Revista Adolescência e Saúde

Revista Oficial do Núcleo de Estudos da Saúde do Adolescente / UERJ

NESA Publicação oficial
ISSN: 2177-5281 (Online)

Vol. 15 nº 1 - Jan/Mar - 2018

Original Article Imprimir 

Páginas 80 a 88


Metabolic Syndrome in Adolescents with Systemic Lupus Erythematosus

Síndrome Metabólico en adolescentes con Lupus Eritematoso Sistémico

Síndrome Metabólica em adolescentes com Lúpus Eritematoso Sistêmico

Autores: Jorgiane das Graças Vilar de Araujo1; Flavio Sztajnbok2; Denise Tavares Giannini3

1. Mastering in Sciences by the College of Medical Sciences at University of the State of Rio de Janeiro (UERJ). Rio de Janeiro, RJ, Brazil. Nutritionist at the School of Health Sciences, Rio Grande University (Unigranrio). Duque de Caxias, RJ, Brazil
2. Doctorate in Clinical Medicine by the Federal University of Rio de Janeiro (UFRJ). Rheumatologist at the Department of Rheumatology, Center for Adolescent Health Studies (NESA), Pedro Ernesto University Hospital (HUPE), State University of Rio de Janeiro (UERJ). Rio de Janeiro, RJ, Brazil
3. Doctorate in Sciences from the State University of Rio de Janeiro (UERJ). Nutritionist at the Division of Nutrition in the Center for Adolescent Health Studies (NESA), Pedro Ernesto University Hospital (HUPE), State University of Rio de Janeiro (UERJ). Rio de Janeiro, RJ, Brazil

Correspondência:
Jorgiane das G. V. de Araujo
Estrada Professor Daltro Santos, 445, Campo Grande
Rio de Janeiro, RJ, Brasil. CEP: 23092-205
(jo@jvnutricionista.com.br)

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Keywords: Lupus Erythematosus, Systemic, metabolic syndrome X, adolescent.
Palabra Clave: Lúpus Eritematoso Sistémico, síndrome X metabólica, adolescente.
Descritores: Lúpus Eritematoso Sistêmico, síndrome X metabólica, adolescente.

Abstract:
OBJECTIVE: Determine the frequency of metabolic syndrome and its components in adolescents with systemic lupus erythematosus.
METHODS: A cross-sectional study was carried out at the Rheumatology Outpatient Clinic of the Center for the Study of Adolescent Health at Pedro Ernesto University Hospital. We analyzed adolescents from 10 to 19 years old with diagnosis of systemic lupus erythematosus. Metabolic syndrome was diagnosed through the criteria of the Internation Diabetes Federation. Were analyzed Clinical, sociodemographic, laboratorial variables, and physical activity.
RESULTS: The study evaluated 42 adolescents with a mean age of 16.8 ± 1.5 years, of which 37 (88%) were female and five (12%) were male. The Metabolic Syndrome was diagnosed in seven lupus patients (16.7%), all of whom were between 17 and 19 years old. Sedentarism, disease activity and unfavorable socioeconomic conditions were the variables most associated with the presence of metabolic syndrome in adolescents. Among the components that integrate it, high waist circumference, hypertension and low HDL-c were the most prevalent.
CONCLUSION: This study made it possible to conclude that the adolescents with the highest prevalence of metabolic syndrome belonged to the female sex, with ages ranging from 17 to 19 years old, attending high school, with a family income of less than three minimum wages. The most frequent clinical features were obesity, use of antimalarials, sedentary and with time of disease diagnosis in the period of 1 to 3 years.

Resumen:
OBJETIVO: Determinar La frecuencia de síndrome metabólico y de sus componentes en adolescentes con lupus eritematoso sistémico.
MÉTODOS: Fue realizado un estudio transversal en el ambulatorio de reumatología del Núcleo de Estudios de Salud del Adolescente del Hospital Universitario Pedro Ernesto. Fueron analizados adolescentes de 10 a 19 años con diagnóstico de lupus eritematoso sistémico. El síndrome metabólico fue diagnosticado a través de los criterios del International Diabetes Federation. Fueron analizadas variables clínicas, sociodemográficas, de laboratorio y actividad física.
RESULTADOS: El estudio evaluó 42 adolescentes con media de edad de 16,8 ± 1,5 años, siendo 37 (88%) del sexo femenino y cinco (12%) del sexo masculino. El Síndrome Metabólico fue diagnosticado en siete pacientes con lupus (16,7%), siendo todos éstos de la franja etaria entre 17 a 19 años. Sedentarismo, actividad de enfermedad y condiciones socioeconómicas desfavorables fueron las variables más asociadas a la presencia de síndrome metabólico en los adolescentes. Entre los componentes que la integran, la circunferencia de cintura elevada, hipertensión y HDL-c bajo fueron los más prevalentes.
CONCLUSIÓN: Este estudio posibilitó concluir que los adolescentes que presentaron mayor prevalencia de síndrome metabólico pertenecían al sexo femenino, con franja etaria entre 17 a 19 años, cursando enseñanza media, con renta familiar menor a tres salarios mínimos. Las características clínicas más frecuentes fueron la obesidad, uso de antimaláricos, sedentarios y con tiempo de diagnóstico de enfermedad en el período de 1 a 3 años.

Resumo:
OBJETIVO: Determinar a frequência de síndrome metabólica e de seus componentes em adolescentes com lúpus eritematoso sistêmico.
MÉTODOS: Foi realizado um estudo transversal no ambulatório de reumatologia do Núcleo de Estudos da Saúde do Adolescente do Hospital Universitário Pedro Ernesto. Foram analisados adolescentes de 10 a 19 anos com diagnóstico de lúpus eritematoso sistêmico. A síndrome metabólica foi diagnosticada através dos critérios do International Diabetes Federation. Foram analisadas variáveis clínicas, sociodemográficas, laboratoriais e atividade física.
RESULTADOS: O estudo avaliou 42 adolescentes com média de idade de 16,8 ± 1,5 anos, sendo 37 (88%) do sexo feminino e cinco (12%) do sexo masculino. A Síndrome Metabólica foi diagnosticada em sete pacientes lúpicos (16,7%), sendo todos estes da faixa etária entre 17 a 19 anos. Sedentarismo, atividade de doença e condições socioeconômicas desfavoráveis foram as variáveis mais associadas à presença de síndrome metabólica nos adolescentes. Dentre os componentes que a integram, a circunferência da cintura elevada, hipertensão e HDL-c baixo foram os mais prevalentes.
CONCLUSÃO: Este estudo possibilitou concluir que os adolescentes que apresentaram maior prevalência de síndrome metabólica pertenciam ao sexo feminino, com faixa etária entre 17 a 19 anos, cursando ensino médio, com renda familiar menor que três salários mínimos. As características clínicas mais frequentes foram a obesidade, uso de antimaláricos, sedentários e com tempo de diagnóstico de doença no período de 1 a 3 anos.

INTRODUCTION

Systemic Lupus Erythematosus (SLE) is an autoimmune, multisystem inflammatory disease of unknown origin characterized by the presence of several autoantibodies1. It is reported in the literature that lupus patients are more likely to develop cardiovascular events, although their mechanism is still unknown. It is proposed that lupus itself, as an inflammatory disease, triggers chronic activation of the immune system, with increased stimulation of inflammatory cytokines, leading to the formation of premature atherosclerosis2.

Among the modifiable risk factors for atherosclerosis in adolescents with SLE, obesity, systemic arterial hypertension (SAH), insulin resistance, diabetes mellitus, dyslipidemia - high low density lipoprotein - Low Density Lipoprotein (LDL), increased triglycerides (HDL), smoking, increased homocysteine and interleukins (IL-1), (IL-6) and (IL-8)³. Non-modifiable factors include age, sex, genetics, and family history. Modifiable cardiovascular risk factors are more prevalent in lupus patients, leading to changes in the vascular endothelium integrity, with presence in the active phase or remission of the disease4.

Metabolic syndrome (MS) is a set of risk factors for cardiovascular diseases, including abdominal obesity, insulin resistance, hypertension and dyslipidemia5. MS became a frequent disorder in Brazil, affecting about 7.5% to 30% of the Brazilian population, being considered a major public health problem6.

A study carried out with lupus patients showed a high prevalence of overweight, which increases the chance of SM7 development by 50%. It reinforces the magnitude with which these individuals are susceptible to the development of metabolic disorders throughout the therapy, being of great importance the early detection of metabolic alterations that enable measures to stimulate the improvement of the quality of life and health promotion8. the lack of studies on the metabolic profile of adolescents with SLE. In view of this, the objective of this study was to determine the frequency of MS, and its components in adolescents with SLE.


METHOD

A cross-sectional study was carried out at the Rheumatology outpatient clinic of the Center for the Study of Adolescent Health at the Pedro Ernesto University Hospital. All the adolescents diagnosed with SLE9 of both sexes, aged between 10 and 19 years, who signed the free and informed consent form, participated in the study. The exclusion criteria were inability to stay in orthostatism or in the supine position to perform the nutritional evaluation.

The anthropometric measures were weight (kg), measured by a Micheletti scale with a capacity of 200kg and a graduation of 0.05kg, and stature (cm) with the aid of a stadiometer fixed to the wall of the Sanny brand with an accuracy of 0, 1 cm. Body mass index (BMI) was calculated according to weight (kg) / height (m2), with a subsequent classification of nutritional status, according to criteria established for adolescents of the World Health Organization (WHO) in 200710. Waist circumference (CC) was used in millimeter inelastic tape at the midpoint between the last fixed rib and the upper border of the right iliac crest, measured at the end of a normal expiration. For the classification of CC, the parameters of Freedman11 were used. Criteria for diagnosis of MS were performed according to the recommendations of the International Diabetes Federation (IDF) 12 as shown in table 1.




Patients were selected in groups with one, two or more of two components of MS. The diagnostic criteria referred to by the IDF (2007)12 were abdominal obesity - which includes waist circumference increased according to a percentile> 90 for age and sex, triglycerides> 150mg / dl, HDL <40mg / dl, systolic blood pressure 130 and diastolic ≥ 80mmHg, or use of hypotensive medication, fasting glycemia ≥ 100mg / dl or use of hypoglycemic medication. For the evaluation of fasting glycemia, the enzymatic hexokinase method was used, for the dosage of triglycerides, total cholesterol and HDL was used the enzymatic colorimetric method. Laboratory tests were performed in the hospital's own laboratory after an indication of a 12-hour fast.

Data referring to schooling and family income were extracted from patients' charts. The arterial pressure (BP) was measured in the right arm with appropriate cuff, determined by the arm circumference (CB), covering approximately 80% of the distance between the olecranon and the acromion, using the oscillometric method, using the Omron 705 -IT®. Three measures were performed with a three-minute interval, after the teenager rested for five minutes. Adolescents with systolic and / or diastolic BP below the 90th percentile for height, gender and age were considered normotensive; with borderline BP, if systolic and / or diastolic BP were between the 90th and 95th percentiles; such as hypertension, systolic and / or diastolic BP above the 9513 percentile.

The Physical Activity Questionnaire 36 Questionnaire for Older Children (PAQ-C) was applied in the investigation of the level of physical activity. Those who scored> 300 minutes / week were classified as active and those <300 minutes / week, inactive. Subjects with a level above 2,100 minutes / week of physical activity were excluded from this variable14.

The SLEDAI index (Systemic Lupus Erythematosus Disease Activity Index) was used to determine disease activity in adolescents with SLE15 and a ≥ 3 cutoff value was used to classify disease activity. The use or not of corticosteroids and antimalarial was analyzed, adopting as a cutoff the continuous administration of at least one month of use16.

For the analysis of data, they were first stored in a spreadsheet of the Excel version 7 software. Later, they were analyzed through the software STATA version 10. The continuous variables were described by mean and standard deviation and the categorical ones, by proportion. The variables were tested using the Kolgomorov-Smirnov test to verify if they had a normal distribution. Those with normal distribution were compared using Student's t-test and those with non-parametric distribution using the Mann-Whitney test. For the categorical variables, the chi-square test was used. For all analyzes, a value of (P <0.05) was adopted for significance.


RESULTS

42 adolescents were analyzed, being 37 girls (88%) and 5 boys (12%). The mean age was 16.8 ± 1.5 years. As to the classification of nutritional status, a greater number of eutrophic individuals (57.1%) were followed, obese (26.2%), overweight (12%) and low weight (4.7%). It was observed that 24 adolescents used steroids (57.2%) and 37 antimalarials (88.1%). In relation to the disease activity, the SLEDAI index was altered in 23 patients (54.7%). The other results are shown in table 2.




In the individual analysis of the MS components, 15 adolescents (35.7%) presented two risk factors, 13 (30.9%) presented a risk factor and no patient presented the four components used in the IDF criteria. MS was diagnosed in seven patients (16.7%). Of these, five (71%) were female and two (29%) were male. Of the seven adolescents diagnosed with MS, all were between the ages of 17 and 19, and six of these (85%) had family income ≤ 3 minimum wages. In the same context, it was observed that in the SM group, five (71%) presented SLEDAI ≥ 3. As shown in table 3, the mean BMI was significantly higher in the individuals with SM presence (p = 0.006) when compared with the mean of those without MS (28.4kg / m2 vs. 23.6kg / m2). For CC, a statistically significant mean (p = 0.0006) was found in those with MS. As for fasting glycemia, it was higher in adolescents with MS. A relevant aspect in this study was the percentage of sedentary adolescents in the study (62.5%), and of these, 24% had MS. Table 4 shows the frequency of the SM components, where elevated blood pressure, hypertension and low HDL were the most prevalent.






DISCUSSION

In this study, the frequency of MS was 16.7%. Ford et al. found a predominance of 4.5% of MS using diagnostic IDF in a population of healthy American adolescents17. Another study carried out with 79 obese adolescents showed a prevalence of 45.5% of SM18. Regarding the diagnostic criteria for MS stratified in relation to nutritional status, in the present study it was confirmed that MS was more prevalent in obese patients (27.3%).

The percentage of overweight measured in the study was 38.2%. The research developed by Mina et al. with children and adolescents with SLE, showed a prevalence of 25% of obesity in a sample of 202 patients, where this metabolic disorder correlated with a negative impact on quality of life, including reduction of physical capacity, social and emotional dysfunction19. The study performed by Sinicato et al. Revealed a frequency of 31% of obese Lupus adolescent, associated with high levels of inflammatory cytokines, with statistical significance for TNF-alpha20.

The treatment of SLE is individualized with respect to administered drugs and their dosages, depending on the degree of organ or tissue impairment21. Glucocorticoids are the drugs most used in the treatment of SLE, and their daily doses will differ according to individualized protocol22. According to a study by Mok et al., Which evaluated 29 lupus patients for seismic, it was observed that those who used high doses of corticosteroids had a correlation with changes in BMI, increase of fat percentage and reduction of lean mass23. In this study, more than half of lupus adolescents used steroids and most used antimalarials. A study by Reis et al.24 found a frequency of 93.7% of prednisone use and 69.6% of antimalarials.

The frequency of adolescents considered active according to IPAQ-C was 37.5% (n = 15). Considering the total sample, about 62.5% (n = 25) of the adolescents analyzed were considered sedentary, and of these, 24% (6) had MS, corroborating the importance of practicing physical activity in the prevention of risk factors for MS . The literature reinforces the importance of improving the body composition of lupus patients with physical activity, as well as resistance to exercise, better cardiorespiratory capacity and quality of life, without stimulating disease activity25.

The SLEDAI index, used to classify disease activity, was altered by more than 50% in the sample, indicating disease activity. In the research performed with lupus women in the University Hospital of the Federal University of Mato Grosso do Sul (HU-UFMS), there was a 22.1% change26.

After analysis of the components alone, CHD was altered in 31% of adolescents with lupus. It is assumed that CC elevation becomes an aggravating factor of MS in children and adolescents and could be used to identify risk of CVD in clinical practice27.

Mean fasting blood glucose levels remained higher in adolescents with MS when compared to those without MS. A study by Sánchez-Pérez et al. verified the presence of IR through HOMA-IR and C-peptide analyzes in individuals with SLE, when compared to the control group28. Although our data have not verified IR in lupus adolescents, it is known that it is important to periodically monitor this parameter as a form of prevention for chronic non-communicable diseases, such as Diabetes mellitus29.

Elevated levels of LDL cholesterol and low HDL are closely related to the atherogenesis process30. However, in this study no significant value was found that related HDL to MS. However, the values of LDL and total cholesterol (CT), although not part of the diagnosis recommended by the IDF, remained high in those with SM. The presence of dyslipidemia aggravates the progression of atherosclerosis, especially when the levels of CT, LDL and TG are high and HDL is reduced31.

HBP is an independent risk factor for the occurrence of atherosclerotic vascular damage in lupus. Rahman et al. described an important association between hypertension, hypercholesterolemia and vascular events in SLE patients32. In the mentioned study, 50% of the patients presented alterations in BP. In a study by Telles et al., The most prevalent risk factor for CVD in lupus patients was hypertension, present in 48.8% of the individuals studied33.


CONCLUSION

In the present study it was possible to conclude that the individuals with the highest prevalence of MS were female adolescents, with ages ranging from 17 to 19 years old, attending high school, family income less than three minimum wages, obese, using antimalarial, sedentary and with disease time ranging from one to three years. As a limitation of the study, the absence of individual doses of corticosteroids used by adolescents during the research is exposed.

The metabolic syndrome is a serious public health disorder, and it is extremely important to monitor individuals at metabolic risk so that prevention and control measures can be established. Particularly, the young population with SLE may present along the therapeutic trajectory, metabolic dysfunctions with significant complications, and early monitoring to alleviate future intercurrences, especially the prevention of NCDs. In addition, healthy lifestyles, such as physical activity and balanced eating, are paramount for maintaining proper nutritional status. Therefore, this work alerts to the screening of MS in adolescents with SLE, so that more attention is paid to the early detection of metabolic abnormalities.


REFERENCES

1. Borba EF, Latorre LC, Brenol JC, Kayser C, Silva NA, Zimmermann AF et al. Consenso de lúpus eritematoso sistêmico. RevBrasReumatol 2008; 48(4):196-207.

2. Thomas GN, Tam LS, Tomlinson B, Li EK. Accelerated atherosclerosis in patients with systemic lupus erythematosus: A review of the causes and possible prevention. HKMJ 2002; 8:26-32.

3. Borba EF, Bonfá E. Dyslipoproteinemias in systemic lupus erythematosus: influence of disease, activity, and anticardiolipin antibodies. Lupus 1997; 6:533-539.

4. Borba EF, Bonfá E, Vinagre CG, Ramires JAF, Maranhão RC. Chylomicron metabolism in markedly altered in systemic lupus erythematosus. Arthritis Rheum 2000; 43:1033-1040.

5. Sociedade Brasileira de Hipertensão. I Diretriz Brasileira de Diagnóstico e Tratamento da Síndrome Metabólica. Revista da Sociedade Brasileira de Hipertensão 2004; 7:122-162

6. Oliveira EP, Souza MLA, Lima MDA. Prevalência de síndrome metabólica em uma área rural do semi-árido baiano. ArqBrasEndocrinolMetab 2006; 50:456-465.

7. Chung CP, Avalos I, Oeser A, Gebretsadik T, Shintani A, Raggi P, et al. High prevalence of the metabolic syndrome in patients with systemic lupus erythematosus: association with disease characteristics and cardiovascular risk factors. Ann Rheum Dis 2007; 66:208-214.

8. Chaiamnuay S, Bertoli AM, Fernandez MM, Apte M, Vilá LM, Reveille JD, et al. The impact of increased body mass index on systemic lupus erythematosus: data from LUMINA, a multiethnic cohort (LUMINA XLVI). J ClinRheumatol 2007; 13:128-133.

9. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. ArthritisRheum 1997; 40:1725.

10. World Health Organization. Growth reference data for 5-19 years, WHO reference 2007. Acesso em 25 de maio de 2013.

11. Freedman DS, Serdula MK, Srinivasan SR, Berenson, GS. Relation of circumferences and skinfold thickness to lipid and insulin concentrations in children and adolescents: the Bogalusa Heart Study. Am J ClinNutr 1999; 69:308-317.

12. Zimmet P, Alberti KGMM, Kaufman F, Tajima N, Silink M, Arslanian S, et al. DF Consensus Group. The metabolic syndrome in children and adolescents - an IDF consensus report. Pediatric Diabetes2007;8(5): 299-306.

13. National High Blood Pressure Education Program Working Group on Hipertension Control in Children and Adolescents. The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 2004;114:555-576.

14. Kowalski KC, Crocker PRE, Donen RM. The Physical Activity Questionnaire for Older Children (PAQ-C) and Adolescents (PAQ-A) Manual. College of Kinesiology. University of Saskatchewan, Canadá, 2004.

15. Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH. Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. ArthritisRheum 1992; 35:630-640.

16. Bruce IN. Factors that contribute to accelerated atherosclerosis and premature coronary heart disease in systemic lupus erythematosus. Rheumatology (Oxford) 2005; 44:1492-1502.

17. Ford ES, Li C, Zhao G, Pearson WS, Mokdad AH.  Prevalence of the metabolic syndrome among U.S. adolescents using the definition from the International Diabetes Federation. Diabetes Care 2008; 31(3):587-589.

18. Mina R, Klein-Gitelman, MS, Nelson, S, Eberhard BA, Higgins G, Singer NG, et al. Effects of obesity on health-related quality of life in juvenile-onset systemic lupus erythematosus. Lupus 2015; 24:191-197.

19. Sinicato NA, Postal M, Peres FA, Peliçari KO, Marini R, Santos AO, et al. Obesity and Cytokines in Childhood-Onset Systemic Lupus Erythematosus. Journal of Immunology Research 2014; 1-6.

20. Sato E.I. Lúpus eritematoso sistêmico (LES). In: Sato EI. Guia de reumatologia. Barueri: Manole, 2004:146 -152.

21. Gobato AO, Vasques ACJ, Zambon MP, Barros Filho AA, Hessel G. Síndrome metabólica e resistência à insulina em adolescentes obesos. Rev Paul Pediatr 2014; 32:55-62.

22. Kirou KA, Boumpas DT: Systemic glucocorticoid therapy in systemic lupus erythematosus. In: Wallace DJ, Hahn BH (Eds.) Dubois lupus erythematosus. 7 ed. Philadelphia: Lippincott Williams & Wilkins; 2007:1175-1197.

23. Mok CC, To CH, Ma KM. Changes in body composition after glucocorticoid therapy in patients with systemic lupus erythematosus. Lupus 2008; 17:1018-1022.

24. Reis MG, Costa IP. Qualidade de vida relacionada à saúde em pacientes com lúpus eritematoso sistêmico no Centro-Oeste do Brasil. RevBrasReumatol 2010; 50:408-422.

25. Carvalho MRP, Sato EI, Tebexreni AS, Heidecher RT, Schenkman S, Neto TL. Effects of supervised cardiovascular training program on exercise tolerance, aerobic capacity and quality of life in patients with systemic lupus erythematosus. Arthritis Rheum 2005; 53:838-844.

26. Ayache DCG, Costa IPC. Traços de personalidade e suas alterações em mulheres com lúpus. Ver Bras Reumatol 2009;49:643-657.

27. Pitangueira, JCD, Silva, LR, Santana, MLP, Silva MCM, Costa PRF, Almeida VD. Metabolic syndrome and associated factors in children and adolescents. Nutr Hosp 2014; 29:865-872.

28. Sánchez-Perez H, Tejera-Segura B, de Vera-González A, González-Delgado A, Olmos JM, Hernández JL. Insulin resistance in systemic lupus erythematosus patients: contributing factors and relationship with subclinical atherosclerosis. Clin Exp Rheumatol 2017; 35(6):885-892.

29. Sinha R, Fisch G, Teague B, Tamborlane WV, Banyas B, Allen K, et al. Prevalence of impaired glucose tolerance among children and adolescents with marked obesity. N Engl J Med 2002; 346:802-810.

30. Ettinger WH, Goldberg AP, Applebaum-Bowden D, Hazzard WR. Dyslipoproteinemia in systemic lupus erythematosus. Effectofcorticosteroids. Am J Med 1987; 83:503-508.

31. Malcon C, Achaval M, Komlos F, Partata W, Sauressig M, Ramirez G, et al. GMP protects against quinolinic acid-induced loss of NADPH- diaphorase- positive cells in the rat striatum. Neurosci Lett 1997; 225:145-148.

32. Rahman P, Aguero S, Gladman DD, Hallett D, Urowitz MB. Vascular events in hypertensive patients with systemic lupus erythematosus. Lupus 2000; 9:672-675.

33. Telles RW, Lanna CD, Ferreira GA, Carvalho MAP, Ribeiro AL. Frequência de doença cardiovascular aterosclerótica e de seus fatores de risco em pacientes com lúpus eritematoso sistêmico. Rev Bras de Reumatologia 2007; 47:165-172.
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