Rachel: Correlation between coronary and valve calcification: Review of current evidence.

Introduction

Coronary artery calcification (CAC) has become known as sub-clinical atherosclerosis and is widely used as a marker for coronary artery disease (CAD) and is an independent predictor of cardiovascular (CV) events and all-cause mortality1. CAC has been much studied as an entity in itself, while calcification of other arteries and cardiac valves has been considered of less direct clinical value, despite potential relationships between them. Aortic valve calcification (AVC) is the most frequent cause of aortic stenosis in the west and is an actively regulated process2, while mitral annular calcification (MAC) is a degenerative process that can occasionally have serious clinical consequences, such as mitral stenosis, cerebral emboli, arrhythmia and bacterial endocarditis3.

This article examines the pattern of relationships between CAC and calcification of other arteries and the aortic and mitral valves. We also looked at the potential relationships between calcification locations and risk factors, although we did not conduct a rigorous analysis of the individual risk factors from these studies.

Multiple arterial beds

In two studies of asymptomatic patients, the presence of calcification in one artery correlated with presence in other arteries, although with respect to the coronary artery the correlation was only modest4,5. Calcification appeared first in the coronary artery but was widespread in the elderly with the highest prevalence in the aorta6. Male gender, hypertension and age were risk factors for systemic calcification7,8, while in postmenopausal women the premenopausal LDL concentration may also be a risk factor.

The aorta

A number of studies comparing calcification of the aorta and other arteries show an association between prevalence, extent or progression of aortic calcification and CAC9,10,11,12,13,14,15,16,17,18,19,20,21,22,23, irrespective of symptoms or the area of the aorta that was scanned. There was also a correlation between the prevalence of aortic and carotid calcification24. The prevalence and extent of aortic calcification generally appears to be higher than the prevalence and extent of CAC25 and a substantial proportion of those with abdominal aortic calcification had zero CAC26,27; nevertheless, one study found that in symptomatic patients CAC was more prevalent than thoracic aorta calcification (TAC)28. In symptomatic Chinese, the abdominal aorta and aortic arch displayed the highest prevalence and extent of calcium deposition, followed by the descending and ascending aortas29, while in asymptomatic subjects calcification progression may be faster in the abdominal than in the thoracic aorta30. Aortic baseline values of zero tended to remain at zero at follow-up31, suggesting that calcium begets calcium in the aorta as well as the coronary artery.

Although age was more strongly associated with aortic calcification than CAC in some studies32,33, Wong et al found that in asymptomatic subjects CAC prevalence was higher than TAC prevalence until age 50, when there was a rapid increase in TAC to coincide with CAC prevalence by the 8th decade (>80%)34. Although some studies show no gender prevalence with respect to calcification of the aorta as a whole, the prevalence of abdominal aortic calcification (AAC) was significantly higher among women, although they had a substantially lower prevalence of CAC at all age groups35,36 and indeed two studies found the severity of TAC was more strongly associated with CAC presence in women than men37,38. Nevertheless, a score of >2000 for calcification of the aortic arch in asymptomatic subjects was seen twice as often in men as in women and the correlation with CAC was stronger in men39. The correspondence of conventional CV risk factors between CAC and aortic calcification was not generally assessed, although there was little consistency in risk factors for aortic calcification between studies, with only systolic hypertension occurring regularly (although curiously diastolic pressure40 and smoking41 showed an inverse association in two studies).

Other arteries

Irrespective of symptoms, good correlation has been found between calcification prevalence in the carotid, subclavian, renal and peripheral arteries and that of the coronary artery42,43,44 and aorta45,46,47, although a large study investigating the subclavian artery in asymptomatic subjects found that correlation with CAC was only borderline48. In asymptomatic subjects, the presence of calcium in the abdominal aorta had the highest sensitivity for any renal artery calcification (94.5%)49. Risk factors were rarely assessed and generally it is only age and male gender, possibly with hypertension, that are consistently associated50,51,52, although, curiously, low body mass index and low diastolic blood pressure were risk factors for presence and extent respectively of subclavian artery calcification53.

Arterial calcification - Discussion

There appears to be a consistent correlation between CAC prevalence, extent and progression and calcification in other vascular beds, although the strength of the association varies. In the few studies investigating calcification in noncoronary beds, there are also correlations between the aorta, carotid and renal arteries. From the undoubted association between calcification prevalence at various sites, it is clear that calcification is a systemic diffuse disease, affecting the arterial tree as a whole. In most studies, calcification seems to appear first in the coronary artery in younger adults but could be more prevalent in the aorta in the elderly, suggesting that age is a stronger risk factor for aortic calcification. Nevertheless, a higher prevalence of early aortic and carotid calcification in asymptomatic women has been reported, suggesting that in younger women the measurement of aortic, particularly abdominal aortic, rather than coronary calcium may provide the earliest and most accurate evaluation of the underlying atherosclerotic burden54,55.

In general, age and male gender were fairly consistent risk factors for calcification, although this was not the case for the aorta, where there was either no gender prevalence or in specific areas of calcification one gender predominated. However, there appears to be little uniformity with respect to other conventional risk factors, although systolic hypertension was among the most common. Furthermore, CAC was such a strong marker of aortic calcification that in multivariate analyses it eliminated all conventional risk factors except age56.

Because the contributors to calcification in each artery may be different57, it has been suggested that an index of measures may provide a more consistent association with risk factors than any individual measure of calcification58. Nevertheless, several authors have pointed out that since CAC is almost always found in the intima, while calcification in other arteries may be found in either the intima or the media, the summation of the calcium scores may not be a fair comparison of extent of calcification between arteries since intimal calcification cannot be differentiated from medial calcification on any scanning modality. Furthermore, while CAC is commonly described as a form of subclinical atherosclerosis, this may not be an appropriate description for medial calcification in the other arteries, since this is more a reflection of the oxidative damage and uraemia of type 2 diabetes and chronic kidney disease. 59,60,61 Moreover, others have speculated that it is the different geometries and various local tensile and shear stresses which might contribute to different susceptibilities between arteries for calcium deposition62.

Combined valve calcification

There is little correlation between calcification presence in the two valves; in symptomatic patients and Japanese women with osteoporosis there was no correlation 63,64 although in asymptomatic subjects there was moderate correlation between calcification of the two annuli65. Nevertheless, studies of asymptomatic subjects show a good correlation between calcification of the combined annuli and most vascular beds66,67, with calcification of the thoracic aorta being the strongest correlation68, while renal artery calcification presence appears to be associated with AVC but not with MAC69. In asymptomatic subjects, aortic valve calcification is more prevalent than MAC, with incidence up to three times higher70,71, while in symptomatic patients there were almost equal numbers with MAC and AVC73. Coronary artery calcified and mixed plaques (but not non-calcified plaques) were found to be more extensive in those with combined valve calcification than those with no valve calcification or isolated AVC . Extensive CAC does not always imply valve calcification, however; in a small study 5% of patients with a CAC score of >400 had no cardiac calcification74. Few of these studies looked at conventional CV risk factors, although there was always a positive correlation between age and cardiac calcium scores75,76,77,78; only hypertension was significantly associated with calcification of both annuli in asymptomatic subjects79, while in symptomatic patients, diabetes and hypertension were associated with combined valve calcification80.

Aortic valve

Most studies of asymptomatic subjects show that AVC prevalence and progression is independently associated with prevalence and increasing severity of CAC, with 38% of those with CAC >/=400 also having AVC81,82,83,84, with higher followup CAC scores also predicting de novo AVC85. With respect to calcification of the aortic root, one study found that CAC was a weak predictor, with TAC presence having the highest odds ratio86. AVC scores increased faster with higher baseline AVC score, showing that calcium begets calcium in the aortic valve as well as arteries87. Similar results were seen in symptomatic patients, with a significant association between prevalence of AVC and prevalence of aortic calcification and CAC and extent of CAC88,89,90,91. A smaller study found no correlation between baseline AVC and CAC although there was a significant correlation between the extent of annual progression of CAC and AVC92. In high risk hypertensives, AVC was an independent predictor of CAC>300 and triple vessel coronary calcification93.

Age is an independent predictor of AVC presence in most studies94,95,96,97,98,99,100,101, but does not appear to be predictive of progression,. Prevalence rates between AVC and CAC grew more similar with age in asymptomatic subjects, with CAC appearing around seven years before AVC . Studies are divided over whether male gender is also a risk factor for AVC105,106,107,108,109. Although there are associations of conventional risk factors with AVC presence in both symptomatic and asymptomatic subjects, there is no consistency among studies.

Mitral valve

Studies of asymptomatic subjects by Allison et al found that calcification of all arterial beds was a significant predictor of MAC with the exception of the coronary, iliac and renal arteries, while the presence of abdominal aorta calcification gave the highest odds for MAC110,111. Nevertheless, other studies have found a strong association between the presence and extent of MAC and presence and progression of CAC112,113, although the prevalence of CAC appears to be much higher than prevalence of MAC (50% vs 9%)114. In symptomatic patients, MAC showed a sensitivity and specificity 71% and 56% respectively for detecting a CAC score >/=400, although advanced MAC (>/=5mm) had markedly reduced sensitivity but improved specificity115. Studies of hypertensives with additional risk factors show mixed results but all agree that advanced MAC was an independent predictor of a CAC score >300116,117,118 and presence of MAC is associated with TAC119.

In the few studies that considered gender, there was no difference between men and women in the association of MAC with CAC in asymptomatic subjects120, or as a risk factor for MAC121,122, although in symptomatic patients MAC, particularly advanced MAC, was more prevalent among postmenopausal women123,124. Age, hypertension and diabetes were fairly consistent risk factors, irrespective of symptoms125,126, although some studies found no associated conventional risk factors127,128.

Valvular Calcification - Discussion

There is a clear association between the prevalence, extent and progression of aortic valve and arterial calcification in multiple arterial beds but the association with CAC, although significant, is only modest, and symptomatic patients with high CAC may not necessarily have valve calcification. Some studies show no relationship between MAC and CAC, while only in symptomatic patients is advanced MAC predictive of higher CAC, although the association between MAC and calcification of other arterial beds, particularly the aorta, appears stronger. There is negligible relationship between calcification of the two valves and in asymptomatic subjects, MAC occurs much less frequently than AVC but this difference may disappear as symptoms develop. AVC scores increased faster with higher baseline AVC, showing that in the aortic valve, calcification also begets calcification. CAC appears before AVC in asymptomatic subjects but the prevalence is similar in the elderly. Studies appear divided on whether there is a gender prevalence for AVC, while MAC tends to be more prevalent among postmenopausal women. In the few studies considering predictors of valve calcification, age and possibly hypertension were risk factors for prevalence but not necessarily for progression; there was no consistency with respect to other conventional risk factors for AVC or MAC.

A number of authors have linked the development of valvular calcification to atherosclerosis, citing the fact that both are actively regulated processes with histological, risk factor and CV outcome similarities129,130,131,132,133,134,135,136,137,138,139. Furthermore, Takasu et al noted that all patients with progression of AVC had progression of CAC, while 80% of those with stabilisation of AVC also had stable CAC, indicating parallel development140. The aortic valve contains cells similar to myofibroblasts that have been shown to differentiate into osteoblast-like cells which form calcific nodules in vitro; these myofibroblasts are phenotypically analogous to vascular smooth muscle cells, which can also undergo differentiation into calcifying cells141. Supporting this, Adler et al noted that foam cells (representing early atherosclerotic lesions) are present on the ventricular surface of the posterior mitral leaflet and on the aortic aspect of each aortic valve cusp, as well as on the endothelium of the epicardial coronary arteries142. Nevertheless, because some patients have AVC without atherosclerosis and statins cannot prevent calcium deposition in advanced AVC, other mechanisms for valvular calcification may also exist independently143,144. Although histology and CV outcome is beyond the scope of this article, our review found no consistent evidence of any conventional CV risk factor for valvular calcification other than age and possibly hypertension, indicating that one of the pillars of the association of valvular calcification with atherosclerosis may not hold.

Conclusions

There appears to be a consistent correlation between the prevalence, extent and progression of arterial and valvular calcification, although the strength of the association varies and may only be modest for associations with CAC. From the unequivocal association between calcification prevalence at various sites, it is clear that calcification is a systemic diffuse disease, affecting the arterial tree as a whole as well as the cardiac valves. Despite this, some patients with severe CAC may have zero calcification elsewhere. MAC is much less prevalent than AVC and there is little correlation of calcification between the two valves. The correlation between MAC and CAC is frequently weak or non-existent, suggesting that MAC may have little to do with atherosclerosis. AVC and aortic calcification scores increase faster with higher baseline values, showing that, as in the coronary artery, calcification also begets calcification in these locations. In general, age, possibly male gender, and systolic hypertension were fairly consistent risk factors for calcification, although MAC and AAC were more prevalent in postmenopausal women. There appears to be little uniformity with respect to other risk factors, and, curiously, on more than one occasion, BMI and diastolic blood pressure proved to be inversely associated. Despite other similarities, this inconsistency of conventional risk factors between studies might cast doubt over the association of valvular calcification with atherosclerosis and there is little additional evidence to support the view that MAC is a manifestation of atherosclerosis. Nevertheless, our review suggests that calcification of one area of the CV system is indicative of the likelihood of calcification elsewhere and since it tends to be initiated in the coronary artery, this can be used as a guide to later calcification in other arteries and valves.

References

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Allison MA, Criqui MH, Wright CM ‘Patterns and risk factors for systemic calcified atherosclerosis’. Arterioscler Thromb Vasc Biol. 2004; 24(2)331–6

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Odink AE, van der Lugt A, Hofman A, Hunink MG, Breteler MM, Krestin GP, Witteman JC ‘Association between calcification in the coronary arteries, aortic arch and carotid arteries: the Rotterdam study’. Atherosclerosis. 2007; 193(2)408–13

8 

Allison MA, Criqui MH, Wright CM ‘Patterns and risk factors for systemic calcified atherosclerosis’. Arterioscler Thromb Vasc Biol. 2004; 24(2)331–6

9 

Kuller LH, Matthews KA, Sutton-Tyrrell K, Edmundowicz D, Bunker CH ‘Coronary and aortic calcification among women 8 years after menopause and their premenopausal risk factors: the healthy women study’. ArteriosclerThrombVasc Biol. 1999; 19(9)2189–98

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Post W, Bielak AF, Ryan KA, Cheng YC, Shen H, Rumberger JA et al ‘Determinants of coronary artery and aortic calcification in the Old Order Amish’. Circulation. 2007; 115(6)717–24

11 

Sutton-Tyrrell K, Kuller LH, Edmundowicz D, Feldman A, Holubkov R, Givens L, Matthews KA ‘Usefulness of electron beam tomography to detect progression of coronary and aortic calcium in middle-aged women’. Am J Cardiol. 2001; 87(5)560–4

12 

Kalsch H, Lehmann N, Mohlenkamp S, Hammer C, Mahabadi AA, Moebus S et al ‘Prevalence of thoracic aortic calcification and its relationship to cardiovascular risk factors and coronary calcification in an unselected population-based cohort: the Heinz Nixdorf Recall Study’. Int J Cardiovasc Imaging. 2012; Epub ahead of print.

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Eisen A, Tenenbaum A, Koren-Morag N, Tanne D, Shemesh J, Golan A et al ‘Coronary and aortic calcifications inter-relationship in stable angina pectoris: A Coronary Disease Trial Investigating Outcome with Nifedipine GITS (ACTION)-Israel spiral computed tomography substudy’. Isr Med Assoc J. 2007; 9(4)277–80

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19 

Takasu J, Budoff MJ, O’Brien KD, Shavelle DM, Probstfield JL, Carr JJ, Katz R ‘Relationship between coronary artery and descending thoracic aortic calcification as detected by computed tomography: the Multi-Ethnic Study of Atherosclerosis’. Atherosclerosis. 2009; 204(2)440–6

20 

Cury RC, Ferencik M, Hoffmann U, Ferullo A, Moselewski F, Abbara S et al ‘Epidemiology and association of vascular and valvular calcium quantified by multidetector computed tomography in elderly asymptomatic subjects’. Am J Cardiol. 2004; 94(3)348–51

21 

Eisen A, Tenenbaum A, Koren-Morag N, Tanne D, Shemesh J, Golan A et al ‘Coronary and aortic calcifications inter-relationship in stable angina pectoris: A Coronary Disease Trial Investigating Outcome with Nifedipine GITS (ACTION)-Israel spiral computed tomography substudy’. Isr Med Assoc J. 2007; 9(4)277–80

22 

Wu MH, Chern MS, Chen LC, Lin YP, Sheu MH, Liu JC, Chang CY ‘Electron beam computed tomography evidence of aortic calcification as an independent determinant of coronary artery calcification’. J Chin Med Assoc. 2006; 69(9)409–14

23 

Adler Y, Fisman EZ, Shemesh J, Schwammenthal E, Tanne D, Batavraham IR et al ‘Spiral computed tomography evidence of close correlation between coronary and thoracic aorta calcifications’. Atherosclerosis. 2004; 176(1)133–8

24 

Sutton-Tyrrell K, Kuller LH, Matthews KA, Holubkov R, Patel A, Edmundowicz D, Newman A ‘Subclinical atherosclerosis in multiple vascular beds: an index of atherosclerotic burden evaluated in postmenopausal women’. Atherosclerosis. 2002; 160(2)407–16

25 

Kuller LH, Matthews KA, Sutton-Tyrrell K, Edmundowicz D, Bunker CH ‘Coronary and aortic calcification among women 8 years after menopause and their premenopausal risk factors: the healthy women study’. ArteriosclerThrombVasc Biol. 1999; 19(9)2189–98

26 

Wong ND, Lopez VA, Allison M, Detrano RC, Blumenthal RS, Folsom AR et al ‘Abdominal aortic calcium and multi-site atherosclerosis: the Multiethnic Study of Atherosclerosis’. Atherosclerosis. 2011; 214(2)436–41

27 

Sutton-Tyrrell K, Kuller LH, Edmundowicz D, Feldman A, Holubkov R, Givens L, Matthews KA ‘Usefulness of electron beam tomography to detect progression of coronary and aortic calcium in middle-aged women’. Am J Cardiol. 2001; 87(5)560–4

28 

Eisen A, Tenenbaum A, Koren-Morag N, Tanne D, Shemesh J, Golan A et al ‘Coronary and aortic calcifications inter-relationship in stable angina pectoris: A Coronary Disease Trial Investigating Outcome with Nifedipine GITS (ACTION)-Israel spiral computed tomography substudy’. Isr Med Assoc J. 2007; 9(4)277–80

29 

Wu MH, Chern MS, Chen LC, Lin YP, Sheu MH, Liu JC, Chang CY ‘Electron beam computed tomography evidence of aortic calcification as an independent determinant of coronary artery calcification’. J Chin Med Assoc. 2006; 69(9)409–14

30 

Ryu Y, Yoshida K, Suzuki Y, Nakadate M, Umehara I, Tomita M, Shibuya H ‘Long-term changes of aortic (18)F-FDG uptake and calcification in healthscreening subjects’. Ann Nucl Med. 2012; Epub ahead of print.

31 

Sutton-Tyrrell K, Kuller LH, Edmundowicz D, Feldman A, Holubkov R, Givens L, Matthews KA ‘Usefulness of electron beam tomography to detect progression of coronary and aortic calcium in middle-aged women’. Am J Cardiol. 2001; 87(5)560–4

32 

Post W, Bielak AF, Ryan KA, Cheng YC, Shen H, Rumberger JA et al ‘Determinants of coronary artery and aortic calcification in the Old Order Amish’. Circulation. 2007; 115(6)717–24

33 

Adler Y, Fisman EZ, Shemesh J, Schwammenthal E, Tanne D, Batavraham IR et al ‘Spiral computed tomography evidence of close correlation between coronary and thoracic aorta calcifications’. Atherosclerosis. 2004; 176(1)133–8

34 

Wong ND, Sciammarella M, Arad Y, Miranda-Peats R, Polk D, Hachamovich R et al ‘Relation of thoracic aortic and aortic valve calcium to coronary artery calcium and risk assessment’. Am J Cardiol. 2003; 92(8)951–5

35 

Wong ND, Lopez VA, Allison M, Detrano RC, Blumenthal RS, Folsom AR et al ‘Abdominal aortic calcium and multi-site atherosclerosis: the Multiethnic Study of Atherosclerosis’. Atherosclerosis. 2011; 214(2)436–41

36 

Oei HH, Vliegenthart R, Hak AE, Iglesias del Sol A, Hofman A, Oudkerk M, Witteman JC ‘The association between coronary calcification assessed by electron beam computed tomography and measures of extracoronary atherosclerosis: the Rotterdam Coronary Calcification Study’. J Am Coll Cardiol. 2002; 39(11)1745–51

37 

Kalsch H, Lehmann N, Mohlenkamp S, Hammer C, Mahabadi AA, Moebus S et al ‘Prevalence of thoracic aortic calcification and its relationship to cardiovascular risk factors and coronary calcification in an unselected population-based cohort: the Heinz Nixdorf Recall Study’. Int J Cardiovasc Imaging. 2012; Epub ahead of print.

38 

Takasu J, Budoff MJ, O’Brien KD, Shavelle DM, Probstfield JL, Carr JJ, Katz R ‘Relationship between coronary artery and descending thoracic aortic calcification as detected by computed tomography: the Multi-Ethnic Study of Atherosclerosis’. Atherosclerosis. 2009; 204(2)440–6

39 

Odink AE, van der Lugt A, Hofman A, Hunink MG, Breteler MM, Krestin GP, Witteman JC ‘Association between calcification in the coronary arteries, aortic arch and carotid arteries: the Rotterdam study’. Atherosclerosis. 2007; 193(2)408–13

40 

Wong ND, Sciammarella M, Arad Y, Miranda-Peats R, Polk D, Hachamovich R et al ‘Relation of thoracic aortic and aortic valve calcium to coronary artery calcium and risk assessment’. Am J Cardiol. 2003; 92(8)951–5

41 

Eisen A, Tenenbaum A, Koren-Morag N, Tanne D, Shemesh J, Golan A et al ‘Coronary and aortic calcifications inter-relationship in stable angina pectoris: A Coronary Disease Trial Investigating Outcome with Nifedipine GITS (ACTION)-Israel spiral computed tomography substudy’. Isr Med Assoc J. 2007; 9(4)277–80

42 

Odink AE, van der Lugt A, Hofman A, Hunink MG, Breteler MM, Krestin GP, Witteman JC ‘Association between calcification in the coronary arteries, aortic arch and carotid arteries: the Rotterdam study’. Atherosclerosis. 2007; 193(2)408–13

43 

Arad Y, Spadaro LA, Roth M, Scordo J, Goodman K, Sherman S et al ‘Correlations between vascular calcification and atherosclerosis: a comparative electron beam CT study of the coronary and carotid arteries’. J Comput Assist Tomogr. 1998; 22(2)207–11

44 

Qunibi WY, Abouzahr F, Mizani MR, Nolan CR, Arya R, Hunt KJ ‘Cardiovascular calcification in Hispanic Americans (HA) with chronic kidney disease (CKD) due to type 2 diabetes’. Kidney International, 2005; 68: 271–277

45 

Prasad A, Wassel CL, Jensky NE, Allison MA ‘The epidemiology of subclavian artery calcification’. J Vasc Surg. 2011; 54(5)1408–13

46 

Allison MA, DiTomasso D, Criqui MH, Langer RD, Wright CM ‘Renal artery calcium: relationship to systemic calcified atherosclerosis’. Vasc Med. 2006; 11(4)232–8

47 

Freedman BI, Hsu FC, Langefeld CD, Bowden DW, Moossavi S, Dryman BN, Carr JJ ‘Renal artery calcified plaque associations with subclinical renal and cardiovascular disease’. Kidney Int. 2004; 65(6)2262–7

48 

Prasad A, Wassel CL, Jensky NE, Allison MA ‘The epidemiology of subclavian artery calcification’. J Vasc Surg. 2011; 54(5)1408–13

49 

Allison MA, DiTomasso D, Criqui MH, Langer RD, Wright CM ‘Renal artery calcium: relationship to systemic calcified atherosclerosis’. Vasc Med. 2006; 11(4)232–8

50 

Odink AE, van der Lugt A, Hofman A, Hunink MG, Breteler MM, Krestin GP, Witteman JC ‘Association between calcification in the coronary arteries, aortic arch and carotid arteries: the Rotterdam study’. Atherosclerosis. 2007; 193(2)408–13

51 

Freedman BI, Hsu FC, Langefeld CD, Bowden DW, Moossavi S, Dryman BN, Carr JJ ‘Renal artery calcified plaque associations with subclinical renal and cardiovascular disease’. Kidney Int. 2004; 65(6)2262–7

52 

Allison MA, DiTomasso D, Criqui MH, Langer RD, Wright CM ‘Renal artery calcium: relationship to systemic calcified atherosclerosis’. Vasc Med. 2006; 11(4)232–8

53 

Prasad A, Wassel CL, Jensky NE, Allison MA ‘The epidemiology of subclavian artery calcification’. J Vasc Surg. 2011; 54(5)1408–13

54 

Sutton-Tyrrell K, Kuller LH, Matthews KA, Holubkov R, Patel A, Edmundowicz D, Newman A ‘Subclinical atherosclerosis in multiple vascular beds: an index of atherosclerotic burden evaluated in postmenopausal women’. Atherosclerosis. 2002; 160(2)407–16

55 

Sutton-Tyrrell K, Kuller LH, Edmundowicz D, Feldman A, Holubkov R, Givens L, Matthews KA ‘Usefulness of electron beam tomography to detect progression of coronary and aortic calcium in middle-aged women’. Am J Cardiol. 2001; 87(5)560–4

56 

Adler Y, Fisman EZ, Shemesh J, Schwammenthal E, Tanne D, Batavraham IR et al ‘Spiral computed tomography evidence of close correlation between coronary and thoracic aorta calcifications’. Atherosclerosis. 2004; 176(1)133–8

57 

Arad Y, Spadaro LA, Roth M, Scordo J, Goodman K, Sherman S et al ‘Correlations between vascular calcification and atherosclerosis: a comparative electron beam CT study of the coronary and carotid arteries’. J Comput Assist Tomogr. 1998; 22(2)207–11

58 

Sutton-Tyrrell K, Kuller LH, Matthews KA, Holubkov R, Patel A, Edmundowicz D, Newman A ‘Subclinical atherosclerosis in multiple vascular beds: an index of atherosclerotic burden evaluated in postmenopausal women’. Atherosclerosis. 2002; 160(2)407–16

59 

Post W, Bielak AF, Ryan KA, Cheng YC, Shen H, Rumberger JA et al ‘Determinants of coronary artery and aortic calcification in the Old Order Amish’. Circulation. 2007; 115(6)717–24

60 

Adler Y, Fisman EZ, Shemesh J, Schwammenthal E, Tanne D, Batavraham IR et al ‘Spiral computed tomography evidence of close correlation between coronary and thoracic aorta calcifications’. Atherosclerosis. 2004; 176(1)133–8

61 

Eisen A, Tenenbaum A, Koren-Morag N, Tanne D, Shemesh J, Golan A et al ‘Coronary and aortic calcifications inter-relationship in stable angina pectoris: A Coronary Disease Trial Investigating Outcome with Nifedipine GITS (ACTION)-Israel spiral computed tomography substudy’. Isr Med Assoc J. 2007; 9(4)277–80

62 

Wu MH, Chern MS, Chen LC, Lin YP, Sheu MH, Liu JC, Chang CY ‘Electron beam computed tomography evidence of aortic calcification as an independent determinant of coronary artery calcification’. J Chin Med Assoc. 2006; 69(9)409–14

63 

Boon A, Cheriex E, Lodder J, Kessels F ‘Cardiac valve calcification: characteristics of patients with calcification of the mitral annulus or aortic valve’. Heart. 1997; 78(5)472–4

64 

Mori H, Oku Y, Hashiba K, Seto M, Mameya G ‘The relationship of osteoporosis to mitral annular and aortic valvular calcification in elderly women’. J Cardiol. 1990; 20(2)393–9

65 

Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

66 

Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

67 

Cury RC, Ferencik M, Hoffmann U, Ferullo A, Moselewski F, Abbara S et al ‘Epidemiology and association of vascular and valvular calcium quantified by multidetector computed tomography in elderly asymptomatic subjects’. Am J Cardiol. 2004; 94(3)348–51

68 

Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

69 

Allison MA, DiTomasso D, Criqui MH, Langer RD, Wright CM ‘Renal artery calcium: relationship to systemic calcified atherosclerosis’. Vasc Med. 2006; 11(4)232–8

70 

Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

71 

Mori H, Oku Y, Hashiba K, Seto M, Mameya G ‘The relationship of osteoporosis to mitral annular and aortic valvular calcification in elderly women’. J Cardiol. 1990; 20(2)393–9

72 

Boon A, Cheriex E, Lodder J, Kessels F ‘Cardiac valve calcification: characteristics of patients with calcification of the mitral annulus or aortic valve’. Heart. 1997; 78(5)472–4

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Messika-Zeitoun D, Bielak LF, Peyser PA, Sheedy PF, Turner ST, Nkomo VT et al ‘Aortic valve calcification: determinants and progression in the population’. Arterioscler Thromb Vasc Biol. 2007; 27(3)642–8

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Messika-Zeitoun D, Bielak LF, Peyser PA, Sheedy PF, Turner ST, Nkomo VT et al ‘Aortic valve calcification: determinants and progression in the population’. Arterioscler Thromb Vasc Biol. 2007; 27(3)642–8

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Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

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Adler Y, Shemesh J, Tenenbaum A, Hovav B, Fisman EZ, Motro M ‘Aortic valve calcium on spiral computed tomography (dual slice mode) is associated with advanced coronary calcium in hypertensive patients’. Coron Artery Dis. 2002; 13(4)209–13

94 

Mahabadi AA, Bamberg F, Toepker M, Schlett CL, Rogers IS, Nagurney JT et al ‘Association of aortic valve calcification to the presence, extent and composition of coronary artery plaque burden: from the Rule Out Myocardial Infarction using Computer Assisted Tomography (ROMICAT) trial’. Am Heart J. 2009; 158(4)562–8

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Messika-Zeitoun D, Bielak LF, Peyser PA, Sheedy PF, Turner ST, Nkomo VT et al ‘Aortic valve calcification: determinants and progression in the population’. Arterioscler Thromb Vasc Biol. 2007; 27(3)642–8

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Messika-Zeitoun D, Bielak LF, Peyser PA, Sheedy PF, Turner ST, Nkomo VT et al ‘Aortic valve calcification: determinants and progression in the population’. Arterioscler Thromb Vasc Biol. 2007; 27(3)642–8

97 

Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

98 

Wysokinski A, Zapolski T ‘Relationship between aortic valve calcification and aortic atherosclerosis: a transoesophageal echocardiography study’. Kardiol Pol. 2006; 64(7)694–701

99 

Wong ND, Sciammarella M, Arad Y, Miranda-Peats R, Polk D, Hachamovich R et al ‘Relation of thoracic aortic and aortic valve calcium to coronary artery calcium and risk assessment’. Am J Cardiol. 2003; 92(8)951–5

100 

Ribeiro S, Ramos A, Brandao A, Rebelo JR, Guerra A, Resina C et al ‘Cardiac valve calcification in haemodialysis patients: role of calciumphosphate metabolism’. Nephrol Dial Transplant. 1998; 13(8)2037–40

101 

Boon A, Cheriex E, Lodder J, Kessels F ‘Cardiac valve calcification: characteristics of patients with calcification of the mitral annulus or aortic valve’. Heart. 1997; 78(5)472–4

102 

Messika-Zeitoun D, Bielak LF, Peyser PA, Sheedy PF, Turner ST, Nkomo VT et al ‘Aortic valve calcification: determinants and progression in the population’. Arterioscler Thromb Vasc Biol. 2007; 27(3)642–8

103 

Pohle K, Maffert R, Ropers D, Moshage W, Stilianakis N, Daniel WG, Achenbach S ‘Progression of aortic valve calcification: association with coronary atherosclerosis and cardiovascular risk factors’. Circulation. 2001; 104(16)1927–32

104 

Takasu J, Shavelle DM, O’Brien KD, Babaei A, Rosales J, Mao S et al ‘Association between progression of aortic valve calcification and coronary calcification: assessment by electron beam tomography’. Acad Radiol. 2005; 12(3)298–304

105 

Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

106 

Messika-Zeitoun D, Bielak LF, Peyser PA, Sheedy PF, Turner ST, Nkomo VT et al ‘Aortic valve calcification: determinants and progression in the population’. Arterioscler Thromb Vasc Biol. 2007; 27(3)642–8

107 

Wong ND, Sciammarella M, Arad Y, Miranda-Peats R, Polk D, Hachamovich R et al ‘Relation of thoracic aortic and aortic valve calcium to coronary artery calcium and risk assessment’. Am J Cardiol. 2003; 92(8)951–5

108 

Boon A, Cheriex E, Lodder J, Kessels F ‘Cardiac valve calcification: characteristics of patients with calcification of the mitral annulus or aortic valve’. Heart. 1997; 78(5)472–4

109 

Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

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Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

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115 

Pressman GS, Crudu V, Parameswaran-Chandrika A, Romero-Corral A, Purushottam B, Figueredo VM ‘Can total cardiac calcium predict the coronary calcium score?’. Int J Cardiol. 2011; 146(2)202–6

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118 

Tenenbaum A, Fisman EZ, Pines A, Shemesh J, Shapira I, Adler Y et al ‘Gender paradox in cardiac calcium deposits in middle-aged and elderly patients: mitral annular and coronary calcifications interrelationship’. Maturitas. 2000; 36(1)35–42

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120 

Hamirani YS, Nasir K, Blumenthal RS, Takasu J, Shavelle D, Kronmal R, Budoff M ‘Relation of mitral annular calcium and coronary calcium (from the Multi-Ethnic Study of Atherosclerosis [MESA])’. Am J Cardiol. 2011; 107(9)1291–4

121 

Hamirani YS, Nasir K, Blumenthal RS, Takasu J, Shavelle D, Kronmal R, Budoff M ‘Relation of mitral annular calcium and coronary calcium (from the Multi-Ethnic Study of Atherosclerosis [MESA])’. Am J Cardiol. 2011; 107(9)1291–4

122 

Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

123 

Tenenbaum A, Fisman EZ, Pines A, Shemesh J, Shapira I, Adler Y et al ‘Gender paradox in cardiac calcium deposits in middle-aged and elderly patients: mitral annular and coronary calcifications interrelationship’. Maturitas. 2000; 36(1)35–42

124 

Boon A, Cheriex E, Lodder J, Kessels F ‘Cardiac valve calcification: characteristics of patients with calcification of the mitral annulus or aortic valve’. Heart. 1997; 78(5)472–4

125 

Hamirani YS, Nasir K, Blumenthal RS, Takasu J, Shavelle D, Kronmal R, Budoff M ‘Relation of mitral annular calcium and coronary calcium (from the Multi-Ethnic Study of Atherosclerosis [MESA])’. Am J Cardiol. 2011; 107(9)1291–4

126 

Boon A, Cheriex E, Lodder J, Kessels F ‘Cardiac valve calcification: characteristics of patients with calcification of the mitral annulus or aortic valve’. Heart. 1997; 78(5)472–4

127 

Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

128 

Ribeiro S, Ramos A, Brandao A, Rebelo JR, Guerra A, Resina C et al ‘Cardiac valve calcification in haemodialysis patients: role of calciumphosphate metabolism’. Nephrol Dial Transplant. 1998; 13(8)2037–40

129 

Messika-Zeitoun D, Bielak LF, Peyser PA, Sheedy PF, Turner ST, Nkomo VT et al ‘Aortic valve calcification: determinants and progression in the population’. Arterioscler Thromb Vasc Biol. 2007; 27(3)642–8

130 

Mahabadi AA, Bamberg F, Toepker M, Schlett CL, Rogers IS, Nagurney JT et al ‘Association of aortic valve calcification to the presence, extent and composition of coronary artery plaque burden: from the Rule Out Myocardial Infarction using Computer Assisted Tomography (ROMICAT) trial’. Am Heart J. 2009; 158(4)562–8

131 

Adler Y, Shemesh J, Tenenbaum A, Hovav B, Fisman EZ, Motro M ‘Aortic valve calcium on spiral computed tomography (dual slice mode) is associated with advanced coronary calcium in hypertensive patients’. Coron Artery Dis. 2002; 13(4)209–13

132 

Wong ND, Sciammarella M, Arad Y, Miranda-Peats R, Polk D, Hachamovich R et al ‘Relation of thoracic aortic and aortic valve calcium to coronary artery calcium and risk assessment’. Am J Cardiol. 2003; 92(8)951–5

133 

Boon A, Cheriex E, Lodder J, Kessels F ‘Cardiac valve calcification: characteristics of patients with calcification of the mitral annulus or aortic valve’. Heart. 1997; 78(5)472–4

134 

Ahmadi N, Clouse M ‘Aortic valve calcification and subclinical coronary atherosclerosis’. J Cardiovasc Comput Tomogr. 2010; 4: 47–8

135 

Takasu J, Shavelle DM, O’Brien KD, Babaei A, Rosales J, Mao S et al ‘Association between progression of aortic valve calcification and coronary calcification: assessment by electron beam tomography’. Acad Radiol. 2005; 12(3)298–304

136 

Yamamoto H, Shavelle D, Takasu J, Lu B, Mao SS, Fischer H, Budoff MJ ‘Valvular and thoracic aortic calcium as a marker of the extent and severity of angiographic coronary artery disease’. Am Heart J. 2003; 146(1)153–9

137 

Nasir K, Katz R, al-Mallah M, Takasu J, Shavelle DM, Carr JJ et al ‘Relationship of aortic valve calcification with coronary artery calcium severity: the Multi-Ethnic Study of Atherosclerosis (MESA)’. J Cardiovasc Comput Tomogr. 2010; 4(1)41–6

138 

Tenenbaum A, Fisman EZ, Pines A, Shemesh J, Shapira I, Adler Y et al ‘Gender paradox in cardiac calcium deposits in middle-aged and elderly patients: mitral annular and coronary calcifications interrelationship’. Maturitas. 2000; 36(1)35–42

139 

Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

140 

Takasu J, Shavelle DM, O’Brien KD, Babaei A, Rosales J, Mao S et al ‘Association between progression of aortic valve calcification and coronary calcification: assessment by electron beam tomography’. Acad Radiol. 2005; 12(3)298–304

141 

Allison MA, Cheung P, Criqui MH, Langer RD, Wright CM ‘Mitral and aortic annular calcification are highly associated with systemic calcified atherosclerosis’. Circulation. 2006; 113(6)861–6

142 

Adler Y, Shemesh J, Tenenbaum A, Hovav B, Fisman EZ, Motro M ‘Aortic valve calcium on spiral computed tomography (dual slice mode) is associated with advanced coronary calcium in hypertensive patients’. Coron Artery Dis. 2002; 13(4)209–13

143 

Mahabadi AA, Bamberg F, Toepker M, Schlett CL, Rogers IS, Nagurney JT et al ‘Association of aortic valve calcification to the presence, extent and composition of coronary artery plaque burden: from the Rule Out Myocardial Infarction using Computer Assisted Tomography (ROMICAT) trial’. Am Heart J. 2009; 158(4)562–8

144 

Messika-Zeitoun D, Bielak LF, Peyser PA, Sheedy PF, Turner ST, Nkomo VT et al ‘Aortic valve calcification: determinants and progression in the population’. Arterioscler Thromb Vasc Biol. 2007; 27(3)642–8



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