PATHOLOGY
Cone-Beam Computed Tomography Findings in the Early Diagnosis of Calcified Atheromas Artur Dos Santos Soares, DDS,* Ana M arcia Viana Wanzeler, DDS,y Maria Daniela Oliveria Renda,z Cl audia Gemaque Marinho, MSc,x and Fabrıcio Mesquita Tuji, PhDk Purpose:
Computed tomograms of the mandibles of 285 patients with indications for dental implants were evaluated at a private clinic.
Materials and Methods:
This study involved the evaluation of 285 cone-beam computed tomograms of patients 50 to 75 years of age who were referred to the clinic for the evaluation for implant placement images with visible C3 and C5 vertebrae that were obtained using the same I-Cat tomographic device (Imaging Sciences-Kavo, Hatfield, PA). Atheromas in the carotid space were visualized using paraxial images. Data were analyzed using Student t and c2 tests, with a significance level of a P value less than or equal to .05. Atheromas in the carotid space were observed in 17.89% of patients; a significant difference in the incidence of atheromas was observed between men (24.27%) and women (14.29%; P = .034). However, no significant correlation was found between the frequency of occurrence of atheromas and the affected side of the carotid bifurcation (right or left) in women (P = .431) or men (P = .558).
Results:
Conclusion:
Based on these results, cone-beam computed tomography could be a useful tool for the diagnosis of atheroma. Ó 2016 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg -:1-6, 2016
Atherosclerotic lesions of the carotid bifurcation (ie, atheromas)1 can cause cerebrovascular accidents. Atheromas are produced by the deposition of calcium on atherosclerotic plates, promoting obstruction of the vessel lumen, resulting in ischemia on the obstructed side. The accumulation of blood during the course of buildup of atheromas promotes dilations (ie, aneurysms), which increase pressure in the arterial walls, leading to their rupture.2,3 Radiographic examination is an essential diagnostic modality in various specialties of dentistry. The discovery of an atheroma in the carotid artery by panoramic radiography has great value because it could help
prevent possible complications such as cerebrovascular accidents. However, general practitioners do not have the expertise to diagnose an atheroma accurately because this issue is not addressed in radiology courses.4,5 With advances in diagnostic imaging, the ability to obtain images in 3 dimensions with cone-beam computed tomography (CBCT) has increased greatly, in addition to diagnostic ability and planning for dental procedures.6 In the CBCT machine, the x-ray beam has a cone shape and is wide enough to cover the entire region of interest. The resultant images are obtained from
Received from Federal University of Para, Belem, PA, Brazil.
Address correspondence and reprint requests to Dr Dos Santos
*Implantodontics Specialist, Department of Oral Radiology,
Soares: Department of Radiology, Federal University of Para, Travessa
Postgraduate Program in Dentistry.
Djalma Dutra, 1031, Telegrafo, Belem, PA, Brazil; e-mail: artur_
yRadiology Specialist, Department of Oral Radiology, Postgraduate Program in Dentistry.
[email protected] Received January 11 2016
zStudent, Graduate Program in Dentistry.
Accepted June 18 2016
xRadiology Specialist, Department of Oral Radiology, Postgraduate
Ó 2016 American Association of Oral and Maxillofacial Surgeons
Program in Dentistry.
0278-2391/16/30497-9
kRadiology Specialist, Department of Oral Radiology, Postgraduate
http://dx.doi.org/10.1016/j.joms.2016.06.179
Program in Dentistry.
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EARLY CBCT FINDINGS OF CALCIFIED ATHEROMAS
success of treatment, especially in asymptomatic patients who have not been recognized as being at risk for myocardial infarction. Because health professionals often request a CBCT examination, this study aimed to identify imaging findings consistent with atheromas at CBCT and to correlate the incidence of atheromas thus identified with gender, age, size of the calcification, and side of bifurcation corresponding to the location of the calcification. This examination is expected to serve as an aid for the early diagnosis of atheromas, thus enabling the referral of these patients to specialized professionals for specific tests for the confirmation and treatment of the same.11 Given the lack of information in the literature on this topic, this study aimed to evaluate the frequency with which atheromas are visualized in the carotid arteries by CBCT examination.
Table 1. PRESENCE OF ATHEROMAS IN THE CAROTID SPACE ON CONE-BEAM COMPUTED TOMOGRAMS IN WOMEN VERSUS MEN
Women n
Men
%
n
Total
%
n
%
P Value*
Present 26 14.29 25 24.27 51 17.89 .034 Absent 156 85.71 78 75.73 234 82.11 Total 182 — 103 — 285 — — * By c2 test. Soares et al. Early CBCT Findings of Calcified Atheromas. J Oral Maxillofac Surg 2016.
the image-based post-processing performed on the computer, unlike spiral methods, in which images are obtained based on the combination of the original images of the axial sections.7 With the use of CBCT images, evaluation of the bifurcation of the carotid artery is possible at the level of the epiglottis, where the artery bifurcates and gives rise to the external and internal carotid arteries. The most common reference sites used are vertebrae C3 and C4 and the upper region of the thyroid cartilage of the larynx. Despite the limitations of CBCT in soft tissue visualization, verifying the existence of an atheroma is possible with this technique.8 It has been suggested that these carotid artery calcifications might be visualized using panoramic radiography and then confirmed by Doppler ultrasonography.9 In an axial reformatted CBCT image, most atheromas present as a single mass with homogeneous opacification. They commonly present posterolaterally to the anterior tubercle of the cervical vertebrae and are positioned medially and inferiorly to the angle of the jaw in sagittal sections, with vertical positioning between the C3 and C5 vertebrae.10 Because the identification of atheromas can influence the myocardial prognosis and cerebrovascular accidents, an accurate diagnosis is essential to the
Materials and Methods This study was approved by the committee of ethics and research of the Institute of Health Sciences of the Federal University of Para (Belem, Para, Brazil; 1.049.252). This study involved the evaluation of 285 CBCT images with visible C3 and C5 vertebrae obtained using the same I-Cat tomographic device (Imaging Sciences-Kavo, Hatfield, PA). Atheromas in the carotid space were visualized using paraxial images created with InVivoDental 1.0.511.0 (Anatomage, Inc, San Diego, CA) on a 17-inch liquid crystal display monitor with a resolution of 1,280 1,024 pixels by 2 investigators who had been calibrated for viewing this pathology. CBCT images selected for this study included men and women 50 to 75 years of age who were referred to the clinic for the evaluation of implant placement. Exclusion criteria were patients with a syndrome, patients with a history of neck surgery, patients outside the age range, and the risk group.
Table 2. PRESENCE OF ATHEROMA IN THE CAROTID SPACE ON CONE-BEAM COMPUTED TOMOGRAMS IN WOMEN VERSUS MEN AND RIGHT VERSUS LEFT SIDE
Women Right Side
Present Absent Total
Men
Left Side
Right Side
Left Side
n
%
n
%
Total, n
P Value
n
%
n
%
Total, n
P Value*
12 170 182
6.59 93.41 —
16 166 182
8.79 91.21 —
28 336 364
.431
14 89 103
13.59 86.41 —
17 86 103
16.50 83.50 —
31 175 206
.558
—
* By c2 test. Soares et al. Early CBCT Findings of Calcified Atheromas. J Oral Maxillofac Surg 2016.
—
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SOARES ET AL
Table 3. PRESENCE OF ATHEROMA IN THE CAROTID SPACE ON CONE-BEAM COMPUTED TOMOGRAMS IN MEN VERSUS WOMEN AND BY AGE
Gender
n
Average Age
SD
t
P Value*
Men Women
103 182
59.74 60.68
7.75 8.25
0.94
.34
Abbreviation: SD, standard deviation. * By Student t test. Soares et al. Early CBCT Findings of Calcified Atheromas. J Oral Maxillofac Surg 2016.
Statistical tests were used for the analysis of parametric and nonparametric data, and the results were evaluated using the BioEstat 5.0 (Informer Technologies; available at: http://www.informer.com/) with a 5% significance level for all tests. A c2 test was performed to assess the correlation of the incidence of atheromas in the carotid artery with the patient’s gender and the affected side of the carotid bifurcation for men and women. The Student t test was performed to assess the difference in mean age between men and women and to analyze the correlation between the incidence of atheromas in the carotid artery and the mean age of the men and women.
Results In total, 285 CBCT scans of 182 women and 103 men were analyzed in this study. An atheroma in the carotid artery was visualized in 17.89% of patients, with a significant difference noticed in its incidence between men (24.27%) and women (14.29%; P = .034; Table 1). However, no significant correlation was found between the frequency of occurrence of atheromas and the affected side of the carotid bifurcation (right or left) in women (P = .431) or men (P = .558; Table 2). For age, no significant difference between women (mean age, 60.68 yr) and men (mean age, 59.74 yr; P = .34) based on mean age were found among affected patients (Table 3).
Discussion A CBCT examination providing an overview of the anatomic structures is often requested by oral surgeons for the diagnosis and planning of the surgical intervention of oral disorders. CT scans also have been shown to identify changes not directly related to dentistry, such as calcifications within the carotid arteries.12,13 CBCT can visualize soft tissue, but information about soft tissues cannot be obtained, because CBCT does not allow the use of the window for soft
FIGURE 1. Axial cone-beam computed tomographic view showing a circular hyperdensity of the external carotid space (arrow). Soares et al. Early CBCT Findings of Calcified Atheromas. J Oral Maxillofac Surg 2016.
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EARLY CBCT FINDINGS OF CALCIFIED ATHEROMAS
FIGURE 2. Sagittal cone-beam computed tomographic view showing a circular hyperdensity (arrow) between vertebrae C3 and C4. Soares et al. Early CBCT Findings of Calcified Atheromas. J Oral Maxillofac Surg 2016.
tissue.14 However, it does permit the visualization of calcifications in the cervical region (carotid space), where the atheromas are located. In this study, the authors observed the presence of calcifications in the coronal, axial, and sagittal planes (Figs 1-3, respectively). The authors rated the prevalence of calcified atheroma, in which the incidence was 8.3%; this was not considered high compared with that of patients with cardiovascular disease and neoplasms of the head and neck region. However, the authors observed a 17.89% prevalence of calcified atheroma in patients who underwent CBCT.15 The methodology of this
study aimed to assess the prevalence of calcified atheromas and not atheromas in general (most atheromas are not calcified; thus, they cannot be observed by CBCT). According to the American Heart Association,16 atheromas can be classified as follows: Type I: initial lesion with foam cells Type II: multiple foam cell layers Type III: preatheroma with extracellular lipids Type IV: mature atheroma with central lipid core Type V: fibro-atheroma Type VI: unstable plaque with surface irregularities, hemorrhage, or thrombus Type VII: calcified plaque
FIGURE 3. Coronal cone-beam computed tomographic view showing a circular hyperdensity of the external carotid space (arrows) bilaterally. Soares et al. Early CBCT Findings of Calcified Atheromas. J Oral Maxillofac Surg 2016.
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SOARES ET AL
FIGURE 4. Doppler ultrasound image of the same patient showing a calcified LCA. LCA, left common carotid artery; LIC, left internal carotid artery. Soares et al. Early CBCT Findings of Calcified Atheromas. J Oral Maxillofac Surg 2016.
Type VIII: fibrotic plaque without lipid core The authors suggested that panoramic radiographs are valuable resources for the detection of calcifications in the carotid artery as potential risks for cerebrovascular accidents.17 When calcified, atheromatous plaques can be seen on panoramic radiographs in
the region of the C3 and C4 vertebrae, 2 to 4 cm below the angle of the jaw, above or below the hyoid bone. In this study, 1,548 panoramic radiographs were evaluated, and 4.2% of those of patients older than 55 years presented with calcifications. In this survey of the CBCT findings, 17.89% of patients presented with calcifications, and the mean age of the affected women was 60.68 years and that of the affected men was 59.74 years. The incidence of atheromas reported in the literature is 2 to 5% of the adult population and higher in women after menopause and in individuals at least 65 years old.18 However, in the present study, a higher prevalence of atheromas was found in men (24.27%) than in women, and the mean age of the men with atheromas was 59.74 years. Sialolithiasis, tonsilloliths, and the calcification of lymph nodes and blood vessels can occur in the cervical region. The necessity to differentiate these calcifications not only from one another but also from other anatomic structures and calcifiable structures, such as the stylohyoid ligament, triticeous cartilage, and upper horn of the thyroid cartilage, complicates the diagnosis of atheromas. Although the similarity between CBCT findings of atheromas and those of a few other anatomic and pathologic structures might confuse an oral surgeon, the possibility of detecting
FIGURE 5. Doppler ultrasound image of the same patient showing a calcified LIC with decreased blood flow. LIC, left internal carotid artery. Soares et al. Early CBCT Findings of Calcified Atheromas. J Oral Maxillofac Surg 2016.
6 carotid atheromas at CBCT allows for the possibility of early treatment, thus decreasing the risk of morbidity and mortality.19 Hypertension, diabetes mellitus, hyperlipidemia, radiation therapy, menopause, kidney disease, and obstructive sleep apnea are known accelerators of the formation of atheromas in the carotid artery.20 Despite the ability of CT to identify calcifications suggestive of atheroma, it does not allow for the assessment of the degree of carotid obstruction or the accurate localization of the atheroma. Thus, other options become necessary for a definitive diagnosis. Doppler ultrasonography is the most appropriate method to confirm the presence, location, and size of the carotid atheroma (Figs 4, 5). Then, the oral surgeon can identify these calcifications in the carotid artery and refer these patients for appropriate medical treatment to prevent possible complications.21 Analysis of the present results showed that CBCT could be a useful tool for the diagnosis of atheroma because it showed a statistically relevant difference in the incidence of atheromas between women and men and no difference between the right and left sides of the carotid bifurcation and the patients’ age.
References 1. Hamedani S, Dabbaghmanesh MH, Zare Z, et al: Relationship of elongated styloid process in digital panoramic radiography with carotid intima thickness and carotid atheroma in Doppler ultrasonography in osteoporotic females. J Dent 16:93, 2015 2. Friedlander AH: Association between clinically identified diagonal earlobe creases and calcified carotid artery atheromas evidenced on panoramic radiography. J Oral Maxillofac Surg 68: 227, 2010 3. Friedlander AH: Calcified carotid artery atheromas. J Am Dent Assoc 138:1191, 2007 4. Brito AC, Nascimento HA, Argento R, et al: Prevalence of suggestive images of carotid artery calcifications on panoramic radiographs and its relationship with predisposing factors. Ci^encia & Sa ude Coletiva 21:2201, 2011
EARLY CBCT FINDINGS OF CALCIFIED ATHEROMAS 5. Guimar~aes Henriques JC, Kreich EM, Helena Baldani M, et al: Panoramic radiography in the diagnosis of carotid artery atheromas and the associated risk factors. Open Dent J 5:79, 2011 6. Almog DM, Padberg FT Jr, Carmel G, et al: Previously unappreciated carotid artery stenosis diagnosed by cone beam computerized tomography. J Oral Maxillofac Surg 71:702, 2013 7. Almog DM, Tsimidis K, Moss ME, et al. Evaluation of a training program for detection of carotid artery calcifications on panoramic radiographsOral Surg Oral Med Oral Pathol Oral Radiol Endod 90:111, 2000 8. Angelopoulos C: Cone beam tomographic imaging anatomy of the maxillofacial region. Dent Clin North Am 52:731, 2008 9. Romano-Dousa CM, Krejci L, Medeiros FM, et al: Diagnostic agreement between panoramic radiographs and color Doppler images of carotid atheroma. J Appl Oral Sci 17:45, 2009 10. Abreu TQ, Ferreira EB, de Brito Filho SB, et al: Prevalence of carotid artery calcifications detected on panoramic radiographs and confirmed by Doppler ultrasonography: Their relationship with systemic conditions. Indian J Dent Res 26:345, 2015 11. Ekanayke L, Perera I: Factors associated with perceived oral health status in older individuals. Int Dent J 55:31, 2005 12. Arad Y, Goodman KJ, Roth M, et al: Coronary calcification, coronary disease risk factors, C-reactive protein, and atherosclerotic cardiovascular disease events. J Am Coll Cardiol 46:158, 2005 13. Greenberg BL, Glick M, Goodchild J, et al: Screening for cardiovascular risk factors in a dental setting. J Am Dent Assoc 138: 798, 2007 14. Schulze D, Heiland M, Schnelzle R, et al: Diagnostic possibilities of cone-beam computed tomography in the facial skeleton. Int Congr Ser 1268:1179, 2004 15. Guerreiro da Silva N Jr, Pedreira EN, Tuji FM, et al: Prevalence of calcified carotid artery atheromas in panoramic radiographs of HIV-positive patients undergoing antiretroviral treatment: A retrospective study. Oral Surg Oral Med Oral Pathol Oral Radiol 117:67, 2014 16. Cai JM, Hatsukami TS, Ferguson MS, et al: Classification of human carotid atherosclerotic lesions with in vivo multicontrast magnetic resonance imaging. Circulation 106:1368, 2002 17. Friedlander AH, Lande A: Panoramic radiographic identification of carotid arterial plaques. Oral Surg Oral Med Oral Pathol 52: 102, 1981 18. Madden RP, Hodges JS, Salmen CW, et al: Utility of panoramic radiographs in detecting cervical calcified carotid atheroma. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 103:543, 2007 19. Friedlander AH, Garret NR, Chin EE, et al: Ultrasonographic confirmation of carotid artery atheromas diagnosed via panoramic radiography. J Am Dent Assoc 136:635, 2005 20. Kanzu O, Ozbek M, Aveu N, et al: The prevalence of carotid artery calcification on the panoramic radiographs of patients with renal disease. Dentomaxillofac Radiol 34:16, 2005 21. Mupparapu M, Kim IH: Calcified carotid artery atheroma and stroke. J Am Dent Assoc 138:483, 2007
