|Year : 2015 | Volume
| Issue : 1 | Page : 42-47
Calcified carotid atherosclerotic plaques on digital panoramic radiographs in patients with Type II diabetes mellitus: A case control study
Neha Khambete1, Rahul Kumar2
1 Department of Oral Medicine, Diagnosis and Radiology, CSMSS Dental College and Hospital, Aurangabad, India
2 Department of Conservative Dentistry and Endodontics, MGM Dental College and Hospital, Navi Mumbai, Maharashtra, India
|Date of Submission||19-Nov-2014|
|Date of Acceptance||03-Aug-2015|
|Date of Web Publication||12-Oct-2015|
C/O Khambete Hospital, Ward No. 1, Opposite Railway Goods Yard, Shrirampur - 413 709, Maharashtra
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Aim: Diabetes mellitus is associated with accelerated carotid artery atherosclerosis and increased risk of stroke. This study was conducted with the objective of determining the prevalence of calcified atherosclerotic plaques on panoramic radiographs of patients with Type II diabetes mellitus. Materials and Methods: Panoramic radiographs of 100 patients (age range 50-84 years) with known history of type II diabetes mellitus, visiting the outpatient department were evaluated for the presence of calcified atherosclerotic plaques. Age- and sex-matched controls were evaluated in the same manner. Statistical comparison of prevalence rates was done. Results: The radiographs of diabetics (mean age: 64.45 years) revealed that 26% had atheromatous plaques, whereas those of controls (mean age: 65.36 years) revealed that 6% had atheromatous plaques. A statistically significant difference (P = 0.01410) was obtained using Yates' Chi-square test. Conclusion: People with diabetes mellitus had a greater prevalence of calcified atherosclerotic plaques on panoramic radiographs than non-diabetics. Panoramic radiographs of diabetic patients should be screened for the presence of carotid artery atheromatous plaques for timely medical referral of asymptomatic patients and avoiding any further serious consequences like cerebrovascular accidents.
Keywords: Carotid artery atheromas, diabetes mellitus, digital, panoramic radiography
|How to cite this article:|
Khambete N, Kumar R. Calcified carotid atherosclerotic plaques on digital panoramic radiographs in patients with Type II diabetes mellitus: A case control study. J Indian Acad Oral Med Radiol 2015;27:42-7
|How to cite this URL:|
Khambete N, Kumar R. Calcified carotid atherosclerotic plaques on digital panoramic radiographs in patients with Type II diabetes mellitus: A case control study. J Indian Acad Oral Med Radiol [serial online] 2015 [cited 2018 Dec 12];27:42-7. Available from: http://www.jiaomr.in/text.asp?2015/27/1/42/167075
| Introduction|| |
Cerebrovascular accidents or strokes are the third most common cause of morbidity and mortality worldwide. The main cause of cerebrovascular accidents is rupture of atherosclerotic plaques present in carotid arteries. The carotid bifurcation is at the highest risk of atherosclerosis. At carotid arterial bifurcation, flow velocity and shear stress are reduced, and flow departs in a laminar, unidirectional pattern. Fatty streaks located at bifurcations may progress to smooth muscle-rich fibrous plaques that are prone to calcification.  Diabetes mellitus increases the risk of cerebrovascular accidents leading to death. Diabetic people are at heightened risk of stroke because hyperglycemia, hyperlipidemia, and hypertension often associated with the disorder have been implicated as the cause of atherosclerosis of the cervical portion of the carotid artery. Besides the well-recognized microvascular complications of diabetes, there is increased incidence of macrovascular complications like diseases of coronary arteries, peripheral arteries, and carotid vessels. The risk of stroke is increased by 150-400% in patients with diabetes. ,
In recent years, a number of publications have described the detection of calcifications in the region of carotid bifurcation on panoramic radiographs. Previous studies have reported a prevalence rate of 2-11% for calcified carotid artery atheromatous plaques (CCAAP) on panoramic radiographs in general dental patient population.  Various studies have shown that panoramic radiographs taken routinely to evaluate the oral status of diabetic patients due to the high occurrence of dental infections can also be used in detection of CCAAP presence and evaluation of the possible risk of stroke in them. ,,,,, The present study was undertaken with the objectives to determine the prevalence of calcified atherosclerotic plaques on panoramic radiographs of patients with Type II diabetes mellitus and to determine whether patients with diabetes mellitus have higher prevalence of atherosclerotic plaques on panoramic radiograph as compared to non-diabetics.
| Materials and Methods|| |
The proposed study proforma was presented to the institutional ethical committee and approval was obtained. One hundred patients with known history of Type II diabetes mellitus and who were under treatment for the same, visiting the outpatient department of the hospital were selected randomly for the study after obtaining their informed consent. The inclusion criteria for patients were:
- History of Type II diabetes mellitus.
- Patients undergoing treatment for the same.
- Age greater than 55 years.
- Fasting blood sugar (FBS) ≥130 mg/dl in the last month.
One hundred age- and sex-matched non-diabetic patients were selected in the control group. Exclusion criterion for both the groups was: History of transient ischemic attack and cerebrovascular accidents. The medical records of all patients were reviewed for the factors related to atherosclerosis, including hypertension, renal diseases, and smoking. Each patient was subjected to digital panoramic radiographic examination by OPG machine, Panorex Dental X-Ray System [Meditronics (Asia) Pvt Ltd, Mumbai, India] at 70-74 kVp, 10 mA, for 10 s using phosphor plates of size 6″ × 12″. Panoramic radiography was performed with the mandible placed on the chin rest of the machine and the patient in standing position. While positioning the patient for radiographic examination, a larger phosphor plate was used. Care was taken to include a relatively wide area distal and inferior to the angle of mandible, in order to avoid missing the carotid vessel calcification. The plates were processed in CR system Regius Nano CR reader (Konica Minolta Medical Imaging Inc., New Jersey, USA) with a high resolution of 87.5 microns. The images were recorded in DICOM format. The images were enhanced for obtaining optimum density, contrast, and brightness.
The images were then carefully scrutinized by a trained oral radiologist for the presence of nodular, punctuate, and linear radiopacities in the soft tissues of the neck posteroinferior to the angle of mandible at the lower margin of third and fourth cervical vertebra (the area of bifurcation of the common carotid artery) [Figure 1], [Figure 2], and [Figure 3]. For the differential diagnosis of carotid atheromatous plaques, other cervical calcifications such as calcified triticeous cartilage, calcified thyroid cartilage, hyoid bone, and submandibular salivary gland sialoliths were excluded, as described by Almog et al. in their study.  The calcified triticeous cartilage appears as a radiopacity of the size of a grain of wheat, just below the tip of the greater cornu of the hyoid bone. The superior horn of calcified thyroid cartilage is seen sometimes on panoramic radiographs at a much inferior level. The greater cornua of hyoid bone has a definite cortex and trabecular pattern, while the submandibular salivary gland sialoliths appear below the inferior border of the mandible in the third molar ramus area. They are usually smooth in outline and diffusely calcified [Figure 1]. The radiographic findings were recorded in a tabulated form.
|Figure 1: Schematic diagram representing areas of interest as they appear on panoramic radiographs: calcified triticeous cartilage (T), superior cornu of calcified thyroid cartilage (Th) and calcifi ed carotid atheroma (C), epiglottis (E), greater cornua of the hyoid bone (G)|
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|Figure 2: Cropped digital panoramic radiograph of a diabetic patient showing radiopaque body at the right C3-C4 junction suggestive of calcified atheromatous plaque (arrow)|
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|Figure 3: Cropped panoramic radiograph of a non-diabetic patient showing radiopaque body at the right C3-C4 junction suggestive of calcified atheromatous plaque (arrow)|
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The collected data were then subjected to statistical analysis using SPSS statistical package (version 16.0; SPSS, Inc., Chicago, IL, USA) and relevant results were obtained. The patients who had atheromatous plaques on the panoramic radiographs and ultrasound examination were referred to the physicians for further management.
| Results|| |
The sample consisted of 200 subjects (134 males and 66 females) with a mean age of 64.45 years. The study sample consisted of 100 diabetic subjects (68 males and 32 females) with age ranging between 50 and 84 years and a mean age of 64.45 years. The control sample consisted of 100 subjects (66 males and 34 females) with age range of 52-84 years and a mean age of 65.36 years [Table 1]. Out of 100 diabetic patients, 26 (26%) showed CCAAP, while out of 100 non-diabetic patients, 6 (6%) showed the presence of atheromatous plaques on panoramic radiographs. The prevalence of CCAAP on panoramic radiographs of patients with diabetes mellitus was found to be 26% as compared to 6% found in the non-diabetic control group. The difference in the prevalence of CCAAP between these groups was statistically significant (P = 0.01410 using Yates' corrected Chi-square test) [Table 2]. [Table 1] shows the side-wise distribution of CCAAP. In the study population, 6 CCAAP were located on right side, 14 on the left side, and in 6 cases they were located bilaterally, whereas in the control population, all the CCAAP were located on the right side. [Table 3] shows the age-wise distribution of CCAAP. In the study population, the six patients who showed the presence of CCAAP were in the oldest age group of 70 years and above.
|Table 1: Distribution of study groups according to Mean and SD age, gender and side|
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|Table 2: Distribution of study subjects according to study groups and presence of CCAAP on panoramic radiographs|
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|Table 3: Age-wise and side-wise distribution of patients with respect to CCAAP on panoramic radiographs|
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| Discussion|| |
In diabetes, hyperglycemia, excess free fatty acid release, and insulin resistance engender adverse metabolic events within the endothelial cells. Activation of these systems impairs endothelial function, augments vasoconstriction, increases inflammation, and promotes thrombosis. There is abnormal activity of platelets, which may exacerbate the progression of atherosclerosis and the consequences of plaque rupture. In addition to potentiating platelet function, diabetes augments blood coagulability, making it more likely that atherosclerotic plaque rupture or erosion will result in thrombotic occlusion of the artery. In addition to enhancing the initiation of atherogenesis, diabetes promotes plaque instability and clinical sequelae. , The prevalence of CCAAP on panoramic radiographs of patients with diabetes mellitus was found to be 26% as compared to 6% found in the non-diabetic control group. The difference in the prevalence of CCAAP between these groups was statistically significant (P = 0.01410 using Yates' corrected Chi-square test).
These results were comparable to those published in literature. In 2000, Friedlander et al. reported 20.4% prevalence.  In 2002, the same authors reported 24% prevalence in non-insulin-dependent diabetic group and 36% prevalence in insulin-dependent diabetic group of patients.  According to Griniatsos et al., a statistically significant association was found between diabetes mellitus and presence of CCAAP.  Friedlander et al. in their study suggested a new possibility of co-occurrence of Type 2 diabetes mellitus and obstructive sleep apnea. They showed that this association had statistically significant value in association with the presence of CCAAP.  Pornprasertsuk-Damrongsri et al. conducted a study in patients with occult metabolic syndrome and found presence of CCAAP in 22.4% of subjects, all of whom had diabetes mellitus.  Chang et al. revealed that individuals with Syndrome Z had significantly greater atherogenic burden and slightly higher prevalence of CCAAP, when compared with individuals with obstructive sleep apnea. 
Careful history and inspection of panoramic radiographs using software and magnifying selected areas allowed us to rule out the other pathological radiopacities such as sialoliths, phleboliths, and calcified lymph nodes. CCAAP seen in both the populations had similar morphologic appearance. The atheromatous plaques were unilateral in 20% of diabetic patients, in 6 patients on only the right side (6%), in 14 patients on only the left side (14%) and bilateral in 6 (6%) out of 100 patients. While in the control population all the six (6%) calcified atheromatous plaques were unilateral and all were present on the right side. According to Adachi, the carotid bifurcation level to the cervical vertebrae in Japanese people differs in the left and right sides. Normally, it is said that the bifurcation level of the right carotid artery is more often located between C3 and C4, whereas the bifurcation level of the left carotid artery is located between C4 and C5. In this study, a radiopaque nodular mass or masses adjacent to the cervical vertebrae at or below the intervertebral space between C3 and C4 was regarded as a calcified carotid atheroma. Also, the C5 is not completely projected on panoramic radiographs with 6-inch cassette. Therefore, it is speculated that calcified carotid atheromas in the left side are less often detected than those in the right side on panoramic radiographs.  Sisman et al. also reported that most of the calcified atheromas were located on the right side.  However, majority of the reports say that in the normal population, the calcified atheromatous plaques are unilateral and located on the left side. In our study, most of the calcified atheromatous plaques in the study population were located on the left side while all the calcified atheromatous plaques in the control population were located on the right side. The calcified plaques on both left and right sides were located at C3-C4 level. Hence, we think that these different locations of CCAAP may be related to sample size of the studies.
Increasing age is a predisposing factor for progression of atherosclerosis. Generally people over 55 have a greater risk of having a stroke and the risk increases as one gets older.  We found that the highest prevalence of CCAAP was in the age group of 70-79 years. A total of 14 patients out of 32 showed the presence of CCAAP in the age group 70-79 years. These findings were consistent with the ones reported Beckstrom et al. who showed higher prevalence of CCAAP in patients of higher age group. 
Male gender is supposed to be a predisposing factor in the progression of atherosclerosis. According to Beckstrom et al., a significantly higher prevalence of CCAAP was observed in male cancer patients before treatment.  In a study conducted by Kumagai et al., the authors reported significantly higher prevalence of CCAAP in male smoker patients.  According to Bayram et al.  and Kumagai et al.,  the prevalence of CCAAP was 2-3 times more in females. However, the difference between male and female gender was statistically not significant in our study. According to the studies conducted by Carter et al.,  Pornprasertsuk-Damrongsri et al.,  and Sisman et al.,  no statistically significant difference was observed between male and female gender. A slight higher prevalence in males could be attributed to the paucity of female subjects in our study group. Also, the prevalence of deleterious habits like tobacco abuse and alcohol abuse was more in male patients. We suggest that a larger study population may be necessary to accurately determine the influence of gender on CCAAP.
The patients were also evaluated for presence of other associated risk factors like hypertension, ischemic heart disease, radiotherapy, renal diseases, tobacco abuse, smoking, and alcohol consumption. Out of the 26 patients with CCAAP in the diabetic population, 18 (69.2%) patients had associated hypertension and the patients were under medication. Four (15.38%) patients gave a history of ischemic heart disease and 2 (7.69%) patients had history of radiotherapy. Sixteen (61.53%) patients gave a history of tobacco use and 4 (15.38%) gave a history of smoking. Three patients from the diabetic group had history of head and neck radiotherapy. Out of these patients, only one had CCAAP. This patient also had concomitant history of hypertension, ischemic heart disease, and tobacco abuse [Figure 4]. Although various studies by Friedlander et al. ,,, and Freymiller et al.  have reported a higher prevalence of CCAAP in patients who had received head and neck radiation, we could not associate the presence of CCAAP solely to radiotherapy as other predisposing factors for atherosclerosis were also present in this patient.
|Figure 4: Cropped panoramic radiograph of a patient with history of concomitant radiotherapy, hypertension, and tobacco abuse showing multiple radiopaque bodies suggestive of calcified atheromatous plaque (arrow)|
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Within the scope and limitations of present study, patients with diabetes mellitus had a higher prevalence of CCAAP (26%) as compared with age- and sex-matched non-diabetic patients (6%). In the diabetic population, most of the CCAAP were located on the left side, while in the control group, most of them were located on the right side. However, due to smaller sample size, our results are inconclusive to determine the predisposition of CCAAP on a particular side. Prevalence of CCAAP was higher in males. However, this may be due to the larger sample size of males in the study sample. The prevalence of CCAAP increased with increasing age. The highest prevalence of CCAAP was seen in the highest age group (70 years and above). The possibility of CCAAP increased with the presence of other risk factors, namely, hypertension, ischemic heart disease, head and neck irradiation, and tobacco abuse.
| Conclusion|| |
Thus, we conclude that prevalence of CCAAP on panoramic radiographs of patients with diabetes mellitus was significantly higher than those in age- and sex-matched controls. Panoramic radiographs can help in detecting CCAAP in patients susceptible to vascular diseases predisposing to cerebrovascular accidents. It is advisable to screen the panoramic radiographs of diabetic patients thoroughly for presence of CCAAP, as they can help in detecting the asymptomatic CCAAP and in timely referral of the patients to physicians so as to prevent the adverse outcomes of the same.
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Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3]