- Email: [email protected]
Prevalence in digital panoramic radiographs of carotid area calcification among Iraqi individuals with stroke-related disease
Prevalence in digital panoramic radiographs of carotid area calcification among Iraqi individuals with stroke-related disease Asmaa Tahseen Uthman, BDS, MSc,a and Asmaa Basheer Al-Saffar, BDS, MSc,b Baghdad and Mosul, Iraq UNIVERSITY OF BAGHDAD AND UNIVERSITY OF MOSUL
Objective. The purpose of this study was to determine the prevalence of carotid calcification on digital dental panoramic tomography in a group of the Iraqi population who have some stroke-related vascular and or metabolic disease. Study design. Digital dental panoramic tomographic images of 157 adult patients of age range 40-80 years having chronic illnesses such as coronary heart diseases, hypertension, type 2 diabetes, and hyperlipidemia and of 43 control subjects (age range 40-71 years, free of systemic diseases) were made and examined for the presence of carotid artery calcification adjacent or just below the intervertebral space between C3, C4, and C5 on both sides of patient’s neck. The study group was subclassified into vascular, metabolic, and vascular-metabolic groups. Determinations were made of the prevalence, number, and distribution of carotid area calcifications. Forward stepwise logistic regression analysis was used to determine which risk factor is more liable to develop carotid artery area calcification. Results. The statistical difference between patients with stroke-related diseases (vascular, metabolic, and vascularmetabolic groups) versus patients in the control group was highly significant concerning the prevalence of carotid area calcifications (P ⬍ .01). Carotid area calcification was identified in 38.8% of the study group. Bilateral calcifications were observed more than unilateral calcification for both genders (26.6% vs. 13.9% for men; 24.4% vs. 12.8% for women). Conclusion. People with stroke-related vascular and/or metabolic diseases have greater prevalence of calcified area calcifications seen on panoramic radiographs than people who are otherwise healthy. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105:e68-e73)
Stroke, or cerebrovascular accident (CVA), is the third leading cause of death in most countries in the world, following cardiovascular diseases and cancer.1 It is considered to be a significant public health issue, owing not only to its high incidence, but also to the high costs involved in the physical and psychologic rehabilitation of the patients. About 60% of the patients who survive a stroke suffer a long-term physical and psychologic disability.2 Although stroke may be preventable, a major challenge is to find effective methods of detection of stroke-prone patients. Most noncardiogenic strokes occur as a result of atherosclerosis involving the proximal internal carotid artery, calcification of which can be detected on dental panoramic radiography.3 Friedlander and Lande,4 for the first time, published the possibility a
Assistant Professor, Department of Oral Diagnosis, College of Dentistry, University of Baghdad. b Assistant Lecturer, Department of Oral Diagnosis, College of Dentistry, University of Mosul. Received for publication Sep 14, 2007; returned for revision Oct 24, 2007; accepted for publication Nov 7, 2007. 1079-2104/$ - see front matter © 2008 Mosby, Inc. All rights reserved. doi:10.1016/j.tripleo.2007.11.009
e68
of identifying calcified atheroma plaque within the carotid artery on panoramic radiograph. Carotid artery atheroma (CAA) is defined radiologically as a radiopaque mass appearing adjacent to the cervical spine and hyoid bone at the level of the lower margin of the third (C3) and the entirety of the fourth (C4) cervical vertebrae, about 1.5-2.5 cm inferior-posterior to the angle of the mandible.5 Such calcification may appear as either a nodular radiopaque mass or radiopaque vertical lines inferior to the angle of the mandible.4 Carotid atherosclerosis is not the only cause of soft tissue calcification seen anterior to the cervical vertebrae in panoramic radiographs. Care needs to be applied to differentiate carotid calcification from calcified triticious or thyroid cartilages as well as calcified lymph nodes.6 Factors predisposing carotid atherosclerosis include advancing age, male gender, systolic hypertension, hyperchlolestrolemia, cigarette smoking, diabetes mellitus, physical inactivity, obesity, and coronary artery diseases.7 Lewis and Brooks8 recommend the use of panoramic radiographs to identify patients at risk for developing a CVA. Reduction in morbidity and mortality through early identification of stroke-prone patients would have powerful humanitarian and economic
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Table I. Distribution of presumed calcified carotid artery atheromas (CCAAs) in the study group Radiographic finding
Fig 1. Bilateral CCAA.
significance.3 It is for this reason that the dentist’s careful evaluation of the dental panoramic radiographs might be instrumental in saving a patient’s life. Cohen et al.9 considered panoramic radiographs to be powerful markers for subsequent vascular events, and patients who have carotid calcification should be referred for cerebrovascular and cardiovascular evaluation and management. Therefore, the present study was made to determine the prevalence of calcified atherosclerotic lesions among a group of Iraqi patients with strokepromoting chronic illnesses. MATERIALS AND METHODS Two hundred individuals were enrolled in the study. The study group consisted of 157 patients (79 men and 78 women, age range 40-80 years) with chronic illnesses: 1. Vascular group: comprising 75 patients (38 men and 37 women) having hypertension and/or coronary heart disease. 2. Metabolic group: comprising 42 patients (21 men and 21 women) having type 2 diabetes mellitus and/or hyperlipedemia. 3. Vascular-metabolic group: comprising 40 patients (20 men and 20 women) having combined vascular and metabolic diseases. The control group comprised 43 age-matched healthy individuals, without vascular or metabolic disease. All individuals were radiographed using the Planmeca Proline CC digital dental panoramic system. Data was processed using Dimax Pro/Classic software version 3.2.1 in high resolution mode. To optimize the image for carotid area calcification detection, a radiograph was made with the patient 1 cm anterior and 1 cm superior to the focal trough suggested by the manufacturer of the panoramic system. METHODS The medical records of all individuals in the studied group were reviewed for factors related to atheroscle-
Carotid artery calcification Right side calcification Left side calcification Unilateral CCAAs Bilateral CCAAs
Men (n ⫽ 79)
Women (n ⫽ 78)
Total (n ⫽ 157)
n
%
n
%
n
%
32
40.5
29
37.2
61
38.85
24
30.4
25
32.1
49
31.2
29
36.7
23
29.5
52
33.1
11 21
13.9 26.6
10 19
12.8 24.4
21 40
13.37 25.4
rosis. Hypertension was characterized as the current use of an antihypertension medication or a systolic blood pressure of ⬎140 mm Hg and/or a diastolic blood pressure of ⬎90 mm Hg on 3 occasions. Hyperlipidemia was construed as a note in the medical record identifying elevation of a fasting total serum cholesterol level of more than 200 mg/dL. Coronary heart diseases (angina and myocardial infarction) were characterized in the patient’s medical records with 2 recent ECG reports confirming the diagnosis. A diagnosis of patients with type 2 diabetes was made by having a fasting plasma glucose ⬎125 mg/dL on 2 separate occasions. All radiographic interpretations were performed by one of the authors, who was blinded to which cohort each radiographic image belonged. All radiographic images were examined in subdued light for the presence of presumed calcified carotid artery atheroma (CCAA). Data analysis consisted of using Fisher exact test to compare the prevalence rate for presumed CCAA found on digital dental panoramic images. Forward stepwise logistic regression analysis also was used to determine the risk factors that may lead to development of presumed CCAA. RESULTS Presumed CCAA was identified in 61 out of 157 individuals (38.8%) in the study groups (Fig. 1). They were identified on the panoramic images of 32 men (40.5% of the men in the study groups) and in 29 women (37.2% of the women in the study groups). Bilateral presumed CCAAs were identified in 21 male (26.6%) and 19 female (24.4%), whereas unilateral carotid artery calcification (CAC) was observed in 11 male (13.9%) and 10 female (12.8%) patients (Table I). Table II shows the numbers and the percentages of presumed CCAA for the right and left sides in the study group. A nonsignificant statistical difference (P ⬎ .05) was seen between the 2 sides. Moreover, a nonsignificant statistical difference was also seen between gen-
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Table II. Distribution of presumed calcified carotid artery atheromas (CCAAs) in the right and left sides in the men and women of the study group Right side Men
Left side
Women
Total
Men
Side finding
n
%
n
%
n
%
Positive Negative Single Multiple C3-C4 C4-C5
24 55 17 7 20 4
30.4 69.6 70.8 29.2 83.3 16.7
25 53 22 3 23 2
32.1 67.9 88 12 92 8
49 108 39 10 43 6
31.2 68.8 79.6 20.4 87.8 12.2
ders regarding the side (right and left), number of calcified masses (single or multiple), and vertebral location of these calcifications. Among 43 age-matched healthy individuals, only 5 (11.6%) had a presumed CCAA in their panoramic radiographic image. One had bilateral calcification and the other 4 had unilateral presumed CCAA. Vascular group Among 75 patients with vascular diseases, 31 patients (41.3%) had positive presumed CCAA findings on dental panoramic radiographs. Twenty-two patients (11 from each gender) had bilateral presumed CCAA, constituting 71.0% of the total positive presumed CCAA findings in this group. The remaining 9 patients had unilateral presumed CCAA findings. Single calcified mass findings were more common than multiple calcified masses (21 cases vs. 5 only on the right side and 18 cases vs. 9 on the left side). The C3-C4 location of these masses was the most common location on both sides (Tables III and IV). Metabolic group Forty-two patients suffering from either type 2 diabetes or hyperlipidemia were enrolled in the study. Among them, only 15 patients had positive presumed CCAA in panoramic radiographs. Nine patients (6 men and 3 women) had bilateral presumed CCAA (60% of the total positive presumed CCAA findings in this group), and 6 patients had unilateral presumed CCAA. Single calcification was more common than multiple calcifications on both right and left sides (Tables III and IV). Vascular-metabolic group This group included 40 patients who had either hypertension with diabetes, coronary heart disease with diabetes, or hyperlipidemia with any vascular diseases. Presumed CCAA was seen in 15 patients (37.5% of the total number of this group). Bilateral presumed CCAA
P value P P P P P P
⬎ ⬎ ⬎ ⬎ ⬎ ⬎
.05 .05 .05 .05 .05 .05
Women
Total
n
%
n
%
n
%
29 50 21 8 24 5
36.7 63.3 72.4 27.6 82.8 17.2
23 55 15 8 20 3
29.5 70.5 65.2 34.8 87 13
52 105 36 16 44 8
33.1 66.9 69.2 30.8 84.6 15.4
P value P P P P P P
⬎ ⬎ ⬎ ⬎ ⬎ ⬎
.05 .05 .05 .05 .05 .05
was seen in 9 patients (4 men and 5 women), constituting 60% of the positive presumed CCAA findings in this group. Unilateral CAC was seen in 3 men and 3 women. A single mass was seen in 10 cases, and multiple presumed CCAA masses were seen in 2 cases (Tables III and IV). Forward stepwise logistic regression analysis was applied on each disease independently to determine the strongest risk factor that may lead to the development of presumed CCAA. Table V shows the relationship between presumed CCAA findings on the left and right side and the systemic diseases included in this study. Angina, hyperlipidemia, and myocardial infarction contributed substantially more to the occurrence of presumed left side CCAA than did hypertension. DISCUSSION Incidental finding of calcification lying in the carotid bifurcation region is seen on oral panoramic radiographs in 1%-5% of the adult population when analog film radiography is performed.8 Such carotid-area calcifications are more prevalent in patients with systemic diseases such as type 2 diabetes,10 renal transplantation and dialysis,11 head and neck radiation therapy,12 cardiac myopathy,13 and stroke.14 Calcification is a morphologic complication in the evolution of atheromatous plaque. Generally, CCAAs are found at the branch point of artery vessels where turbulent flow is increased.15 Patients found to have carotid calcification on panoramic radiographs should be referred for cerebrovascular and cardiovascular evaluation and aggressive management of vascular risk factors. Cohen et al.9 suggested 3 potential explanations of why carotid calcification appears to carry an ominous cerebrovascular and cardiovascular prognosis: 1. Carotid calcifications are a sign of underlying significant carotid stenosis. 2. Carotid calcifications are simply another indication of a heavy factor burden.
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Table III. Distribution of presumed calcified carotid artery atheromas (CCAAs) in the study and control groups Vascular group (n ⫽ 75) Finding Total Total Total Total Total Total
CCAA in men CCAA in women unilateral CCAAs in men unilateral CCAAs in women bilateral CCAAs in men bilateral CCAAs in women
Metabolic group (n ⫽ 42)
Vascularmetabolic group (n ⫽ 40)
Control group (n ⫽ 43)
n
%
n
%
n
%
n
%
15 16 4 5 11 11
48.4 51.6 44.4 55.6 50 50
10 5 4 2 6 3
66.7 33.3 66.6 33.3 66.6 33.3
7 8 3 3 4 5
46.6 54.4 50 50 44.4 56.6
4 1 4 0 0 1
80 20 100 0 0 100
Table IV. Comparison of calcified carotid artery atheromas (CCAAs) findings in panoramic radiographs between control and study groups
Right side finding Positive Negative No. of masses (right) Single Multiple Vertebral location C3-C4 C4-C5 Left side finding Positive Negative No. of masses (left) Single Multiple Vertebral location C3-C4 C4-C5
Group 4: vascularmetabolic (n ⫽ 40)
Group 1: control (n ⫽ 43) n %
Group 2: vascular (n ⫽ 75) n %
Group 3: metabolic (n ⫽ 42) n %
n
%
3 40
7.0 93.0
26 49
34.7 65.3
11 31
26.2 73.8
12 28
3 0
100 0.0
21 5
80.77 19.23
8 3
72.73 27.27
3 0
100 0.0
21 5
80.77 19.23
11 0
3 40
7.0 93.0
27 48
36.0 64.0
3 0
100 0.00
18 9
3 0
100 0.0
22 5
P value G1 vs. G2
G1 vs. G3
G1 vs. G4
30.0 70.0
.001
.01
.006
10 2
83.33 16.67
.55
.45
.63
100.0 0.0
11 1
91.67 8.33
.55
.82
.8
13 29
31.0 69.0
12 28
30.0 70.0
.001
.003
.006
66.67 33.33
8 5
61.54 38.46
10 2
83.33 16.67
.33
.3
.63
81.48 18.52
12 1
92.31 7.69
10 2
83.33 16.67
.57
.81
.63
3. Carotid calcifications are an independent risk factor of cerebrovascular and cardiovascular diseases. Radiographs remain the most useful diagnostic aid. The utility of this type of observation obviously will depend on the prevalence and amount of calcium with these lesions, which varies from patient to patient. Because calcium is such a common component of atherosclerotic plaque, the presence of calcium in an unusual location, especially lying over the course of a blood vessel commonly affected by this disease, is presumptive evidence of some degree of atherosclerosis.16 Thousands of dentists have an opportunity each year to identify and refer for treatment patients at risk of experiencing adverse vascular events.17 In the
present study, presumed CCAAs were identified in 52 individuals (33.1% of the total studied sample) on the left side and in 49 individuals (31.2%) on the right side, with nonsignificant statistical differences between the 2 sides (P ⬎ .05). This finding is not in agreement with Ohba et al.,18 who reported CCAA in a selected Japanese sample to be 3 times more prevalent on the right side than on the left side (74% vs. 26%). This difference between 2 studies may be due to different population characteristics. The male-female ratio for presumed CCAA in the present study was 1.1:1 with nonsignificant gender difference. The same finding was reported by Ohba et al.18 and Bayram et al.19 However, Tamura et al.20 identified about 106 carotid calcifica-
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Table V. Forward stepwise logistic regression for risk factors developing left and right presumed calcified carotid artery atheromas (CCAAs) Parameter Left side presumed CCAAs Angina Hyperlipidemia Myocardial infarction Diabetes mellitus Right side presumed CCAAs Myocardial infarction Angina Hyperlipidemia Hypertension
n
Positive finding
Negative finding

OR
95% CI
P value
33 17 7 75
25 14 5 34
8 3 2 41
3.63 3.53 3.49 1.81
37.63 34.05 32.93 6.09
8.81-160.73 4.75-244.33 2.22-488.3 1.8-20.55
⬍.001 ⬍.001 .01 ⬍.001
7 33 17 94
5 22 10 40
2 11 7 54
2.15 1.89 1.22 0.94
8.58 6.65 3.40 2.56
1.13-65.17 2.59-17.09 1.02-11.32 1.02-6.43
.04 ⬍.001 .05 .05
OR, Odds ratio; CI, confidence interval; , regression coefficient.
tions on panoramic radiographs with a male-female ratio of 1:3. This ratio was about 3 times higher than that of the present study. Tanaka et al.21 found a significant correlation between patients with history of past vascular diseases and CCAA. The incidence of CCAA was reported by Fukuta et al.22 to be 14.7 times as high as that of those who had no cardiovascular or cerebrovascular disease. This is in agreement with the present finding concerning the high prevalence of presumed CCAA in patients with vascular disease (41.3%). Patients with type 2 diabetes, irrespective of treatment modality, have high rates of calcified atheromas on carotid arteries as visualized on panoramic radiography. The resultant hyperglycemia and other risk factors associated with the disease may be the reason for the presence of a high percentage of CCAA. Patients with combined metabolic and vascular disorders had presumed CCAA in 37.5% of the sample in the present study. This finding was higher than that recorded by Friedlander and Maeder10 for patients with type 2 diabetes alone. The findings in the present study lend some support to the view of Crouse23 that aggressive modification of risk factors can retard progression (and may promote regression) of atherosclerotic lesions in both cardiac and cerebrovascular disturbances. CONCLUSIONS Peoples with stroke-related vascular and/or metabolic diseases have greater prevalence of calcified atheromas on their panoramic radiographs than people who are otherwise healthy. This detection could potentially increase the length and quality of life for peoples with CACs through early diagnosis and prevention of fatal consequences of these lesions, along with focusing on more traditional strategies, such as instituting a tobacco cessation program or referring patients for management
of obesity or hypertension, which have a significant impact on reduction the risk of stroke. REFERENCES 1. Fatahzadeh M, Glick M. Stroke: epidemiology, classification, risk factors, complications, diagnosis, prevention and medical and dental management. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006;102:180-91. 2. Friedlander AH. Identification of stroke-prone patients by panoramic and cervical spine radiography. Dentomaxillofac Radiol 1995;24:160-4. 3. Carter LC, Tsimidis K, Fabiano J. Carotid calcifications on panoramic radiography identify an asymptomatic male patient at risk for stroke. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;85:119-22. 4. Friedlander AH, Lande A. Panoramic radiographic identification of carotid arterial plaques. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1981;52:20-4. 5. Friedlander AH, August M. The role of panoramic radiography in determining an increased risk of cervical atheromas in patients treated with therapeutic irradiation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;85:339-44. 6. Carter LC. Discrimination between calcified triticeous cartilage and calcified carotid atheromas on panoramic radiography. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90:108-10. 7. Friedlander AH, Friedlander IK. identification of stroke prone patients by panoramic dental radiography. Aust Dent J 1998;43:51-4. 8. Lewis DA, Brooks SL. Carotid artery calcification in a general dental population: a retrospective study of panoramic radiographs. Gen Dent 1999;47:98-103. 9. Cohen SN, Friedlander AH, Jolly DA, Date L. Carotid calcification on panoramic radiographs: an important marker for vascular risk. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2002;94:510-4. 10. Friedlander AH, Maeder LA. The prevalence of calcified carotid artery atheromas on the panoramic radiographs with type 2 diabetes mellitus. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;89:20-4. 11. Kansu O, Ozbeck M, Avcu N, Genctoy G, Kansu H, Turgan C. The prevalence of carotid artery calcification on the panoramic radiographs of patients with renal disease. Dentomaxillofac Radiol 2005;34:16-9. 12. Freymiller E.G., Sung EC, Friedlander AH. Detection of radia-
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13.
14.
15.
16.
17.
18.
tion-induced cervical atheromas by panoramic radiographs. Oral Oncol 2000;36:175-9. Sung EC, Friedlander AH, Kobashigawa JA. The prevalence of carotid artery atheromas on the panoramic radiographs of patients with dilated cardiomyopathy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004;97:404-7. 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 Oral Radiol Endod 1994;77:669-77. Friedlander AH, Altman L. Carotid artery atheromas in post menopausal women. Their prevalence on panoramic radiographs and their relationship to atherogenic risk factors. J Am Dent Assoc 2001;132:130-6. Almog DM, Tsimidis K, moss ME, Gottlieb RH, Carter LC. Evaluation of training program for detection of carotid artery calcification on panoramic radiography. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;89:111-7. Friedlander AH, Garrett NR, Chin EE, Baker JD. Ultrasonographic confirmation of carotid artery atheromas diagnosed via panoramic radiography. J Am Dent Assoc 2005;36:35-40. Ohba T, Takata Y, Ansai T, Morimoto Y, Tanaka T, Kito S. Evaluation of carotid artery atheromas detected by panoramic radiograph among 80-year-olds. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003;96:647-50.
Uthman and Al-Saffar e73 19. Bayram B, Uckan S, Acikgoz A, Muderrisoglu H, Aydinalp A. Digital panoramic radiography: a reliable method to diagnose carotid artery atheromas. Dentomaxillofac Radiol 2006;35: 266-70. 20. Tamura T, Inui M, Akase M, Nakamura S, Okamura K, Tagawa T. Clinicostatistical study of carotid calcification on panoramic radiographs. Oral Dis 2005;11:314-7. 21. Tanaka T, Morimoto Y, Ansai T, Okabe S, Yamada T, Tagushi A, et al. Can the presence of carotid artery calcification on panoramic radiographs predicts the risk of vascular diseases among 80-year-olds? Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006;101:777-83. 22. Fukuta Y, Kimura T, Totsuka M. Oral findings of patients with cardiovascular disease: remaining tooth number and panoramic radiographic findings. Jpn J Oral Diag Oral Med 2003;16:15-21. 23. Crouse JR. Heart of the matter with cerebral arterial sclerosis. Lancet 1996;348:766. Reprint requests: Dr. Asmaa T. Uthman Al-Mansur PO Box 6040 Baghdad, Iraq [email protected]
Objective. The purpose of this study was to determine the prevalence of carotid calcification on digital dental panoramic tomography in a group of the Iraqi population who have some stroke-related vascular and or metabolic disease. Study design. Digital dental panoramic tomographic images of 157 adult patients of age range 40-80 years having chronic illnesses such as coronary heart diseases, hypertension, type 2 diabetes, and hyperlipidemia and of 43 control subjects (age range 40-71 years, free of systemic diseases) were made and examined for the presence of carotid artery calcification adjacent or just below the intervertebral space between C3, C4, and C5 on both sides of patient’s neck. The study group was subclassified into vascular, metabolic, and vascular-metabolic groups. Determinations were made of the prevalence, number, and distribution of carotid area calcifications. Forward stepwise logistic regression analysis was used to determine which risk factor is more liable to develop carotid artery area calcification. Results. The statistical difference between patients with stroke-related diseases (vascular, metabolic, and vascularmetabolic groups) versus patients in the control group was highly significant concerning the prevalence of carotid area calcifications (P ⬍ .01). Carotid area calcification was identified in 38.8% of the study group. Bilateral calcifications were observed more than unilateral calcification for both genders (26.6% vs. 13.9% for men; 24.4% vs. 12.8% for women). Conclusion. People with stroke-related vascular and/or metabolic diseases have greater prevalence of calcified area calcifications seen on panoramic radiographs than people who are otherwise healthy. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105:e68-e73)
Stroke, or cerebrovascular accident (CVA), is the third leading cause of death in most countries in the world, following cardiovascular diseases and cancer.1 It is considered to be a significant public health issue, owing not only to its high incidence, but also to the high costs involved in the physical and psychologic rehabilitation of the patients. About 60% of the patients who survive a stroke suffer a long-term physical and psychologic disability.2 Although stroke may be preventable, a major challenge is to find effective methods of detection of stroke-prone patients. Most noncardiogenic strokes occur as a result of atherosclerosis involving the proximal internal carotid artery, calcification of which can be detected on dental panoramic radiography.3 Friedlander and Lande,4 for the first time, published the possibility a
Assistant Professor, Department of Oral Diagnosis, College of Dentistry, University of Baghdad. b Assistant Lecturer, Department of Oral Diagnosis, College of Dentistry, University of Mosul. Received for publication Sep 14, 2007; returned for revision Oct 24, 2007; accepted for publication Nov 7, 2007. 1079-2104/$ - see front matter © 2008 Mosby, Inc. All rights reserved. doi:10.1016/j.tripleo.2007.11.009
e68
of identifying calcified atheroma plaque within the carotid artery on panoramic radiograph. Carotid artery atheroma (CAA) is defined radiologically as a radiopaque mass appearing adjacent to the cervical spine and hyoid bone at the level of the lower margin of the third (C3) and the entirety of the fourth (C4) cervical vertebrae, about 1.5-2.5 cm inferior-posterior to the angle of the mandible.5 Such calcification may appear as either a nodular radiopaque mass or radiopaque vertical lines inferior to the angle of the mandible.4 Carotid atherosclerosis is not the only cause of soft tissue calcification seen anterior to the cervical vertebrae in panoramic radiographs. Care needs to be applied to differentiate carotid calcification from calcified triticious or thyroid cartilages as well as calcified lymph nodes.6 Factors predisposing carotid atherosclerosis include advancing age, male gender, systolic hypertension, hyperchlolestrolemia, cigarette smoking, diabetes mellitus, physical inactivity, obesity, and coronary artery diseases.7 Lewis and Brooks8 recommend the use of panoramic radiographs to identify patients at risk for developing a CVA. Reduction in morbidity and mortality through early identification of stroke-prone patients would have powerful humanitarian and economic
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Table I. Distribution of presumed calcified carotid artery atheromas (CCAAs) in the study group Radiographic finding
Fig 1. Bilateral CCAA.
significance.3 It is for this reason that the dentist’s careful evaluation of the dental panoramic radiographs might be instrumental in saving a patient’s life. Cohen et al.9 considered panoramic radiographs to be powerful markers for subsequent vascular events, and patients who have carotid calcification should be referred for cerebrovascular and cardiovascular evaluation and management. Therefore, the present study was made to determine the prevalence of calcified atherosclerotic lesions among a group of Iraqi patients with strokepromoting chronic illnesses. MATERIALS AND METHODS Two hundred individuals were enrolled in the study. The study group consisted of 157 patients (79 men and 78 women, age range 40-80 years) with chronic illnesses: 1. Vascular group: comprising 75 patients (38 men and 37 women) having hypertension and/or coronary heart disease. 2. Metabolic group: comprising 42 patients (21 men and 21 women) having type 2 diabetes mellitus and/or hyperlipedemia. 3. Vascular-metabolic group: comprising 40 patients (20 men and 20 women) having combined vascular and metabolic diseases. The control group comprised 43 age-matched healthy individuals, without vascular or metabolic disease. All individuals were radiographed using the Planmeca Proline CC digital dental panoramic system. Data was processed using Dimax Pro/Classic software version 3.2.1 in high resolution mode. To optimize the image for carotid area calcification detection, a radiograph was made with the patient 1 cm anterior and 1 cm superior to the focal trough suggested by the manufacturer of the panoramic system. METHODS The medical records of all individuals in the studied group were reviewed for factors related to atheroscle-
Carotid artery calcification Right side calcification Left side calcification Unilateral CCAAs Bilateral CCAAs
Men (n ⫽ 79)
Women (n ⫽ 78)
Total (n ⫽ 157)
n
%
n
%
n
%
32
40.5
29
37.2
61
38.85
24
30.4
25
32.1
49
31.2
29
36.7
23
29.5
52
33.1
11 21
13.9 26.6
10 19
12.8 24.4
21 40
13.37 25.4
rosis. Hypertension was characterized as the current use of an antihypertension medication or a systolic blood pressure of ⬎140 mm Hg and/or a diastolic blood pressure of ⬎90 mm Hg on 3 occasions. Hyperlipidemia was construed as a note in the medical record identifying elevation of a fasting total serum cholesterol level of more than 200 mg/dL. Coronary heart diseases (angina and myocardial infarction) were characterized in the patient’s medical records with 2 recent ECG reports confirming the diagnosis. A diagnosis of patients with type 2 diabetes was made by having a fasting plasma glucose ⬎125 mg/dL on 2 separate occasions. All radiographic interpretations were performed by one of the authors, who was blinded to which cohort each radiographic image belonged. All radiographic images were examined in subdued light for the presence of presumed calcified carotid artery atheroma (CCAA). Data analysis consisted of using Fisher exact test to compare the prevalence rate for presumed CCAA found on digital dental panoramic images. Forward stepwise logistic regression analysis also was used to determine the risk factors that may lead to development of presumed CCAA. RESULTS Presumed CCAA was identified in 61 out of 157 individuals (38.8%) in the study groups (Fig. 1). They were identified on the panoramic images of 32 men (40.5% of the men in the study groups) and in 29 women (37.2% of the women in the study groups). Bilateral presumed CCAAs were identified in 21 male (26.6%) and 19 female (24.4%), whereas unilateral carotid artery calcification (CAC) was observed in 11 male (13.9%) and 10 female (12.8%) patients (Table I). Table II shows the numbers and the percentages of presumed CCAA for the right and left sides in the study group. A nonsignificant statistical difference (P ⬎ .05) was seen between the 2 sides. Moreover, a nonsignificant statistical difference was also seen between gen-
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Table II. Distribution of presumed calcified carotid artery atheromas (CCAAs) in the right and left sides in the men and women of the study group Right side Men
Left side
Women
Total
Men
Side finding
n
%
n
%
n
%
Positive Negative Single Multiple C3-C4 C4-C5
24 55 17 7 20 4
30.4 69.6 70.8 29.2 83.3 16.7
25 53 22 3 23 2
32.1 67.9 88 12 92 8
49 108 39 10 43 6
31.2 68.8 79.6 20.4 87.8 12.2
ders regarding the side (right and left), number of calcified masses (single or multiple), and vertebral location of these calcifications. Among 43 age-matched healthy individuals, only 5 (11.6%) had a presumed CCAA in their panoramic radiographic image. One had bilateral calcification and the other 4 had unilateral presumed CCAA. Vascular group Among 75 patients with vascular diseases, 31 patients (41.3%) had positive presumed CCAA findings on dental panoramic radiographs. Twenty-two patients (11 from each gender) had bilateral presumed CCAA, constituting 71.0% of the total positive presumed CCAA findings in this group. The remaining 9 patients had unilateral presumed CCAA findings. Single calcified mass findings were more common than multiple calcified masses (21 cases vs. 5 only on the right side and 18 cases vs. 9 on the left side). The C3-C4 location of these masses was the most common location on both sides (Tables III and IV). Metabolic group Forty-two patients suffering from either type 2 diabetes or hyperlipidemia were enrolled in the study. Among them, only 15 patients had positive presumed CCAA in panoramic radiographs. Nine patients (6 men and 3 women) had bilateral presumed CCAA (60% of the total positive presumed CCAA findings in this group), and 6 patients had unilateral presumed CCAA. Single calcification was more common than multiple calcifications on both right and left sides (Tables III and IV). Vascular-metabolic group This group included 40 patients who had either hypertension with diabetes, coronary heart disease with diabetes, or hyperlipidemia with any vascular diseases. Presumed CCAA was seen in 15 patients (37.5% of the total number of this group). Bilateral presumed CCAA
P value P P P P P P
⬎ ⬎ ⬎ ⬎ ⬎ ⬎
.05 .05 .05 .05 .05 .05
Women
Total
n
%
n
%
n
%
29 50 21 8 24 5
36.7 63.3 72.4 27.6 82.8 17.2
23 55 15 8 20 3
29.5 70.5 65.2 34.8 87 13
52 105 36 16 44 8
33.1 66.9 69.2 30.8 84.6 15.4
P value P P P P P P
⬎ ⬎ ⬎ ⬎ ⬎ ⬎
.05 .05 .05 .05 .05 .05
was seen in 9 patients (4 men and 5 women), constituting 60% of the positive presumed CCAA findings in this group. Unilateral CAC was seen in 3 men and 3 women. A single mass was seen in 10 cases, and multiple presumed CCAA masses were seen in 2 cases (Tables III and IV). Forward stepwise logistic regression analysis was applied on each disease independently to determine the strongest risk factor that may lead to the development of presumed CCAA. Table V shows the relationship between presumed CCAA findings on the left and right side and the systemic diseases included in this study. Angina, hyperlipidemia, and myocardial infarction contributed substantially more to the occurrence of presumed left side CCAA than did hypertension. DISCUSSION Incidental finding of calcification lying in the carotid bifurcation region is seen on oral panoramic radiographs in 1%-5% of the adult population when analog film radiography is performed.8 Such carotid-area calcifications are more prevalent in patients with systemic diseases such as type 2 diabetes,10 renal transplantation and dialysis,11 head and neck radiation therapy,12 cardiac myopathy,13 and stroke.14 Calcification is a morphologic complication in the evolution of atheromatous plaque. Generally, CCAAs are found at the branch point of artery vessels where turbulent flow is increased.15 Patients found to have carotid calcification on panoramic radiographs should be referred for cerebrovascular and cardiovascular evaluation and aggressive management of vascular risk factors. Cohen et al.9 suggested 3 potential explanations of why carotid calcification appears to carry an ominous cerebrovascular and cardiovascular prognosis: 1. Carotid calcifications are a sign of underlying significant carotid stenosis. 2. Carotid calcifications are simply another indication of a heavy factor burden.
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Table III. Distribution of presumed calcified carotid artery atheromas (CCAAs) in the study and control groups Vascular group (n ⫽ 75) Finding Total Total Total Total Total Total
CCAA in men CCAA in women unilateral CCAAs in men unilateral CCAAs in women bilateral CCAAs in men bilateral CCAAs in women
Metabolic group (n ⫽ 42)
Vascularmetabolic group (n ⫽ 40)
Control group (n ⫽ 43)
n
%
n
%
n
%
n
%
15 16 4 5 11 11
48.4 51.6 44.4 55.6 50 50
10 5 4 2 6 3
66.7 33.3 66.6 33.3 66.6 33.3
7 8 3 3 4 5
46.6 54.4 50 50 44.4 56.6
4 1 4 0 0 1
80 20 100 0 0 100
Table IV. Comparison of calcified carotid artery atheromas (CCAAs) findings in panoramic radiographs between control and study groups
Right side finding Positive Negative No. of masses (right) Single Multiple Vertebral location C3-C4 C4-C5 Left side finding Positive Negative No. of masses (left) Single Multiple Vertebral location C3-C4 C4-C5
Group 4: vascularmetabolic (n ⫽ 40)
Group 1: control (n ⫽ 43) n %
Group 2: vascular (n ⫽ 75) n %
Group 3: metabolic (n ⫽ 42) n %
n
%
3 40
7.0 93.0
26 49
34.7 65.3
11 31
26.2 73.8
12 28
3 0
100 0.0
21 5
80.77 19.23
8 3
72.73 27.27
3 0
100 0.0
21 5
80.77 19.23
11 0
3 40
7.0 93.0
27 48
36.0 64.0
3 0
100 0.00
18 9
3 0
100 0.0
22 5
P value G1 vs. G2
G1 vs. G3
G1 vs. G4
30.0 70.0
.001
.01
.006
10 2
83.33 16.67
.55
.45
.63
100.0 0.0
11 1
91.67 8.33
.55
.82
.8
13 29
31.0 69.0
12 28
30.0 70.0
.001
.003
.006
66.67 33.33
8 5
61.54 38.46
10 2
83.33 16.67
.33
.3
.63
81.48 18.52
12 1
92.31 7.69
10 2
83.33 16.67
.57
.81
.63
3. Carotid calcifications are an independent risk factor of cerebrovascular and cardiovascular diseases. Radiographs remain the most useful diagnostic aid. The utility of this type of observation obviously will depend on the prevalence and amount of calcium with these lesions, which varies from patient to patient. Because calcium is such a common component of atherosclerotic plaque, the presence of calcium in an unusual location, especially lying over the course of a blood vessel commonly affected by this disease, is presumptive evidence of some degree of atherosclerosis.16 Thousands of dentists have an opportunity each year to identify and refer for treatment patients at risk of experiencing adverse vascular events.17 In the
present study, presumed CCAAs were identified in 52 individuals (33.1% of the total studied sample) on the left side and in 49 individuals (31.2%) on the right side, with nonsignificant statistical differences between the 2 sides (P ⬎ .05). This finding is not in agreement with Ohba et al.,18 who reported CCAA in a selected Japanese sample to be 3 times more prevalent on the right side than on the left side (74% vs. 26%). This difference between 2 studies may be due to different population characteristics. The male-female ratio for presumed CCAA in the present study was 1.1:1 with nonsignificant gender difference. The same finding was reported by Ohba et al.18 and Bayram et al.19 However, Tamura et al.20 identified about 106 carotid calcifica-
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Uthman and Al-Saffar
Table V. Forward stepwise logistic regression for risk factors developing left and right presumed calcified carotid artery atheromas (CCAAs) Parameter Left side presumed CCAAs Angina Hyperlipidemia Myocardial infarction Diabetes mellitus Right side presumed CCAAs Myocardial infarction Angina Hyperlipidemia Hypertension
n
Positive finding
Negative finding

OR
95% CI
P value
33 17 7 75
25 14 5 34
8 3 2 41
3.63 3.53 3.49 1.81
37.63 34.05 32.93 6.09
8.81-160.73 4.75-244.33 2.22-488.3 1.8-20.55
⬍.001 ⬍.001 .01 ⬍.001
7 33 17 94
5 22 10 40
2 11 7 54
2.15 1.89 1.22 0.94
8.58 6.65 3.40 2.56
1.13-65.17 2.59-17.09 1.02-11.32 1.02-6.43
.04 ⬍.001 .05 .05
OR, Odds ratio; CI, confidence interval; , regression coefficient.
tions on panoramic radiographs with a male-female ratio of 1:3. This ratio was about 3 times higher than that of the present study. Tanaka et al.21 found a significant correlation between patients with history of past vascular diseases and CCAA. The incidence of CCAA was reported by Fukuta et al.22 to be 14.7 times as high as that of those who had no cardiovascular or cerebrovascular disease. This is in agreement with the present finding concerning the high prevalence of presumed CCAA in patients with vascular disease (41.3%). Patients with type 2 diabetes, irrespective of treatment modality, have high rates of calcified atheromas on carotid arteries as visualized on panoramic radiography. The resultant hyperglycemia and other risk factors associated with the disease may be the reason for the presence of a high percentage of CCAA. Patients with combined metabolic and vascular disorders had presumed CCAA in 37.5% of the sample in the present study. This finding was higher than that recorded by Friedlander and Maeder10 for patients with type 2 diabetes alone. The findings in the present study lend some support to the view of Crouse23 that aggressive modification of risk factors can retard progression (and may promote regression) of atherosclerotic lesions in both cardiac and cerebrovascular disturbances. CONCLUSIONS Peoples with stroke-related vascular and/or metabolic diseases have greater prevalence of calcified atheromas on their panoramic radiographs than people who are otherwise healthy. This detection could potentially increase the length and quality of life for peoples with CACs through early diagnosis and prevention of fatal consequences of these lesions, along with focusing on more traditional strategies, such as instituting a tobacco cessation program or referring patients for management
of obesity or hypertension, which have a significant impact on reduction the risk of stroke. REFERENCES 1. Fatahzadeh M, Glick M. Stroke: epidemiology, classification, risk factors, complications, diagnosis, prevention and medical and dental management. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006;102:180-91. 2. Friedlander AH. Identification of stroke-prone patients by panoramic and cervical spine radiography. Dentomaxillofac Radiol 1995;24:160-4. 3. Carter LC, Tsimidis K, Fabiano J. Carotid calcifications on panoramic radiography identify an asymptomatic male patient at risk for stroke. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;85:119-22. 4. Friedlander AH, Lande A. Panoramic radiographic identification of carotid arterial plaques. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1981;52:20-4. 5. Friedlander AH, August M. The role of panoramic radiography in determining an increased risk of cervical atheromas in patients treated with therapeutic irradiation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;85:339-44. 6. Carter LC. Discrimination between calcified triticeous cartilage and calcified carotid atheromas on panoramic radiography. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90:108-10. 7. Friedlander AH, Friedlander IK. identification of stroke prone patients by panoramic dental radiography. Aust Dent J 1998;43:51-4. 8. Lewis DA, Brooks SL. Carotid artery calcification in a general dental population: a retrospective study of panoramic radiographs. Gen Dent 1999;47:98-103. 9. Cohen SN, Friedlander AH, Jolly DA, Date L. Carotid calcification on panoramic radiographs: an important marker for vascular risk. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2002;94:510-4. 10. Friedlander AH, Maeder LA. The prevalence of calcified carotid artery atheromas on the panoramic radiographs with type 2 diabetes mellitus. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;89:20-4. 11. Kansu O, Ozbeck M, Avcu N, Genctoy G, Kansu H, Turgan C. The prevalence of carotid artery calcification on the panoramic radiographs of patients with renal disease. Dentomaxillofac Radiol 2005;34:16-9. 12. Freymiller E.G., Sung EC, Friedlander AH. Detection of radia-
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