1
1
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Detection of spondylosis
OPEN ACCESS deformans in thoracolumbar and
lumbar lateral X-ray images of
EDITED BY
Ryou Tanaka,
Tokyo University of Agriculture and
Technology, Japan
REVIEWED BY
dogs using a deep learning
Seungjo Park,
Chonnam National University,
Republic of Korea
network
Sang-Kwon Lee,
Kyungpook National University,
Republic of Korea Junseol Park1,2† , Hyunwoo Cho3† , Yewon Ji1 , Kichang Lee1 and
*CORRESPONDENCE Hakyoung Yoon1,2*
Hakyoung Yoon
1
[email protected] Department of Veterinary Medical Imaging, College of Veterinary Medicine, Jeonbuk National
University, Iksan, Republic of Korea, 2 Biosafety Research Institute and College of Veterinary Medicine,
†
These authors have contributed equally to Jeonbuk National University, Iksan, Republic of Korea, 3 Department of Electronic Engineering, Sogang
this work and share first authorship University, Seoul, Republic of Korea
KEYWORDS
disc instability, intervertebral disc space, artificial intelligence, bony spur, intervertebral
disc disease, canine
FIGURE 1
Grading of spondylosis deformans. Grade 0: no bony spur at the vertebral endplate; Grade 1: small bony spur at the edge of the vertebral endplate
not extending past the endplate; Grade 2: more developed bony spurs, but not connected to adjacent vertebra; Grade 3: bony spur connected to
adjacent vertebra forming bony bridges.
FIGURE 2
Example of manual segmentations. In the thoracolumbar lateral X-ray images (A), the vertebral body (yellow), intervertebral disc space (green),
intervertebral foramen (pink), and spondylosis deformans (orange) are labeled with separate colors using a segmentation tool (MediLabel software) to
distinguish them (B).
validation, and test followed an approximate ratio of 80:10:10, and 2.2.2 Evaluation of radiographic images
the training and validation data were chosen randomly. A total On thoracolumbar lateral radiographs, the vertebral body from
of 119 thoracolumbar lateral X-ray images (92 images for training T10 to L3 was evaluated, while on lumbar lateral radiographs, the
data, 13 images for validation data, and 14 images for test data) and vertebral body from L1 to L7 was evaluated. Spondylosis deformans
146 lumbar lateral X-ray images (124 images for training data, 12 was classified into three grades, as shown in Figure 1 (1, 6, 20). The
images for validation data, and 10 images for test data) were used area where spondylosis deformans occurred was checked, and the
to develop deep learning model. most frequently affected area was evaluated.
FIGURE 3
Example of data augmentation during the training phase. (A) The original image is randomly augmented by (B) adaptive histogram equalization, (C)
horizontal flip, (D) vertical flip, (E) rotation, (F) zoom-in, and (G) zoom-out. All spatial augmentations were performed using cropping or
zero-padding to match the original dimensions. The rotation angle was randomly selected between −45 and 45 and the zoom range was selected
between 0.5× and 1.5× of the original dimensions.
2.3 Deep learning model development resolutions. To maintain the aspect ratio and detailed information
of the images, we set the input resolution to 1024 pixels in
2.3.1 Manual segmentation height and 512 pixels in width. To increase data diversity and
The X-ray images used in this study were manually labeled robustness, the images were augmented by flipping (horizontal,
by 13 veterinary clinicians (residents in the Veterinary Medical vertical), rotation, adaptive histogram equalization (21), zooming
Imaging Department of the Teaching Hospital of Jeonbuk in with random cropping, and zooming out with a zero pad.
National University) using MediLabel software (Ingradient, Inc., Each augmentation was utilized during the training phase with a
Seoul, South Korea). In thoracolumbar and lumbar lateral X- probability of 0.5. Figure 3 shows an example of the augmented
ray images, separate colors were used for labeling to distinguish samples. In addition, the image intensity was normalized into the
spondylosis deformans, vertebral bodies, intervertebral disc space, range of 0 to 1 as shown in Eq. 1, where I is the original image, and
and intervertebral foramen. To label the areas of spondylosis Imax and Imin represent the maximum and minimum values of the
deformans, two veterinarians analyzed the radiographs and selected image intensity, respectively.
areas of common agreement. Figure 2 shows an example of manual
segmentation of a lumbar lateral X-ray image. I − Imin
Inorm = (1)
Imax − Imin
FIGURE 4
Structural diagram of the employed deep learning model. In the encoding stage, the features were downsampled (indicated by the orange arrow),
whereas the feature dimensions were expanded using convolution blocks (highlighted by the green arrow). Each convolution block comprised a 3 ×
3 convolution and an activation function. In the decoding stage, the features from the encoding stage were concatenated with the upsampled
features after the implementation of a skip connection and an attention gate. Subsequently, the features were sequentially upsampled to their
original resolutions. The final prediction included three channels, each representing a different pixel class.
FIGURE 5
Examples of manual vs. automated segmentation of vertebrae, intervertebral disc space, and foramen. Results of manual segmentation (A, C) of
vertebral body, spondylosis deformans, intervertebral disc space and intervertebral foramen; automatic segmentation (B, D) in thoracolumbar and
lumbar lateral radiographs.
of this model is based on attention U-Net (22), which has shown 2.3.4 Loss function and implementation details
promising results in medical image segmentation tasks. To cope Recent studies proposed various loss functions for successful
with the large variance in dog size (range: 1.64 kg−36 kg), the segmentation under various conditions (23, 24). To successfully
modified attention U-Net in this study was designed to have train the designed model to simultaneously segment the
deeper feature extraction (i.e., multiscale features) than the original vertebral bodies and detect spondylosis deformans, we utilized
attention U-Net (22) architecture. The designed network extracts a combination of two loss functions. The utilized loss function
features at 7 levels, reducing the spatial resolution from (1024, 512) consists of a region-based loss function and a distribution-based
to (8, 16) for height and width, respectively. The filter dimensions loss function (23, 24). The region-based loss function allows the
of the model (F1 , F2 , F3 , F4 , F5 , F6 , F7 ) were selected as deep learning model to successfully segment the vertebral bodies
16, 32, 64, 128, 256, 512, and 1024, respectively. The attention from images, and the objective of the distribution-based loss
gate introduced in the attention U-Net retained in its original function is to create a deep learning model to detect spondylosis
structure (22). deformans pixel-wise. The weighted categorical cross-entropy loss
TABLE 1 Cohen’s kappa analysis between a veterinary clinician and deep learning model for detection of spondylosis deformans.
Kappa value Sensitivity (%) Specificity (%) PPV (%) NPV (%)
∗
Validation dataset 0.813 87.5 98.5 77.8 99.3
∗
Test dataset 0.839 98.4 86.3 86.1 98.4
95% CI, 95% confidence interval; PPV, positive predictive value; NPV, negative predictive value.
Experimental values were considered significant at p < 0.01∗ .
2 100 26 26
(25) and focal Tversky loss function (26) were used. The total loss To evaluate how closely matched spondylosis deformans were
function is expressed as follows: detected by the deep learning model and veterinary clinicians,
Cohen’s kappa analysis was performed to check sensitivity and
1 + yŷ
TI(y, ŷ) = specificity. Additionally, Cohen’s kappa test was used to determine
1 + yŷ + β(1 − y)ŷ + (1 − β)y(1 − ŷ) inter-veterinarian agreement on the areas determined to have
X
3
spondylosis deformans. Cohen’s kappa results were interpreted
LFTL (ŷ, y) = (1 − TIc )γ
as follow: values ≤ 0.00–0.20 indicated non- to slight, 0.21–0.40
c=1
indicated fair, 0.40–0.60 indicated moderate, 0.60–0.80 indicated
X
3
LWCE (ŷ, y) = − w(c) × y(c) log ŷ(c) substantial, and 0.80–1.00 indicated almost perfect agreement (31).
c=1 To identify the relationship between the presence of
LTOTAL (ŷ, y) = LWCE (ŷ, y) + LFTL (ŷ, y) spondylosis deformans and the occurrence of thoracolumbar
disc disease-related neurologic signs, a Chi-square test was
where y, ŷ represent the prediction and ground-truth probability performed. The values were determined to be statistically
map, c is the corresponding class (i.e., background, normal significant at p < 0.05.
vertebral body, spondylosis deformans), w is the class weighting SPSS version 29.0 (SPSS Corp., Armonk, NY, USA) was used for
factor, and β, γ are hyperparameters. The w was set to 1, 1, and statistical analyses.
5 for the background, normal vertebral body, and spondylosis
deformans. β, γ were set at 0.3 and 0.75. The weighting factors
and hyperparameters were determined empirically to obtain the
best results. To optimize the utilized loss function, the Adam 3 Results
optimiser (27) with a learning rate of 1e−4 was used, and early
stopping criteria were used to obtain the best result. The proposed 3.1 Animals
methods were implemented using MONAI (28) and PyTorch
(29) frameworks. A total of 29 breeds were enrolled in the study: Maltese (n = 39),
Pomeranian (n = 18), Poodle (n = 16), Dachshund (n = 13), mixed
breed (n = 11), Shih Tzu (n = 9), Pekingese (n = 9), Cocker Spaniel
2.4 Time measurement (n = 8), Miniature Poodle (n = 5), Chihuahua (n = 4), Bichon Frise
(n = 4), Beagle (n = 3), Yorkshire Terrier (n = 3), Golden Retriever
For the 25 lateral thoracolumbar and lumbar X-ray images used (n = 2), German Shepherd (n = 2), Old English Sheepdog (n = 2),
as validation data, the time required per image to detect spondylosis Jindo (n = 2), Boston Terrier (n = 1), Labrador Retriever (n = 1),
deformans by a veterinary clinician and by the deep learning model Miniature Pinscher (n = 1), Pompitz (n = 1), Samoyed (n = 1),
through auto-segmentation was recorded and compared. Siberian Husky (n = 1), Schnauzer (n = 1), Shetland Sheepdog (n
= 1), Spitz (n = 1), Welsh Corgi (n = 1), Sapsaree (n = 1), and
Whippet (n = 1). The average weight was 7.42 kg (range: 1.64–
2.5 Model accuracy and statistical analysis 36 kg), and the average age was 8.81 years (range: 0.7–17 years), and
for seven dogs, there were no information regarding body weight.
Dice similarity coefficient (DSC) was used to confirm whether This study included 91 male dogs (24 intact, 67 castrated) and 71
auto-segmentation and manual segmentation were in close female dogs (20 intact, 51 spayed).
TABLE 3 Relationship of the presence or grade of spondylosis and clinical signs related to the disc disease in 152 dogs.
No. of dogs not presenting neurologic signs 64 (42.1%) 13 (8.6%) 9 (5.9%) 8 (5.3%) 94 (61.8%)
To evaluate the performance of the model, the DSC between Grade 2 2 (0) 3 (1) 6 (0) 1 (0) 6 (1) 7 (0)
manual and automated segmentation was calculated for a Grade 3 0 (0) 0 (0) 4 (1) 2 (0) 6 (1) 3 (1)
validation dataset of 25 dogs. Post-processing, the average DSC
T, thoracic; L, lumbar; Numbers in parentheses indicate number of dorsal spondylosis
value for the vertebral body was 0.910 ± 0.038 (mean ± SD). deformans cases.
The DSC values of the intervertebral disc space and foramen
TABLE 5 Number of spondylsis deformans cases and grading of dogs in
were 0.787 ± 0.056 and 0.779 ± 0.083, respectively. Figure 5
146 lumbar lateral X-ray images.
shows an example of manual and automated segmentation of the
vertebral body, spondylosis deformans, intervertebral disc space, L1- L2- L3- L4- L5- L6-
and intervertebral foramen. L2 L3 L4 L5 L6 L7
Grade 1 11 (3) 11 (0) 5 (1) 6 (3) 1 (1) 2 (2)
FIGURE 6
Distribution of sites for spondylosis deformans and grading of dogs in 119 thoracolumbar lateral X-ray images. T, thoracic; L, lumbar.
FIGURE 7
Distribution of sites for spondylosis deformans and grading of dogs in 146 lumbar lateral X-ray images. L, lumbar.
images of dogs have been developed and commercialized, and However, in this study, the DSC for the intervertebral disc
studies have been conducted to auto-segment gross head and space and intervertebral foramen were slightly lower, reaching up to
neck tumors for radiation therapy and automatically detect kidney 0.787 and 0.779 respectively. The DSC value for the intervertebral
calculi and measure kidney volume in CT images in dogs; however, disc space and foramen were unavailable in the aforementioned
there have been no studies in the literature on a deep learning human study, which is likely because the size of the disc space and
model to automatically recognize disc diseases in X-ray images of intervertebral foramen is relatively smaller than that of the vertebral
dogs (32–34). bodies. Inconsistent imaging of the vertebral endplates can cause
First, a segmentation model was developed to automatically disc space distances to appear shorter than they actually are or
detect the vertebrae and disc space and was then compared to deep results in unclear margins. Moreover, intervertebral foramen may
learning models developed for lumbar vertebrae detection in prior have ambiguous borders with adjacent structures. Additionally,
human literature. The mean intersection over union value, a term the substantial relative weight difference between breeds in dogs
similar to DSC for vertebral bodies, was found to be 0.8–0.88 in a compared to humans might have also affected this value. We
human study, and when the DSC value of the vertebral body (0.910) assume that training with a larger number of images will be
in this study was converted to the mean intersection over union required to improve the recognition rate of disc spaces and
value, it was found to be 0.835, showing the ability to recognize intervertebral foramen.
the vertebral body at a similar level to the previous human In this study, the most affected areas of spondylosis deformans
research (9). in thoracolumbar and lumbar lateral radiographs of dogs were
identified as T12-T13 and L2-L3, with T12-L5 being more affected When the association between the presence of spondylosis
overall. Previous studies (3, 4, 35) have found that the most deformans and thoracolumbar and lumbar disc disease-related
affected area was somewhat different (L1-L3); however, the overall clinical signs was examined, no statistical significance was found.
commonality of occurrence in the vertebral region (T12-L5) was However, dogs with spondylosis deformans were more likely to
similarly confirmed. exhibit clinical signs associated with disc disease. However, no
Of the total 163 cases of spondylosis deformans identified association was found between clinical signs and the grade of
in 265 animals, 30 cases of dorsal spondylosis deformans spondylosis deformans, and the presence of spondylosis deformans
(18.4%) were identified. However, of the total 63 spondylosis did not differ by breed in this study. Previous studies also
deformans in the test dataset, only 3 cases of dorsal spondylosis have similarly shown that spondylosis deformans is detected on
deformans (2 sites for grade 1 and 1 site for grade 2) were radiographic images in 17.8%−32.8% of normal dogs without
identified, but the deep learning model accurately recognized specific clinical signs related to disc diseases (35–37). However
all of them as spondylosis deformans. Although the number a higher rate of prevalence of spondylosis deformans (∼47%) is
of images with dorsal spondylosis deformans in the test identified in patients with intervertebral disc protrusion, a form of
dataset is insufficient to evaluate accuracy, in the training and intervertebral disc disease (IVDD) (38). Hence, while the presence
validation datasets, the deep learning model also demonstrated of spondylosis deformans is not specific for IVDD, it can be useful
accurate recognition in the training and validation datasets, in the diagnosis of disc disease when considered in conjunction
identifying 26 out of 27 dorsal spondylosis deformans. This with radiologic findings such as intervertebral space narrowing.
suggests a high likelihood of accurate recognition for dorsal In conclusion, the deep learning model developed in this
spondylosis deformans. study is expected to help clinical veterinarians accurately and
Even for very small lesions such as grade 1 spondylosis rapidly evaluate spondylosis deformans by determining sites of
deformans, the model successfully detected 25 out of 26 disc instability. Moreover, the vertebral body segmentation model
sites, achieving a remarkably high sensitivity of 96.2% and a developed in this study can be applied to develop deep learning
very high negative predictive value of 98.4%. The specificity models that automatically detect vertebral body diseases such as
and positive predictive values were also high, at 86.3% and tumors, discospondylitis, dislocation of vertebrae, and abnormal
86.1%, respectively. These results suggest that the deep learning narrowed intervertebral disc space.
model in this study exhibited higher sensitivity toward very
small spondylosis deformans than two clinicians. This may
likely be attributed to the criteria of the model, which that Data availability statement
considered a site as true spondylosis deformans only if both
clinicians identified it as spondylosis deformans. Notably, when The raw data supporting the conclusions of this article will be
we identified 10 sites in our test dataset as spondylosis made available by the authors, without undue reservation.
deformans using the deep learning model alone, 6 of them
were sites judged as spondylosis deformans by one of the
two clinicians. Ethics statement
In addition, the time taken by the deep learning model
to auto-segment spondylosis deformans in radiographic images The animal studies were approved by the Institutional Animal
was significantly faster than that by a veterinary clinician to Care and Use Committee of Jeonbuk National University (approval
visually evaluate them, which we believe could ultimately save the nos. JBNU NON2022-085 and NON2023-023). The studies were
interpretation time of veterinary clinicians. conducted in accordance with the local legislation and institutional
In case of the test dataset, images of the vertebral region requirements. Written informed consent was obtained from the
cropped from the lateral abdominal X-ray were used, when owners for the participation of their animals in this study.
checked ability of the deep learning model to detect spondylosis
deformans, observed that the sensitivity, specificity, positive
predictive rate, and negative predictive rate were all higher Author contributions
than 86%. These results mean that the deep learning model
can detect spondylosis deformans highly accurately not only in JP: Conceptualization, Data curation, Investigation, Writing
thoracolumbar and lumbar lateral X-ray images taken with precise – original draft, Formal analysis, Methodology, Validation,
vertebral endplate alignment but also in lateral abdominal X-ray Writing – review & editing. HC: Conceptualization, Investigation,
images taken routinely for general medical examinations, which Methodology, Writing – original draft, Writing – review
is expected to be useful in veterinary clinical practice. However, & editing, Data curation, Formal analysis, Validation. YJ:
when applying the deep learning model to uncropped plane Conceptualization, Methodology, Writing – review & editing,
lateral abdominal X-ray images, detection capability of vertebral Investigation. KL: Conceptualization, Project administration,
bodies and spondylosis deformans is slightly lower than applying Writing – review & editing, Supervision. HY: Conceptualization,
cropped images. Therefore, additional advancements training are Data curation, Investigation, Project administration, Supervision,
considered necessary to fully apply it to general plane lateral Writing – review & editing, Methodology, Validation, Writing –
abdominal X-ray images. original draft.
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