Association of calcified carotid atheromas visualized on panoramic images and aortic arch calcifications seen on chest radiographs of postmenopausal women

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Association of calcified carotid atheromas visualized on panoramic images and aortic arch calcifications seen on chest radiographs of postmenopausal women Arthur H. Friedlander, Suzie M. El-Saden, Nona Aghazadehsanai, Tina I. Chang, Nancy D. Harada and Neal R. Garrett JADA 2014;145(4):345-351 10.14219/jada.2013.46 The following resources related to this article are available online at jada.ada.org (this information is current as of June 29, 2014): Updated information and services including high-resolution figures, can be found in the online version of this article at: http://jada.ada.org/content/145/4/345

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ARTICLE 2

Association of calcified carotid atheromas visualized on panoramic images and aortic arch calcifications seen on chest radiographs of postmenopausal women Arthur H. Friedlander, DMD; Suzie M. El-Saden, MD; Nona Aghazadehsanai, DDS; Tina I. Chang, DMD, MD; Nancy D. Harada, PhD; Neal R. Garrett, PhD

A

therosclerosis of the coronary and carotid arteries resulting in myocardial infarction and stroke is the leading cause of death among  postmenopausal women in western Europe, North America and parts of Asia.1 The illness, which differs from that in men, usually begins 10 years later than in men (≥ 55 years versus ≥ 45 years) when menopauserelated alterations in circulating levels of endogenous sex hormones accelerate the process.2 Menopause-related mobilization of calcium from bone, as seen in osteopenia and osteoporosis, is associated with reciprocal calcification of previously noncalcified atherosclerotic lesions.3,4 The disorder often does not have recognized symptoms and traditional risk factors. Of greatest concern is that the initial indication of disease in 60 percent of instances is a fatal cardiovascular event.5,6 The construct that women often have occult atherosclerosis after menopause has prompted researchers to evaluate a multiplicity of imaging studies used for other purposes to determine which of them also might be used to identify patients with occult calcific vascular disease.7 Specifically, the results of studies conducted in Japan,8,9 China,10 Greece,11,12 Korea,13 Germany14 and the United States15,16 have demonstrated that medically indicated, as well as routine or screening, posterior-anterior (PA) chest radiographs (CRs) of women showing calcified plaques in the aortic arch often are indicative of concurrent cardiovascular disease confirmed by means of both angiography and coronary artery calcium scores on noncontrast enhanced computed tomography (CT). These findings frequently herald an increased risk of experiencing death from myocardial infarction and stroke. The arch, lying within the mediastinum, is formed by the confluence of the ascending and descending aorta and is visible on a PA CR as an opaque bump (the aortic knob) on the left side of the mediastinal shadow, lateral to the air in the trachea at the level of the second and third ribs (Figure 1). In 2009, a method of grading the severity of

abstract Background. Occult atherosclerotic disease is the leading cause of death among older women. The authors hypothesized that women with calcified carotid artery plaque (CCAP) visualized on panoramic images were more likely to have aortic arch calcifications (AAC) that were visible on chest radiographs (CRs), a risk indicator of experiencing cardiovascular events, than would matched cohorts who did not have atheromas. Methods. The authors obtained the CRs of 36 female veterans (≥ 50 years) who had CCAP and atherogenically risk-matched them to those of 36 women without CCAP. A radiologist evaluated the CRs for AAC. Other study variables included age, ethnicity, body mass index and presence or absence of hypertension, diabetes and dyslipidemia. The authors computed descriptive and bivariate statistics. Results. Women 60 years or older who had evidence of CCAP on their panoramic radiographs were significantly (P =. 022; 95 percent confidence interval, 1.29826.223) more likely to have evidence of AAC on their CRs than were similarly aged women who did not have evidence of CCAP. This association was not evident in women younger than 60 years. Among women who were both younger and older than 60 years, there was no evident association between the presence of CCAP and the severity (on a four point scale [0-3]) of AAC calcification. Conclusion. Prevalence of carotid plaque on panoramic images of women 60 years or older is significantly associated with presence of aortic arch calcifications on CRs. Practical Implications. Panoramic images of women 60 years or older must be evaluated for CCAP, given their association with AAC. Patients with atheromas should be referred to their physicians for further evaluation given the systemic implications. Key Words. Atherosclerosis; panoramic radiography. JADA 2014;145(4):345-351. doi:10.14219/jada.2013.46   JADA 145(4)  http://jada.ada.org  April 2014  345

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Figure 1. A posterior-anterior chest radiograph showing the aortic knob (arrow) on the left side of the mediastinal shadow. Grade 0, no visible calcification.

aortic arch calcifications (AAC) on PA CRs was developed,8 and in 2010 it was shown to be a strong independent predictor of adverse cardiovascular events beyond traditional risk factor indicators.9 Each year in the United States, approximately 15 million women undergo panoramic radiographic studies.17 Images obtained from large populations of women attending dental school clinics revealed that approximately 5 percent of those in their mid-50s (ethnic distribution was not defined) had evidence of calcified carotid artery plaque (CCAP).18,19 Figure 2 shows CCAP on a panoramic radiograph. Confirmation of the presence of CCAP lesions by means of ultrasonography demonstrated that panoramic imaging was highly accurate20 and had 80 percent sensitivity, 81 percent specificity and 81 percent accuracy.21 Although the results of longitudinal studies conducted in men have demonstrated that CCAP lesions detected by means of panoramic radiography are associated with near-term myocardial infarction and stroke, no such prognostic information has yet been garnered for women.22 We conducted a study to determine the prevalence and severity of AAC on incidentally obtained PA CRs of women who also had CCAPs that were visible on their panoramic images. We hypothesized that a group of women with CCAP would have a significantly greater prevalence and severity of AAC than would an atherogenically matched group of women who did not have CCAP. We also wanted to determine which, if any, of the traditional atherogenic risk factors distinguished women having both CCAP and AAC on their imaging studies from those who had only CCAP on their panoramic images. Methods

Study design and patient sample. We designed and implemented a retrospective study. The Institutional Re-

Figure 2. A panoramic image of the maxillofacial complex that has been cropped and digitally enhanced with the manufacturer’s provided software shows calcified carotid artery plaque (arrow). The globular opacity lies inferior to the horns of the hyoid bone and anterior to the cervical spine.

view Board (project coordinating center 2013-030328) of the Veterans Affairs Greater Los Angeles Healthcare System approved the study protocol. With the assistance of a medical librarian, we accessed the Veterans Affairs (VA) medical center’s dental and radiology services digital libraries and electronic medical records and reviewed the imaging studies of all female patients 50 years or older obtained by members of the VA’s medical and dental staff between March 1, 2006, and June 30, 2012. Chest radiographic examinations were performed by VA staff radiology technicians at a distance of 180 centimeters with the patient standing upright in a PA position during full inspiration. To be included in the study, patients had to have a panoramic image that showed evidence of CCAP as jointly determined by two dentists (A.H.F., T.I.C.) who were certified by the American Board of Oral and Maxillofacial Surgery and who used the American Academy of Oral and Maxillofacial Radiology–sponsored training packet for identification of carotid artery calcifications on panoramic radiographs.23 Consistent with these guidelines, these two dentists diagnosed heterogeneous radiopacities in a verticolinear orientation 1.5 to 2.5 cm inferioposterior to the angle of the mandible, adjacent or inferior to the hyoid bone, epiglottis and cervical vertebrae at, above or below the intervertebral space from C3 through C4 as CCAP after ruling out confounding radiopacities that lay in close proximity to the vessel such as salivary calculi, calcified lymph nodes, tonsilABBREVIATION KEY. AAC: Aortic arch calcifications. BMI: Body mass index. CCAP: Calcified carotid artery plaque. CR: Chest radiograph. CT: Computed tomography. PA: Posterior-anterior. VA: Veterans Affairs.

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loliths, styloid complex, calcified triticeous cartilage and superior cornu of calcified thyroid cartilage.24 Patients also had to have a PA CR obtained within 36 months of the panoramic image. We excluded from the study patients whose medical records showed they had a history of therapeutic irradiation or surgery of the chest. We invoked this criterion to obviate the confounding issue of therapeutic irradiation–induced atherosclerosis. Given ethnic variation in the loci of atherosclerotic lesions,25 we divided the participants into two groups: white participants (group 1) and African American participants (group 2). Given the paucity of Hispanic and Asian patients in the potential study population, we excluded them from the study. We selected members of the control group from the image pool of patients with a properly executed panoramic image that showed the area of interest (2.5 cm inferior and 2.5 cm posterior to the cortical rim of the midpoint of the mandibular angle but devoid of CCAP) and matched the control member to a member of the ethnically appropriate study group if they were of similar age (± 7 years), had approximate (± 3 units) body mass index (BMI) and had a contemporaneously obtained CR. The exclusion criteria were identical to those for participants in the study group. Study variables and data source retrieval. The primary measure was the presence and severity of AAC on the CR. A physician (S.M.E.) certified by the American Board of Radiology who had not seen the images before performed the assessments for our study. This physician and all other members of our research group were masked to the patients’ existing CR reports. In addition, the physician radiologist had no previous knowledge regarding the patients’ panoramic images or their medical histories. She scored the area of calcification as one of four grades: grade 0, no visible calcification (Figure 1); grade 1, small spots of calcification or a single thin area of calcification of the aortic knob (Figure 3); grade 2, one or more areas of thick calcification (Figure 4); and grade 3, circular calcification of the aortic knob (Figure 5).8,9 In terms of detection of AAC, a score of 0 was considered negative for AAC and scores of 1, 2 or 3 were considered positive for AAC. Additional demographic and proatherogenic conditions based on the patient’s medication regimen were recorded. The demographic variables were age and ethnicity, and the proatherogenic variables were BMI and the presence or absence of hypertension, dyslipidemia and diabetes mellitus. The demographic data and determination of the presence of comorbid illnesses (determined by the list of physician-prescribed medications) were derived from the participants’ medical records. Furthermore, the senior author (A.H.F.) reviewed the medical records of each of the study’s 72 patients and found convincing historical information and medical diagnostic testing data to substantiate the comorbid diagnoses and medication regimens.

Figure 3. Grade 1, small spot of calcification (arrow).

Figure 4. Grade 2, area of thick calcification (arrows). This is the posterior-anterior chest radiograph of the same patient whose panoramic image is shown in Figure 2.

Figure 5. Grade 3, circular calcification of the aortic knob (arrows).

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44.4 percent) and had a mean (standard deviation Study and control group patient characteristics. [SD]) age of 62 (9.4) years. CHARACTERISTIC STUDY GROUP CCAP* CONTROL GROUP CCAP SIGNIFICANCE, The average patient was PRESENT (n = 36) ABSENT (n = 36) P VALUE classified by the World Age, Mean, in Years 62 62 Health Organization as 9.4 9.6 SD† .922 obese class I (BMI, 30.2).26 51-80 53-90 Range A review of the patients’ Race, No. (%) medical histories revealed 20 (55.6) 23 (63.9) White .632 that a large percentage 16 (44.4) 13 (36.1) African American was taking medication to Body Mass Index 30.2 30.0 control hypertension (88.9 5.5 5.3 SD .871 percent), diabetes (44.4 21-45 21-43 Range percent) and dyslipidemia Hypertension, No. (%) 32 (88.9) 32 (88.9) ≈ 1.000 (75.0 percent). The deDiabetes Mellitus, No. (%) 16 (44.4) 9 (25.0) .137 mographic data, medical histories and extent of AAC Dyslipidemia, No. (%) 27 (75.0) 26 (72.0) ≈ 1.000 did not differ significantly Aortic Arch Calcification, 19 (52.8) 13 (36.1) .236 No. (%) between participants with * CCAP: Calcified carotid artery plaque. CCAP and those without † SD: Standard deviation. CCAP. We found no significant Data analysis. We recorded and de-identified the association between CCAP and AAC, using either the data, entered them into a standardized electronic datafull four-point scale (0-3) of AAC scores (Table 2) (maxibase and imported them into statistical software (PASW mum likelihood ratio c2 P = .490) or having or not havStatistics 18, IBM, Somers, N.Y., and SAS, Version 9.2, ing AACs (binary variable) (maximum likelihood ratio SAS Institute, Cary, N.C.). The descriptive statistics we c2 P = .205). As expected, we found that AAC is related used included measures of central tendency and disperstrongly to age. We found no evidence of a relationship sion for age and BMI, as well as frequency distributions between race and BMI, hypertension, diabetes mellitus for the categorical atherosclerotic risk factor variables. or dyslipidemia. We compared the relationships between CCAP and AAC The results of the logistic regression analysis for AAC and the atherogenic risk factors (hypertension, diabetes, (absence/presence) showed a significant interaction dyslipidemia) by means of logistic regression analyses. (P = .044) between older age (< 60 years and ≥ 60 years) We compared age and BMI between CCAP groups by as defined by the World Health Organization27 and means of t tests. The α value for each statistical compari- CCAP although not for AAC scores 0-3 (P = .161). Table son was 0.05. 3 shows that AAC is present less often in women younger For the logistic regression, we evaluated AAC as a than 60 years (12 of 38 [32 percent]) than in those 60 binary variable (absence/presence; 0/1-3) and as a ranked years or older (20 of 34 [59 percent]). Although having variable using the full four-point (0-3) scale. A score of AACs was not different in the younger-than-60-years 0 indicated that participants had a complete absence of group with (28 percent) or without (35 percent) CCAP, AAC. in those 60 years or older, AAC was significantly more likely (P = .022) in the group of participants who had Results CCAP (78 percent) than in the group of participants who The medical records librarian identified 647 women who did not have CCAP (38 percent). had a complete set of imaging studies performed during Discussion the prescribed period. We deemed that the panoramic images of 76 women were unacceptable because they The results of our study indicate that older women were overexposed or underexposed or because patient (those 60 years or older) who have CCAP on their panpositioning errors precluded us from viewing the area oramic images are more likely to have evidence of AAC of interest. Forty (approximately 7 percent) of the 571 on a CR than would a matched cohort devoid of carotid satisfactory imaging studies showed CCAP. disease. This is not surprising, given that atherosclerosis The physician radiologist evaluated the CRs of these often is present in multiple arterial territories. This is a 40 women and determined that 36 of these images finding of great import given that the presence of AAC were technically acceptable for evaluation of AAC. The on a CR is a validated risk indicator of adverse vascular women (Table 1) with satisfactory sets of images were of events in older women.8-15 In fact, investigators in studies diverse ethnic background (white, 55.6 percent; black, conducted in Japan8,9 and Greece11,12 who used the same TABLE 1

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TABLE 2

Descriptive characteristics of female participants with and without CCAP* and their concomitant AAC† scores. CHARACTERISTIC

CCAP PRESENT (n = 36)

CCAP ABSENT (n = 36)

AAC ABSENCE/ PRESENCE MAXIMUM LIKELIHOOD, c2 (P VALUE)

AAC 0-3 MAXIMUM LIKELIHOOD, c2 (P VALUE)

AAC Score

0

1

2

3

0

1

2

3

NA ‡

NA

CCAP (No.)

17

6

9

4

23

3

6

4

1.608 (.205)

0.477 (.490)

58 (7.7)

62 (9.5)

66 (9.1)

70 (10.3)

60 (6.7)

55 (2.9)

65 (12.9)

75 (13.1)

5.727 (.017)

9.590 (.002)

Age, Mean, in Years (SD § ) African American/White, No.

8/9

3/3

4/5

1/3

9/14

2/1

2/4

1/3

0.004 (.949)

0.024 (.877)

Body Mass Index (SD)

31.0 (4.4)

30.5 (6.0)

30.2 (7.6)

26.4 (2.9)

29.8 (5.0)

34.6 (4.7)

30.3 (6.5)

27.6 (5.1)

0.002 (.969)

0.021 (.886)

Hypertension, No. (%)

14 (39)

6 (17)

8 (22)

4 (11)

19 (53)

3 (8)

2 (6)

4 (11)

1.736 (.188)

1.670 (.196)

Diabetes Mellitus, No. (%)

5 (14)

3 (8)

5 (14)

3 (8)

6 (17)

1 (3)

0 (0)

2 (6)

0.686 (.408)

1.732 (.188)

Dyslipidemia, No. (%)

12 (33)

5 (14)

7 (19)

3 (8)

16 (44)

3 (8)

4 (11)

3 (8)

0.042 (.838)

0.000 (.999)

* † ‡ §

CCAP: Calcified carotid artery plaque. AAC: Aortic arch calcification. NA: Not applicable. SD: Standard deviation.

TABLE 3

Relationship between presence and absence of CCAP* and AAC† in two age groups. AGE, YEARS

Younger Than 60 (n = 38) 60 or Older (n = 34)

CCAP

AAC ABSENT, NO.

AAC PRESENT, NO.

PROPORTION

ODDS

Absent

13

7

0.350

0.538

Present

13

5

0.278

0.385

Absent

10

6

0.375

0.600

Present

4

14

0.778

3.500

ODDS RATIO

95 PERCENT CONFIDENCE INTERVAL

P VALUE

0.714

0.179-2.843

.633

5.833

1.298-26.223

.022

* CCAP: Calcified carotid artery plaque. † AAC: Aortic arch calcification.

protocol as we did noted that the specificity and sensitivity of using arch calcifications on CRs to identify severe coronary artery atherosclerosis documented by means of arteriography was 66 percent and 87 percent and 48 percent and 97 percent, respectively. The results of our study showed that the prevalence of AAC among women with CCAP increased the longer a woman was postmenopausal (that is, the older she was). Our finding was consistent with that of Japanese geriatricians who evaluated 123 women (mean [SD] age 63.2 [10.0] years) for a variety of medical problems and obtained CRs. In their study, the older a woman was, the more likely she was to demonstrate AAC.8,9 This is not a surprising finding, because the calcification process of atherosclerotic lesions in most women accelerates in the years after the onset of menopause.7 Investigators have postulated that this process occurs because estrogen deficiency is related to changes in calcium hemostasis, which manifests as a rapid loss of bone mass accompanied by

a reciprocal increase in the prevalence and severity of calcified atherosclerotic lesions.14,28 Although a conventional PA CR is not as precise as a chest CT in defining AAC, it has been established as the standard imaging modality used to assess AAC in large epidemiologic studies owing to both lower cost and less radiation dosage required.12,29 Furthermore, physicians in general practices with ambulatory patients and those in emergency departments admitting patients to hospitals frequently obtain conventional CRs to assist in initially defining a patient’s complaints or diagnosing abnormal findings from physical examinations. The imaging study allows for evaluation of airways, pulmonary parenchyma and vessels, mediastinum, heart, pleura and chest wall. In an era of CT, the standard CR obtained in the appropriate clinical context remains an important diagnostic tool.30 Recognition by physicians regarding the association between calcified atheromas on panoramic images and   JADA 145(4)  http://jada.ada.org  April 2014  349

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CRs may help improve cardiovascular risk projection beyond that provided by traditional risk factor analysis.31,32 For example, in the Framingham Heart Study, more than 75 percent of all hard cardiovascular events (for example, fatal and nonfatal myocardial infarction) occurred in patients classified as being at low or intermediate risk and, consequently, they were not offered optimal preventive therapy.5,33 Thus, when dentists refer patients to their physicians owing to the presence of an atheroma on a panoramic image, it also is appropriate for them to suggest that physicians review any available CRs for the concomitant presence of AAC. There were a few limitations in our study. Our analysis was limited by the study population. It included only patients who were preselected according to risk factors that required them to have a panoramic image and a CR. The study’s most significant weakness was that, owing to its retrospective nature, we did not use ultrasonographic studies to confirm the presence of CCAP on the panoramic images. Thus, some calcifications other than those caused by carotid atheroma may have been included. In addition, because we adhered to the original protocols as developed by Hashimoto and colleagues8 and Iijima and colleagues,9 we did not include lateral CRs34 in our image analyses, which may have resulted in our underestimating AAC. Furthermore, although we have found an association between CCAP on panoramic images and AAC on the CRs of women 60 years or older and have suggested that this indicates enhanced risk of experiencing future adverse cardiovascular outcomes, a direct link with incident cardiovascular disease remains to be established. Lastly, we recognize that the significant relationship between CCAP and AAC was found only in those 60 years or older. The result seems plausible given the need for cumulative damage to occur and be detectable by the imaging systems we used in our study, which remain relatively crude compared with carotid artery ultrasonography and chest CT.14,35-37 conclusions

Our research findings show that in a limited population of female veterans with CCAP visible on their panoramic images, a small subset had AAC on their CRs. Although the identification of AAC on CR appears crude in today’s world of computerized images, it is an important finding owing to the confirmation in the medical literature that blood vessel calcification (irrespective of specific vascular distribution) heralds future adverse cardiovascular events (myocardial infarction and stroke) in older women. To substantiate the results, we are planning to engage our university affiliates in a multicenter study evaluating a larger number of patients. Dentists must be vigilant for the presence of CCAP when evaluating the panoramic images of older women. If a lesion is identified, the clinician should consider referring the patient to her primary care physician and

including a detailed note describing the panoramic image findings and a suggestion for obtaining a Duplex Doppler ultrasonographic study. This is an opportune moment for primary prevention before a clinical event takes place. n Dr. Friedlander is the associate chief of staff and the director of graduate medical education, Veterans Affairs Greater Los Angeles Healthcare System; the director of quality assurance, Hospital Dental Service, Ronald Reagan University of California Los Angeles Medical Center; and professor-in-residence of oral and maxillofacial surgery, School of Dentistry, University of California, Los Angeles. Address correspondence to Dr. Friedlander at Veterans Affairs Greater Los Angeles Healthcare System, 11301 Wilshire Blvd., Los Angeles, Calif. 90073, e-mail arthur. [email protected]. Dr. El-Saden is the chief of imaging service, Veterans Affairs Greater Los Angeles Healthcare System, and an associate clinical professor of radiology, David Geffen School of Medicine, University of California Los Angeles. Dr. Aghazadehsanai is a research oral and maxillofacial surgery fellow, Veterans Affairs Greater Los Angeles Healthcare System. Dr. Chang is the director of research fellowship and inpatient oral and maxillofacial surgery, Veterans Affairs Greater Los Angeles Healthcare System, and an instructor of oral and maxillofacial surgery, School of Dentistry, University of California Los Angeles. Dr. Harada is the associate director of graduate medical education and a member of the Geriatric Research Education and Clinical Center, Veterans Affairs Greater Los Angeles Healthcare System, and a professor of medicine, David Geffen School of Medicine, University of California Los Angeles. Dr. Garrett is an associate dean for education and a professor of advanced prosthodontics, Weintraub Center for Reconstructive Biotechnology, School of Dentistry, University of California Los Angeles. Disclosure. None of the authors reported any disclosures. Elements of the study described in this article were conducted in a facility constructed with support from Research Facilities Improvement Program grant CO6 RR-14529-01 from the National Center for Research Resources, National Institutes of Health. 1. Mathers CD, Boerma T, Ma Fat D. Global and regional causes of death. Br Med Bull 2009;92(1):7-32. 2. Pappa T, Alevizaki M. Endogenous sex steroids and cardio- and cerebro-vascular disease in the postmenopausal period. Eur J Endocrinol 2012;167(2):145-156. 3. Christian RC, Harrington S, Edwards WD, Oberg AL, Fitzpatrick LA. Estrogen status correlates with the calcium content of coronary atherosclerotic plaques in women. J Clin Endocrinol Metab 2002;87(3): 1062-1067. 4. Hak AE, Pols HA, van Hemert AM, Hofman A, Witteman JC. Progression of aortic calcification is associated with metacarpal bone loss during menopause: a population-based longitudinal study. Arterioscler Thromb Vasc Biol 2000;20(8):1926-1931. 5. Ridker PM, Buring JE, Rifai N, Cook NR. Development and validation of improved algorithms for the assessment of global cardiovascular risk in women: the Reynolds Risk Score. JAMA 2007;297(6):611-619. 6. Wenger NK. Coronary heart disease: the female heart is vulnerable. Prog Cardiovasc Dis 2003;46(3):199-229. 7. Allison MA, Criqui MH, Wright CM. Patterns and risk factors for systemic calcified atherosclerosis. Arterioscler Thromb Vasc Biol 2004;24(2):331-336. 8. Hashimoto H, Iijima K, Hashimoto M, et al. Validity and usefulness of aortic arch calcification in chest x-ray. J Atheroscler Thromb 2009;16(3):256-264. 9. Iijima K, Hashimoto H, Hashimoto M, et al. Aortic arch calcification detectable on chest X-ray is a strong independent predictor of cardiovascular events beyond traditional risk factors. Atherosclerorsis 2010;210(1):137-144. 10. Xu L, Jiang CQ, Lam TH, Thomas GN, Zang WS, Cheng KK. Aortic arch calcification and vascular disease: the Guangzhou Biobank Cohort

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Downloaded from jada.ada.org on June 29, 2014

ORIGINAL CONTRIBUTIONS

Study. Cardiology 2010;117(4):260-264. 11. Symeonidis G, Papanas N, Giannakis I, et al. Gravity of aortic arch calcification as evaluated in adult Greek patients. Int Angiol 2002;21(3): 233-236. 12. Papanas N, Tziakas D, Mavridis G, et al. Aortic arch calcification predicts the extent of coronary atherosclerosis in patients with or without type 2 diabetes: short communication. Acta Clin Belg 2007:62(1):52-55. 13. Yun KH, Jeong MH, Oh SK, et al. Clinical significance of aortic knob width and calcification in unstable angina. Circ J 2006;70(10):1280-1283. 14. Bannas P, Jung C, Blanke P, et al. Severe aortic arch calcification depicted on chest radiography strongly suggests coronary artery calcification (published online ahead of print May 10, 2013). Eur Radiol 2013;23(10):2652-2657. doi:10.1007/s00330-013-2877-z. 15. Iribarren C, Sidney S, Sternfeld B, Browner WS. Calcification of the aortic arch: risk factors and association with coronary heart disease, stroke, and peripheral vascular disease. JAMA 2000;283(21):2810-2815. 16. Li J, Galvin HK, Johnson SC, Langston CS, Sclamberg J, Preston CA. Aortic calcification on plain chest radiography increases risk for coronary artery disease. Chest 2002;121(5):1468-1471. 17. American Dental Association. 2005-2006 Survey of Dental Services Rendered. Chicago: American Dental Association; 2007. 18. Carter LC, Haller AD, Nadarajah V, Calamel AD, Aguirre A. Use of panoramic radiography among an ambulatory dental population to detect patients at risk of stroke. JADA 1997;128(7):977-984. 19. Lewis DA, Brooks SL. Carotid artery calcification in a general dental population: a retrospective study of panoramic radiographs. Gen Dent 1999;47(1):98-103. 20. Romano-Sousa CM, Krejci L, Medeiros FM, et al. Diagnostic agreement between panoramic radiographs and color Doppler images of carotid atheroma. J Appl Oral Sci 2009;171(1):45-48. 21. Ertas ET, Sisman Y. Detection of incidental carotid artery calcifications during dental examinations: panoramic radiography is an important aid in dentistry. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2011;112(4):e11-e17. doi:10.1016./j.tripleo.2011.02.048. 22. Friedlander AH, Cohen SN. Panoramic radiographic atheromas portend adverse vascular events. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;103(6):830-835. 23. Almog DM, Tsimidis K, Moss, ME, Gottlieb RH, Carter LC. Evaluation of a teaching program for detection of carotid artery calcifications on panoramic radiographs. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90(1):111-117. 24. MacDonald D, Chan A, Harris A, Vertinsky T, Farman AG, Scarfe WC. Diagnosis and management of calcified carotid artery atheroma: dental perspectives. Oral Surg Oral Med Oral Pathol Oral Radiol 2012;114(4):533-547.

25. Woodard GA, Narla VV, Ye R, et al. Racial differences in the association between carotid plaque and aortic and coronary artery calcification among women transitioning through menopause. Menopause 2012;19(2):157-163. 26. World Health Organization. Global database on body mass index: BMI classification. http://apps.who.int/bmi/index.jsp?introPage=intro_3. html. Accessed Jan. 17, 2014. 27. World Health Organization. Health statistics and health information systems: definition of an older or elderly person. www.who.int/ healthinfo/survey/ageingdefnolder/en/. Accessed Jan. 17, 2014. 28. Kiel DP, Kauppila LI, Cupples LA, Hannan MT, O’Donnell CJ, Wilson PW. Bone loss and progression of abdominal aortic calcification over a 25 year period: the Framingham Heart Study. Calcif Tissue Int 2011;68(5):271-276. 29. Mehta AC, Chua AP, Gleeson F, Meziane M. The debate on CXR utilization and interpretation is only just beginning: a pro/con debate. Respirology 2010;15(8):1152-1156. 30. Speets AM, van der Graaf Y, Hoes AW, et al. Chest radiography in general practice: indications, diagnostic yield and consequences for patient management. Br J Gen Pract 2006;56(529):574-578. 31. Muntendam P, McCall C, Sanz J, Falk E, Fuster V; High-Risk Plaque Initiative. The BioImage Study: novel approaches to risk assessment in the primary prevention of atherosclerotic cardiovascular disease—study design and objectives. Am Heart J 2010;160(1):49-57.e1. doi:10.1016/j. ahj.2010.02.021. 32. Nambi V, Chambless L, Folsom AR, et al. Carotid intima-media thickness and presence or absence of plaque improves the prediction of coronary heart disease risk: the ARIC (Atherosclerosis Risk in Communities) study. J Am Coll Carodiol 2010;55(15):1600-1607. 33. Wilson PW, Pencina M, Jacques P, Selhub J, D’Agostino R Sr, O’Donnell CJ. C-reactive protein and reclassification of cardiovascular risk in the Framingham Heart Study. Circ Cardiovasc Qual Outcomes 2008;1(2):92-97. 34. Danielsen R, Sigvaldason H, Thorgeirsson G, Sigfusson N. Predominance of aortic calcification as an atherosclerotic manifestation in women: the Reykjavik study. J Clin Epidemiol 1996;49(3):383-387. 35. Khosropanah SH, Shahidi SH, Bronoosh P, Rasekhi A. Evaluation of carotid calcification detected using panoramic radiography and carotid Doppler sonography in patients with and without coronary artery disease. Br Dent J 2009;207(4):E8. doi:10.1038/sj.bdj.2009.762. 36. Friedlander AH. Odd practice. Br Dent J 2009;207(10):464-465. 37. Kurugol S, San Jose Estepar RS, Ross J, Washko GR. Aorta segmentation with a 3D level set approach and quantification of aortic calcifications in non-contrast chest CT. Conf Proc IEEE Eng Med Biol Soc 2012; 2012:2343-2346.

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