Keywords
implant-induced osteoporosis - radial–ulnar fractures - small-breed dogs - refracture
- risk factor
Introduction
Radial–ulnar fractures in small dogs are common; 14% of long bone fractures occur
in the distal one-third region of the radius.[1] A higher complication rate is reported in treating distal radial–ulnar fractures
in small-breed dogs than in large-breed dogs.[2] The treatment success rate with internal fixation using plates and screws is high,
and bone union was achieved in all cases without the development of nonunion.[3] In recent reports, the major postoperative complications requiring revision surgery
for fracture treatment using conventional and locking plate systems were 3%[4] and 9%,[5] respectively. However, no reports included refracture after radial union as a complication
for consideration. In human medicine, refracture is “a fracture caused by a load that
the normal bone can bear after bone union occurred. The fracture line coincides with
the initial fracture line or within the bone area that has changed due to the fracture
and its treatment.”[6] Refracture of the long bone diaphysis after bone union is a major postoperative
complication,[7] which can occur with and without plate removal. Plate removal may be a risk factor
for refracture. However, as no studies in small animal orthopaedics have investigated
the relationship between refracture after radial–ulnar union and plate removal, no
consensus exists that retaining the plate can reduce the refracture rate.
Structural changes (cortical bone necrosis and thinning of the cortical bone beneath
the plate) have been reported to be induced in the cortical bone where the plates
and screws are placed[8] and are termed implant-induced osteoporosis (IIO). Clinically, IIO is a cause of
refracture that occurs after implant removal.[9] A previous study reported that small-breed dogs with radial–ulnar fractures treated
with plates and screws developed IIO during the healing process.[10] However, no studies have investigated the association between refracture and IIO
after plate removal in treating radial–ulnar fractures in small-breed dogs. Therefore,
the aim of this study was to identify the risk factors for refracture after radial
union in small-breed dogs with and without plate removal.
Materials and Methods
Case Selection Criteria
This study included radial–ulnar fractures in small-breed dogs (weighing ≤5 kg) treated
with plates and screws from January 2010 to December 2016 at 10 hospitals (Asakadai
Animal Hospital, Hiro Animal Hospital, YPC Tokyo Animal Orthopedic Surgery Hospital,
Japan Animal Medical Centre, Mizuno Animal Clinic, Nippon Veterinary and Life Science
University Animal Medical Centre, Pet Clinic Anihos, Senkawa Dog and Cat Hospital,
Tanoue Animal Hospital, and Zephyr Animal Hospital). The inclusion criteria for this
study were as follows: the radial fracture was the first fracture; the radius fracture
was treated with a single plate and screws; no postoperative findings of bone and
implant infection; the radial union was achieved; no other orthopaedic injuries; and
no neurological, endocrine, digestive, or urological disorders.
Groups
All fractured limbs were classified into two groups based on plate removal during
the treatment period: non-plate removal group (plate group; P group) and plate removal
group (removal group; R group). In the R group, plate removal was not caused by structural
bone changes (osteopenia and decreased bone diameter) but rather by the owner's choice
to avoid implant-related complications. Implant-related complications (including skin
irritation, cold conduction, and implant loosening) were informed by veterinarians
based on previous reports.[11]
Medical Records Review
General information was extracted from the medical records in all cases regarding
the state of fractures, method of repair, and postoperative course, including general
information (dog breeds, age in months, weight at surgery, and sex), the state of
the fracture, method of repair (affected limb, method of fixation, and method of application),
and postoperative course (days until confirmed radial fracture healing, with or without
ulnar union, time to final follow-up or refracture after surgery, and age at the time
of the last follow-up).
In the P group, the final follow-up time was defined as the time at the last radiograph
for the non-refractured limb and the time at the refracture of the limb. The follow-up
period was the time between the fracture reduction surgery and the final follow-up.
In the R group, the period of plate fixation and the presence and duration of cast
splinting after plate removal were also recorded. The final follow-up time was the
time at the last radiograph for the non-refractured limb and the time at the refracture
of the limb. The follow-up period was the time between plate removal and the final
follow-up.
Radiography
Radiography was performed using digital radiography devices (VPX-40A, VPX-40B1, VPX-100A,
VPX-120A, VPX-200, VPX-500A; TOSHIBA, Tokyo, Japan), and the images of the forearm
were acquired in orthogonal orientation (kV and mAs as per the device). The X-ray
recording devices were XG-1V (Computed Radiography system, 10-bit grayscale resolution;
FUJIFILM, Tokyo, Japan), Capsula 2 (Computed Radiography system, 10-bit grayscale
resolution; FUJIFILM), Capsula V (Computed Radiography system, 10-bit grayscale resolution;
FUJIFILM), DR-ID300 (indirect flat panel detector, 10-bit grayscale resolution; FUJIFILM),
and Aero DR (indirect flat panel detector, 12-bit grayscale resolution; KONICA MINOLTA,
Tokyo, Japan).
Measurement Parameters for Radiographic Examination
Commercially available software (OsiriX MD ver. 10.0.2; Pixmeo, Bernex, Switzerland)
was used to measure the location of the fracture line, plate and screw positions,
radial morphology, and pixel values for the affected limb of each fracture from the
radiographs. Radial healing was evaluated using orthogonal radiographs with callus
formation and fracture line barely visible (stage of early clinical union) or fracture
line not visible, defined as a bone union.[12]
In the P group, the location of the fracture line at the initial and final follow-up,
the position and amount of relative change in the position of the most distal and
proximal screws at the time of fracture reduction surgery and final follow-up, working
length (WL), plate screw density, screw-to-bone diameter ratio (SBDR), radial thickness
(most distal and most proximal to the plate and at the site of the initial fracture),
and bone growth distal and proximal to the plate were measured. Working length, plate
screw density, and SBDR were measured as in the previous report.[5] Specifically, the number of empty holes between screws in bone fragments closest
to the fracture line was defined as WL. Plate screw density was defined as the percentage
of the number of screws to the total number of holes in the plate (number of fixed
screws/total number of holes in the plate × 100 [%]). Screw-to-bone diameter ratio
was calculated by dividing screw diameter (actual screw values) by radial width at
non-fracture limbs (screw diameter/radial width × 100 [%]). In the craniocaudal view
of the radiograph, as the presence of the plate renders it difficult to measure the
radial width, the radial width was measured at the narrowest point of the radius of
the non-fracture limbs when SBDR was calculated. In the R group, the location of the
fracture line at the initial and final follow-up and radial thickness and width (most
distal and most proximal to the plate, initial fracture site) were measured.
The pixel values were measured on the lateral radiographs of the affected limb immediately
after the reduction surgery, at the time of plate removal, and final follow-up. The
measurement area was between the most distal screw of the proximal fracture fragment
and the most proximal screw of the distal fracture fragment. As the pixel values differed
depending on the radiographic conditions, they were calculated as the pixel value
ratio (PVR) based on the humeral condyles on the same image and used as the bone mineral
density value ([Fig. 1]). The measurement methods were the same as those used in a previous study.[10]
Fig. 1 Measurements of pixel value ratio on a radiograph of the radius beneath the plate.
The area of measurement was the distance between the most distal and proximal screws
of the proximal and distal fracture fragments (rectangle). The pixel value ratio was
calculated based on the humeral condyle (circle) of the same radiograph.
In the mediolateral and craniocaudal views, the lines connecting the midpoints of
the distal and proximal radial articular surfaces were used as the length of the radius.
The fracture line location and the most distal and proximal screw positions were calculated
as a percentage of the length from the distal end of the radius and the length of
the radius (length from the distal end of the radius to the fracture line, most distal
screw position, or most proximal position/radial length × 100 [%]; [Fig. 2]). The amount of relative change in position of the most distal and most proximal
screws was calculated by subtracting the respective positions at the time of radial
reduction from the respective positions at the time of final follow-up (most distal
or most proximal screw positions at final follow-up [%] − most distal or most proximal
screw positions at radial reduction [%]). Moreover, the radial thickness and width
were calculated as ratios based on the radial length on the same radiograph (radial
thickness/radial length or radial width/radial length; [Figs. 3] and [4]).
Fig. 2 Measurement of the location of the fracture line on the radiograph. The location
of the fracture line was calculated as a percentage of the length from the distal
end of the radius and the length of the radius (length from the distal end of the
radius to the fracture line/radius length × 100 [%]). The method of measurement of
the most distal and most proximal screw positions is the same.
Fig. 3 Measurements of radial thickness on radiographs (mediolateral view). The radial thickness
was measured at the initial fracture site and the most distal or proximal to the plate.
In the mediolateral view, the line connecting the midpoints of the distal or proximal
articular surfaces of the radius was used as the length of the radius. The radial
thickness was calculated as ratios based on the radial length on the same radiograph
(radial thickness/radial length).
Fig. 4 Measurements of radial width on radiographs (craniocaudal view). (A) After plate removal. (B) After reduction. The radial width was measured at the initial fracture site and
the most distal or proximal to the plate. In the craniocaudal view, the line connecting
the midpoints of the distal or proximal articular surfaces of the radius was used
as the length of the radius. The radial width was calculated as ratios based on the
radial length on the same radiograph (radial width/radial length).
Statistical Analysis
Statistical analysis was performed on all affected limbs, with refracture as one of
the variables. The with or without plate removal, sex, affected limb (right or left),
fixation method (locking system or conventional system), plate application method
(bridging or compression), and the presence or absence of ulnar union were tested
with Fisher's exact test using IBM SPSS Statistics for Windows, version 28.0 (IBM
Corp., Armonk, NY).
Logistic regression analysis was performed within the P and R groups using Stata,
with the occurrence of refracture as the dependent variable and each variable under
ination as the independent variable. After extracting independent variables with p < 0.05 in univariate analysis, the final model was created using the forward–backward
stepwise selection method. Independent variables with strong correlations were excluded
to avoid multicollinearity. Multivariate analysis was performed using the final model
with a significance level of p < 0.05.
Normally and non-normally distributed data are shown as mean ± standard deviation
and median (range, minimum to maximum), respectively.
Results
Cases
The study included 181 limbs. Dog breeds in all cases are shown in [Appendix Table 1] (available in the online version). There were 56 male, 27 castrated male, 62 female,
and 31 spayed female dogs. The median age was 9 months (range, 1–107 months), and
the median body weight was 2.4 kg (range, 0.9–5.0 kg).
Among the 181 limbs affected by the fracture, 77 and 104 were right and left forelimbs,
respectively. Moreover, 116 and 65 plates were used in the locking and conventional
systems, respectively. A list of plates used for fracture reduction is shown in the
[Supplementary Table S1] (available in the online version). The techniques used for applying the plate for
fracture reduction were the bridging and compression methods in 174 and 7 limbs, respectively.
There were 161 and 20 affected limbs with and without ulnar union, respectively.
Refractures were observed in 10 of the 181 limbs (5.5%). Fisher's exact test revealed
a significant association between the occurrence of refracture and plate removal (p = 0.04). The adjusted residuals indicated significantly more non-refractured limbs
in the P group than in the R group. However, as the coefficient of association was
ϕ = 0.16, little association was found between the refracture and plate removal. Refracture
occurrence was not associated with sex, affected limb (right or left), fixation method
(locking system or conventional system), plate application method (bridge or compression),
and the presence or absence of ulnar union.
Non-plate Removal Group
In the P group, 141 limbs were included. Refractures were observed after radial union
in 5 of the 141 limbs (3.5%; [Appendix Table 2] [available in the online version]), and the remaining 136 (96.5%) were non-refracture
limbs. All refractures in this group occurred through the most distal screw hole (18.7 ± 3.5%
from the distal radius; [Fig. 5]). In some cases in the P group, only the screws were removed without plate removal
to reduce the stiffness of the plate and screw construction. The screws were removed
when the radial union was observed on the radiographs. Among the non-refractured limbs,
93 underwent screw removal, whereas 43 did not. Moreover, among the refractured limbs,
two underwent screw removal, whereas three did not. In both cases, screw removal was
performed approximately 2 months after fracture reduction. At this time, the screws
were removed, leaving only the most distal and proximal screws. Refracture occurred
approximately 40 days after screw removal in one case and approximately 110 days after
screw removal in the other.
Fig. 5 Case of refracture in the P group: case number 4. (A) At initial fracture (craniocaudal view). (B) After reduction (craniocaudal view). (C) At radial union (55 days after surgery: craniocaudal view). (D) Before refracture (108 days after surgery: craniocaudal view). (E) After refracture (205 days after surgery: craniocaudal view). (F) At initial fracture (mediolateral view). (G) After reduction (mediolateral view). (H) At radial union (55 days after surgery: mediolateral view). (I) Before refracture (108 days after surgery: mediolateral view). (J) After refracture (205 days after surgery: mediolateral view). The patient fractured
the radial–ulnar bone at 4 months and was treated with a plate and screws. Postoperative
weight-bearing was well-improved, and the radius union was observed at 55 days postoperatively
on radiographs. After 205 days postoperatively, however, the patient refractured at
the most distal screw site of the plate.
[Appendix Table 3] (available in the online version) shows the P group's general information and univariate
logistic regression analysis results. Univariate analysis revealed a significantly
lower age in months at the initial fracture and the final follow-up in the refracture
group than in the non-refracture group (p = 0.02 and p = 0.04, respectively). Moreover, days until confirmed radius fracture healing were
significantly lower in the refracture group than in the non-refracture group in the
univariate analysis (p = 0.02).
[Appendix Table 4] (available in the online version) shows the P group's radiographic measurements
and univariate logistic regression analysis results. In univariate analysis, there
was a significantly greater amount of position change of the most distal screw in
the refracture group than in the non-refracture group (p < 0.01). Moreover, the SBDR was significantly higher in the refracture group than
in the non-refracture group (p = 0.02).
The amount of position change of the most distal position of the screw and age in
months at the time of final follow-up were included in the final model and evaluated
using multivariate analysis. Age in months at the time of initial fracture was excluded
as it showed a strong correlation with age in months at the final follow-up. Multivariate
analysis indicated p < 0.05 for the amount of position change at the most distal screw position (odds
ratio [OR]: 1.79, p = 0.04, 95% confidence interval (CI): 1.01–3.14), which satisfied the significance
level (R
2 = 0.37, Hosmer–Lemeshow test p = 0.95).
Plate Removal Group
The R group included 40 limbs. Non-refracture was observed after radial union in 35
of the 40 limbs (87.5%), whereas refractures were observed in the remaining 5 limbs
(12.5%; [Appendix Table 5] [available in the online version]). All refractures in this group occurred at the
same site as that of the initial fracture (29.7 ± 7.4% from the distal radius; [Fig. 6]). The refracture site was identical to the initial fracture site based on the length
from the distal radius to the refracture site on the radiographs and subjective assessment.
Fig. 6 Case of refracture in the R group: case number 4. (A) At initial fracture (craniocaudal view). (B) After reduction (craniocaudal view). (C) At radial union (71 days after surgery: craniocaudal view). D) After plate removal (76 days after surgery: craniocaudal view). (E) After refracture (78 days after surgery: craniocaudal view). (F) At initial fracture (mediolateral view). (G) After reduction (mediolateral view). (H) At radial union (71 days after surgery: mediolateral view). (I) After plate removal (76 days after surgery: mediolateral view). (J) After refracture (78 days after surgery: mediolateral view). The patient fractured
the radial–ulnar bone at 10 months and was treated with a plate and screws. Postoperative
weight-bearing was well improved, and the radius union was observed at 71 days postoperatively
on radiographs. It was determined that radial union had been achieved, leading to
the removal of the screws except for the most distal and proximal. After 78 days postoperatively,
however, the patient refractured at the same site as the initial fracture site.
No p-values satisfied the significance level in the univariate logistic regression analysis
for each variable of the general information in the R group.
[Appendix Table 6] (available in the online version) shows the measurement of radiographs and the results
of the univariate logistic regression analysis in the R group. In the univariate analysis,
a significantly lower PVR at the final follow-up was observed in the refracture group
than in the non-refracture group (p = 0.03). Moreover, a significantly lower radial thickness ratio at the final follow-up
was observed in the refracture group than in the non-refracture group (p = 0.04).
The PVR at the final follow-up and radial thickness ratio at the initial fracture
site were included in the final model for multivariate analysis. Multivariate analysis
indicated that PVR (OR: 0.67, p = 0.04, 95% CI 0.47–0.97) and radial thickness ratio (OR: 0.05, p = 0.04, 95% CI 0.01–0.81) had p < 0.05 and satisfied the significance level (R
2 = 0.57, Hosmer–Lemeshow test p = 0.99).
Discussion
This study aimed to identify the risk factors for refracture after radial union with
and without plate removal in small-breed dogs. In the P group, only the amount of
position change of the most distal screw demonstrated statistical significance in
the final multivariate analysis model. Additionally, in univariate analysis, increased
SBDR and younger age in months were observed in the refracture group than in the non-refracture
group. These results indicate that the amount of position change of the most distal
screw, SBDR, and age in months may be risk factors for refracture in this population.
This suggests that the screw placed in the distal radius is relatively proximal as
the distal radius grows, resulting in the screw diameter becoming relatively large
compared with the bone width, thereby reducing bone strength and increasing the risk
of refracture.
In the plate removal group, PVR and radial thickness ratio of the initial fracture
site at the last follow-up demonstrated statistical significance in multivariate and
univariate analyses. These results indicate that bone mineral density and radial thickness
at the initial fracture site after plate removal may be risk factors for refracture.
This suggests that the IIO occurring beneath the plate increases the risk of refracture.
Internal fixation using plates and screws is a reliable treatment method for radial–ulnar
fractures in small dogs.[3]
[4]
[13] However, complications associated with this treatment, including dermatitis, cold
sensitivity, osteopenia, plate failure, screw loosening, malunion, and nonunion, have
also been reported.[14] It is considered that refractures after bone union are more likely to occur at the
same site as the initial fracture or from the screw removal site if the plate and
screws were all removed[15] or at the most distal and most proximal screw sites if the plate was not removed.[16] In the current cases where the plate was not removed, all refracture sites were
at the most distal screw hole, and a significant increase was found in the amount
of position change at the most distal position of the screw. Although no significant
differences were observed in the final model in the multivariate analysis, dogs in
the refracture group had younger age in months than those in the non-refracture group;
thus, the elongation of the radius during the growing period may have caused screw
position change. Generally, screws placed in the distal radial fragment are positioned
proximal to the growth plate. Therefore, when the radius grows, the distance between
the distal articular surface of the radius and the most distal screw increases, which
results in the most distal screw being relatively proximal. Moreover, radial–ulnar
fractures in small-breed dogs have been reported to occur more frequently (15–37%)
in the distal radius.[17] The refracture location in the P group (mean 18.7 ± 3.5% from the distal end of
the radius) is also consistent with the location where the highest frequency of radial–ulnar
fractures in small-breed dogs occurs. In the univariate analysis, the refracture group
in the P group had a significantly increased SBDR and younger age in months than the
non-refracture group. This may have resulted in a narrower bone width and larger SBDR.
As a large screw diameter relative to the bone width reduces bone strength, it is
recommended that SBDR should not exceed 0.4.[18] Similarly, in the external fixation techniques, External Skeletal Fixation (ESF)-related
fractures have been reported to occur when pins with diameters close to 30% of the
bone diameter were used.[19]
In vivo experiments on canine femurs showed that when 20% of the femoral bone diameter was
defective, there was a 42% reduction in torsional failure strength.[20] These results suggest that in dogs with a radial–ulnar fracture at the age of 3
to 5 months, the screw placed at the distal radius is relatively proximal as the bone
grows, and the screw diameter becomes relatively large compared with the bone width
at the most frequent site of distal radius fracture, which may result in reduced bone
strength and risk of refracture. When two screws are placed parallel to the radius
(T-plate or condylar plate), the SBDR is larger than when screws are longitudinally
placed (straight plate), which may contribute to the fracture through the screw holes.
However, in this study, four of the five cases of refracture with the retaining plates
were straight plates (screws could not be placed in parallel) and one was a condylar
plate (screws could be placed in parallel). These findings in this study are more
likely to occur in growing dogs, where there is some period of radial lengthening
after plate fixation. Therefore, repairing fractures of the distal end of the radius
in such dogs may require a smaller SBDR within which plate failure does not occur,
postoperative motion restrictions, and external splint fixation. Moreover, a report
has shown that longer WLs reduce the stiffness of the plate and screw constructions[21]; thus, the destabilization method may also be beneficial.
Refracture can occur as a complication after plate removal and is associated with
IIO, characterized by cortical bone necrosis and thinning beneath the plate.[22] IIO occurs early (8–12 weeks) after plate placement due to inadequate blood supply[23] and later (24–36 weeks) due to reduced mechanical stress.[24] Moreover, bone mineral density decreases at 28 weeks after plate placement in the
femur owing to changes in apatite orientation caused by reduced mechanical stress
on the cortical bone.[25] The increased inflammatory cytokines are associated with decreased bone mineral
density, resulting in cortical osteonecrosis at 36 weeks after plate placement in
the radius[26]; thus, there are many undefined pathogenesis of IIO. These reports suggest that
IIO is a risk factor for refracture after plate removal. However, risk factors for
refracture after plate removal in clinical cases have not been reported in dogs. Risk
factors for refracture after plate removal in clinical cases in animals have been
reported in horses, while comminuted fractures, aging, and infection are reported
risk factors for refracture, apart from IIO.[27] In this study, all refractures observed after plate removal occurred at the same
site as the initial fracture site. Additionally, the PVR and radial thickness ratio
of the initial fracture site at the final follow-up were significantly lower in cases
with plate removal, suggesting that refracture after plate removal in dogs is associated
with IIO. In the R group, PVR was significantly different only at the final follow-up;
therefore, we considered that PVR did not increase over time in the refracture group,
whereas it increased in the non-refractured group. It has been reported that the bone
remodelling cycle in 1- to 2-year-old dogs is approximately 12 weeks.[28] As refracture in the R group was observed in four of the five cases within 90 days
after plate removal, we considered that refracture may have occurred before bone mineral
density developed. However, the accurate cause of the nondevelopment of bone mineral
density remains unclear, and further case–control and long-term follow-up studies
are needed.
A limitation of this study is that variations in radial morphology between breeds
were not considered. As the length, thickness, width, and cortical and medullary bone
area of the radius vary between breeds, variations in measurement results are expected.
Another one is that the degree and duration of exercise limitation after plate removal
were not considered. As the bone remodelling cycle is approximately 12 weeks in 1-
to 2-year-old adult dogs,[28] it may be necessary to remove the exercise limits carefully and gradually after
plate removal. However, the degree of exercise limitation was not clearly documented
in the medical records. Not considering the size of the implants (plates and screws)
in the plate removal group is also a limitation. In this study, since the plate removal
group focused on the post-plate removal follow-up, the size of the implants was not
measured. Because IIO is caused by reduced mechanical stress on the bone beneath the
plate, the decreased radial thickness and reduced PVR may have been influenced by
the implant sizes. However, since radial thickness and PVR were significantly different
at the final follow-up (at the time of refracture) rather than immediately after plate
removal, it remains unclear whether implant sizes affected the results of this study.
Additionally, PVR was not measured in the P group. Although the coefficient of association
was lower, the refracture rate was higher in the R group than in the P group (12.5
vs. 3.5%, p = 0.04, ϕ = 0.16). All refracture cases in the P group were under 6 months of age
at the time of radius fracture, and the refractures occurred after 2 months during
the postoperative period. Our previous study reported that patients aged <6 months
of age at the time of radius fracture recovered from IIO after 2 months postoperatively.[10] Although plate removal may be possible in theory, refracture rates have increased
with plate removal. Deciding whether or not to remove the plate becomes challenging,
especially when both causes of refracture in the P and R groups occur simultaneously.
Additional study is needed on the long-term prognosis and management of IIOs that
occur after plate fixation to bone.
This study indicated a significant association between the occurrence of refracture
and plate removal (although the coefficient of association was ϕ = 0.16). In cases
where the radial fracture occurs at a young age, and the screw positioned at the most
distal end of the radius is expected to be relatively proximal as the bone grows,
it may require a smaller SBDR within which plate failure does not occur, postoperative
motion restrictions, and external splint fixation. Moreover, in cases with decreased
radial thickness and bone mineral density beneath the plate during plate removal,
not removing the plate may be an option as the risk of refracture is higher.
