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Nutritional aspects and cardiovascular risk in systemic lupus erythematosus

SUMMARY

OBJECTIVE:

Patients with systemic lupus erythematosus present with a higher number of classic risk factors for coronary diseases and a higher prevalence of metabolic syndrome resulting from the disease itself. To evaluate the nutritional indicators of the cardiovascular risk of patients with systemic lupus erythematosus by analyzing eating habits, anthropometry, laboratory data, and disease activity and to describe the prevalence of patients fulfilling the criteria for metabolic syndrome.

METHODS:

Anthropometric measurements including waist circumference, food recall, and laboratory tests.

RESULTS:

The population presented an insufficient daily intake of micronutrients. Anthropometry revealed that 37.5% of the patients were classified with degree II obesity by body mass index and 76.8% by abdominal obesity. Regarding metabolic syndrome, 18 patients (16%) fulfilled the diagnostic criteria.

CONCLUSIONS:

Individuals with systemic lupus erythematosus presented with increased risk factors, as determined using anthropometric measurements and laboratory tests, for cardiovascular disease, indicating the need for nutritional guidance in this population to reduce cardiovascular risk, increase the quality of life, and increase survival of these patients.

KEYWORDS:
Nutrition; Cardiovascular system; Systemic lupus erythematosus

INTRODUCTION

Systemic lupus erythematosus (SLE) is an autoimmune, chronic, multisystemic, relapsing-remitting autoimmune disease characterized by mucocutaneous lesions, hematological changes, and inflammation in joints, kidneys, serous membranes, and other organs associated with the presence of self-reactive antibodies and occurring predominantly in women. The Systemic Lupus International Collaborating Clinics Damage Index (SLICC) and the Systemic Lupus Erythematosus Disease Activity Index (SLEDAI) are used to evaluate chronicity and disease activity. Cardiovascular disease (CVD) is an important cause of premature death in patients with SLE11. Kostopoulou M, Nikolopoulos D, Parodis I, Bertsias G. Cardiovascular disease in systemic lupus erythematosus: recent data on epidemiology, risk factors and prevention. Curr Vasc Pharmacol. 2020;18(6):549-65. https://doi.org/10.2174/1570161118666191227101636
https://doi.org/https://doi.org/10.2174/...
. Compared to the general population, patients with SLE have a greater number of classic risk factors for CVD, such as obesity, dyslipidemia, and metabolic syndrome (MS), which are partly associated with nutritional aspects11. Kostopoulou M, Nikolopoulos D, Parodis I, Bertsias G. Cardiovascular disease in systemic lupus erythematosus: recent data on epidemiology, risk factors and prevention. Curr Vasc Pharmacol. 2020;18(6):549-65. https://doi.org/10.2174/1570161118666191227101636
https://doi.org/https://doi.org/10.2174/...
,22. Medina G, Vera-Lastra O, Peralta-Amaro AL, Jiménez-Arellano MP, Saavedra MA, Cruz-Domínguez MP, et al. Metabolic syndrome, autoimmunity and rheumatic diseases. Pharmacol Res. 2018;133:277-88. https://doi.org/10.1016/j.phrs.2018.01.009
https://doi.org/https://doi.org/10.1016/...
.

MS causes a 1.5-fold increase in overall mortality and a 2.5-fold increase in the risk for CVD11. Kostopoulou M, Nikolopoulos D, Parodis I, Bertsias G. Cardiovascular disease in systemic lupus erythematosus: recent data on epidemiology, risk factors and prevention. Curr Vasc Pharmacol. 2020;18(6):549-65. https://doi.org/10.2174/1570161118666191227101636
https://doi.org/https://doi.org/10.2174/...
,22. Medina G, Vera-Lastra O, Peralta-Amaro AL, Jiménez-Arellano MP, Saavedra MA, Cruz-Domínguez MP, et al. Metabolic syndrome, autoimmunity and rheumatic diseases. Pharmacol Res. 2018;133:277-88. https://doi.org/10.1016/j.phrs.2018.01.009
https://doi.org/https://doi.org/10.1016/...
, with a prevalence ranging from 20 to 28.4% in patients with SLE22. Medina G, Vera-Lastra O, Peralta-Amaro AL, Jiménez-Arellano MP, Saavedra MA, Cruz-Domínguez MP, et al. Metabolic syndrome, autoimmunity and rheumatic diseases. Pharmacol Res. 2018;133:277-88. https://doi.org/10.1016/j.phrs.2018.01.009
https://doi.org/https://doi.org/10.1016/...
,33. Mok CC, Tse SM, Chan KL, Ho LY. Effect of the metabolic syndrome on organ damage and mortality in patients with systemic lupus erythematosus: a longitudinal analysis. Clin Exp Rheumatol. 2018;36(3):389-95. PMID: 29148424. The prevalence of dyslipidemia in patients with SLE ranges from 36% at diagnosis to 60% or more after 3 years44. Szabó MZ, Szodoray P, Kiss E. Dyslipidemia in systemic lupus erythematosus. Immunol Res. 2017;65(2):543-50. https://doi.org/10.1007/s12026-016-8892-9
https://doi.org/https://doi.org/10.1007/...
,55. Atta AM, Silva JPCG, Santiago MB, Oliveira IS, Oliveira RC, Sousa Atta MLB. Clinical and laboratory aspects of dyslipidemia in Brazilian women with systemic lupus erythematosus. Clin Rheumat. 2018;37(6):1539-46. https://doi.org/10.1007/s10067-018-4051-0
https://doi.org/https://doi.org/10.1007/...
. Its occurrence is specifically related to inflammatory disease activity and corticosteroid use44. Szabó MZ, Szodoray P, Kiss E. Dyslipidemia in systemic lupus erythematosus. Immunol Res. 2017;65(2):543-50. https://doi.org/10.1007/s12026-016-8892-9
https://doi.org/https://doi.org/10.1007/...
. The treatment of systemic inflammation with corticosteroids, in addition to disordered eating habits and reduced physical activity, may increase the predisposition of accumulating body fat and of developing a coronary disease in patients with SLE. Abdominal obesity is commonly associated with the development of atheroma and CVD66. Monção CSA, Martins LN, Penteado MPS, Reis RCP, Santos FMM, Lanna CCD, et al. Incidence of cardiovascular risk factors in female patients with systemic lupus erythematosus: a 3-year follow-up cohort. Lupus. 2018;27(11):1790-98. https://doi.org/10.1177/0961203318790676
https://doi.org/https://doi.org/10.1177/...
.

Regarding nutritional aspects in SLE, a review article showed that patients with SLE can benefit from a nutritionally balanced diet to maintain ideal body weight and from effective calorie control to avoid insulin resistance, by increasing high-density lipoprotein (HDL) and decreasing triglyceride levels77. Klack K, Bonfa E, Borba Neto EF. Diet and nutritional aspects in systemic lupus erythematosus. Rev Bras Reumatol. 2012;52(3):384-408. PMID: 22641593.

In addition to dietary characteristics, the identification of anthropometric indicators helps in the early identification of nutritional aspects that increase the risk for CVD. The objective of this study was to evaluate the nutritional profile of patients with SLE by analyzing food intake, anthropometric indicators, and the association of disease activity and cardiovascular risk.

METHODS

Study design and population

This is a cross-sectional study with 112 patients diagnosed with SLE according to the diagnostic classification criteria described in 1982 and updated in 199788. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40(9):1725. https://doi.org/10.1002/art.1780400928
https://doi.org/https://doi.org/10.1002/...
. The studied population included random patients treated in an outpatient clinic created specifically for patients with SLE at the Rheumatology Service of the Hospital de Clínicas de Porto Alegre, Rio Grande do Sul, Brazil. The data were collected from May 2015 to February 2018. During routine consultations, patients were invited to participate in a study on the nutritional aspects of SLE to support the creation of future nutritional clinical strategies as treatment. All patients who agreed to participate signed an informed consent form. The exclusion criteria were the presence of metabolic modifying factors that could interfere with the nutritional evaluation, such as acquired immunodeficiency syndrome (AIDS) and being pregnant or breastfeeding at the time of evaluation.

Nutritional profile evaluation

The evaluation consisted of anthropometric, dietary, and laboratory measurements. Anthropometric data were measured according to the standards of the World Health Organization99. World Health Organization. Physical status: the use and interpretation of anthropometry. Report of a WHO expert committee. Geneva: World Health Organization; 1995.. Body mass index (BMI) was calculated using the formula BMI=weight/height22. Medina G, Vera-Lastra O, Peralta-Amaro AL, Jiménez-Arellano MP, Saavedra MA, Cruz-Domínguez MP, et al. Metabolic syndrome, autoimmunity and rheumatic diseases. Pharmacol Res. 2018;133:277-88. https://doi.org/10.1016/j.phrs.2018.01.009
https://doi.org/https://doi.org/10.1016/...
. Body fat percentage (BFP) was determined by body density using the equations proposed by Siri in 19611010. Siri WE. Body composition from fluid spaces and density. In: Brozec J, Henschel A (eds). Techniques for measuring body composition. Washington: National Academy of Science; 1961. p. 223-44.. Abdominal obesity was determined by waist circumference (WC) using the cutoff points of ≥90 cm for men and ≥80 cm for women1111. Alberti KGMM, Zimmet P, Shaw J. Metabolic syndrome--a new world-wide definition. A consensus statement from the international diabetes federation. Diabet Med. 2006;23(5):469-80. https://doi.org/10.1111/j.1464-5491.2006.01858.x
https://doi.org/https://doi.org/10.1111/...
. An anthropometric variable called metabolic risk (MR) was created for the present study and defined as the group of participants concomitantly presenting all the anthropometric classifications of obesity.

Dietary indicators were evaluated using 24-hour dietary recall, which was subsequently processed in the DietWin Nutritional Analysis software version 2.0®.

The criteria for MS classification were based on the identification of three or more factors in the same person: abdominal obesity (≥90 cm in men and ≥80 cm in women); HDL-cholesterol <40 mg/dL in men and <50 mg/dL in women; triglycerides ≥150 mg/dL; systemic blood pressure ≥135/85 mmHg or use of antihypertensive drugs; and, fasting glucose ≥110 mg/dL1212. Alberti KGMM, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120(16):1640-5. https://doi.org/10.1161/CIRCULATIONAHA.109.192644
https://doi.org/https://doi.org/10.1161/...
.

Laboratory measurements

The results of the following tests were collected directly from the patients’ medical records: complete blood count; creatinine, glucose, total cholesterol, HDL, low-density protein (LDL), triglycerides, anti-double-stranded DNA, complement (C3 and C4) levels; and qualitative urine test.

Statistical analysis

The Statistical Package for Social Sciences software (SPSS) version 1.8.0 was used in the statistical analyses. The Fisher’s exact test was used to determine the association between two or more qualitative random variables. The Pearson’s Chi-square test was used to analyze probability in categorical data for unpaired samples. The Mann-Whitney test was used for independent samples. A p<0.05 was considered statistically significant.

Ethical aspect

The identity of the study participants was kept confidential and all participants signed an informed consent form. The study was approved by the Research Ethics Committee of the Federal University of Rio Grande do Sul under Certificado de Apresentação para Apreciação Ética (CAAE) no. 4338331 4.2.0000.5347.

RESULTS

The study population consisted of 112 patients, 106 (94.6%) of whom were women. Age ranged from 40 to 61 years for men and from 28 to 80 years for women. A total of 77 patients (68.8%) patients presented a score of 0 in the SLICC, similar to scores for disease activity, with 73 patients (62.5 %) presenting a score of 0 in the SLEDAI. The 25th to 75th percentiles of the medians were 0 to 1 for the SLICC and SLEDAI, as shown in Table 1.

Table 1.
Descriptive data of the study population.

Anthropometric data showed an obesity classification grade II according to BMI in 42 patients (37.5%), whereas 26 (23.2%) had grade I obesity, and 35 (31.3%) were overweight. The evaluation of adiposity according to BFP showed 48 patients (42.9%) and 25 patients (22.3%) being classified as very high and high risk, respectively, totaling 73 patients (65.2%) classified as having high body fat. Abdominal obesity was present in 86 patients (76.8%), as shown in Table 2. Regarding eating habits, there was an insufficient daily intake of micronutrients, mainly of potassium, copper, boron, and vitamin B1, with 100% of the participants consuming less than the daily quantity recommended.

Table 2.
Anthropometric data of the study population.

MR was present in 58 patients (51.8%) who showed an association between MR and low dietary intake of vitamin B9, choline, and sulfur, as shown in Table 3. Regarding MS, 18 patients (16%) met the classification criteria. Laboratory tests showed that 31 patients (27.7%) had a high LDL level, 64 (57.1%) had a moderate or high-risk HDL level, seven (6.3%) had a high-risk cholesterol level, and 10 (8.9%) had triglyceride levels above the borderline cutoff.

Table 3.
Association of metabolic risk and insufficient micronutrient intake.

DISCUSSION

The patients in this study had low SLICC and SLEDAI scores, which indicates little accumulated damage and controlled disease at the time of evaluation, possibly indicating more controlled disease in this population11. Kostopoulou M, Nikolopoulos D, Parodis I, Bertsias G. Cardiovascular disease in systemic lupus erythematosus: recent data on epidemiology, risk factors and prevention. Curr Vasc Pharmacol. 2020;18(6):549-65. https://doi.org/10.2174/1570161118666191227101636
https://doi.org/https://doi.org/10.2174/...
. The anthropometric evaluation showed a high prevalence of high BMI, corroborating the literature. Some studies show a high prevalence of obesity and suggest that obesity is associated with disease activity1313. Patterson SL, Schmajuk G, Jafri K, Yazdany J, Katz P. Obesity independently associates with worse patient-reported outcomes in women with systemic lupus erythematosus. Arthritis Care Res (Hoboken). 2019;71(1):126-33. https://doi.org/10.1002/acr.23576
https://doi.org/https://doi.org/10.1002/...
,1414. Meza-Meza MR, Vizmanos-Lamotte B, Muñoz-Valle JF, Parra-Rojas I, Garaulet M, Campos-López B, et al. Relationship of excess weight with clinical activity and dietary intake deficiencies in systemic lupus erythematosus patients. Nutrients. 2019;11(11):2683. https://doi.org/10.3390/nu11112683
https://doi.org/https://doi.org/10.3390/...
. There was a high BFP in 62.5% of the patients when high- and very-high-risk classifications were grouped. Some studies had similar results despite the use of other body adiposity measurement techniques. Borges et al.1515. Borges MC, dos Santos FMM, Telles RW, Lanna CCD, Correia MITD. Nutritional status and food intake in patients with systemic lupus erythematosus. Nutrition. 2012;28(11-12):1098-103. https://doi.org/10.1016/j.nut.2012.01.015
https://doi.org/https://doi.org/10.1016/...
used bioimpedance and reported that 59.2% of the study population had a BFP above the recommended range.

This study showed excess abdominal fat according to WC in 86 patients (76.8%), which represents a risk for CVD. A cohort study reported a high prevalence of abdominal obesity and a high incidence of cardiovascular risk in the SLE population66. Monção CSA, Martins LN, Penteado MPS, Reis RCP, Santos FMM, Lanna CCD, et al. Incidence of cardiovascular risk factors in female patients with systemic lupus erythematosus: a 3-year follow-up cohort. Lupus. 2018;27(11):1790-98. https://doi.org/10.1177/0961203318790676
https://doi.org/https://doi.org/10.1177/...
. Hormonal factors may be associated with increased weight and body fat in women with SLE, which were not addressed in the present study. However, they may be a topic for future research, as Li et al.1616. Li Z, Shang J, Zeng S, Wu H, Zhou Y, Xu H. Altered body composition and increased visceral adipose tissue in premenopausal and late postmenopausal patients with SLE. Clin Rheumatol. 2019;38(11):3117-27. https://doi.org/10.1007/s10067-019-04701-3
https://doi.org/https://doi.org/10.1007/...
stated that menopause was associated with increased BMI and abdominal obesity in patients with SLE. The literature emphasizes the association between abdominal obesity and CVD in the general population1717. Barroso TA, Marins LB, Alves R, Gonçalves ACS, Barroso SG, Rocha GS. Association of central obesity with the incidence of cardiovascular diseases and risk factors. Int J Cardiovasc Sci. 2017;30(5):416-24. https://doi.org/10.5935/2359-4802.20170073
https://doi.org/https://doi.org/10.5935/...
. An experimental study on SLE showed that a high-fat diet was associated with visceral obesity1818. Gilbert EL, Ryan MJ. High dietary fat promotes visceral obesity and impaired endothelial function in female mice with systemic lupus erythematosus. Gend Med. 2011;8(2):150-5. https://doi.org/10.1016/j.genm.2011.03.006
https://doi.org/https://doi.org/10.1016/...
.

Regarding eating habits, although this study was limited to only one type of food survey, insufficient consumption of micronutrients was identified. Similar results were observed in the Mexican SLE population, regarding both the insufficient consumption of micronutrients and the excess weight1414. Meza-Meza MR, Vizmanos-Lamotte B, Muñoz-Valle JF, Parra-Rojas I, Garaulet M, Campos-López B, et al. Relationship of excess weight with clinical activity and dietary intake deficiencies in systemic lupus erythematosus patients. Nutrients. 2019;11(11):2683. https://doi.org/10.3390/nu11112683
https://doi.org/https://doi.org/10.3390/...
.

In another study, low fruit and vegetable consumption and insufficient dietary calcium and iron intake were observed1515. Borges MC, dos Santos FMM, Telles RW, Lanna CCD, Correia MITD. Nutritional status and food intake in patients with systemic lupus erythematosus. Nutrition. 2012;28(11-12):1098-103. https://doi.org/10.1016/j.nut.2012.01.015
https://doi.org/https://doi.org/10.1016/...
. The literature reports low micronutrient intake in patients with SLE and its possible association with atherosclerosis in this population1919. Lourdudoss C, Elkan AC, Hafström I, Jogestrand T, Gustafsson T, van Vollenhoven R, et al. Dietary micronutrient intake and atherosclerosis in systemic lupus erythematosus. Lupus. 2016;(14):1602-9. https://doi.org/10.1177/0961203316655211
https://doi.org/https://doi.org/10.1177/...
. The present study found an association of insufficient intake of some micronutrients with MR; i.e., an insufficient intake of folic acid (vitamin B9), choline, and sulfur was associated with the grouping of anthropometric indicators for obesity.

To date, there are no studies in the literature in the SLE population reporting similar results, possibly owing to the diversity of methodologies, although a study demonstrated that a dietary folic acid deficiency in SLE may be associated with atherosclerosis1919. Lourdudoss C, Elkan AC, Hafström I, Jogestrand T, Gustafsson T, van Vollenhoven R, et al. Dietary micronutrient intake and atherosclerosis in systemic lupus erythematosus. Lupus. 2016;(14):1602-9. https://doi.org/10.1177/0961203316655211
https://doi.org/https://doi.org/10.1177/...
, which in the present study was associated with MR. High micronutrient intake was reported as protective against excess weight in the Mexican SLE population1414. Meza-Meza MR, Vizmanos-Lamotte B, Muñoz-Valle JF, Parra-Rojas I, Garaulet M, Campos-López B, et al. Relationship of excess weight with clinical activity and dietary intake deficiencies in systemic lupus erythematosus patients. Nutrients. 2019;11(11):2683. https://doi.org/10.3390/nu11112683
https://doi.org/https://doi.org/10.3390/...
. General population studies show micronutrient deficiencies in obese people, mainly of fat-soluble vitamins, B vitamins, and folic acid2020. Astrup A, Bügel S. Overfed but undernourished: recognizing nutritional inadequacies/deficiencies in patients with overweight or obesity. Int J Obes (Lond.). 2019;43(2):219-32. https://doi.org/10.1038/s41366-018-0143-9
https://doi.org/https://doi.org/10.1038/...
. An experimental study found an association of choline deficiency with obesity2121. Maswoswe SM, Tremblay GC. Biosynthesis of hippurate, urea and pyrimidines in the fatty liver: studies with rats fed orotic acid or a diet deficient in choline and inositol, and with genetically obese (Zucker) rats. J Nutr. 1989;119(2):273-9. https://doi.org/10.1093/jn/119.2.273
https://doi.org/https://doi.org/10.1093/...
.

In the present study, 18 participants (16%) met the classification criteria for MS. A meta-analysis study reported an MS prevalence of 26% in patients with SLE2222. Sun C, Qin W, Zhang YH, Wu Y, Li Q, Liu M, et al. Prevalence and risk of metabolic syndrome in patients with systemic lupus erythematosus: a meta-analysis. Int J Rheum Dis. 2017;20(8):917-28. https://doi.org/10.1111/1756-185X.13153
https://doi.org/https://doi.org/10.1111/...
. Regarding the lipid profile of this population, there was a predominance of results above the normal range, and the literature shows that patients with SLE often present changed plasma lipids and decreased HDL-cholesterol levels44. Szabó MZ, Szodoray P, Kiss E. Dyslipidemia in systemic lupus erythematosus. Immunol Res. 2017;65(2):543-50. https://doi.org/10.1007/s12026-016-8892-9
https://doi.org/https://doi.org/10.1007/...
,55. Atta AM, Silva JPCG, Santiago MB, Oliveira IS, Oliveira RC, Sousa Atta MLB. Clinical and laboratory aspects of dyslipidemia in Brazilian women with systemic lupus erythematosus. Clin Rheumat. 2018;37(6):1539-46. https://doi.org/10.1007/s10067-018-4051-0
https://doi.org/https://doi.org/10.1007/...
. Dietary intake of saturated fats is one of the factors associated with an increased lipid profile and can play an important role in increasing these levels, and there is evidence of excessive oil and fat consumption by patients with SLE1414. Meza-Meza MR, Vizmanos-Lamotte B, Muñoz-Valle JF, Parra-Rojas I, Garaulet M, Campos-López B, et al. Relationship of excess weight with clinical activity and dietary intake deficiencies in systemic lupus erythematosus patients. Nutrients. 2019;11(11):2683. https://doi.org/10.3390/nu11112683
https://doi.org/https://doi.org/10.3390/...
,2323. achet JC, Borba Neto EF. Dyslipidaemia and atherosclerosis in systemic lupus erythematosus. Rev Bras Reumatol. 2003;43(5):324-8.. In a study with 170 patients1515. Borges MC, dos Santos FMM, Telles RW, Lanna CCD, Correia MITD. Nutritional status and food intake in patients with systemic lupus erythematosus. Nutrition. 2012;28(11-12):1098-103. https://doi.org/10.1016/j.nut.2012.01.015
https://doi.org/https://doi.org/10.1016/...
, 142 (83.8%) consumed excess fat according to a food frequency questionnaire not used in the present study. The present study shows the importance of controlling risk factors through nutritional monitoring, preventing overweight, and decreasing anthropometric values, especially WC, which is the most associated with CVD, in addition to controlling adequate nutrient consumption. Nutritional profile factors can be modified in this population, indicating that risk factors can be controlled and/or treated with early nutritional clinical care, thus improving their metabolic complication outcomes.

CONCLUSIONS

Patients with SLE had a nutritional profile that increases CVD risk factors, which could possibly be reduced with clinical nutritional monitoring.

REFERENCES

  • 1
    Kostopoulou M, Nikolopoulos D, Parodis I, Bertsias G. Cardiovascular disease in systemic lupus erythematosus: recent data on epidemiology, risk factors and prevention. Curr Vasc Pharmacol. 2020;18(6):549-65. https://doi.org/10.2174/1570161118666191227101636
    » https://doi.org/https://doi.org/10.2174/1570161118666191227101636
  • 2
    Medina G, Vera-Lastra O, Peralta-Amaro AL, Jiménez-Arellano MP, Saavedra MA, Cruz-Domínguez MP, et al. Metabolic syndrome, autoimmunity and rheumatic diseases. Pharmacol Res. 2018;133:277-88. https://doi.org/10.1016/j.phrs.2018.01.009
    » https://doi.org/https://doi.org/10.1016/j.phrs.2018.01.009
  • 3
    Mok CC, Tse SM, Chan KL, Ho LY. Effect of the metabolic syndrome on organ damage and mortality in patients with systemic lupus erythematosus: a longitudinal analysis. Clin Exp Rheumatol. 2018;36(3):389-95. PMID: 29148424
  • 4
    Szabó MZ, Szodoray P, Kiss E. Dyslipidemia in systemic lupus erythematosus. Immunol Res. 2017;65(2):543-50. https://doi.org/10.1007/s12026-016-8892-9
    » https://doi.org/https://doi.org/10.1007/s12026-016-8892-9
  • 5
    Atta AM, Silva JPCG, Santiago MB, Oliveira IS, Oliveira RC, Sousa Atta MLB. Clinical and laboratory aspects of dyslipidemia in Brazilian women with systemic lupus erythematosus. Clin Rheumat. 2018;37(6):1539-46. https://doi.org/10.1007/s10067-018-4051-0
    » https://doi.org/https://doi.org/10.1007/s10067-018-4051-0
  • 6
    Monção CSA, Martins LN, Penteado MPS, Reis RCP, Santos FMM, Lanna CCD, et al. Incidence of cardiovascular risk factors in female patients with systemic lupus erythematosus: a 3-year follow-up cohort. Lupus. 2018;27(11):1790-98. https://doi.org/10.1177/0961203318790676
    » https://doi.org/https://doi.org/10.1177/0961203318790676
  • 7
    Klack K, Bonfa E, Borba Neto EF. Diet and nutritional aspects in systemic lupus erythematosus. Rev Bras Reumatol. 2012;52(3):384-408. PMID: 22641593
  • 8
    Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40(9):1725. https://doi.org/10.1002/art.1780400928
    » https://doi.org/https://doi.org/10.1002/art.1780400928
  • 9
    World Health Organization. Physical status: the use and interpretation of anthropometry. Report of a WHO expert committee. Geneva: World Health Organization; 1995.
  • 10
    Siri WE. Body composition from fluid spaces and density. In: Brozec J, Henschel A (eds). Techniques for measuring body composition. Washington: National Academy of Science; 1961. p. 223-44.
  • 11
    Alberti KGMM, Zimmet P, Shaw J. Metabolic syndrome--a new world-wide definition. A consensus statement from the international diabetes federation. Diabet Med. 2006;23(5):469-80. https://doi.org/10.1111/j.1464-5491.2006.01858.x
    » https://doi.org/https://doi.org/10.1111/j.1464-5491.2006.01858.x
  • 12
    Alberti KGMM, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120(16):1640-5. https://doi.org/10.1161/CIRCULATIONAHA.109.192644
    » https://doi.org/https://doi.org/10.1161/CIRCULATIONAHA.109.192644
  • 13
    Patterson SL, Schmajuk G, Jafri K, Yazdany J, Katz P. Obesity independently associates with worse patient-reported outcomes in women with systemic lupus erythematosus. Arthritis Care Res (Hoboken). 2019;71(1):126-33. https://doi.org/10.1002/acr.23576
    » https://doi.org/https://doi.org/10.1002/acr.23576
  • 14
    Meza-Meza MR, Vizmanos-Lamotte B, Muñoz-Valle JF, Parra-Rojas I, Garaulet M, Campos-López B, et al. Relationship of excess weight with clinical activity and dietary intake deficiencies in systemic lupus erythematosus patients. Nutrients. 2019;11(11):2683. https://doi.org/10.3390/nu11112683
    » https://doi.org/https://doi.org/10.3390/nu11112683
  • 15
    Borges MC, dos Santos FMM, Telles RW, Lanna CCD, Correia MITD. Nutritional status and food intake in patients with systemic lupus erythematosus. Nutrition. 2012;28(11-12):1098-103. https://doi.org/10.1016/j.nut.2012.01.015
    » https://doi.org/https://doi.org/10.1016/j.nut.2012.01.015
  • 16
    Li Z, Shang J, Zeng S, Wu H, Zhou Y, Xu H. Altered body composition and increased visceral adipose tissue in premenopausal and late postmenopausal patients with SLE. Clin Rheumatol. 2019;38(11):3117-27. https://doi.org/10.1007/s10067-019-04701-3
    » https://doi.org/https://doi.org/10.1007/s10067-019-04701-3
  • 17
    Barroso TA, Marins LB, Alves R, Gonçalves ACS, Barroso SG, Rocha GS. Association of central obesity with the incidence of cardiovascular diseases and risk factors. Int J Cardiovasc Sci. 2017;30(5):416-24. https://doi.org/10.5935/2359-4802.20170073
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  • Funding: none

Publication Dates

  • Publication in this collection
    17 Sept 2021
  • Date of issue
    June 2021

History

  • Received
    25 Jan 2021
  • Accepted
    06 Feb 2021
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