(Stroke. 1996;27:69-75.)
© 1996 American Heart Association, Inc.
Articles |
Risk Factors and Segment-Specific Carotid Arterial Enlargement in the Atherosclerosis Risk in Communities (ARIC) Cohort
From Bowman Gray School of Medicine, Winston-Salem, NC (J.R.C., G.E., W.R.); National Heart, Lung, and Blood Institute, Bethesda, Md (U.G., J.P., A.R.S., P.S.); and the University of North Carolina, Chapel Hill (G.H.).
Correspondence to Dr John R. Crouse, Bowman Gray School of Medicine, Medical Center Blvd, Winston-Salem, NC 27157-1047.
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Abstract |
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 Top Abstract IntroductionSubjects and Methods Results Discussion References |
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Background and Purpose B-mode ultrasound imaging affords the opportunity to quantify both intimal-medial thickness (IMT) and lumen diameter of extracranial carotid arteries in ambulatory populations. Since the relation of IMT to lumen diameter may be complex, we asked whether cardiovascular disease risk factors (previously shown to be associated with greater arterial IMT) are related to smaller lumen diameters.
Methods We used B-mode ultrasound to quantify lumen diameter, interadventitial diameter, and IMT of the extracranial carotid arteries and assessed the relationship of these measures to body mass index, smoking, low-density lipoprotein (LDL) and high-density lipoprotein cholesterol, hypertension, and diabetes in 6088 male and 7493 female participants in the Atherosclerosis Risk in Communities (ARIC) cohort.
Results Smoking, hypertension, and LDL cholesterol were consistently related to greater IMT in the common and internal carotid arteries of men and women, as has been previously reported. In the internal carotid artery, smoking, hypertension, and LDL cholesterol were consistently related to smaller lumens. In the common carotid artery, body mass index, smoking, and hypertension were related to significantly larger, and LDL cholesterol to smaller, lumens. Thus, only LDL cholesterol was consistently associated with smaller lumens in both the common and internal carotid arteries.
Conclusions Risk factors relate positively to IMT in both the common and internal carotid arteries and inversely with lumen diameter in the internal carotid artery, in parallel with their relation to clinical events. However, their association with lumen diameters of the common carotid artery in population-based samples is more complex, and in some cases adverse levels of risk factors may be associated with larger lumens.
Key Words: arteriosclerosis • carotid arteries • risk factors • ultrasonics
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Introduction |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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Risk factors have been evaluated for their relation to IMT of the extracranial carotid artery1 2 3 4 5 and to progression and regression of IMT.6 7 In addition, three clinical trials have recently demonstrated that hyperlipidemia treatment favorably influences progression of common carotid IMT.8 9 10 Increased IMT of the extracranial carotid arteries has been related to prevalent coronary artery disease11 12 and transient ischemic attack13 and to the incidence of symptomatic coronary heart disease.14 Narrowing of the lumen of the internal carotid arteries has also been related to risk factors15 16 17 18 and to clinical outcome.19 20 21 In general, these explorations have led to the conclusion that risk factors are associated with narrowing of arterial lumens.
Studies of coronary arteries in vivo22 and in vitro23 24 have indicated the complexity of the relationship of wall thickening to lumen reduction. IMT is often related to little or no narrowing of the arterial lumen. Our previous exploration of the relation of IMT and lumen diameter in the common carotid arteries led to similar conclusions.25 However, symptomatic cardiovascular disease is most often related to lumen compromise.21 26 It therefore becomes important to understand how risk factors affect the lumen as well as IMT. Earlier explorations of these effects that suggested straightforward relationships of risk factors to lumen reduction may have been biased in some cases by the symptomatic nature of the populations studied and in others by the methodology used (eg, Doppler ultrasound, which cannot assess minor reduction of lumen diameter15 16 17 18 ). Furthermore, these associations have generally been obtained from examinations of the internal carotid artery. To define the relationship of risk factors to lumen diameter of both the common and internal carotid arteries in a population-based sample, we have quantified risk factors and carotid artery dimensions in 6088 men and 7493 women in the ARIC cohort.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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ARIC is a community-based cohort study that has been previously described and consists of a probability sample of 15 800 men and women aged 45 to 64 years from four US communities. All participants provided informed consent before participation. In three of the four communities the sample was drawn from all those aged 45 to 64 years in the community; in Jackson, Miss, the fourth community, the sample was drawn from black residents aged 45 to 64 years. Details of cohort selection have been published.27
The ARIC ultrasound methods used in this study are the same as those used in our previous communication25 and will be described only briefly here. The ARIC ultrasound examination consists of a standardized baseline examination of the left and right carotid arteries with measurements of the near and far walls of the common carotid, the bifurcation, and the internal carotid arteries. We analyzed data from only the common and internal carotid arteries on both the left and right sides. For this analysis the common carotid was defined as a 1-cm segment immediately proximal to the beginning of the dilation associated with the bifurcation, and the internal carotid artery was defined as a 1-cm segment immediately distal to the flow divider. These segments were chosen for the current analyses because their walls are parallel and those of the bifurcation are not. Ultrasound tapes are digitized and read in a central laboratory by trained and certified readers who attempt to identify the adventitial-medial and intimal-luminal interfaces at the near wall (closest to the ultrasound probe) and far wall in each segment. The distance between these interfaces on the near and far walls is the wall thickness or IMT. The distance from the near border of the media of the near wall to the far border of the media on the far wall defines the "interadventitial diameter." For this study we used two separate definitions of the arterial lumen. In the first (algorithm A), the lumen was defined as the average interadventitial diameter over the 1-cm segment less twice the maximum far wall IMT over the same segment. This is the definition we had used previously,25 and it was chosen because of the generally higher quality of visualization of far wall boundaries compared with those from the near wall. The second algorithm (algorithm B) defined the lumen as the interadventitial diameter at the site of maximum far wall IMT less (maximum far wall IMT+near wall IMT at that site or at the closest site nearby). Participants in whom interadventitial diameter at the site of maximum far wall IMT could not be obtained were excluded, as were those for whom no near wall measurement could be made. This algorithm was chosen to incorporate information from both the near and far walls in the definition of the lumen, but with the understanding that it would result in a loss of evaluable participants because of the poorer visualizability of the near wall. Diameter measurements were made during systole, ie, at their maximum over the cardiac cycle. Results using the two algorithms for definition of arterial lumen were nearly precisely the same (see below), and therefore data are presented for algorithm A only.
In ARIC the following definitions are used: prevalent hypertension is
defined as systolic blood pressure 
160 mm Hg,
diastolic blood pressure 95 mm Hg, or use of
antihypertensive medications. Diabetes is defined as fasting blood
glucose 140 mg/dL, nonfasting blood glucose 200 mg/dL, use of
medication for diabetes, or reported physician diagnosis of diabetes.
Participant long-term cigarette smoking behavior is characterized
according to pack-years from information obtained during a standard
interview; participants are also classified as current or noncurrent
smokers. Lipids and lipoproteins are quantified in a Centers for
Disease Control standardized laboratory at Baylor College of Medicine.
Total cholesterol and triglyceride are
quantified by enzymatic methods, and HDL cholesterol is
quantified after dextran-magnesium precipitation. LDL
cholesterol is estimated by the Friedewald
formula.28 LDL cholesterol was treated as both
continuous and categorical variables. It was dichotomized with 160
mg/dL (4.1376 mmol/L) as a cutoff, as well as grouped into the
following categories: <100, 100 to <125, 125 to <140, 140 to <160,
and 160 mg/dL (<2.568, 2.568 to <3.2325, 3.2325 to <3.6204,
3.6204
to <4.1376, and 4.1376 mmol/L).
Because of our previous observation that age and height were related to increased interadventitial and lumen diameter of the common carotid artery,25 all analyses involving risk factor relationships have been age and height adjusted. Race and community were also adjusted for in multivariate analyses by the use of indicators reflecting participant status (yes, no) as Forsyth County, NC, black; Forsyth County, NC, white; Jackson, Miss, black; Washington County, Md, white; and suburban Minneapolis, Minn, white. This approach was taken because race is associated with arterial dimensions,29 but in ARIC race is partly confounded by center since all the participants from Jackson, Miss, are black. The numbers of black participants from suburban Minneapolis and Washington County were so small (n=17 and n=28, respectively) that they were excluded from analysis. Analyses were carried out separately for men and women for descriptive purposes to demonstrate consistency of results and to highlight the important differences in arterial dimensions associated with sex.
A general linear models approach was used to estimate the relationship of each risk factor with the arterial measurements after the data were investigated for model fit and outlying observations. Specifically, since measurements were made on both the left and right carotid arteries, we used a repeated-measures regression model that permitted us to incorporate data from arterial dimensions of both the left and right internal carotid arteries (jointly) to estimate an average association of each risk factor with internal carotid artery dimensions. A similar model was run for the common carotid artery. We used the statistical program BMDP 5V to provide maximum-likelihood estimates for the regression coefficients30 and included all participants for whom either the right or left lumen diameter could be estimated. The coefficients using both left and right measurements differed little from those using either the left or right side alone, although the standard errors of the coefficients were slightly decreased, as would be expected from use of more information in the repeated-measures regression model.
For the figures, we calculated mean values of the arterial measurements for categories of risk factors using the general linear models approach described above.
Of the 15 800 ARIC participants, 13 581 were included in analyses for this report. Among the exclusions were 8 individuals who did not meet eligibility requirements. Most of the exclusions were due to absence of all eight artery measurements (left and right common and internal carotid artery wall thicknesses and interadventitial diameters, n=1382) and absence of one or more of the other variables included in analyses (n=733). The remaining 89 participants excluded were races other than black or white or the Minneapolis and Washington County blacks mentioned previously.
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Results |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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Table 1
presents mean values of various artery
characteristics and risk factors for men and women. Tables
2 and 3 identify the relationships of
body mass index, cigarette smoking, hypertension, diabetes, LDL
cholesterol, and HDL cholesterol with IMT,
interadventitial diameter, and lumen diameter of the internal and
common carotid arteries in men and women. Associations with the
quantitative risk factors are shown in relation to approximate standard
deviations (eg, 40 mg/dL, 1.03 mmol/L for LDL cholesterol).
For each artery measurement in these tables the first column shows
relationships that have been adjusted for age, height, race, and
community with the use of the regression model. The second column shows
the relationship adjusted for age, height, race, community, and each of
the other risk factors in the table. Smoking, hypertension, and LDL
cholesterol were consistently and positively
related to increased IMT of the common and internal carotid arteries in
men and women, as has been previously reported.1
Relationships of risk factors with interadventitial diameter and lumen
diameter were similar in men and women but differed according to
segment (internal versus common carotid artery).
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In the internal carotid artery (Table 2), body mass index
was
positively related and LDL cholesterol negatively related
to interadventitial diameters in both sexes; lifetime smoking was
positively related to interadventitial diameter only in men. Of those
risk factors that were associated with increased wall thickness,
lifetime smoking, hypertension, and LDL cholesterol were
significantly related to smaller lumens in both sexes. Fig 1 is
based on analyses similar to those in Table 2 for LDL
cholesterol, except that LDL is grouped rather
than treated continuously. As shown in Table 2, Fig
1 illustrates that
the IMT increases with increasing LDL cholesterol while the
interadventitial diameter decreases, resulting in a decrease of the
lumen. In Fig 2, the relationships between the risk
factors and lumen of the internal carotid artery are summarized. The
lumen is reduced for smokers, hypertensives, diabetics, and those with
elevated LDL cholesterol.
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In the common carotid artery (Table 3), body mass index,
smoking,
hypertension, and diabetes were related to greater interadventitial
diameters in both men and women. Relationships between lipids and
interadventitial diameter were not striking: differences in LDL
cholesterol and HDL cholesterol equal to their
approximate standard deviations were related to differences in
interadventitial diameter of generally <0.07 mm. Most of those risk
factors that related to greater arterial wall thickness and
interadventitial diameters, namely, smoking, hypertension, and
diabetes, were also related to larger lumens (significant for smoking
and hypertension, nonsignificant for diabetes; Table 3, lumen
diameter,
model 2). LDL cholesterol was related to smaller lumens in
both sexes. A significant relationship between HDL
cholesterol and lumen diameter in men was also apparent.
Fig 2
summarizes the relationships between the risk factors and
lumen
of the common carotid artery.
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As described above, for this study we explored the use of a second algorithm (algorithm B) for definition of arterial lumen diameter. Because the definition of the interadventitial diameter in algorithms A and B was the same, there was no difference in interadventitial diameters of the common or internal carotid artery with the two methods.
The associations of risk factors with common carotid arterial diameter described above were essentially the same whether algorithm A or B was used. All the univariate and multivariate relationships observed with algorithm A remained significant when algorithm B was used with the exception of LDL in the common carotid, which became nonsignificantly associated with smaller lumens in multivariate analysis in women only. However, algorithm B required availability of more boundary measurements than algorithm A and resulted in our being unable to quantify lumen diameter in approximately 25% of the participants in whom we could quantify lumen diameters according to algorithm A.
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Discussion |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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Availability of methodology that images arterial walls and lumens affords the opportunity to relate arterial IMT to lumen diameter in vivo and to estimate the relationships of risk factors to both the wall and the lumen. Previous observations suggested that relationships of risk factors to lumen stenosis might be similar to their relationships to IMT as measured noninvasively.1 2 3 4 5 6 15 16 17 18 However, associations with lumen diameter are invariably obtained with the use of echo-Doppler to interrogate the internal carotid artery. Our data from the internal carotid artery are generally in agreement with and extend these observations of other investigators. In contrast, for the common carotid artery our previously published data show that in a population-based sample, increased wall thickness associated with lumen narrowing is observed in only <10% of men and <5% of women, and in the common carotid artery older individuals have larger lumens.25 The data presented in this communication from a population-based study suggest that for the majority of asymptomatic persons, both the interadventitial diameter and the lumen of the common carotid artery tend to be larger in relationship to certain risk factors that are associated with increased IMT (namely, smoking, hypertension, and diabetes). These relationships between risk factors and lumen diameter were observed with the use of two different algorithms for defining lumen diameter.
There is a large body of literature that identifies a complex relation of wall thickness to lumen stenosis in the coronary arteries. Previous autopsy studies have shown that lumen diameter only imperfectly reflects wall thickness,23 24 and these observations have been confirmed at cardiothoracic surgery with epicardial echocardiography22 and at coronary angiography with intravascular ultrasound.31 Clarkson et al24 have shown that diabetes and hypertension are associated with larger coronary artery plaques but not with narrow coronary artery lumens in postmortem specimens, and this reflects arterial enlargement associated with risk factors. If some arteries or segments of arteries frequently dilate in relation to exposure to atherosclerotic risk factors, then the process responsible for constriction of the lumen in relation to atherosclerosis takes on new significance.
Smoking is related to greater interadventitial diameter and greater
lumen diameter of the common carotid artery in both sexes. Greater
lumen diameters associated with smoking have been observed in other
arteries: in particular, there is a strong, previously observed
relationship of smoking with death from aortic
aneurysm32 that may be related to an effect of
smoking on elastic tissue.33 Aneurysms have
decreased elastin and increased elastase activity in the
intima-media.34 Cigarette smoking has been linked to
increased secretion of pancreatic proteases,35 increased
plasma neutrophil elastase activity,36 increased
release of elastase from neutrophils,37 inactivation
of 
1-proteinase inhibitor,38
and decreased levels of 1-antitrypsin.39
Thus, smoking may be related to elastin damage or production of
functionally deficient elastin. This is in contrast to decreased
flow-mediated arterial dilatation in
smokers.40
The positive association of hypertension with the lumen of the common carotid arteries in this cohort may partly result from measuring arterial diameters in systole. However, other investigators have also observed increased arterial diameters in end-diastole with high blood pressure,16 41 and these observations are congruent with ours.
Diabetes was also related to increased interadventitial diameters
(significantly) and to increased lumen diameters (nonsignificantly) in
the common carotid artery in men and women (Fig 1). We are
unaware of
any previous reports of carotid artery diameters in diabetic patients;
however, our common carotid artery results are in agreement with those
of Clarkson et al24 obtained from the coronary
artery.
Like other risk factors, LDL cholesterol is positively
associated with IMT. However, the effects of LDL
cholesterol on arterial diameters appeared to
differ qualitatively from those of nonlipid risk factors (Fig
2).
Whereas smoking, hypertension, and diabetes were related to larger
interadventitial and lumen diameters of the common carotid artery, LDL
cholesterol was related to smaller interadventitial and
lumen diameters. Thus LDL cholesterol, compared with the
other major atherosclerosis risk factors, seems to
convey a risk for narrowing of the common carotid artery out of
proportion to its relation to arterial IMT.
In contrast to the common carotid artery, which manifested larger
interadventitial diameters and larger lumens in relation to most risk
factors, smoking, hypertension, and diabetes were related to slightly
and sometimes insignificantly larger interadventitial diameters of the
internal carotid artery, whereas LDL cholesterol was
consistently and significantly related to smaller
interadventitial diameters. The lumen of the internal carotid artery
was smaller in relation to hypertension, smoking, and LDL
cholesterol in both men and women (Table 2, Fig
2) and
nonsignificantly smaller in relation to diabetes. Studies that have
used Doppler ultrasound to quantify lumen stenosis in the
internal carotid artery are generally consistent with these
findings.15 16 17 18 The
association of risk factors, generally,
with smaller lumens in the internal carotid artery is
consistent with the predilection of this site for
stenosis and its relation to cerebrovascular events.
The effects of HDL cholesterol were not marked and were inconsistent in men and women. Because of the strong associations between HDL cholesterol and plasma triglyceride concentrations, we did not evaluate the relationships of triglyceride concentrations to arterial dimensions.
In general, the effects on wall thickness and arterial lumen diameter associated with risk factors in this investigation are small. A 40 mg/dL (1.03 mmol/L) higher LDL cholesterol, for example, was associated with IMT differences of 0.02 to 0.05 mm. This represents approximately 5% of the population mean IMT of 0.7 mm. However, this increase is expected to reflect changes located almost exclusively in the intima, the site of initial atherogenesis, which may be only an endothelial cell thick in the absence of disease. Fewer than 1% of the ARIC population had mean carotid IMT values >1.5 mm. Thus, our findings relate to very early stages in carotid atherogenesis, which clearly are predominant in this free-living, middle-aged population.
Furthermore, these results bear on the cross-sectional area measurement of IMT. The intimal-medial cross-sectional area is a function of both IMT and lumen diameter, and thus the cross-sectional area associated with a given IMT is greater for larger arteries, and the IMT measurement alone may underestimate the magnitude of the change in cross-sectional area in cohort studies or clinical trials if it is assumed that there is no increase in the lumen diameter or overestimate the magnitude if there is a decrease in interadventitial diameter.
Differences in relationships of risk factors to lumens in the common carotid arteries (larger) compared with the internal carotid arteries (smaller) were reflected in different relationships of risk factors with interadventitial diameters in these two arteries: in the common carotid artery risk factors are related to greater interadventitial diameter, which "compensates" for the greater IMT related to them, whereas no such relationship (or a more modest relationship) of risk factors with interadventitial diameter is observed in the internal carotid artery. These relationships may reflect differences in pathogenesis of plaque in the two arteries: in the internal carotid artery factors related to endothelial dysfunction and turbulent flow in the region of the bifurcation and above it (eg, growth factors and factors related to thrombosis) may play more of a role, and the effects of risk factors at this site may interact with the effects of turbulence.42 An additional difference observed in this study was the unique association of LDL cholesterol with narrower arterial diameters in the common carotid artery. If this association were present in the coronary arteries, it might partly explain the particularly adverse prognosis for heart disease associated with this risk factor. A developing theme from these investigations is that, whereas intimal-medial thickening related to risk factors may be commonplace, in some arterial segments associated lumen reduction may be uncommon and result from specific pathophysiological processes related to differences in arterial response and/or turbulence. To the extent that these processes differ in individuals or relate to specific arterial segments, risk factors may or may not associate with lumen compromise, and this may partly explain heterogeneity in the development of symptomatic cardiovascular disease.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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The ARIC Study is performed as a collaborative study supported by National Heart, Lung, and Blood Institute contracts NO1-HC-55015, NO1-HC-55016, NO1-HC-55018, NO1-HC-55019, NO1-HC-55020, NO1-HC-55021, and NO1-HC-55022. Dr Goldbourt was a visiting scholar at the National Heart, Lung, and Blood Institute in 1991 and 1992. To accomplish the goals of ARIC, the following are acknowledged: University of North Carolina, Chapel Hill: Catherine Burke, Deanna Horwitz, Carol Summers, Carmen Woody, Peter DeSaix, Mal Foley, Tom Goodwin, Richard Hayes; University of Mississippi Medical Center, Jackson: Cora Walls, Dorothy Washington, Mattye Watson, Nancy Wilson; University of Minnesota, Minneapolis: Barbara Kuehl, Anne Murrill, Bryna Lester, Jennifer Hill; The Johns Hopkins University, Baltimore, Md: Joel G. Hill, Patricia M. Crowley, Joyce B. Chabot, Patricia Hawbaker; University of Texas Medical School, Houston: Valerie Stinson, Pam Pfile, Hoang Pham, Teri Trevino; Methodist Hospital, Houston, Tex: Val Creswell, Julita Samoro, Wanda Wright, Karima Ghazzaly; and Bowman Gray School of Medicine, Winston-Salem, NC: Regina deLacy, Delilah Cook, Carolyn Bell, Teresa Crotts, Suzanne Pillsbury. The authors wish to acknowledge the assistance of Sally Bigg in manuscript preparation.
Received August 21, 1995; revision received October 18, 1995; accepted October 18, 1995.
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