Prevalence and risk factors of symptomatic and asymptomatic peripheral arterial disease in a tertiary care hospital, Rio de Janeiro, Brazil

Abstracts

BACKGROUND: Peripheral arterial disease (PAD) is defined as an ankle-brachial index (ABI) < 0.90 in individuals aged 40 years or over. Prevalence is known to increase with age. OBJECTIVE: To detect the prevalence of asymptomatic and symptomatic PAD using ABI, in association with risk factors. METHODS: A descriptive cohort of patients ≥ 30 years old was identified at the outpatient angiology clinic of a tertiary referral center, from December 2006 to December 2007. Previous pathologies and risk factors were analyzed in relation to PAD prevalence. ABI < 0.90 and a specific questionnaire defined symptomatic PAD with claudication, and asymptomatic PAD without claudication, both in comparison with patients without PAD (ABI 0.90-1.30). Statistical analyses were performed with SPSS, considering p < 0.05. RESULTS: Of the 407 patients, 248 had PAD; 52.2% were females, with a mean age of 70.1±10.2 years (p < 0.005). PAD prevalence was 60.9% (95%CI 56-60), divided as follows: asymptomatic, 10.1% (95%CI 6.3-13.8); and symptomatic, 89.9% (95%CI 86.2-93.7). Among the symptomatic patients, 32.2% (95%CI 26.4-38.1) presented critical ischemia. Age- and sex-adjusted analyses revealed a dramatically increased prevalence in patients aged 55-74 years, with a predominance of female patients aged > 74 years (1.35:1). The prevalence of asymptomatic and symptomatic PAD was affected by smoking, hypertension, diabetes (both self-reported and confirmed), obesity, acute coronary heart disease and stroke (p < 0005). Mean ABI was lower in symptomatic PAD (0.57±0.17) (p < 0.005). CONCLUSION: ABI was able to detect PAD with variable degrees of severity, associated with risk factors, by identifying symptomatic and asymptomatic PAD patients at a tertiary center.

Peripheral arterial disease, symptomatic, asymptomatic; diagnostic; ankle-brachial index; prevalence; risk factors

CONTEXTO: Doença arterial periférica é caracterizada pelo índice tornozelo-braquial (ITB) < 0,90, em indivíduos ≥ 40 anos, aumentando a prevalência com a idade. OBJETIVO: Detectar a prevalência de doença arterial periférica assintomática e sintomática, com introdução do ITB, associada a fatores de risco demarcados. MÉTODOS: Coorte descritiva identificada em unidade hospitalar terciária de angiologia, de dezembro de 2006 a dezembro de 2007, com idade ≥ 30 anos. Doenças pregressas e fatores de risco foram analisados associados à prevalência. ITB < 0,90 e questionário padronizado definiram doença arterial periférica sintomática com claudicação e assintomática com ausência de claudicação, ambas comparadas aos sem doença arterial periférica (ITB 0,90-1,30). A análise estatística utilizou programa SPSS, com significância de p < 0,05. RESULTADOS: Dos 407 pacientes, 248 apresentaram doença arterial periférica, sendo 52,2% do sexo feminino, com média de idade de 70,1±10,2 anos (p < 0,005). A prevalência de 60,9% (IC95% 56-66) foi subdividida em: assintomática, 10,1% (IC95% 6,3-13,8); e sintomática, 89,9% (IC95% 86,2-93,7). Destes, 32,2% (IC95% 26,4-38,1) apresentaram isquemia crítica. Ajustada por sexo e idade, a prevalência aumenta significativamente entre 55-74 anos, com predomínio do feminino (1,35:1) nos indivíduos acima de 74 anos. A prevalência dos assintomáticos e sintomáticos foi influenciada por tabagismo, hipertensão, diabéticos autorreferidos e confirmados, sobrepeso, infarto agudo do miocárdio e acidente vascular encefálico (p < 0,005). A média do ITB foi mais baixa nos sintomáticos (0,57±0,17) (p < 0,005). CONCLUSÃO: O ITB detectou doença arterial periférica com graus variáveis de gravidade associada a fatores de risco, identificando os assintomáticos não-claudicantes e os sintomáticos em unidade terciária.

Doença arterial periférica sintomática e assintomática; diagnóstico; índice tornozelo-braquial; prevalência; fatores de risco

ORIGINAL ARTICLE

Prevalence and risk factors of symptomatic and asymptomatic peripheral arterial disease in a tertiary care hospital, Rio de Janeiro, Brazil

Marilia Duarte Brandão Panico^I; Ethel Stambovsky Spichler^II; Mario Fritsch Neves^III; Liana Wernersbach Pinto^VI; David Spichler^V

^IChefe, Disciplina de Angiologia, Faculdade de Ciências Médicas, Hospital Universitário Pedro Ernesto (HUPE), Universidade do Estado do Rio de Janeiro (UERJ), Rio de Janeiro, RJ, Brazil

^IIProfessora titular visitante, Faculdade de Ciências Médicas, HUPE, UERJ, Rio de Janeiro, RJ, Brazil

^IIIDoutor. Professor e chefe, Departamento de Clínica Médica, Faculdade de Ciências Médicas, HUPE, UERJ, Rio de Janeiro, RJ, Brazil

^IVPesquisadora, Saúde Pública, Centro Latino-Americano de Estudos de Violência e Saúde Jorge Careli (CLAVES), Escola Nacional de Saúde Pública (ENSP), Fundação Oswaldo Cruz (FIOCRUZ), Rio de Janeiro, RJ, Brazil

^VLivre-docente, Cirurgia Vascular, Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Rio de Janeiro, RJ, Brazil

^{Correspondence}

ABSTRACT

Background: Peripheral arterial disease (PAD) is defined as an ankle-brachial index (ABI) < 0.90 in individuals aged 40 years or over. Prevalence is known to increase with age.

Objective: To detect the prevalence of asymptomatic and symptomatic PAD, using ABI, in association with risk factors.

Methods: A descriptive cohort of patients ≥ 30 years old was identified at the outpatient angiology clinic of a tertiary referral center, from December 2006 to December 2007. Previous pathologies and risk factors were analyzed in relation to PAD prevalence. ABI < 0.90 and a specific questionnaire defined symptomatic PAD with claudication, and asymptomatic PAD without claudication, both in comparison with patients without PAD (ABI 0.90-1.30). Statistical analyses were performed with SPSS, considering p < 0.05.

Results: Of the 407 patients, 248 had PAD; 54% were females, with a mean age of 70.1±10.2 years (p < 0.005). PAD prevalence was 60.9% (95%CI 56-66), divided as follows: asymptomatic, 10.1% (95%CI 6.3-13.8); and symptomatic, 89.9% (95%CI 86.2-93.7). Among the symptomatic patients, 32.2% (95%CI 26.4-38.1) presented critical ischemia. Age- and sex-adjusted analyses revealed a dramatically increased prevalence in patients aged 55-74 years, with a predominance of female patients aged > 74 years (1.35:1). The prevalence of asymptomatic and symptomatic PAD was affected by smoking, hypertension, diabetes (both self-reported and confirmed), obesity, acute coronary heart disease and stroke (p < 0.005). Mean ABI was lower in symptomatic PAD (0.57±0.17) (p < 0.005).

Conclusion: ABI was able to detect PAD with variable degrees of severity, associated with risk factors, by identifying symptomatic and asymptomatic PAD patients at a tertiary center.

Keywords: Peripheral arterial disease, symptomatic, asymptomatic, diagnostic, ankle-brachial index, prevalence, risk factors.

Introduction

Peripheral arterial disease (PAD) affects 8 million Americans, who often experience intermittent claudication. The ankle-brachial index (ABI) < 0.90 is regarded as a reliable and accurate measure both for the diagnosis and as a marker of PAD progression.^1-3 However, 20 to 50% are detected as asymptomatic PAD.⁴

An overview described by Weitz et al.,⁵ was endorsed by several studies.^4,6-9 These authors have outlined the progression of PAD, shown in Figura 1, updated by Hirsch et al.⁴

The incidence of amputations in the city of Rio de Janeiro, southeastern Brazil, as an unfavorable outcome, presented rates of 31/100,000 inhabitants, 209/100,000 diabetic patients and 359/100,000 PAD patients, the latter being the main etiology, with an incidence of 56.4% among 65-year-old individuals.^10,11 Diagnostic accuracy compared ABI with gold standard, angiography, concluding that ABI was superior regarding hemodynamic vs. morphological information.¹²

Objective

To detect the prevalence and risk factors of symptomatic and asymptomatic PAD, using ABI, in association with predetermined risk factors.

Methods

The study sample, a descriptive cohort, was identified at the Angiology Unit of Hospital Universitário Pedro Ernesto (HUPE), at Universidade do Estado do Rio de Janeiro (UERJ), Brazil, between December 2006 and December 2007. The study project was submitted and approved by the Research Ethics Committee of HUPE, and all patients signed an informed consent form.

Inclusion criteria predetermined age ≥ 30 years and a risk-factor profile,¹³ excluding pseudoclaudications.¹⁴ Age (stratified, 30-54, 55-74 and > 74), sex, race (white, nonwhite), smoking (smoker, ex-smoker, and nonsmoker), hypertension, and diabetes were self-reported. Previous cardiovascular diseases, such as acute coronary heart disease and stroke, were considered as selected risk factors. Diabetes mellitus was either self-reported, with or without hypoglycemic therapy, or glucose-confirmed. Diagnostic criteria: fasting glycemia ≥ 126 mg/dL and casual glycemia ≥ 200 mg/dL.¹⁵ In the analysis of diabetes mellitus and symptomatic PAD, these above-mentioned criteria were considered in addition to hypoglycemic therapy. Regarding systemic arterial hypertension, criteria were: systolic blood pressure ≥ 140 mmHg and/or diastolic blood pressure ≥ 90 mmHg,¹⁶ or whether controlled with antihypertensive drugs or self-reported.

For body mass index (BMI = kg/m²), criteria were: ≥ 19; 20-24.9; 25-29.9; and ≥ 30 kg/m², overweight being defined as 25-29.9, and obesity as ≥ 30,¹⁷ as well as for waist circumference (visceral adiposity): ≥ 102 cm (men) and ≥ 88 cm (women).¹⁸

ABI, calculated by dividing the highest systolic blood pressure of the ankle (dorsalis pedis or posterior tibial) by the highest of the left and right arm brachial systolic blood pressures, after lying supine at rest for 5 minutes,^1,2 was measured using a Parks Electronics^® ultrasonic blood flow detector, with a 8.5 MHz probe. The following was evaluated: arm brachial, dorsalis pedis and posterior tibial, separately, calculated individually for each extremity, with PAD definition being < 0.90, the lowest values considered. Analysis was stratified as follows: normal, 0.90-1.30 (> 1.30 non-compressible artery); with PAD subdivided as: incipient (< 0.90-0.80), mild (0.79-0.70), moderate (0.69-0.50), and severe (< 0.50) stenosis. This analysis was adapted from the diagnostic criteria by the American Diabetes Association (ADA).³

A standardized questionnaire, adapted from the San Diego Claudication Questionnaire,¹⁹ identified the prevalence of intermittent claudication in the lower limb, classifying as classic claudication and/or poor functioning when walking without pain.

Symptomatic PAD: ABI < 0.90 and claudication; asymptomatic PAD: ABI < 0.90 without claudication; both with degree of severity according to decrease in ABI; and control group without PAD and ABI 0.90-1.30.⁴

Statistical analysis was performed with the Statistical Package for the Social Sciences (SPSS). The Mann-Whitney test was used when variables were measured, at least, at ordinal level. Morbidity factors were evaluated using relative risk (RR). When at nominal level, the Mantel-Haenszel chi-square test was used, and, when this was invalid, we reduced table order or used the Fisher's exact test, in the case of irreducible tables (2 x 2). Odds ratio (OR), adjusted with 95% confidence interval (95%CI), was estimated with logistic regression model in the analysis of risk factors and associated pathologies. Statistical significance was p < 0.05.

Results

The sample was composed of 407 patients, ABI < 0.90 with DAP (n = 248) and ABI 0.90-1.30 without DAP (n = 159). Most patients were women (52.2%), and mean age was 70.1±10.2 and 65.8±10.4 years, patients with and without DAP, respectively (p < 0.001). Prevalence estimative was obtained, as well as by 95%CI (with ABI < 0.90), reaching a value of 60.9 (56-66). Classes were grouped as follows: symptomatic, with 89.9% (86.2-93.7); resulting from critical ischemia, with 32.2% (26.4-38.1); and asymptomatic, with 10.1% (6.3-13.8). Symptomatic patients with typical claudication was, therefore, nine fold than the asymptomatic. Critical ischemia (ABI < 0.50, symptomatic subgroup) corresponded to 32% of these patients. We underscore the importance of detecting asymptomatic patients with significant prevalence in a population attending a health care facility at a university hospital. Figure 2 shows an analysis of prevalence adjusted for sex and age, an estimation that increases as age advances, both in men and women.

Among patients aged 55-74 and patients aged 30-54 years, the first group showed a 20-fold and an 18-fold increase for men and women, respectively. However, an inverse relation was observed for patients aged > 74 years, with female predominance (1.35:1). Demographic and anthropometric characteristics associated with symptomatic, asymptomatic, and without PAD groups are described in Table 1.

Table 1
– Patients with and without PAD according to demographic and anthropometric characteristics

Characteristics	PAD (n = 248)		Without PAD (n = 159)	p (χ2)
	Symptomatic (n = 223) n (%)	Asymptomatic (n = 25) n (%)
Male	107 (48.0)	8 (32)	55 (34.6)	< 0.019
Age 55 to 74 years	133 (59.6)	16 (64)	112 (70.4)	< 0.001
BMI 25 to 29.9 kg/m2	88 (39.5)	9 (36)	66 (41.5)	< 0.004

The influence of the 55-74-year age group, 59.6 and 64% in symptomatic and asymptomatic, respectively, as well as of male sex, was considered significant (p < 0.001), although the same was not observed regarding race. Overweight was positively associated with prevalence, what had not occurred regarding visceral adiposity. A BMI of 19.9 to 25-29.9 increased prevalence by over five times, whereas diabetes mellitus increased prevalence by one and a half time, when compared to those without PAD.

The variables described in Table 2, in an analysis of pre-morbid history, confirmed that systemic arterial hypertension and diabetes mellitus are related to both symptomatic and asymptomatic patients, compared to patients without PAD, with their respective RR. All variables significantly affected PAD prevalence (p < 0.001).

Table 2
– Patients with and without PAD according to pre-morbid history, DM and
arterial hypertension

Characteristics	PAD (n = 248)		Without PAD (n = 159) n (%)	RR (95%CI)	p (χ2)
	Symptomatic (n = 223) n (%)	Asymptomatic (n = 25) n (%)
Hypertension*	177 (80.1)	18 (72)	103 (65.6)	1.34 (1.02-1.70)	< 0.002
Stroke	27 (12.,2)	2 (8.3)	6 (3.8)	1.40 (1.10-1.60)	< 0.005
Acute coronary heart disease	73 (33)	6 (25)	26 (16.4)	1.35 (1.14-1.55)	< 0.001
Smoker/ex-smoker	162 (73)	13 (52)	113 (71.1)	2.03 (1.65-2.43)	< 0.001
DM (mg/dL)	88 (30.9)	6 (24.0)	19 (19.6)	1.13 (1.01-1.26)	< 0.025
Hypertension (mmHg)	168 (75.3)	19 (76)	84 (52.8)	1.53 (1.26-1.90)	< 0.001

Smoking RR affecting ABI < 0.90, both in symptomatic and asymptomatic groups, was twice as high as that of nonsmokers. Traditional cardiovascular risk factors were associated with PAD, with OR ranging from 2.03, 2.36, 2.74 and 3.30 for self-reported hypertension, acute coronary heart disease, confirmed systemic arterial hypertension, and stroke, with their respective 95%CI, as shown in Figure 3.

It was demonstrated an OR for PAD ranging from two to three times, except for smoking, which contributed with a 6-fold increased risk. An analysis of the selected risk factors and ABI, as mean and standard deviation, is described in Table 3.

Table 3
– Mean and standard deviation of selected risk factors and ABI

Characteristics	PAD (n = 248)		Without PAD (n = 159) Mean (SD)	p (χ2)
	Symptomatic (n = 223) Mean (SD)	Asymptomatic (n = 25) Mean (SD)
Age (years)	71 (10)	69 (13)	65.8 (10.4)	< 0.001
Glycemia (mg/dL)	124 (53.3)	116 (38)	117.5 (47.3)	< 0.025
Systolic blood pressure (mmHg)	156 (28)	150 (41)	138.6 (23.2)	< 0.002
Systolic blood pressure (mmHg)	88 (10)	85 (13)	83.9 (7.3)	< 0.002
ABI	0.57 (0.17)	0.70 (0.16)	1.04 (0.12)	< 0.000

ABI = ankle-brachial index; PAD = peripheral arterial disease; SD = standard deviation.

Symptomatic and asymptomatic PAD showed more advanced age, 71±10 and 69±13 years, respectively, when compared to the group without PAD, 65.8±10.4 years, with a significant influence (p < 0.001). Concerning glycemia, such difference is not so evident, although significantly associated with the symptomatic, asymptomatic and without PAD groups (p < 0.025). Systolic and diastolic blood pressures were associated with symptomatic and asymptomatic patients when compared to those without PAD (p < 0.001). Mean ABI was lower in symptomatic (0.57±0.17) than in asymptomatic (0.7±0.16) patients (p < 0.001). There was an agreement between the two PAD categories, analyzed according to the adaptation from the San Diego Claudication Questionnaire,¹⁹ indicating a correlation between lower ABI means and the presence or absence of claudication, with significance in relation to the highest ABI mean in patients without PAD (p < 0.001).

Figures 4A and 4B show the logistic regression analysis of the association of systolic blood pressure and glycemia, with ABI as the dependent variable. An inversely proportional relation is observed, i.e., the higher the systolic blood pressure (150-180) the lower the ABI (0.60 to 0.40) (p < 0.001).

Figure 4C

Regarding glycemia, values were lower and clustered, around 125-130 mg/dL, with ABI between 0.70 and 0.40 (p < 0.025).

Discussion

Hirsch et al.²⁰ demonstrated that PAD is easily detected and diagnosed by an ABI < 0.90 in primary health care, with a prevalence of 29% and underreporting in more than 50%, which may result in complications that are not treated appropriately at a proper time, increasing cardiovascular morbidity, mortality and amputation of the lower limb. The authors estimated that 8 to 12 million people will need primary diagnosis and appropriate clinical intervention.

Criqui et al.¹⁹ studied a correlation between symptoms and ABI in the diagnosis of PAD using the San Diego Population Claudication Questionnaire. Symptoms resulted from intermittent claudication progressing into critical ischemia. Patients who improved showed an ABI very close to normal, due to the development of sufficient collateral circulation; thus, they were not referred to clinical or laboratory evaluation, characterizing underreporting.

In the general population, 10% presented classic symptoms of intermittent claudication, 40% did not present such symptoms, and the remaining 50% reported atypical symptoms.^4,13 McDermott et al.²¹ reported that, in a population of elderly women, asymptomatic PAD is independently associated with function of the lower limbs. Lange et al.,²² in turn, discussed different methodologies, using duplex scanning in the antecubital fossa, to determine systolic blood pressure, and in the anterior and posterior tibial arteries, diversifying the criteria for ABI calculation:

1) The highest tibial blood pressure above the ankle.

2) Only systolic blood pressure of posterior tibial.

3) Only systolic blood pressure of anterior or dorsal tibial.

4) After exercising, only in posterior tibial artery.

5) A difference of 10 mmHg was expressed between the upper limbs, suggesting that the highest value should be used to determine ABI.

The authors also studied prevalence in Germany, in 34 primary care centers, evaluating 50,000 individuals. PAD was present in 9.2%, including patients with claudication (4.6%), comparing patients with Rose questionnaire (2.3%).²² Using the five methods described, they showed prevalence ranging between 18, 34.5, 29, 24.2, and 27.8%, respectively. Another influence on prevalence concerns the center, whether it is a primary, secondary or tertiary care center. Nunes et al.,²³ in a tertiary care center, demonstrated prevalence of 34.3% in patients referred to coronary angiography. The results from the present study showed a prevalence of 60.9%, i.e., twice as much as that described in the studies by Nunes et al.²³ and Lange et al.,²² who measured only systolic blood pressure of posterior tibial artery. Increased prevalence in this study might have resulted from the fact that the study was carried out in a specific university tertiary care center, and patients referred to clinical evaluation were smokers with previous cardiovascular diseases.

This sample estimated asymptomatic in 10.1%; symptomatic, 89.9%; and of the latter, with critical ischemia, 32.2%; whereas Bhatt et al.²⁴ recorded that, despite risks and prevalence, only 25% are on treatment.

McDermott et al.²⁵ reported that 8 million Americans presented PAD with classic manifestation of intermittent claudication. However, when using ABI < 0.90, 20 to 50% are asymptomatic; pointing out that asymptomatic clinical significance is yet to be defined.

In the present study sample, we found 10.1% with ABI < 0.90, without claudication, which represents half of the 20% reported by McDermott et al.,²⁵ probably because it is a tertiary care center. Another observation concerns the fact that the asymptomatic patients in the present study showed an ABI of 0.70±0.16, similar to that of 0.63±0.16 reported by McDermott et al.²⁵ and described as close to normal by Criqui et al.,¹⁹ whereas in asymptomatic patients with intermittent claudication we found a lower ABI (0.57±0.17).

In asymptomatic patients, the development of a sufficient collateral circulation may have occurred, beyond the limitation of work-related activities, thus reducing the patient's quality of life. The results from this study indicate that asymptomatic patients do not have a benign condition, since they referred previous acute coronary heart disease and stroke in 12.2 and 8.3%. However, cardiovascular risk factors are similar. Diabetes mellitus and smoking significantly affected PAD.¹⁹ Diabetes mellitus and smoking significantly affected PAD.19 In the present study, smoking affected ABI < 0.90 both in asymptomatic and symptomatic patients, with RR and OR twice and six times as high as that in nonsmokers, respectively. Self-reported arterial hypertension, confirmed arterial hypertension, acute coronary heart disease, and stroke presented OR of 2.03, 2.74, 2.36 and 3.30, respectively.

Several studies suggest that prevalence is similar between men and women.^3-9 In our sample, female gender was prevalent only in individuals aged > 74years (1.35:1), probably due to a greater survival rate in this age group.

ADA³ reported prevalence of 20 and 29% in patients with PAD and diabetes, over 40 and 50 years old, respectively. In this study, prevalence of PAD with diabetes mellitus is one and a half time greater than in the population without PAD. However, such difference is not so evident, although significantly associated with symptomatic and asymptomatic PAD.

Dolan et al.²⁶ studied 460 PAD patients using ABI and questionnaire; 147 of these had diabetes and neuropathy, observing 4-m speed during 6-minute walk. Mean ABI was similar in PAD patients with and without diabetes. However, diabetic patients were younger, had a higher BMI, neuropathy, and more cardiovascular events than those patients with PAD alone. Diabetic patients showed less classic symptoms of intermittent claudication, walked a shorter distance and at a lower speed, possibly due to neuropathy, when compared to patients without diabetes mellitus.²⁶

In the present study, the results with BMI 25-29 kg/m² suggest that overweight was positively associated with PAD prevalence, although the same was not observed regarding visceral adiposity.

Selvin et al.²⁷ evaluated 2,174 subjects aged > 40 years with ABI < 0.90 for PAD diagnosis. The authors found a prevalence of 4.3% (95%CI 3.1-5.5), which corresponds to approximately 5 million individuals (95%CI 4 to 7 million). However, in individuals aged > 70 years prevalence was 14.5% (95%CI 10.8-18.2). The authors also pointed out that more than 95% presented at least one of the cardiovascular risk factors. Epidemiologic studies have demonstrated that approximately 2 to 3% of men and 1 to 2% of women aged ≥ 60 years have mild or moderate claudication.^4,5,14 Prevalence increases as age advances, and approximately 20% of those over 70 years old present PAD.²⁸ These patients will develop complications resulting from peripheral vascular occlusions. After 5 to 10 years, 1/3 of patients with claudication progress to critical ischemia, approximately 20% require vascular intervention, and 10% require primary amputation of the lower limb.^4,5,10,11,29

Mohler III,¹⁴ in a prognostic study, reported that ABI presents a correlation with the degree of PAD symptom progression, with cardiovascular events and cerebrovascular mortality.

Conclusion

This study highlights the importance of the introduction of ABI in the diagnosis of PAD, with degrees of obstruction graded as incipient, mild, moderate, and severe for symptomatic patients and the identification of asymptomatic ones, thus allowing interventions for predetermined risk factors and the control of complications resulting from these conditions.

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Article submitted Sep 01 2008, accepted for publication Jan 15 2009.

This study was carried out at Disciplina de Angiologia, Faculdade de Ciências Médicas, Hospital Universitário Pedro Ernesto (HUPE), Universidade do Estado do Rio de Janeiro (UERJ), Rio de Janeiro, RJ, Brazil.

No conflicts of interest declared concerning the publication of this article.

Publication Dates

• Publication in this collection
  05 June 2009
• Date of issue
  June 2009

History

• Accepted
  15 Jan 2009
• Received
  01 Sept 2008