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Jornal Vascular Brasileiro

Print version ISSN 1677-5449On-line version ISSN 1677-7301

J. vasc. bras. vol.7 no.4 Porto Alegre Dec. 2008  Epub Jan 30, 2009 



Carotid atherosclerosis evaluated by Doppler ultrasound: association with risk factors and systemic arterial disease



Procopio de FreitasI; Carlos Eli PiccinatoII; Wellington de Paula MartinsIII; Francisco Mauad FilhoIV

IPhD student, Graduate Program in Surgical Clinic, Department of Surgery and Anatomy, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo (USP), Ribeirão Preto, SP, Brazil.
IIProfessor, Vascular Surgery, Department of Surgery and Anatomy, Faculdade de Medicina de Ribeirão Preto, USP, Ribeirão Preto, SP, Brazil.
IIIPhD. Professor, Escola de Ultra-Sonografia e Reciclagem Médica de Ribeirão Preto (EURP), Ribeirão Preto, SP, Brazil.
IVAssociate professor, Department of Obstetrics and Gynecology, Faculdade de Medicina de Ribeirão Preto, USP, Ribeirão Preto, SP.





BACKGROUND: A high prevalence of carotid atherosclerosis in the population and its frequent association with several risk factors contribute to high morbidity and mortality rates.
OBJECTIVE: To investigate frequency and association of extracranial carotid atherosclerosis with age, sex, hypertension, ischemic coronary disease, smoking, type 2 diabetes mellitus, obesity, peripheral arterial disease, stroke, carotid occlusion, intima-media thickness and kinking.
METHODS: The carotid and bilateral extracranial arteries of 367 individuals (132 males and 235 females), with a mean of 63 years of age (35-91 years) were evaluated via anamnesis, clinical semiology and ultrasonography. The possible association between carotid atherosclerosis, represented by unspecific atheromatous plaques with stenosis > 10% or discrete and diffuse atheromatosis with stenosis < 10% and the risk factors listed above was statistically analyzed by the odds ratio with a confidence interval of 95%.
RESULTS: The frequency of carotid atherosclerosis and intima-media thickness was, respectively, 52 and 30.2%. There was an association between atherosclerosis types and age (≥ 64 years), stroke, obesity and smoking. When only carotid stenosis ≥ 60% was considered, there was an association with age (≥ 64 years), carotid occlusion and coronary disease. Intima-media thickness was associated with age (≥ 64 years), kinking, carotid occlusion, hypertension and ankle-brachial index < 0.9.
CONCLUSION: Carotid atherosclerosis is highly prevalent in the population (52%) and is associated with age, obesity, stroke, coronary disease, and smoking.

Keywords: Atherosclerosis, carotid stenosis, ultrasonography, Doppler, risk factors.


CONTEXTO: A aterosclerose carotídea apresenta alta prevalência populacional e associação com vários fatores de risco, contribuindo para altos índices de morbidade e mortalidade.
OBJETIVO: Pesquisar a freqüência e associação da aterosclerose de carótidas extracranianas com: idade, sexo, hipertensão arterial, doença coronária isquêmica, tabagismo, diabetes melito tipo 2, obesidade, doença arterial oclusiva periférica, acidente vascular cerebral, oclusão carotídea, espessamento médio-intimal e acotovelamento.
MÉTODOS: Foram avaliadas as artérias carótidas extracranianas, bilateralmente, de 367 indivíduos (132 homens e 235 mulheres) com idade média de 63 anos (35 a 91 anos) por anamnese, semiologia clínica e ultra-sonografia. A possibilidade da associação entre aterosclerose carotídea representada por placas ateromatosas inespecíficas com estenose > 10%, ateromatose discreta e difusa com estenose < 10% e os fatores de risco enunciados foi analisada estatisticamente pelo odds ratio e seus intervalos de confiança de 95%.
RESULTADOS: A freqüência da aterosclerose carotídea foi de 52%, e do espessamento médio-intimal, de 30,2%. Houve associação entre a aterosclerose (ateromatose discreta e difusa e placas ateromatosas inespecíficas) com idade ≥ 64 anos, acidente vascular cerebral, obesidade e tabagismo. Considerando-se somente estenoses carotídeas ≥ 60%, houve associação com idade ≥ 64 anos, oclusão carotídea e doença coronária. O espessamento médio-intimal apresentou associação com idade ≥ 64 anos, acotovelamento, oclusão carotídea, hipertensão arterial e índice tornozelo-braquial < 0,9.
CONCLUSÃO: A aterosclerose carotídea apresentou alta freqüência populacional (52%) e associação com idade, obesidade, acidente vascular cerebral, coronariopatia e tabagismo.

Palavras-chave: Aterosclerose, estenose das carótidas, ultra-sonografia Doppler, fatores de risco.




Atherosclerosis is a degenerative disease of a multiple-cause etiology. Different risk factors (genetic and acquired) acting in combination may determine its occurrence in more than 50% of the world adult population. Several diseases may affect the carotid arteries of men and women, from birth to old age.1

Among all carotid artery lesions responsible for extracranial cerebrovascular disease, 90% occur as a consequence of atherosclerosis. The others are represented by non-atherosclerotic diseases, such as kinking,2-5, Takayasu's arteritis, fibromuscular dysplasia, extrinsic compressions, intima dissection, aneurysm, and trauma.6

Another aspect of carotid disease to be considered is its relationship with intima-media thickness (IMT), which can be a good marker of evolution and prediction of future systemic strokes.7

In normal individuals, maximal thickening of the intima-media complex (IMC) of the common carotid artery prebifurcation is 0.8 mm. Values between 0.9 and 1.4 mm are considered as thickening. Thickness over 1.4 mm characterizes atheromatous plaque.8,9

Considering the importance of extracranial carotid atherosclerosis and its high population frequency, this study evaluates it using ultrasound and verifies its association with some risk factors, such as age, gender, hypertension, smoking, type 2 diabetes mellitus, and obesity. In addition to these factors, association of carotid atherosclerosis with intermittent claudication, ankle-brachial index (ABI < 0.9), common carotid IMT, and carotid kinking was evaluated in a population sample of 367 adult individuals.



The population sample was represented by 367 individuals registered at Centro de Saúde Escola da Faculdade de Medicina de Ribeirão Preto da Universidade de São Paulo, coming from the district of Sumarezinho, in Ribeirão Preto (SP), and calculated according to the international incidence of carotid atherosclerosis10 and number of inhabitants in that district aged 35 years or older. Distribution of age and gender of the sample is shown in Table 1. Inclusion criteria were age between 35 and 91 years and agreement to participate in the study after signing a consent term. The study was approved by the Research Ethics Committee of Centro de Saúde Escola (no. 015/2004). No individuals were excluded, therefore all received a complete evaluation by anamnesis, clinical semiology and ultrasound examinations of extracranial carotid arteries bilaterally by a single examiner. All instrumental approaches were performed with the individual in a supine position and at an acclimatized room (mean temperature of 25 ºC).


Table 1 - Click to enlarge



Anamnesis was performed by usual clinical observation of complaints and duration, followed by analysis of current disease history, interrogation of different devices, and personal and family history. Emphasis was given on ischemic heart disease, diabetes mellitus, intermittent claudication of the lower limbs, strokes, and transient ischemic attack (TIA). These data were obtained from information provided by the individuals or their escorts.

Register of blood pressures

Blood pressure measurements were performed according to a specific protocol.11 Individuals were classified as normotensive when they had systolic and diastolic pressures lower than 140 and 90 mmHg, respectively; and hypertensive when systolic and diastolic pressures were higher than 140 and 90 mmHg,11 or when using anti-hypertensive medication.

Calculation of the ankle-brachial index

Calculation of the ABI was performed according to a specific protocol.12,13 Values between 0.9-1.2 were considered as normal.

Body mass index

Body mass index (BMI) > 30 kg/m2 was considered to indicate obesity.14-17

Ultrasound assessment

The ultrasound examination aimed at locating and quantifying atheromatous lesions of internal and external common carotid arteries. The IMC was quantified only in common carotid arteries bilaterally.18

Values between 0.4-0.8 mm were considered as normal for the IMC. Values between 0.9-1.4 mm were considered as thickening, and higher than 1.5 mm indicated atheromatous plaque.19

Classification of stenotic lesions

Regarding percentage of stenoses, atheromatous lesions were classified as follows: discrete and diffuse atheromatosis (DDA), without hemodynamic changes, with stenosis < 10%; unspecific atheromatous plaques (UAP), with stenosis > 10%; and plaques with stenosis < 60 and ≥ 60% (non-hemodynamic and significant hemodynamic, respectively).

Statistical analysis

As the responses are dichotomic, a logistic regression model was proposed for data analysis. Odds ratio was the suggested model.. Stratification according to age into age groups of approximately 64 years was proposed based on epidemiological studies for carotid atherosclerosis.20,21

Evaluated variables, from the perspective of power of association, were age, gender, IMT, intermittent claudication of the lower limbs, carotid artery kinking , occlusion of any artery in the carotid system, hypertension, type 2 diabetes mellitus, TIA, stroke, obesity, smoking, ABI, and ischemic coronary disease.



Ultrasound showed atherosclerosis of extracranial carotid systems at a 52% frequency, with predominance of the common carotid bifurcation, internal carotid bulb (Table 2). The ultrasound study of these systems showed parietal lesions represented by IMT, protruded atheromas into the arterial lumen with stenoses of varied dimensions and kinkings with or without significant hemodynamic changes.


Table 2 - Click to enlarge


Of a sample of 367 individuals, age ranged between 35-91 years (mean age of 63 years), 235 were female (64%) and 132 were male (36%). Of this population, 92 (25%) individuals were obese (BMI > 30), 50 (13.6%) had diabetes mellitus, and 46 (12.5%) were smokers. In terms of vascular diseases, 136 (37%) individuals were hypertensive, 35 (9.5%) had ischemic heart disease, 28 (7.6%) had past history of stroke, 35 (9.5%) had history of TIA, 13 (3.5%) had occlusion of one artery in the carotid system, 191 (52%) had DDA and UAP, and 58 (15.8%) had carotid kinking (Table 2).

Carotid atherosclerosis was associated with age ≥ 64 years, stroke, obesity, and smoking. There were no associations with claudication, kinking, gender, hypertension, diabetes, TIA, ABI < 0.9, and ischemic heart disease (Table 3). When only cases of hemodynamically significant stenoses were analyzed (≥ 60%), there were associations with age ≥ 64 years and ischemic heart disease (Table 4).


Table 3 - Click to enlarge



Table 4 - Click to enlarge


IMT, present in 111 (30.2%) individuals, was associated with age ≥ 64 years, kinking, hypertension, and ABI < 0.9. There was no association with claudication, female gender, diabetes, TIA, stroke, obesity, smoking, and ischemic heart disease (Table 5).


Table 5 - Click to enlarge


With regard to peripheral occlusive arterial disease, 31 (8.4%) individuals had ABI < 0.9, and 10 (2.7%) reported intermittent claudication for less than 500 m on flat ground in one or both lower limbs (Table 2). There were no associations between low ABI values and carotid atherosclerosis and IMT (Tables 4 and 5).



Carotid atherosclerosis and common carotid IMT (primary variables) may have correlation with systemic hypertension and ischemic arterial diseases, among them ischemic heart disease, mesenteric ischemia and intermittent claudication.22,23 Irrespective of individual genetic inheritance, atherosclerosis may be manifested by a set of situations generated by the external environment and the organism itself (risk factors). The main risk factors are age, gender, genetic predisposition, hyperlipidemia, obesity, hypertension, smoking, type 2 diabetes mellitus, homocysteinemia, and parietal infection.24 Many studies have confirmed the relationship between carotid artery atheromatosis and risk factors for systemic atherosclerosis8 or the relationship between extension of atheromatous lesions of carotid arteries and severity of coronary atheromatosis.25

This study evaluated the power of association of carotid atherosclerosis and IMT with age, gender, intermittent claudication of the lower limbs, carotid kinking, occlusion of any artery in the carotid system, systemic hypertension, diabetes mellitus, TIA, stroke, obesity, smoking, ABI < 0.9, and ischemic heart disease. Genetic predisposition, hyperlipidemia, homocysteinemia, and infection were not included in this study.

Joakimsen et al.,10 in a similar study, evaluated 6,420 individuals of both genders, aged between 25-84 years, and showed presence of carotid atheromatosis in 55.4% of the sample and increasing frequency with age.

When these results were compared with similar studies and populations by other authors26-29 there were similarities regarding the power of association between carotid atherosclerosis and risk factors (age, obesity, smoking), stroke, carotid artery occlusion, and ischemic heart disease.

Diabetes mellitus had frequency of 13.6% – the highest was 21.4% between 65-74 years – and associations with other risk factors, such as age, stroke and obesity. Cantú-Brito et al.,30 in a study evaluating risk factors for atherosclerosis, reported a strong association between carotid atherosclerosis, hypertension and diabetes mellitus. Stroke was evaluated in this study by anamnesis and had frequency of 7.5%; the highest occurrence was 10.7% in the age group 65-74 years and showed association with carotid occlusion. TIA was observed in 9.5% of the population sample, and the highest frequency was in the age group 65-74 years.

Obesity, considered as risk factor by Brazilian and international authors, had incidence of 25% and was more prevalent in the age group 55-64 years, associated with atherosclerosis and age. Frequency of smoking was 12.5%, higher in the age group 45-54 years. There was no association between smoking and IMT, in agreement with the study by Fan et al.,31 who evaluated 413 smokers aged 40-60 years.31 On the other hand, there were associations between smoking, ABI < 0.9 and TIA, in addition to an association between atherosclerosis (UAP) and smoking.

Incidence of ischemic heart disease was 9.5%, more prevalent in the age group 75-84 years, and association only with age higher than 64 years and carotid stenoses > 60%. There were no associations with other risk factors or with generalized carotid atheromatosis, as demonstrated by Tanaka et al.32 in a 2-year prospective study evaluating 50 patients with coronary arterial disease. Incidence of kinking was 15.8%, and the female/male ratio was 3:1. The highest frequency was found in the age group 85-91 years. Pellegrino et al.,33 in a population study similar to ours, found tortuosities in 39.9% of males and 60.1% of females, and the male/female ratio was 1:1.5. This study showed association between kinking, age, female gender and stroke.

Intermittent claudication of the lower limbs was present in 2.7% of the sample, higher (5.5%) in the age group 85-91 years and with no associations with other risk factors. ABI < 0.9 had frequency of 8.4%, higher in the age group 85-91 years, similar to the studies published by Meijer et al.34 and Murabito et al.35

In this study there were no associations between low ABI values, carotid atherosclerosis and IMT, as reported by Meijer et al.,34 who evaluated a population of 6,389 individuals, mean age of 55 years.

IMT and carotid atheromatosis had correlation with other ischemic arterial diseases. A strong association between IMT, age and diabetes mellitus has been demonstrated.36 Bots et al.,37 in a study of 7,893 individuals aged 55 years or more, also observed increased common carotid IMT over a 30-month period and associated with cerebrovascular and cardiovascular events.

There was IMT incidence of 30.2% (higher in the age group above 85 years) in the sample; however, according to published studies, its relationship with risk factors is more important than frequency, since its presence can be predictive for atherosclerosis and future cardiovascular events, regardless of age.9 IMT had associations with age (≥ 64 years), hypertension, ABI < 0.9, arterial occlusion in the carotid system and presence of kinking, as previously reported.38 There were no associations between IMT, coronary arterial disease or carotid atherosclerosis, as previously described.22,39

In summary, a 52% incidence of atherosclerosis and the results obtained in relation to its associations with risk factors were similar to those found in Brazilian and international publications, except for the associations between IMT and intermittent claudication, male gender, diabetes mellitus, stroke, obesity, smoking, and ischemic heart disease. There were also no associations between carotid atherosclerosis, intermittent claudication, ABI < 0.9, kinking, gender, hypertension, diabetes mellitus, and TIA.

Carotid atherosclerosis had high population frequency and association with many risk factors. Among stenotic lesions, IMT of carotid arteries and risk factors, there was association with age, obesity, systemic hypertension, smoking, stroke, ABI < 0.9, carotid arterial occlusions, and kinking. On the other hand, although parietal manifestations of atherosclerosis are centered on stenosing plaques, the study of IMC hyperplastic behavior should be contained in the work-up protocol of the carotid system. Although IMT is not representative of atherosclerosis evolutionary stages, it has been widely used as a marker for diagnosis of systemic atherosclerosis onset and predictive for ischemic cardiovascular events, such as stroke and myocardial infarction.



Carotid atherosclerosis had high population frequency (52%) and association with many risk factors (age, obesity, stroke, ischemic heart disease, and smoking).



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Procópio de Freitas
Rua Visconde de Inhaúma, 2065, Bairro Jardim Sumaré
CEP 14025-100 - Ribeirão Preto, SP, Brazil

Manuscript received January 18, 2008, accepted October 20, 2008.



This study was conducted at Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo (USP), and at Escola de Ultra-Sonografia e Reciclagem Médica de Ribeirão Preto (EURP), Ribeirão Preto, SP, Brazil.
No conflicts of interest declared concerning the publication of this article.

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