Abstract
Objectives:
This study aimed to analyze the characteristics of carotid artery calcification (CAC) in stroke and nonstroke patients using computed tomography angiographic (CTA) and panoramic images.
Methods:
This is a retrospective study on patients who acquired both CTA and panoramic images at the Neurology Department of Kyungpook National University Hospital, Daegu, South Korea, between 2011 and 2016. The patients were divided into stroke (n = 109) and nonstroke (n = 355) groups based on the final diagnosis. CAC was analyzed in each group based on its presence, shape, and severity using the 2 test. The differences in age and sex between the two groups were examined using a two-sample t-test. A measure of intraobserver reliability was obtained using Cohen’s κ index.
Results:
CAC was more frequently observed in the stroke group than in the nonstroke group using both CTA (stroke group, 100%; nonstroke group, 23.1%) and panoramic (stroke group, 83.5%; nonstroke group, 16.6%) images. Although scattered CAC shape and mild severity occupied the largest portion in both groups, vessel-outlined CAC was more common in nonstroke patients than in stroke patients. In age and sex analyses, only females patients in their 70 s showed significant differences in CAC shape between the stroke and nonstroke groups.
Conclusions:
On both CTA and panoramic images, although CAC is found more frequently in the stroke group, vessel-outlined-shaped CAC in the nonstorke group shows significant differences compared to other shapes.
Keywords: Plaque, Atherosclerotic; Stroke; Computed Tomography Angiography; Radiography, Panoramic; Diagnostic imaging
Introduction
Cerebrovascular accident (stroke) is considered the second or third most common cause of mortality in most developed countries, including the Republic of Korea. 1 It is also one of the important factors causing disability in adults. 2 Hemorrhagic and ischemic strokes are the two kinds of strokes. 1,3 Hemorrhagic stroke is caused by bursting or leaking of the cerebral vessel and accounts for 15% of all stroke cases. 1,3 Ischemic stroke represents >85% of all stroke cases and is caused by atherosclerotic plaques and arterial embolic responses. 1,3,4
More than half of stroke cases may be associated with an atherosclerotic disease that occurs near the bifurcation area of the carotid artery. Thus, the identification of well-known factors, such as the atherosclerotic process and carotid artery calcification (CAC), is critical for an early diagnosis. 5
Panoramic images are widely used in dentistry and are useful for diagnosing various diseases, including not only teeth and osseous tissues, but also lesions in the head and neck region. 5 Friedlander and Lande 6 studied the detection of stroke-related CAC on panoramic images for the first time in 1981. 6 Since then, studies on the diagnostic accuracy of early CAC detection with a panoramic image have been reported. 1,7–10 Based on this, many authors demonstrated that panoramic radiography can contribute to early stroke detection by diagnosing CAC during routine dental examinations. 1,5,8 The CAC prevalence observed on panoramic radiographs in the general population was 2–11%. 3,7,11
Cervical spine radiography, 12 ultrasonography (US), 5,8,11–13 computed tomography (CT), 7,14 or computed tomography angiography (CTA) 15 were mainly used as the gold standard for verifying the CAC diagnostic accuracy of the two-dimensional panoramic image. Traditionally, invasive and expensive catheter angiography has been used to detect stenosis of the carotid artery. 16 However, US, CTA, and magnetic resonance angiography are overwhelmingly currently increasing because they are noninvasive and provide good resolution owing to imaging technology development. 17 Among these, CTA is the most useful technology to evaluate carotid disease. It is suitable for observing the anatomy of the small cross-sections of the carotid vessels in the head and neck area because of its superior resolution. 1
Previous studies have focused on the correlation between panoramic images showing CAC and those of healthy individuals or those with stroke risk factors. 3,11 The relationship between the CAC characteristics and actual stroke risk remains unclear although embolic events are responsible for CAC. 2,15
Therefore, this study aimed to compare the prevalence, shape, and severity of extracranial CACs between patients with and without acute ischemic stroke using CTA and panoramic radiography and determine whether differences in the CAC characteristics based on age and sex were related to stroke occurrence.
Methods and materials
Patients
This study enrolled 473 patients who underwent both neck CTA at the Department of Neurology of Kyungpook National University Hospital, Daegu, South Korea, and panoramic radiography at Kyungpook National University Dental Hospital, Daegu, South Korea, from January 2011 to March 2016. One patient who had severe movement on the CTA image and eight patients who had undergone stenting in the carotid artery bifurcation area were excluded. Thus, this retrospective study included 464 patients. The time interval between the two images was 14 ± 13 months. The patients were divided into the acute ischemic stroke (n = 109) and nonstroke (n = 355) groups based on the final diagnosis. These two groups were subdivided by the presence or absence of CAC based on the CTA image as the gold standard. The panoramic image was reanalyzed to confirm CAC using the corresponding CTA. CAC can present on one or both sides of the patient. Thus, the left and right neck sides were separately analyzed.
An exemption for obtaining informed consent was provided by the institution of the current study due to the retrospective nature of the study (IRB number: KNU 2017–0094).
Imaging
Orthopantomograph OP100D and Orthopantomograph OP200D (Instrumentarium Imaging, Tuusula, Finland) were used to obtain the panoramic images. One of three scanners (Revolution EVO, Light speed 16, and Optima CT 660; GE Healthcare, Milwaukee, WI, USA) was used to acquire the neck CTA images. The CTA parameters included 200–500 mm × 200–500 mm field of view at 100–120 kVp and 245–400 mA, slicing thickness of 1.25–2.5 mm, and scanning time of 6.95 s. A nonionic contrast medium (OmnipaqueTM, Amersham Health, Cork, Ireland) at a concentration of 320 mg ml−1 was injected into the cephalic vein at a rate of 4 ml s−1.
Image evaluation
A 21.2 inch WIDE CX30p 3MP Color LED Diagnostic Monitor (WIDE Medical, Gyeonggi-do, Korea) was used to assess the panoramic and CTA images of each patient. In the CTA images, the original axial plane, multiplanar reconstruction, and maximum intensity projections were used to accurately diagnose CAC.
In the panoramic image, the contrast, brightness, and magnification were adjusted to optimally assess CAC. The panoramic images of the subjects with CAC confirmed using CTA were reviewed twice by one evaluator at a 3-month interval. The evaluator was a third-year resident, transcribing more than 7,000 dental X-ray images per year at the Department of Oral and Maxillofacial Radiology.
Both CTA and panoramic radiographs were used to evaluate CAC presence and shape. The CAC was diagnosed based on the CAC diagnostic criteria presented by MacDonald et al 1 and was differentiated from other diseases based on the criteria described by Almog et al. 10 On CTA, the calcification attached to the inside of the blood vessel extending from the common carotid artery located in the neck area to the external and internal carotid arteries through the bifurcation area was diagnosed as CAC. 1 In the panoramic image, calcification was detected in the lateral or inferior area of the hyoid bone and around the cervical vertebra (C2–C5). 1,7 False-positive findings from the panoramic images were excluded by CTA comparison, and the final diagnosis of CACs was made based on CTA. Furthermore, the categories that describe the shapes of the CACs were slightly modified from Garoff et al 9 and were divided into nodular, vessel-outlined, and scattered shapes. Nodular CACs appear as a single mass or a few lumps clustered together and are viewed as one mass (Figure 1A and B). Vessel-outlined CACs are deposited along the trajectory of the carotid artery (Figure 1C and D). Scattered CACs involve both of the above shapes observed at several sites or similar sites (Figure 1E and F). The severity was categorized into mild (thin and discontinuous), moderate (thin and continuous or thick and discontinuous), or severe (thick and continuous) based on CAC thickness and continuity observed in the axial, coronal, and sagittal view of the CTA image as described by Damaskos et al 18 (Figure 2). Additionally, a supplemental study was conducted by adding age and sex to CAC shape and severity analysis using a CTA image. The subjects were divided into five groups: 40–80 years old who were classified using 10-year units (four groups) and >80 years old.
Figure 1.
Classification of CAC shapes. On the panoramic and CTA images, each shape is divided into nodular (A and B), vessel-outlined (C and D), and scattered (E and F), which is observed in different patients. CAC, carotid artery calcification; CTA, CT angiography
Figure 2.
Classification of CAC severity. In the axial view of CTA, mild (A), moderate (B), and severe (C) are categorized based on the thickest CAC part. CAC, carotid artery calcification; CTA, CT angiography
Statistical analysis
The results were evaluated using descriptive statistics (SPSS Statistics for Windows, v.23.0, IBM Corp., Armonk, NY, USA). The possible differences in prevalence, shape, and severity not only between the stroke group and nonstroke group but also between the subgroups of age and sex in each group were determined using the 2 test. The differences in age and sex between the two groups were examined using a two-sample t-test. A measure of intraobserver reliability was obtained using Cohen’s κ index. A <i>p value < 0.05 indicated statistically significant differences.
Results
Of the 109 patients with acute ischemic stroke, CAC was observed in all CTA (100%) and 91 panoramic (83.5%) images. However, among the 355 patients without stroke, 82 (23.1%) and 59 (16.6%) were observed to have CAC on the CTA and panoramic images, respectively. A significant difference in CAC detection (p < 0.05) was confirmed following the stroke expression in each imaging modality (Table 1). On the panoramic images, the intraobserver CAC reliability was substantially high (Cohen’s κ = 0.770, p < 0.05).
Table 1.
Prevalence of CAC on CTA and panoramic images in the stroke and nonstroke patients
|
Stroke patients
(n = 109) |
Non-stroke patients
(n = 355) |
p | |
|---|---|---|---|
| CAC on CTA image (%) | 109 (100) | 82 (23.1) | 0.000a |
| CAC on panoramic image (%) | 91 (83.5) | 59 (16.6) | 0.000a |
CAC, carotid artery calcification; CTA, CT angiography; n, number.
Statistically significant differences were found between the different groups.
Table 1 shows the CAC detection loss in the panoramic image when compared with that of CTA (patients with stroke, 18; patients without stroke, 23). The main causes of CAC diagnosis loss were: (1) CAC was not located within the range covered by the panoramic image (27, 65.8%), (2) the spots were too small or the thickness of the calcified plaque was insufficient (10, 24.4%), and (3) the remainder was misdiagnosed as triticeous cartilage calcification (2, 4.9%), overlapping with the intercervical vertebra (2, 4.9%).
The CAC age and sex distribution are shown in Table 2, and no statistically distinct difference was observed in the mean age and sex between the two groups.
Table 2.
Age and sex distribution between stroke and nonstroke patients with CAC
|
Stroke patients with CAC
(n = 109) |
Nonstroke patients with CAC
(n = 82) |
p | |
|---|---|---|---|
| Mean age ±SD (range) |
71.06 ± 9.11 (48–92) | 69.12 ± 9.15 (50–89) | 0.147 |
| Male/female ratio (%) | 57 (52.2):52 (47.8) | 52 (63.4):30 (36.6) | 0.126 |
CAC, carotid artery calcification; SD, standard deviation; n, number.
In the shape assessment using CTA, the scattered shape was most frequently detected in the sum of both groups, followed by the vessel-outlined and nodular shapes (Table 3). Notable differences were observed only in the vessel-outlined type (p < 0.05). In the shape analysis using the panoramic images, a significant difference was observed in the prevalence of the vessel-outlined type (p < 0.05), although the distribution of each shape was different from that on the CTA images (Table 4).
Table 3.
Shape and severity analysis of CAC between the stroke and nonstroke groups using CTA by affected neck sides
| CTA image | Affected neck sides (%) | p | |||
|---|---|---|---|---|---|
|
Stroke group
(n = 178) |
Nonstroke group
(n = 141) |
Total sum
(n = 319) |
|||
| Shape | Nodular | 55 (30.9) | 38 (27.0) | 93 (29.2) | 0.656 |
| Vessel-outlined | 50 (28.1) | 57 (40.4) | 107 (33.5) | 0.020 | |
| Scattered | 73 (41.0) | 46 (32.6) | 119 (37.3) | 0.066 | |
| Severity | Mild | 69 (38.8) | 51 (36.2) | 120 (37.6) | 0.635 |
| Moderate | 68 (38.2) | 50 (35.5) | 118 (37.0) | 0.615 | |
| Severe | 41 (23.0) | 40 (28.4) | 81 (25.4) | 0.277 | |
CAC, carotid artery calcification; n, number.
Statistically significant differences were found between the different groups.
Table 4.
Shape analysis of CAC between the stroke and nonstroke groups using panoramic images by affected neck sides
| Panoramic image | Affected neck sides (%) | p | |||
|---|---|---|---|---|---|
|
Stroke group
(n = 138) |
Nonstroke group
(n = 92) |
Total sum
(n = 230) |
|||
| Shape | Nodular | 34 (24.6) | 20 (21.7) | 54 (25.7) | 0.638 |
| Vessel-outlined | 40 (29.0) | 39 (42.4) | 79 (37.6) | 0.047 | |
| Scattered | 64 (46.4) | 33 (35.9) | 97 (46.2) | 0.114 | |
CAC, carotid artery calcification; n, number.
Statistically significant differences were found between the different groups.
The mild severity of the total CAC was analyzed using CTA had the largest proportion, followed by moderate and severe degrees, and no significant difference was observed between the stroke and nonstroke groups (Table 3). The CAC distribution by age in each group as well as the total sum in both groups showed that the CAC incidence steadily increased at 40–70 years old and decreased at >80 years old (Tables 5 and 6). Furthermore, the distribution by sex revealed that CAC was more common in males than in females in both groups (Tables 7 and 8). Statistically significant differences were observed between the two groups only in the eighth decade (p < 0.05; Table 5). In the sex analysis of the CAC shape, the trend was consistent with the descending order of vessel-outlined, scattered, and nodular CACs in males of both groups, but no significant differences were observed. The tendency in each subgroup was different among the females; however, a statistically significant difference was observed (p < 0.05; Table 7). Therefore, a significant difference in the CAC shape between the two groups was observed only in females and the group of patients in their 70 s (Tables 5 and 7). Neither trend in the distribution nor a statistically significant difference was found in CAC severity (Tables 6 and 8).
Table 5.
Age distribution and shape comparison between the stroke and nonstroke groups using CTA by affected neck sides
| Age (yrs) | Shape | Affected neck sides (%) | p | ||
|---|---|---|---|---|---|
|
Stroke group
(n = 178) |
Nonstroke group
(n = 141) |
Total sum
(n = 319) |
|||
| 40–49 | Nodular | 1 (100) | 0 | 1 (100) | 1.000 |
| Total | 1 (100) | 0 | 1 (100) | ||
| 50–59 | Nodular | 8 (50.0) | 5 (31.3) | 13 (40.6) | 0.163 |
| Vessel-outlined | 2 (12.5) | 7 (43.8) | 9 (28.1) | ||
| Scattered | 6 (37.5) | 4 (25.0) | 10 (31.3) | ||
| Total | 16 (100) | 16 (100) | 32 (100) | ||
| 60–69 | Nodular | 17 (32.7) | 18 (36.7) | 35 (34.6) | 0.861 |
| Vessel-outlined | 15 (28.8) | 12 (24.5) | 27 (26.7) | ||
| Scattered | 20 (38.5) | 19 (38.8) | 39 (38.6) | ||
| Total | 52 (100) | 49 (100) | 101 (100) | ||
| 70–79 | Nodular | 17 (23.6) | 13 (22.4) | 30 (23.1) | 0.016a |
| Vessel-outlined | 22 (30.6) | 31 (53.4) | 53 (40.8) | ||
| Scattered | 33 (45.8) | 14 (24.1) | 47 (36.2) | ||
| Total | 72 (100) | 58 (100) | 130 (100) | ||
| >80 | Nodular | 9 (24.3) | 2 (11.1) | 11 (20.0) | 0.530 |
| Vessel-outlined | 11 (29.7) | 7 (38.9) | 18 (32.7) | ||
| Scattered | 17 (45.9) | 9 (50.0) | 26 (47.3) | ||
| Total | 37 (100) | 18 (100) | 55 (100) | ||
CTA, CT angiography; n, number.
Statistically significant differences were found between the different groups.
Table 6.
Age distribution and severity comparison between the stroke and non-stroke groups using CTA by affected neck sides
|
Age
(yrs) |
Severity | Affected neck sides (%) | p | ||
|---|---|---|---|---|---|
|
Stroke group
(n = 178) |
Nonstroke group
(n = 141) |
Total sum
(n = 319) |
|||
| 40–49 | Mild | 1 (100) | 0 | 1 (100) | 1.000 |
| Total | 1 (100) | 0 | 1 (100) | ||
| 50–59 | Mild | 8 (50.0) | 8 (50.0) | 16 (50.0) | 0.587 |
| Moderate | 6 (37.5) | 4 (25.0) | 10 (31.3) | ||
| Severe | 2 (12.5) | 4 (25.0) | 6 (18.8) | ||
| Total | 16 (100) | 16 (100) | 32 (100) | ||
| 60–69 | Mild | 22 (42.3) | 21 (42.9) | 43 (42.6) | 0.805 |
| Moderate | 19 (36.5) | 20 (40.8) | 39 (38.6) | ||
| Severe | 11 (21.2) | 8 (16.3) | 19 (18.8) | ||
| Total | 52 (100) | 49 (100) | 101 (100) | ||
| 70–79 | Mild | 30 (41.7) | 17 (29.3) | 47 (36.2) | 0.124 |
| Moderate | 25 (34.7) | 18 (31.0) | 43 (33.1) | ||
| Severe | 17 (23.6) | 23 (39.7) | 40 (30.8) | ||
| Total | 72 (100) | 58 (100) | 130 (100) | ||
| >80 | Mild | 8 (21.6) | 5 (27.8) | 13 (23.6) | 0.880 |
| Moderate | 18 (48.6) | 8 (44.4) | 26 (47.3) | ||
| Severe | 11 (29.7) | 5 (27.8) | 16 (29.1) | ||
| Total | 37 (100) | 18 (100) | 55 (100) | ||
CTA, CT angiography; n, number.
Table 7.
Sex distribution and shape comparison between the stroke and nonstroke groups using CTA by affected neck sides
| Sex | Shape | Affected neck sides (%) | p | ||
|---|---|---|---|---|---|
|
Stroke group
(n = 178) |
Nonstroke group
(n = 141) |
Total sum
(n = 319) |
|||
| Male | Nodular | 29 (31.9) | 22 (25.0) | 51 (28.7) | 0.487 |
| Vessel-outlined | 31 (34.4) | 37 (42.0) | 68 (38.2) | ||
| Scattered | 30 (33.3) | 29 (33.0) | 59 (33.7) | ||
| Total | 90 (100) | 88 (100) | 178 (100) | ||
| Female | Nodular | 26 (29.5) | 16 (30.2) | 42 (29.8) | 0.047a |
| Vessel-outlined | 19 (21.6) | 20 (37.7) | 39 (27.7) | ||
| Scattered | 43 (48.9) | 17 (32.1) | 60 (42.6) | ||
| Total | 88 (100) | 53 (100) | 141 (100) | ||
CTA, CT angiography; n, number.
Statistically significant differences were found between the different groups.
Table 8.
Sex distribution and severity comparison between the stroke and nonstroke groups using CTA by affected neck sides
| Sex | Severity | Affected neck sides (%) | p | ||
|---|---|---|---|---|---|
|
Stroke group
(n = 178) |
Nonstroke group
(n = 141) |
Total sum
(n = 319) |
|||
| Male | Mild | 33 (36.7) | 34 (38.6) | 67 (37.6) | 0.195 |
| Moderate | 36 (40.0) | 25 (28.4) | 61 (34.3) | ||
| Severe | 21 (23.3) | 29 (33.0) | 50 (28.1) | ||
| Total | 90 (100) | 88 (100) | 178 (100) | ||
| Female | Mild | 36 (40.9) | 17 (32.1) | 53 (37.6) | 0.428 |
| Moderate | 32 (36.4) | 25 (47.2) | 57 (40.4) | ||
| Severe | 20 (22.7) | 11 (20.8) | 31 (22.0) | ||
| Total | 88 (100) | 53 (100) | 141 (100) | ||
CTA, CT angiography; n, number.
Discussion
This study suggests that patients presenting with acute ischemic stroke show more CAC than nonstroke patients using panoramic and CTA images. Vessel-outlined CAC is more common in nonstroke patients than in stroke patients. In age and sex analysis, only the females in their 70s showed significant differences in CAC shape between the stroke and nonstroke groups.
This shows the importance of CAC confirmation when dentists transcribe panoramic images. On panoramic radiography, higher CAC prevalence rates were detected in patients with stroke than in those without stroke. Friedlander et al 19 reported that white male patients with a history of cerebral infarction had a higher CAC frequency (37%) on panoramic images. Kumagai et al 8 also found that 20% of Japanese patients had experienced cerebral infarction. This demonstrates that cerebrovascular disease was significantly correlated with CAC detection on panoramic radiography. The American Dental Association Council also supported that a dentist can refer to a physician if a CAC is noted on a panoramic image taken for dental treatment purposes. 8,20 However, some studies that confirmed CAC on panoramic images alone reported a limit in cerebrovascular disease diagnosis and evaluated its accuracy as moderate or poor. 3,12 In the third opinion, CAC detected on panoramic images was useful for the identification of postvascular diseases; however, its future prediction for neurovascular diseases was impractical. 10
Few studies have assessed CACs using CTA and panoramic images. Moreover, this study is believed to be the first to analyze the CAC characteristics of the stroke and nonstroke groups to confirm the relationship between the risk of stroke and CAC imaging features. Previous studies 15,21 have investigated patients with symptoms of ischemic stroke, however, the clinical criteria for ischemic stroke were not uniform, and the number of patients included was <50. Moreover, this study included patients who were accurately diagnosed with acute ischemic stroke as the main comparison subjects. The number of subjects in this study was two to three times higher than those of previous studies. 15,21
CTA has an excellent discriminating resolution for calcified plaques. However, only a few studies have used CTA in final plaque confirmation or characterization. 15 With an excellent spatial resolution, CTA has remarkable benefits of accurate diagnosis, characterization, and differential CAC diagnosis. 15 It allows for the accurate observation of the presence of calcified plaques with a density of >150 HU 22 and a three-dimensional anatomical location. Thus, this study clearly distinguished between CAC and anatomical or pathological radiopaque structures (e.g., the triticeous cartilages, superior portion of the thyroid ligament, epiglottis, hyoid bone, calcified stylohyoid, stylomandibular ligaments, calcified lymph nodes, tonsilloliths, phleboliths, and sialoliths). 10,20
Nevertheless, the CAC prevalence in the panoramic images of the patients with and without stroke was 83.5 and 16.6%, respectively, which was relatively higher than rates shown in other studies. It was unique that the nonstroke group in this study had an average detection rate higher than 2–11%, which is generally mentioned in other studies. 3,7,11 This is because the mean age of the nonstroke group analyzed in this study was 69.12 years, and other risk factors affecting CAC detection increased in proportion to age. 21 In fact, Henriques et al 11 revealed that, on panoramic radiography, CAC prevalence increased by 17–31% compared with that of healthy subjects if accompanied by risk factors (e.g., diabetes mellitus, chronic renal disease, menopause, hypertension, or obesity). Moreover, patients who visited the Department of Neurology were included and may have contributed to increased CAC detection rate although they were not diagnosed with stroke with mild stroke symptoms (e.g., transient ischemic attack). 21
This study hypothesized that patients diagnosed with acute ischemic stroke would have an extensive plaque morphology and exhibit severe calcification. However, the results of this study revealed that the difference between the two groups was observed only in the CAC shapes, especially in the vessel-outlined type. This broad calcification was found to be significantly favorable in the nonstroke group compared to the stroke group. Furthermore, this difference was explained on both CTA and panoramic images. In contrast, Garoff et al 9 found that not only were vessel-outlined CACs more frequent in severe stenosis cases on panoramic radiography, but also specific shapes of CACs, which could be observed on panoramic images, did not improve the positive predictive value in carotid stenosis diagnosis (>50%). However, this was only a verification of the association of stenosis in the form of CAC. Thus, a gap concerning the actual stroke occurrence may exist.
This study found that CAC severity did not affect ischemic stroke occurrence. The results of this study were similar to those reported by Garoff et al. 23 The calcium volume of the actual plaques using carotid endarterectomy did not have any effect on the degree of carotid stenosis and CAC detection on panoramic radiography. Contrarily, the CAC severity is a critical factor in the diagnosis of stenosis in the bifurcation area of the carotid artery, 14 and a study showed that this is proportional to age. 18
The main conclusion from this study was that CAC was more common in patients with ischemic stroke. However, the CAC of the stroke group was not more calcified when CAC between the stroke and nonstroke groups was compared. Severe or vessel-outlined CACs had a lesser correlation with stroke. These data indicate that extensive calcification, such as that in vessel-outlined CACs, has a positive correlation with plaque stability, leading to a decrease in symptomatic cerebrovascular events. 2 Although the atherosclerotic plaques in the carotid bifurcation correlate with the risk of stroke due to embolic, occlusive, or slow-flow stenotic disease, more attention is given to the actual plaque morphology and composition of the atheroma itself. 22 Recent studies have shown that noncalcified plaques are more vulnerable, resulting in a better rupture of the vessel wall and thrombotic or embolic neurological events. 24 Beckman et al 25 also found that a large extent of coronary artery calcification had a direct effect on coronary stability, suggesting that arterial calcification may contribute to the stabilization of atherosclerosis and cardiovascular events. In the pathological study of atheroma calcification concerning clinical symptoms, calcium salt can be assumed to play a role in making the plaque hard and resistant to physical stimuli applied to the blood vessel. 26 Additionally, Johnson et al 27 reported that noncalcified plaques were more likely to induce embolization, ulceration, and hemorrhage in the vessel wall than calcified plaques, inducing better clinical vascular disease symptoms.
The first limitation of this study is that it did not take into account the effect of noncalcified plaques, which cannot be detected on panoramic radiography, considering these have clinical significance as well. 28 CTA alone is also not suitable for conducting qualitative analysis and evaluating plaque instability. 2 Additionally, no consideration of risk factors associated with medical history in CAC formation was noted, except for age, sex, and stroke diagnosis. This study used only the presence or absence of ischemic stroke in the cerebrovascular events as the independent variable. In a follow-up study, investigating clinical symptoms and CAC further by considering other cardiovascular diseases is necessary.
Conclusion
The prevalence of CACs in stroke patients is significantly higher than nonstroke patients on both CTA and panoramic images. The shape of CACs is different between the stroke and nonstroke groups and vessel-outlined shape is significantly more than nodular and scattered shapes in the nonstroke group. On the other hand, no difference in severity is noted between the two groups.
Contributor Information
Chang-Hyeon An, Email: chan@knu.ac.kr.
Karp-Shik Choi, Email: ksichio@knu.ac.kr.
Seo-Young An, Email: syan@knu.ac.kr.
REFERENCES
- 1. MacDonald D, Chan A, Harris A, Vertinsky T, Farman AG, Scarfe WC. Diagnosis and management of calcified carotid artery atheroma: dental perspectives. Oral Surg Oral Med Oral Pathol Oral Radiol 2012; 114: 533–47. doi: 10.1016/j.oooo.2012.06.020 [DOI] [PubMed] [Google Scholar]
- 2. Hunt JL, Fairman R, Mitchell ME, Carpenter JP, Golden M, Khalapyan T, et al. Bone formation in carotid plaques: A clinicopathological study. Stroke 2002; 33: 1214–19. doi: 10.1161/01.str.0000013741.41309.67 [DOI] [PubMed] [Google Scholar]
- 3. Beckstrom BW, Horsley SH, Scheetz JP, Khan Z, Silveira AM, Clark SJ, et al. Correlation between carotid area calcifications and periodontitis: A retrospective study of digital panoramic radiographic findings in pretreatment cancer patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007; 103: 359–66. doi: 10.1016/j.tripleo.2006.08.016 [DOI] [PubMed] [Google Scholar]
- 4. Musuka TD, Wilton SB, Traboulsi M, Hill MD. Diagnosis and management of acute ischemic stroke: speed is critical. CMAJ 2015; 187: 887–93. doi: 10.1503/cmaj.140355 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Bayram B, Uckan S, Acikgoz A, Müderrisoglu H, Aydinalp A. Digital panoramic radiography: A reliable method to diagnose carotid artery atheromas? Dentomaxillofac Radiol 2006; 35: 266–70. doi: 10.1259/dmfr/50195822 [DOI] [PubMed] [Google Scholar]
- 6. Friedlander AH, Lande A. Panoramic radiographic identification of carotid arterial plaques. Oral Surg Oral Med Oral Pathol 1981; 52: 102–4. 10.1016/0030-4220(81)90181-x [DOI] [PubMed] [Google Scholar]
- 7. Yoon SJ, Yoon W, Kim OS, Lee JS, Kang BC. Diagnostic accuracy of panoramic radiography in the detection of calcified carotid artery. Dentomaxillofac Radiol 2008; 37: 104–8. doi: 10.1259/dmfr/86909790 [DOI] [PubMed] [Google Scholar]
- 8. Kumagai M, Yamagishi T, Fukui N, Chiba M. Carotid artery calcification seen on panoramic dental radiographs in the asian population in japan. Dentomaxillofac Radiol 2007; 36: 92–96. 10.1259/dmfr/79378783 [DOI] [PubMed] [Google Scholar]
- 9. Garoff M, Ahlqvist J, Levring Jäghagen E, Johansson E, Wester P. Carotid calcification in panoramic radiographs: radiographic appearance and the degree of carotid stenosis. Dentomaxillofac Radiol 2016; 45(6): 20160147. doi: 10.1259/dmfr.20160147 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Almog DM, Tsimidis K, Moss ME, Gottlieb RH, Carter LC. Evaluation of a training program for detection of carotid artery calcifications on panoramic radiographs. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000; 90: 111–17. doi: 10.1067/moe.2000.107056 [DOI] [PubMed] [Google Scholar]
- 11. Guimarães Henriques JC, Kreich EM, Helena Baldani M, Luciano M, Cezar de Melo Castilho J, Cesar de Moraes L. Panoramic radiography in the diagnosis of carotid artery atheromas and the associated risk factors. Open Dent J 2011; 5: 79–83. doi: 10.2174/1874210601105010079 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Madden RP, Hodges JS, Salmen CW, Rindal DB, Tunio J, Michalowicz BS, et al. Utility of panoramic radiographs in detecting cervical calcified carotid atheroma. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007; 103: 543–48. doi: 10.1016/j.tripleo.2006.06.048 [DOI] [PubMed] [Google Scholar]
- 13. Johansson EP, Ahlqvist J, Garoff M, Karp K, Jäghagen EL, Wester P. Ultrasound screening for asymptomatic carotid stenosis in subjects with calcifications in the area of the carotid arteries on panoramic radiographs: A cross-sectional study. BMC Cardiovasc Disord 2011; 11: 44. doi: 10.1186/1471-2261-11-44 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Woodcock RJ, Goldstein JH, Kallmes DF, Cloft HJ, Phillips CD. Angiographic correlation of CT calcification in the carotid siphon. AJNR Am J Neuroradiol 1999; 20: 495–99. [PMC free article] [PubMed] [Google Scholar]
- 15. Nandalur KR, Baskurt E, Hagspiel KD, Phillips CD, Kramer CM. Calcified carotid atherosclerotic plaque is associated less with ischemic symptoms than is noncalcified plaque on MDCT. AJR Am J Roentgenol 2005; 184: 295–98. doi: 10.2214/ajr.184.1.01840295 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Chen C-J, Lee T-H, Hsu H-L, Tseng Y-C, Lin S-K, Wang L-J, et al. Multi-slice CT angiography in diagnosing total versus near occlusions of the internal carotid artery: comparison with catheter angiography. Stroke 2004; 35: 83–85. doi: 10.1161/01.STR.0000106139.38566.B2 [DOI] [PubMed] [Google Scholar]
- 17. Josephson SA, Bryant SO, Mak HK, Johnston SC, Dillon WP, Smith WS. Evaluation of carotid stenosis using CT angiography in the initial evaluation of stroke and TIA. Neurology 2004; 63: 457–60. 10.1212/01.wnl.0000135154.53953.2c [DOI] [PubMed] [Google Scholar]
- 18. Damaskos S, da Silveira HLD, Berkhout EWR. Severity and presence of atherosclerosis signs within the segments of internal carotid artery: CBCT’s contribution. Oral Surg Oral Med Oral Pathol Oral Radiol 2016; 122: 89–97. doi: 10.1016/j.oooo.2016.03.017 [DOI] [PubMed] [Google Scholar]
- 19. Friedlander AH, Manesh F, Wasterlain CG. Prevalence of detectable carotid artery calcifications on panoramic radiographs of recent stroke victims. Oral Surg Oral Med Oral Pathol 1994; 77: 669–73. 10.1016/0030-4220(94)90332-8 [DOI] [PubMed] [Google Scholar]
- 20. Yoon S-J, Shim S-K, Lee J-S, Kang B-C, Lim H-J, Kim M-S, et al. Interobserver agreement on the diagnosis of carotid artery calcifications on panoramic radiographs. Imaging Sci Dent 2014; 44: 137–41. 10.5624/isd.2014.44.2.137 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Christou P, Leemann B, Schimmel M, Kiliaridis S, Müller F. Carotid artery calcification in ischemic stroke patients detected in standard dental panoramic radiographs - a preliminary study. Adv Med Sci 2010; 55: 26–31. 10.2478/v10039-010-0022-7 [DOI] [PubMed] [Google Scholar]
- 22. Enterline DS, Kapoor G. A practical approach to CT angiography of the neck and brain. Tech Vasc Interv Radiol 2006; 9: 192–204. doi: 10.1053/j.tvir.2007.03.003 [DOI] [PubMed] [Google Scholar]
- 23. Garoff M, Johansson E, Ahlqvist J, Arnerlöv C, Levring Jäghagen E, Wester P. Calcium quantity in carotid plaques: detection in panoramic radiographs and association with degree of stenosis. Oral Surg Oral Med Oral Pathol Oral Radiol 2015; 120: 269–74. doi: 10.1016/j.oooo.2015.04.010 [DOI] [PubMed] [Google Scholar]
- 24. Naghavi M, Libby P, Falk E, Casscells SW, Litovsky S, Rumberger J, et al. From vulnerable plaque to vulnerable patient: A call for new definitions and risk assessment strategies: part I. Circulation 2003; 108: 1664–72. doi: 10.1161/01.CIR.0000087480.94275.97 [DOI] [PubMed] [Google Scholar]
- 25. Beckman JA, Ganz J, Creager MA, Ganz P, Kinlay S. Relationship of clinical presentation and calcification of culprit coronary artery stenoses. Arterioscler Thromb Vasc Biol 2001; 21: 1618–22. 10.1161/hq0901.095554 [DOI] [PubMed] [Google Scholar]
- 26. Wexler L, Brundage B, Crouse J, Detrano R, Fuster V, Maddahi J, et al. Coronary artery calcification: pathophysiology, epidemiology, imaging methods, and clinical implications. a statement for health professionals from the american heart association. writing group. Circulation 1996; 94: 1175–92. 10.1161/01.cir.94.5.1175 [DOI] [PubMed] [Google Scholar]
- 27. Johnson JM, Kennelly MM, Decesare D, Morgan S, Sparrow A. Natural history of asymptomatic carotid plaque. Arch Surg 1985; 120: 1010–12. doi: 10.1001/archsurg.1985.01390330022004 [DOI] [PubMed] [Google Scholar]
- 28. Mupparapu M, Kim IH. Calcified carotid artery atheroma and stroke: A systematic review. J Am Dent Assoc 2007; 138: 483–92. doi: 10.14219/jada.archive.2007.0200 [DOI] [PubMed] [Google Scholar]


