process may predispose spaniels to HCF. The disposes several spaniel breeds to HCF. To test this
pathogenesis of these fractures is unclear, however, hypothesis, further evaluation using radiology, com-
metabolic diseases,6 conformation of the e l b ~ w , ~ .puted~ tomography, nuclear scintigraphy, and his-

From the Department of Companion Animal and Special Species Medicine. the Department of Anatomy/Physiology/Radiology,
College of Veterinary Medicine. and the Department of Animal Science. North Carolina State University. Raleigh, NC.
Funded by the College of Veterinary Medicine, and the Orthopedic Research Group, North Carolina State University, Raleigh,
NC.
Address reprint requests to David 3 . DeYoung, DVM, Diplomate ACVS, Diplomate ACVA, Department of Companion Animal
and Special Species Medicine. College of Veterinary Medicine. North Carolina State University. Raleigh, NC 27606.
OCopyright 1994 by The American College of Veterinary Surgeons
0 16 1-349919412306-0006$3.00/0

47 5
476 INCOMPLETE OSSIFICATION O F THE HUMERAL CONDYLE

tology of fractured and intact humeri of 17 skeletally The following procedures were performed on selected
mature purebred spaniels and a crossbred spaniel dogs from group 3 when circumstances allowed.
with HCF was performed. To test the heritability
and mode of inheritance, 26 generation pedigrees of Biopsy and Histologicul Examination
skeletally mature cocker spaniels with an HCF were
Biopsy samples were obtained from two dogs during
compiled from the American Kennel Club registry surgical repair of the HCF using a 4.1-mm diameter
and familial analysis was performed. hollow crown drill bit (Howmedica, Inc., Rutherford,
NJ) to harvest a 3.2-mm diameter core biopsy specimen
MATERIALS AND METHODS of the lateral fracture fragment. The biopsy site. en-
larged to 4.5 mm, was used as a glide hole for lag screw
The medical records from 157 dogs who were pre- fixation. lnterfragmentary compression was achieved
sented to the North Carolina State University Veteri- with a fully threaded 4.5-mm cortical bone screw
nary Teaching Hospital (NCSU-VTH) between 1983 (Synthes, Inc., Paoli, PA). The bone biopsy specimens
and 1993 for treatment of a humeral fracture were re- were demineralized in ethylenediamine tetraacetate
viewed. Signalment, medical history, physical exami- (EDTA), embedded in paraffin, sectioned, and stained
nation findings, diagnosis, and treatment data were re- with hematoxylin-eosin.
corded for each dog. Standard orthogonal radiographic
projections that had been made of each dog's humeral Comput t.d Tomography
fracture were evaluated.
Twenty-eight of the 157 dogs were skeletally mature Three dogs underwent computed tomography (Model
spaniels with an HCF of unknown origin or occurring 0450, Pfizer, New York, NY) of both elbow joints. The
during normal activity. These 28 spaniels (27 purebred dogs were positioned in ventral recumbency with the
spaniels and one crossbred spaniel) were evaluated as three forelimbs extended. Contiguous 2-mm transverse images
different study groups. of the elbow joint were recorded. Reconstructed images
Group I included all 28 spaniels. Thirty-five fractures in dorsal and sagittal planes were evaluated.
(21 unilateral and seven bilateral) were present in these
dogs. Preoperative radiographs of 32 of the 35 fractures Bone Scint igruphjj
in this group were available for evaluation.
Group 2 consisted of 24 purebred cocker spaniels. Bone scintigraphy was performed on two dogs by in-
Prevalence of unilateral and bilateral fractures, sex, age, travenous injection of 370 to 740 megabequerels (10 to
and failure rate were compared between group 2 and 20 mCi) of 99"technetium-methylene diphosphonate
the other skeletally mature dogs with HCF treated at (osteolite, methylene diphosphonate, E. I. du Pont de
the NCSU-VTH. The weight of 20 male and four female Nemours & Co., Billerica, MA). Static 128 X 128 X 16
nonaffected cocker spaniels, randomly chosen from pixel images were obtained 2 hours after injection using
within the hospital population, was recorded and com- a large field of view gamma camera (ADAC ARC 3000
pared with the weight of the dogs in this group. Twenty- and DPS 3300, ADAC Laboratories, Milpitas, CA) with
nine fractures ( 19 unilateral and five bilateral) were a parallel hole general purpose collimator. Images were
present in these dogs. subjectively evaluated for areas of increased uptake of
Group 3 included 18 spaniels (17 purebred spaniels the radiotracer.
and 1 crossbred spaniel) that were selected for in-depth
follow-up evaluation. Pedigree Study
Using the American Kennel Club registry. 26 genera-
Radiography tion pedigrees were compiled for eight of the cocker span-
In all dogs in group 3 radiographs of the fractured con- iels in group 2. The coefficient of inbreeding (F,) of af-
dyles and the contralateral condyles were reviewed for the fected dogs was determined using the equation:
presence of a fragmented medial coronoid process, un-
united anconeal process, osteochondrosis of the humeral
Fx = z[(l/2)n1tn2t
( 1 + FA)]

condyle, the presence of ulnar subtrochlear sclerosis, and where FA was the inbreeding coefficient of a common
radial, ulnar, or humeral osteophytes." Also, the radio- ancestor, and n , and n2 were the numbers of generations
graphs were evaluated for the presence of periosteal pro- between that ancestor and the sire and the dam. respec-
liferation in the lateral epicondylar crest. tively." The coefficient of inbreeding of 100 cocker span-
M A R C E L L I N - L I T T L E ET A L 477

Table I . Clinical Data in ZX Skeletall) Mature Dogs (27 Purebred Spaniels and a Crossbred Spaniel)
With 35 HCFs Resulting From a Minor Trauma

Dog Agc Weight Surgical Complications/


No. (yrs) Sex (kg) Color Causc o f Fracture Outcome Concurrent Medical Problems

I* 8 15.5 Buff Climbing stairs


2* 8 12.3 Buff Running Diskospondylitis.
fibrocartilaginous embolism
3* 4 15.5 Bufl' Dog fight Urinary tract infection
4* 5 13.8 Buff Chasing ball Right-sided cardiomegaly,
babesiosis
5* 2 13.1 Buff No known trauma Nonunion of the olecranon. Heartworm disease
osteom ye11tis
6* 10 16.5 Buff Dog fight Exuberant callus -
7* 8 14.5 Buff Jumping doun - Heartworm disease
8* 7 18.0 Buff Walking - -

9* 7 13.0 Black No known trauma - -

lot 9 22.7 wsto No known irmma Failure of fixation -

I I* 4 13.6 Buff Jumping down Three failures of fixation


( 2 left side, I right side)
I2* 7 12.7 Black Climhing stairs - -
I3* 7 11.8 Buff Jumping down Failure of fixation -

14* 6 12.5 Black No known lrauma - Hip dysplasia. cruciate ligament


injury
I5* 5 21.8 Black Running - -

16* 7 21.8 Buff Jumping dow,n Three failures of fixation Radius curvus. thrombocytopenia
(same side)
17% 4 12.7 Buff Caught leg in cage door LumbO-SdCra\ disease
I8* 17.2 Buff Going down stairs - -
6
19* 3 11.4 Buff No known trauma Pin tract osteomyelitis -

20* 3 14.9 Black Going down stairs - H ypot hyroidism


21* 6 18.4 Buff Chasing ball -

22* 6 16.0 Black Climbing stairs - Lateral patellar luxation


23* 10 18.2 Buff N o known trauma Two failures of fixation Radius curvus, carpal laxity
(same side)
24* 5 12.3 Buff Dog fight -

25' 5 13.0 Black Jumping down Radius curvus


26t 10 17.7 W&O Jumping down -

27 t I2 17.5 W&M Digging - -


284 6 13.0 Black Chasing ball Delayed union, fixation Radius curvus, medial patellar
fai I u re luxation

5.9 * 2.09 14.9 -+ 2.95

Abbreviations: M, male: M/C. male castrated: F/S. female spayed: W&O, white and orange; W&M. white and mahogany.
* Cocker spaniel.
7 Brittany spaniel.
$ Mixed breed dog: sire. standard poodle: dam. cocker spaniel.
5 Mean and standard deviation. cocker spaniels.

iels without medical history of HCFs registered at the 2 were compared with the number of HCFs occurring
American Kennel Club between I978 and 1988 was col- in the general population presented to the NCSU-VTH
lected as a reference. Ancestors common to the eight af- (Statistical Analysis System [SAS], version 6.07.02, SAS
fected cocker spaniels and absent in the lineage of the 100 Institute Inc., Cary, NC). Also, the sex of affected cocker
cocker spaniels were identified. spaniels was compared with the sex of nonaffected
cocker spaniels presented to the NCSU-VTH during
St at istica 1 A na Iysis the study period. Using 1-tailed Fisher's exact test, the
Using 2-tailed Fisher's exact tests, the number of failure rate after internal fixation for repair of an HCF
unilateral and bilateral HCFs in cocker spaniels in group was compared between skeletally mature cocker span-
478 INCOMPLETE OSSIFICATION OF THE HUMERAL CONDYLE

Table 2. Additional Data in 28 Skeletally Mature Dogs (27 Purebred Spaniels and a Crossbred Spaniel)
With 35 Humeral Condylar Fractures Resulting From a Minor Trauma
~ ~~

Contralateral Condyle-
Affected Condyle Contralateral Condyle-Intact Fractured

Dog Fracture Fracture


No. Type FCP DJD PP Line FCP DJD PP Type FCP DJD PP Further Examination

I* Medial - - - - - - -
2* Y §Yes Yes No - - - -
3* Y Yes Yes No - - - -

4* Y §Yes No No - - - -
5* Y $Yes Yes Yes - - - - -
6* Y No No No - - - - F, .32%
7* Y §Yes No No - - - -
8* Y §Yes Yes No - - - -
9* Lateral §Yes No No - - - - -
lot Lateral - - - - - - - F, = .OO%
I I* Lateral Yes No No - - - - Y Yes No No F, = ,249~
12* Y §Yes Yes No CRL §Yes Yes Yes -
13* Lateral $Yes Yes Yes CRL Yes Yes Yes -
14* Medial Yes No Yes - - - - Medial Yes Yes No Bonescan
15* Y $Yes No No CRL Yes No Yes CT/Bone scan, F, = 2.22%
16* Lateral No Yes No CRL Yes Yes Yes Lateral Yes Yes Yes F, = 25.06%
17* Medial §Yes Yes No CRL $Yes Yes Yes F, = 13.36%
18* Y §Yes Yes No CRL §Yes Yes No F, = 25.17'70
19* Y $Yes No No - - - - Lateral No Yes No -
201 Y $Yes Yes No No Yes Yes No
21* Lateral $Yes Yes No No Yes Yes No -
22* Y §Yes Yes Yes PRL Yes Yes No Bone biopsy. F, = 3.91%
23* Lateral Yes No No PRL Yes No No Lateral Yes Yes No CT scan. Bone biopsy
24* Lateral Yes No No CR L Yes No No F, = 2.34%
25* Medial Yes No No PRL Yes No No -
26t Y §Yes No No - - - - Y §Yes No No F, = 6.25%
27t Lateral No Yes No PRL No Yes No Y $Yes Yes No CT scan
28$ Y - - - CRL Yes Yes Yes

Abbreviations: FCP, radiographic changes consistent with an abnormal medial coronoid process: DJD. degenerative joint disease: PP, periosteal
proliferation; Line, radiolucent line: §Yes. separate fragmented medial coronoid process: --% not available; Y, intercondylar fracture: Medial. fracture
of the medial portion of the humeral condyle: Lateral. fracture of the lateral portion of the humeral condyle: CRL. complete radiolucent line: PRL,
partial radiolucent line: F,. coefficient of inbreeding: CT scan, computed tomography scan.
* Cocker spaniel.
t Brittany spaniel.
$ Mixed breed dog: sire, standard poodle; dam. cocker spaniel.

iels and skeletally mature dogs from all other breeds. etally mature dogs. Thirty-five (64%)of the 5 5 HCFs
Two-tailed Student's t tests were used to compare the in skeletally mature dogs occurred with normal ac-
age of affected cocker spaniels with the age of the general tivity, 1 1 (20%) fractures resulted from major
population with an HCF and to compare the weight of trauma, eight (14%) fractures were of unknown
affected cocker spaniels with the weight of 24 control
cause, and one (2%) fracture was secondary to a fi-
cocker spaniels chosen randomly from within the hos-
pital population. P values < .05 were considered sig-
broblastic osteosarcoma.
nificant. The 43 fractures (seven bilateral) occurring with
normal activity or from an unknown cause occurred
RESULTS in 36 dogs. The breed distribution was 24 cocker
spaniels ( I 9 unilateral and five bilateral HCFs), three
C'linical Data Brittany spaniels (one unilateral and two bilateral
Of the I57 humeral fractures reviewed, 85 (54%) HCFs), two miniature pinschers, one Pekingese, one
were HCFs. Fifty-five of the HCFs occurred in skel- Maltese, one Chihuahua, a mixed breed dog from a
MARCELLIN-LITTLE E T AL 479

standard poodle (sire) and a cocker spaniel (dam), and four ( 17%)were females. The prevalence of HCF
and three mixed breed dogs of unknown lineage. was significantly higher in males than in females
The cocker spaniels had a significantly higher prev- when compared with the male/female ratio of the
alence of HCF than other breeds ( P < .OOO 1). population of cocker spaniels presented to the
Group 1 included 24 cocker spaniels. three Brit- NCSU-VTH during the study period ( P < .OOl).
tany spaniels. and one crossbred spaniel with 35 Dogs in group 2 were significantly older (median
HCFs (28 unilateral and seven bilateral). Data from age, 6 years old) than skeletally mature dogs of other
this group is presented in Tables 1 and 2. Eighteen breeds with HCF (median age, 3 years old; P < .O I).
of 35 HCFs ( 5 1%) were intercondylar fractures'.' The mean weight of dogs in group 2 (14.9 kg +- 2.9)
(also known as "Y" or "T" fractures' and did not differ significantly from the mean weight of
dicondylar'.'.' fractures) with separation of the me- the control cocker spaniels (14.4 kg ? 2.6). Five dogs
dial and lateral portions of the humeral condyle from in this group had bilateral HCF (21%). The preva-
the humeral shaft (Table 2). Twelve of the 35 HCFs lence of bilateral HCF was significantly higher in
(34%)were fractures of the lateral portion of the hu- cocker spaniels than in all other canine breeds ( P
meral condyle. with separation of the lateral portion < .001). Twenty-seven of the 29 HCFs in this group
ofthe humeral condyle from the humeral shaft. Five were surgically reduced and stabilized using internal
of 35 HCFs (1470)were fractures of the medial por- fixation. Follow-up radiographs were available for
tion of the humeral condyle, with separation of the 26 fractures. Implant failure and loss of fracture re-
medial portion of the humeral condyle from the hu- duction occurred in six of 26 fractures repaired
meral shaft. The preoperative radiographs of 32 (23%). Radiographic follow-up after surgical repair
HCFs were available for review. A separate frag- was available in 22 HCFs occurring in skeletally ma-
mented medial coronoid process was observed ra- ture dogs of nonspaniel breeds. Implant failure and
diographically in 18 of 32 HCFs (56%) and radio- loss of fracture reduction occurred in one of these
graphic signs suggestive of elbow degenerative joint 22 fractures (4.6%). The failure rate in group 2
disease and an abnormally shaped medial coronoid tended to be higher than the failure rate in skeletally
process were present in 28 joints with HCFs (88%; mature dogs from all other breeds after repair of
Table 3 ) . Periosteal proliferation was present on the HCF ( P = .078).
lateral epicondylar crest of five fractured condyles Group 3 included 18 spaniels: 15 cocker spaniels
( 16%). Seven dogs in this group, five cocker spaniels (dogs no. 1 1 to no. 25; Table I), two Brittany spaniels
and two Brittany spaniels, had bilateral HCFs (25%). (dogs no. 26 and no. 27; Table I), and a crossbred
Three dogs presented initially with bilateral HCFs. spaniel (dog no. 28; Table 1). Bilateral radiographs
The four other dogs sustained fractures on the con- of the elbow joints were available for all dogs in this
tralateral side 2 weeks (dog no. 11). 3 months (dog group.
no. 27). 6 months (dog no. 23), and 3 1 months (dog
no. 16) after the first HCF. Radiography
Group 2 consisted of 24 purebred cocker spaniels
with 29 HCFs (19 unilateral and five bilateral). The contralateral condyles were intact in 14 of 18
Twenty (83%) of the 24 cocker spaniels were males dogs in this group. Vertical radiolucent lines (0.5

Table 3 . Analksis of Radiographic Data in 32 HCFs Resulting From Minor Trauma in 28 Skeletally Mature Dogs

No. FCP SFCP DJD PP

Fractured condyles 32 28/32. ( 8 W ) 18/32 (56%) 18/32 (56%) 5/32 ( 16'7)


Intact cond\les 14 13/14 (93'7) 3/14 (21%) 10/14 (71%) 6 / I4 (43%)
Condkles with CRL or PRL 12 11/12 (92%) 3/12 (25%) 8/12 (67%) 6/12 (50%)
Condyles with CRL 8 8/X (l00"i) 3/8 (38%) 618 (75%) 618 (75%)
Condyles with PRL 4 314 ( 7 W ) 014 (0%) 2/4 (50%) 0/4 (0%)

Abbreviations: FCP. radiographic changes consistent with an abnormal medial coronoid process; SFCP. separate fragmented medial coronoid
process; DJD. degenerative joint disease; PP. penosteal proliferation: CRL, complete radiolucent line; PRL, partial radiolucent line.
480 INCOMPLETE OSSIFICATION OF THE HUMERAL CONDYLE

mm to 1 .O mm wide) were identified on the cranio-


caudal radiographic projection in 12 (86%)of the 14
intact condyles, and extended proximally from the
articular surface of the trochlea. In the 12 dogs with
a radiolucent line in their intact humeral condyle
the following findings were observed radiographi-
cally: partial radiolucent lines extending proximally
from the articular surface without reaching the phy-
seal scar (Fig 1) in four dogs (33%); complete radio-
lucent lines extending to the physeal scar or the su-
pratrochlear foramen (Figs 2 to 4) in eight dogs
(67%); a separate fragmented medial coronoid pro-
cess in three dogs (25%); radiographic features of an
abnormally shaped medial coronoid process (Fig 3;
Table 3) in 1 1 dogs (92%); degenerative joint disease

Fig 2. Cranio-caudal radiograph of the humeral condyle of dog


no. 18 (6-year-old male cocker spaniel). A radiolucent line ex-
tends from the articular surface proximally (arrow). The position
of the incomplete ossification of the distal humeral condyle is in
the anatomic location where normal fusion between the medial
and lateral humeral centers of ossification occurs.

of the elbow joint (Fig 4) in eight dogs (67%); and


periosteal proliferation on the lateral epicondylar
crest (Fig 3 ) in six dogs (50%).Two dogs in group 3
did not have a radiolucent line in the contralateral
humeral condyle but radiographic features consistent
with a fragmented medial coronoid process were
present. Seven dogs in group 3 had bilateral humeral
fractures. The humeral condyles of three of these
dogs had been evaluated radiographically before the
occurrence of the fracture of the contralateral con-
Fig 1. Cranio-caudal radiograph of the humeral condyle of dog
dyle. Two of these dogs had a partial radiolucent
no. 22 (6-year-old spayed female cocker spaniel). A radiolucent line in the intact condyles (dogs no. 23 and no- 27)-
line extends from the articular surface proximally (arrow). and one dog had a complete radiolucent line (dog
MARCELLIN-LITTLE E T AL 48 I

Fig 3. Cranio-caudal radiograph of the humeral condyle (A) and illustration (B) of dog no. 17 (4-year-old castrated male cocker
spaniel). A radiolucent line (a) extends from the articular surface proximally. A fragmented medial coronoid process (b) is present.
A smooth, chronic periosteal proliferation ( c ) is observed along the lateral epicondylar crest.

no. 16). Four spaniels (dogs no. 16, no. 23, no. 25, with a complete radiolucent line (dog no. 15; Fig
and no. 28; 14%)from group 3 had bilateral radius 6C) in group 3. A planar area of decreased atten-
curvus. uation was present perpendicular to the long axis of
the trochlea. Increased density was observed adjacent
Computed Tomography to the radiolucent line on all three computed to-
Computed tomography was used to evaluate the mography scans.
elbows of two dogs with a partial radiolucent line
(dog no. 23 and no. 27; Fig 5) in group 3. A linear Bone Scintigruphy
area of hypoattenuation had a width, position, and Bone scintigraphy was performed on two dogs in
orientation similar to the radiolucent line, the area group 3. One dog had increased radiotracer uptake
started caudally and extended cranially for one third in both distal humeri. Radiographically, this dog had
to one half of the diameter of the condyle (Fig 6B). a nonunion of the fractured medial portion of the
Computed tomography was performed on one dog humeral condyle bilaterally. Bone scintigraphy was
482 INCOMPLETE OSSIFICATION OF THE HUMERAL CONDYLE

Fig 4. Cranio-caudal radiograph of the humeral condyle (A) an1 illustration (B) of dog no. 28 (6-year-old castrated mixei bree
dog [sire, standard poodle; dam, cocker spaniel]). A radiolucent line (a) extends from the articular surface proximally. Also, signs
of advanced degenerative joint disease are present near the medial coronoid process (b) and the epicondyles (c).

performed on the second dog 5 years after repair of lous bone. Fibrous tissue, increased osteoclastic ac-
a unilateral HCF. The scan demonstrated increased tivity, and an increased number of plasma cells were
radiotracer uptake in the contralateral elbow in the observed at the fracture sites (Fig 8). No chondro-
region of the lateral epicondylar crest. Radiograph- cytes or cartilage matrix were observed microscop-
ically, periosteal proliferation was present on the lat- ically.
eral epicondylar crest.
Genetic Anulysis
Histoputhalogy
The mean coefficient of inbreeding of eight af-
Biopsy samples were collected at the time of sur- fected cocker spaniels from group 3 was 9.08% (+
gical repair of an HCF from two dogs in group 3. 10.73; Table 2). The mean coefficient of inbreeding
Both fractures had occurred 4 days previously. The in the control population of cocker spaniels was
bone at the fracture surfaces in the two biopsy sam- 2.1 1% (+ 5.20). The eight affected animals with ped-
ples grossly appeared smooth and eburnated (Fig 7). igree data all had the same eight common ancestors
Histologically, the tissue consisted of dense cancel- present in their pedigree within 12 generations. At
MARCELLIN-LITTLE E T A L 483

We hypothesized that a heritable condition re-


sulting in incomplete ossification of the distal hu-
meral condyle predisposes several spaniel breeds to
HCF. In the normal canine humeral condyle, two
separate centers of ossification appear at 14 k 8 days
after birth.'* One ossification center includes the
capitulum and the lateral aspect of the humeral con-
dyle, whereas the other ossification center develops
Fig 5. Line drawing demonstrates the positioning of the dogs into the trochlea and the medial aspect of the con-
on the computed tomograph palate, with the elbow in an extended dyle. As ossification progresses, the two centers of
position. The plane indicates the level of the computed tomo- ossification are separated by a thin cartilaginous plate
graphic sections in Fig 6. (Fig 9),* and normally unite at 70 k 14 days after
birth.I3
The radiolucent lines identified on the radiographs
least one of the common ancestors was present on of 1 1 skeletally mature purebred spaniels and one
both the sire and dam sides of the genealogy of af-
crossbred spaniel had an identical location to the
fected dogs. Also, these common ancestors were not cartilaginous remnant present between the lateral
ancestors of any of the 100 control cocker spaniels.
and medial centers of ossification of the humeral
condyle in immature dogs. All 12 dogs in which a
DISCUSSION
radiolucent line was identified had an HCF in the
Spaniels, in general, appear to be predisposed to contralateral elbow. In addition, the HCF of the
fractures involving the distal humeral condyle, in purebred spaniels and crossbred spaniel occurred at
comparison with other breeds treated at the NCSU- the junction of the two condylar ossification centers.
VTH. Affected dogs were often middle-aged males In this study, intercondylar fractures ( 5 1%) were
of normal body weight. These findings are consistent more common than previously reported in
with previous reports of HCF in spaniel^.^.^.^ The Fractures of the lateral portion of the humeral con-
cause of the HCF in our group of spaniels was either dyle (34%) were more common than fractures of the
unknown or considered to be due to minor trauma. medial portion of the humeral condyle (14%).
These findings suggest the presence of a predisposing The radiolucent line in the condyle was observed
factor in spaniels that ultimately results in an HCF. only with a cranio-caudal radiograph of the humeral
Although multiple causes have been suggested in condyle. The correct orientation was achieved by
previous ~ - e p o r t s , ~ .none
~ . ~ *has
* been investigated. placing the dog in ventral recumbency with the fore-

Fig 6. Computed tomographic images from three different dogs taken at the level of the elbow joint illustrated in Fig 5. (A) Normal
humeral condyle, (B) humeral condyle with mildly abnormal ossification (dog no. 23, 10-year-old castrated male cocker spaniel),
and a humeral condyle with severely abnormal ossification (dog no. 15, 5-year-old male cocker spaniel). Arrows point at the area of
incomplete ossification. The subchondral bone is thickened around the area of incomplete ossification in both B and C.
484 INCOMPLETE OSSIFICATION OF T H E HUMERAL CONDYLE

with a complete radiolucent line, periosteal prolif-


eration on the lateral epicondylar crest could result
from two mechanisms. First, microfractures and in-
stability of the lateral aspect of the humeral condyle
could result in a bone healing response. Second, ab-
normal stresses placed on the weakened condyle with
incomplete ossification could lead to remodeling of
the lateral epicondyle to strengthen the bone. Peri-
osteal proliferation was not observed in condyles
with incomplete radiolucent lines, suggesting that
instability was not present.
Four spaniels with incomplete ossification of the
humeral condyle also had bilateral radius curvus,
consistent with premature closure of the distal ulnar
physis. The relationship of these findings to the frag-
mented medial coronoid process and incomplete os-
sification of the humeral condyle cannot be deter-
mined from this study. However, it is possible that
growth discrepancies between the radius and ulna
could alter the forces applied to the growing humeral
condyle and interfere with normal ossification. The
absence of recognized incomplete ossification of the
humeral condyle in severely chondrodysplastic dogs
Fig 7. Fractured surface of the humeral condyle in dog no. 3 with radius curvus makes the association of these
(10-year-old castrated male cocker spaniel), intraoperatively.
Sclerotic cancellous bone is present in the humeral condyle (ar-
two problems purely speculative.
rowheads). A biopsy sample has been collected from the center The consistent presence of radiographic abnor-
of the condyle (arrow). malities in humeral condyles with incomplete ossi-

leg extended, and the radiographic beam directed


from 15" cranio-medially to 15" caudo-laterally.
Rotation of the condyle greater than 5 degrees from
that incidence resulted in an inability to image the
radiolucent line (unpublished data, Marcellin-Little
DJ, 1992). In a recent report of unilateral HCF, the
inability to detect a radiolucent line in the contra-
lateral condyle was possibly caused by malposition-
ing of the limb.'
Fragmented medial coronoid process and devel-
opmental elbow joint disease are uncommon in
spaniel^.'^.'^ In this study, fragmented medial cor-
onoid processes were common findings in elbows
with fractured or intact humeral condyles. Fracture
of the medial coronoid process could result from
motion between the medial and lateral portions of Fig 8. Histology of the fractured surface. (Hematoxylin-eosin;
original magnification X90.) The biopsy sample was collected
the humeral condyle. in a 4-day-old fracture of the lateral portion of the humeral con-
Frequently, a smooth periosteal proliferation was dyle (dog no. 23, 10-year-old castrated male cocker spaniel).
observed radiographically along the lateral and cau- Fibrous tissue (arrows) covers dense cancellous bone (arrow-
dal surface of the humeral condyle. In intact condyles heads).
MARCELLIN-LITTLE ET AL 485

Fig 9. Contact radiograph (A), gross morphology (B), and his-


tology (I lematoxylin-eosin; original magnification X4) (C) of a
distal humeral condyle of a 10-week-old dog. The distal humeral
condylar physeal plate (arrowheads) is observed. A cartilaginous
plate (arrows) separates the centers of ossification of the medial
and lateral aspects of the distal humeral condyle.

fication supports the recommendation for routine trauma), clinical signs (non-weight bearing lameness
radiographic evaluation of the contralateral elbow and pain on flexion of the elbow joint), and the fact
after an HCF occurring with normal activity in a that HCF are often unilateral (75%).
mature spaniel. Examination of the biopsy specimens obtained
Chronic HCF resulting in extensive degenerative from the fracture sites in two dogs showed fibrous
joint disease may be misdiagnosed as a neoplastic pro- tissue and increased numbers of plasma cells, si:g-
cess. In two spaniels presented at NCSU-VTH with gesting a chronic inflammatory process. Dense can-
HCF (dogs no. 10 and no. 27), a preliminary radio- cellous bone adjacent to the fracture site was con-
graphic diagnosis of bone neoplasia had been made. sistent with the radiographic appearance of bone
The radiographic diagnosis of neoplasia is suggested sclerosis, suggesting prior bone remodeling in the
by the signalment (older dogs), history (absence of humeral condyle.
486 INCOMPLETE OSSIFICATION OF THE HUMERAL CONDYLE

The high failure rate of surgical repair in affected The epidemiological, radiographic, and histolog-
cocker spaniels may have been caused by abnormal ical findings in this study support the hypothesis that
healing of the condyle. The presence of fibrous tissue affected spaniels had a disturbance in ossification of
or dense cancellous bone, or both, at the fracture the humeral condyle, resulting in a mechanically
site may have delayed or prevented bone healing. weak region in the condyle, predisposing affected
Micromotion at the fracture site may lead to cyclic dogs to fractures. Incomplete ossification and de-
fatigue and failure of the implant. velopment of a fibrous union within the condyle re-
Very mild abnormalities were present on radio- sulted in variable clinical expression of the disease,
graphs and computed tomography scan of four dogs ranging from partial fusion with no clinical signs to
with partial radiolucent lines. However, with no ap- complete fractuw of the humeral condyle. Osteo-
parent trauma, two of the four dogs fractured their arthritis, supracondylar periosteal reaction, or any
humeral condyle within 6 months after the initial combination of these signs may be observed radio-
evaluation, suggesting that these humeral condyles graphically. Because the disease may have a genetic
were at increased risk of fracture regardless of the basis, we recommend that affected dogs and their
seventy of the radiographic changes. Prophylactic sires and dams not be bred. Elbow joints of the lit-
placement of a transcondylar bone screw in non- termates of affected dogs that are maintained for
fractured condyles could be considered when a ra- breeding should be evaluated radiographically. The
diolucent line or a periosteal reaction are present. coefficient of inbreeding should be kept low in af-
Lameness was inconsistent in dogs with a radio- fected families. Because fractures occur mostly in
lucent line in the humeral condyle. Only two of eight middle-aged dogs, affected dogs may have had off-
dogs (no. 17 and no. 28) with a radiolucent line and spring before a humeral condyle with incomplete
degenerative joint disease were lame. None of the ossification was diagnosed, making control of this
four dogs with a radiolucent line and no degenerative disease difficult. Further studies are necessary to de-
joint disease were lame. The diagnosis of incomplete fine the precise pathogenesis and genetic transmis-
sion of humeral condyles with incomplete ossifica-
ossification of the contralateral humeral condyle was
tion in the dog.
often made after the occurrence of an HCF or a
chronic forelimb lameness caused by degenerative ACKNOWLEDGMENT
joint disease of the elbow joint.
The incomplete ossification of the humeral con- We thank Bonnie DeYoung for her technical assistance;
dyle in cocker spaniels appears to have a genetic ba- Frank Fair of the American Kennel Club for his help in
compiling pedigree information; Ree Coan, Wendy Sav-
sis. The coefficient of inbreeding of the eight affected
age, Jennifer Graeber, and Joe Trumpey for photography
dogs with genetic information tended to be higher and illustration; and Anne Hellkamp and Judith Jaya-
than the coefficient of inbreeding ofthe control pop- wickrama for their statistical assistance.
ulation. Also, specific common ancestors to both the
sire and the dam of affected dogs were identified. REFERENCES
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