BACKGROUND

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Traditionally, screening for cervical carotid artery atheromas was solely within the purview of physicians and was based on auscultation of the neck for a bruit. At best, this was a crude screening method because the examination had only a 50 percent specificity and a 50 percent sensitivity. Collateral confirmation was difficult, but occasionally the lesion could be visualized on a plain radiograph of the cervical spine or on the superior aspect of a standard chest radiograph.

Approximately 25 years ago, dental researchers observed that calcified carotid artery atheromas were detectable on the panoramic radiographs of neurologically asymptomatic patients, and they urged a screening role for dentists.³ However, the dental community resisted this recommendation because many believed that these lesions were merely calcified lymph nodes. Validation was difficult because cerebral angiograms (that is, radiographic images obtained after injecting contrast material into the common carotid artery [CCA] via a catheter passed up from the femoral artery) used to demonstrate the intravascular location of an atheroma were discouraged owing to the associated morbidity/mortality rate, which exceeds 1 percent.⁴

Ultrasonography. About 10 years ago, Friedlander and Baker⁵ used noninvasive duplex ultrasonography (US) to conduct a small pilot study among a group of 10 patients with a calcified atheromatouslike lesion on their panoramic radiographs. These US images confirmed that the atheromas were in the ICA and that they corresponded to the radiographic opacity. These findings were substantiated further using Doppler US (DUS) spectral analysis (that is, velocity and wave-form studies), which demonstrated the excessive speed (jetlike flow) of the red blood cells coursing past the narrowed stenotic sites. These findings are consistent with the physical principle that the velocity of blood flow increases with increasing degrees of vessel luminal narrowing and, in essence, that a given range of velocities corresponds to a certain degree of stenosis.⁶ Using this relatively new modality, the researchers estimated that the degree of ICA stenosis exhibited by these patients ranged from 25 to 70 percent.⁵

The medical histories of subjects with an atheroma on their radiographs revealed that 77 percent were hypertensive.

DUS criteria. In 2003, the consensus panel of the Society of Radiologists in Ultrasound adopted a set of DUS criteria for diagnosing and grading ICA stenosis.⁷ The panel recommended that the severity of stenosis be reported as falling within a range of percentage reduction in lumen diameter. These ranges, or categories of stenosis, were based on previous studies that correlated US data with measurements obtained from cerebral angiograms. Furthermore, these ranges have been incorporated into contemporary clinical practice guidelines that define the appropriate medical or surgical intervention.

The purpose of our study was to conduct DUS studies of neurologically asymptomatic dental patients with radiographically identified atheromas and to use the new US criteria to determine the prevalence of hemodynamically significant (that is, causing 50 percent vessel lumen occlusion) lesions.

	SUBJECTS, MATERIALS AND METHODS

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Subjects. The survey population consisted of 1,614 consecutively treated (between Nov. 1, 2002, and March 31, 2004) outpatients attending the oral surgery section of the dental service at the Veterans Affairs Outpatient Clinic, Sepulveda, Calif. Inclusion criteria for patients were as follows:

– age 50 years or older;

– the ability to undergo panoramic radiography, and if it showed a possible atheroma, the ability to undergo a DUS study.

Exclusion criteria included poor-quality radiographs (that is, overexposed or underexposed, incorrect patient positioning or processing errors) and the presence of neurologic symptoms, or a history of these symptoms, consistent with ICA stenosis (such as transient ischemic attack or CVA).

Equipment. All patients underwent radiography. Dental assistants operated the panoramic X-ray unit at 15 to 16 milliamperes and at a peak kilovoltage between 64 and 73 kV depending on the subject’s jaw size. They processed the exposed radiographs (Kodak Dental Film/T-Mat: G panoramic, PAN/TMG/RA-15, 14.8 x 29.8 centimeters with Intensifying Screen Kodak Lanex Medium, Eastman Kodak, Rochester, N.Y.) according to the manufacturer’s directions and used an automatic film developer.

We performed all DUS studies with scanners that incorporated the latest technology. We used 5- or 7.5-megahertz linear array transducers as dictated by the patient’s body habitus.

Methods. One of us (A.H.F.) examined all of the radiographs in subdued ambient light using transmitted light from a standard viewing box and a rheostat-controlled 75-watt bulb (hot light) for the presence of a calcified carotid artery atheroma. He conducted all of the panoramic radiographic interpretations, and he was blinded to each subject’s medical history and characteristics, including atherogenic risk factors.

An experienced technologist performed all of the DUS studies according to a set protocol.⁸ Angle adjustment for calculation of blood-flow velocity was based on flow direction as depicted by color Doppler. The technologist recorded the highest angle-adjusted peak systolic velocity (PSV) of red blood cell flow from within each ICA. She recorded two additional variables: the PSV in the ICA divided by the PSV in the CCA (that is, ICA PSV-CCA PSV ratio) and the ICA end diastolic velocity (ICA EDV).

We considered the ICA to be normal when the ICA PSV was less than 125 cm/second and no plaque or intimal thickening was visible sonographically. Additional criteria used as an internal check of validity (for example, a discrepancy between the visual assessment of the plaque and the ICA PSV) included an ICA PSV-CCA PSV ratio of less than 2.0 and an ICA EDV of less than 40 cm/second (Table 1). Table 1 also shows the primary and additional criteria for diagnosing and grading ICA stenosis of less than 50 percent, 50 to 69 percent and 70 percent or greater.

View this table: [in this window] [in a new window]   TABLE 1 GRAY-SCALE AND DOPPLER ULTRASONOGRAPHIC (US) CRITERIA FOR DIAGNOSIS AND GRADING OF ICA* STENOSIS.

One of us (A.H.F.) reviewed the patients’ medical records for factors related to the development of atherosclerosis. He specifically noted hypertension, diabetes and hyperlipidemia, as determined by a prescription to treat the entity; the body mass index (BMI) (calculated as weight in kilograms divided by the square of the height in meters, with patients categorized as normal [BMI, 18.5 to 24.9], overweight [BMI, 25 to 29.9] or obese [BMI 30]); and the number of pack-years of smoking history.⁹

	RESULTS

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Sample characteristics and radiographic findings. Of the 1,614 subjects initially evaluated, 66 had radiographs of poor image quality and were excluded. The final sample population of 1,548 consisted of 1,487 men ranging in age from 50 to 83 years (mean age, 61.2 years) and 61 women ranging in age from 50 to 79 years (mean age, 64.3 years).

Of the final sample population of 1,548 patients, 65 (61 men and four women) (4.2 percent) had observable opacities consistent with carotid artery calcification on their panoramic radiographs (Figures 1 and 2). The mean age of these subjects was 6.2 years higher than that of the overall sample population. Thirty-eight patients had bilateral opacities and 27 had unilateral opacities.

View larger version (89K): [in this window] [in a new window]   Figure 1. A standard panoramic radiograph that was scanned and digitized to enhance visualization of the atherosclerotic process. The patient was a 69-year-old man with calcified carotid plaques (arrows) visible in the right and left sides of the neck at the junction of the hyoid bone and epiglottis. Ultrasonographic studies confirmed the intravascular nature of the calcifications and revealed that they were associated with less than 50 percent vessel luminal narrowing.

View larger version (86K): [in this window] [in a new window]   Figure 2. A standard panoramic radiograph that was scanned and digitized to enhance visualization of the atherosclerotic process. The patient was a 65-year-old man with calcified carotid artery plaque (arrows) in the right side of the neck, inferior and posterior to the angle of the mandible. Ultrasonographic studies confirmed the intravascular nature of the calcification and revealed that it was associated with more than 50 percent vessel luminal narrowing.

DUS findings. DUS scans confirmed that all of these 65 patients had atherosclerotic lesions within the lumen of their carotid vessels in locations that coincided with the anatomical region on the radiograph harboring the opacity. Table 2 shows the results of these DUS evaluations of 103 ICAs with a radiographically identified atheroma and 27 ICAs with no radiographic evidence of an atheroma. Of the 103 ICAs with an atheroma, 22 (21 percent) had stenosis of 50 percent or greater.

	DISCUSSION

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The results of this study demonstrated that 4.2 percent of neurologically asymptomatic patients 50 years or older had calcified atheromas in one or both ICAs, as shown on panoramic radiographs. Furthermore, DUS studies demonstrated that 15 patients (23 percent) with radiographically identified atheromas had hemodynamically significant stenotic disease ( 50 percent) that placed them at a heightened risk of developing stroke.

Prevalence of carotid artery disease. In an earlier study than ours, Almog and colleagues¹⁰ reported an even greater prevalence of significant carotid artery disease associated with atheromas detected on panoramic radiographs of neurologically asymptomatic patients receiving dental care. They reported the presence of more than 50 percent luminal narrowing in 50 percent of the carotid vessels with radiographic evidence of calcification. Furthermore, they reported that in the carotid vessels in necks without radiographic calcifications, 21 percent had greater than 50 percent luminal narrowing. We believe that the discrepancies between the results of Almog and colleagues¹⁰ and our results may have arisen from their use of different US criteria and possible selection bias in a small sample size.^11–13

The clinical significance of identifying neurologically asymptomatic patients with carotid artery atherosclerotic lesions of any extent should not be underestimated. In fact, numerous studies have shown that even very early carotid artery lesions often are associated with significant coronary artery disease.^14–16 Dental researchers have expanded on these findings by showing that the presence of calcified carotid artery atheromas on panoramic radiographs often heralds a myocardial infarct.^17–20 These associations are not unexpected, given the fact that extracranial carotid artery and coronary artery atherosclerosis are major manifestations of generalized atherosclerosis and have shared risk factors (that is, age, high levels of low-density lipoprotein cholesterol, elevated triglyceride levels, diabetes, hypertension, low levels of high-density lipoprotein cholesterol, cigarette smoking and increased BMI).

The public health importance of our study findings is significant: 750,000 people experience a stroke each year in the United States and 1.5 million people experience a myocardial infarct.¹ Panoramic radiography is ubiquitous. This means that thousands of dentists have an opportunity each year to identify and refer for treatment patients at risk of experiencing an adverse vascular event. Specifically, 61 percent of general dentists and 73 percent of dental specialists in private practice now have panoramic units; in 1999, these clinicians performed more than 17 million panoramic imaging studies.²¹ With many dental practices having more than 1,000 patients older than 50 years, it is possible that slightly less than 1 percent of patients (or nine to 10 people) may have an undiagnosed hemodynamically significant lesion (> 50 percent stenosis) requiring medical evaluation and possible treatment.

Counseling and referring patients. A dentist caring for a patient with a suspected atheroma on his or her radiograph should show the patient the lesion on the image and explain the lesion’s relationship to the course of the ICA and angle of the mandible. The dentist also should inform the patient that these lesions often are markers of generalized atherosclerosis and that they may be associated with a future CVA, a myocardial infarct or both.

Furthermore, the dentist should give the patient a copy of a written consultation directed toward his or her primary care physician that describes the radiographic findings and suggests that a US study be conducted to confirm the presence and extent of disease. This protocol is consistent with a dentist’s professional responsibilities to diagnose oral manifestations of systemic disease and to counsel patients properly about the importance of arranging for, and following through with, the consultation.²²

The physician likely will attempt to control the patient’s hypertension, hyperlipidemia and hyperglycemia, if present, because aggressive control of risk factors has been shown to retard and possibly reverse the atherogenic process and prevent some strokes and myocardial infarcts. The physician also may suggest a carotid artery endarterectomy, because for certain patients, surgical removal of the atheroma has proven to be a safe and reliable method of reducing the likelihood of an ischemic stroke.²³

	CONCLUSION

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The results of this study demonstrate that when dentists evaluate carefully the panoramic radiographs of neurologically asymptomatic patients for the presence of calcified carotid artery atheromas, they can, on occasion, identify patients with advanced disease. Clinicians should refer all patients with atheromalike lesions on their radiographs to a physician, because aggressive medical treatment of early and advanced atherosclerotic disease has been shown to decrease the likelihood of fatal and nonfatal strokes.