Skip to main content
Top
Published in: Rheumatology International 1/2017

01-01-2017 | Original Article - Observational Research

Lipid profile among girls with systemic lupus erythematosus

Authors: Daniele Machado, Roseli O. S. Sarni, Thaís T. O. Abad, Simone G. L. Silva, Eugênia J. B. Khazaal, Sonia Hix, Milena S. G. Correia, Fabíola I. Suano-Souza, Claudio A. Len, Maria Teresa R. A. Terreri

Published in: Rheumatology International | Issue 1/2017

Login to get access

Abstract

The aim of the study was to describe biomarkers of lipid metabolism associated with increased cardiovascular risk and their correlation with disease variables and markers of inflammation in adolescent females with systemic lupus erythematosus (SLE). This cross-sectional controlled study evaluated 33 adolescent females with juvenile SLE and 33 healthy controls. Anthropometric data, SLE disease activity index (SLEDAI), medications, proteinuria, ultra-sensitive C-reactive protein (us-CRP), lipid profile (total cholesterol, LDL-c, HDL-c and triglycerides), apolipoproteins A and B (Apo A-I and B), paraoxonase, and myeloperoxidase were evaluated. Median age of the patients and the median disease duration were 16.7 years and 54 months, respectively. SLEDAI scores above 4 were observed in 11 (33.3 %) patients. Moreover, 12 (36.4 %) patients were overweight, and 5 (15.2 %) had low height for age ratios. Dyslipidemia was observed in 13 (39.4 %) patients and in 7 (21.2 %) controls with a decrease in HDL-c concentrations in SLE patients even after adjustment for their nutritional status. In the group with SLE, us-CRP concentrations were inversely correlated with LDL-c/ApoB ratio (p = 0.031). After multivariate regression analysis, the SLE group showed lower concentration of Apo A-I and a decreased LDL-c/ApoB ratio. SLE adolescent females with low disease activity, with preserved kidney function and on low dose of corticosteroids, regardless of nutritional status and food intake, have proatherogenic lipid biomarkers, which may contribute to an increased atherosclerotic risk.
Literature
1.
go back to reference Huang YL, Chung HT, Chang CJ, Yeh KW, Chen LC, Huang JL (2009) Lymphopenia is a risk factor in the progression of carotid intima-media thickness in juvenile-onset systemic lupus erythematosus. Arthritis Rheum 60:3766–3775CrossRefPubMed Huang YL, Chung HT, Chang CJ, Yeh KW, Chen LC, Huang JL (2009) Lymphopenia is a risk factor in the progression of carotid intima-media thickness in juvenile-onset systemic lupus erythematosus. Arthritis Rheum 60:3766–3775CrossRefPubMed
2.
go back to reference Hak AE, Karlson EW, Feskanich D, Stampfer MJ, Costenbader KH (2009) Systemic lupus erythematosus and the risk of cardiovascular disease: results from the nurses’ health study. Arthritis Care Res 61:1396–1402CrossRef Hak AE, Karlson EW, Feskanich D, Stampfer MJ, Costenbader KH (2009) Systemic lupus erythematosus and the risk of cardiovascular disease: results from the nurses’ health study. Arthritis Care Res 61:1396–1402CrossRef
3.
go back to reference Manzi S, Meilahn EN, Rairie JE, Conte CG, Medsger TA Jr, Jansen-McWilliams L et al (1997) Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham Study. Am J Epidemiol 145:408–415CrossRefPubMed Manzi S, Meilahn EN, Rairie JE, Conte CG, Medsger TA Jr, Jansen-McWilliams L et al (1997) Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham Study. Am J Epidemiol 145:408–415CrossRefPubMed
4.
go back to reference Soriano A, Afeltra A, Shoenfeld Y (2014) Is atherosclerosis accelerated in systemic sclerosis? Novel insight. Curr Opin Rheumatol 26:653–657CrossRefPubMed Soriano A, Afeltra A, Shoenfeld Y (2014) Is atherosclerosis accelerated in systemic sclerosis? Novel insight. Curr Opin Rheumatol 26:653–657CrossRefPubMed
5.
go back to reference Tisseverasinghe A, Lim S, Greenwood C, Urowitz M, Gladman D, Fortin PR (2006) Association between serum total cholesterol level and renal outcome in systemic lupus erythematosus. Arthritis Rheum 54:2211–2219CrossRefPubMed Tisseverasinghe A, Lim S, Greenwood C, Urowitz M, Gladman D, Fortin PR (2006) Association between serum total cholesterol level and renal outcome in systemic lupus erythematosus. Arthritis Rheum 54:2211–2219CrossRefPubMed
7.
go back to reference Kwankaew J, Leelawattana R, Saignam A, Siripaitoon B, Uea-Areewongsa P, Juthong S (2014) Apolipoprotein B as an independent predictor of arterial stiffness in systemic lupus erythematosus patients. Int J Rheum Dis 18:447–451CrossRefPubMed Kwankaew J, Leelawattana R, Saignam A, Siripaitoon B, Uea-Areewongsa P, Juthong S (2014) Apolipoprotein B as an independent predictor of arterial stiffness in systemic lupus erythematosus patients. Int J Rheum Dis 18:447–451CrossRefPubMed
8.
go back to reference Falaschi F, Ravelli A, Martignoni A, Migliavacca D, Sartori M, Pistorio A et al (2000) Nephrotic-range proteinuria, the major risk factor for early atherosclerosis in juvenile-onset systemic lupus erythematosus. Arthritis Rheum 43:1405–1409CrossRefPubMed Falaschi F, Ravelli A, Martignoni A, Migliavacca D, Sartori M, Pistorio A et al (2000) Nephrotic-range proteinuria, the major risk factor for early atherosclerosis in juvenile-onset systemic lupus erythematosus. Arthritis Rheum 43:1405–1409CrossRefPubMed
9.
go back to reference Posadas-Romero C, Torres-Tamayo M, Zamora-González J, Aguilar-Herrera BE, Posadas-Sánchez R, Cardoso-Saldaña G et al (2004) High insulin levels and increased low-density lipoprotein oxidizability in pediatric patients with systemic lupus erythematosus. Arthritis Rheum 50:160–165CrossRefPubMed Posadas-Romero C, Torres-Tamayo M, Zamora-González J, Aguilar-Herrera BE, Posadas-Sánchez R, Cardoso-Saldaña G et al (2004) High insulin levels and increased low-density lipoprotein oxidizability in pediatric patients with systemic lupus erythematosus. Arthritis Rheum 50:160–165CrossRefPubMed
10.
go back to reference Soep JB, Mietus-Snyder M, Malloy MJ, Witztum JL, von Scheven E (2004) Assessment of atherosclerotic risk factors and endothelial function in children and young adults with pediatric-onset systemic lupus erythematosus. Arthritis Rheum 51:451–457CrossRefPubMed Soep JB, Mietus-Snyder M, Malloy MJ, Witztum JL, von Scheven E (2004) Assessment of atherosclerotic risk factors and endothelial function in children and young adults with pediatric-onset systemic lupus erythematosus. Arthritis Rheum 51:451–457CrossRefPubMed
11.
go back to reference Lilleby V, Haugen M, Mørkrid L, Frey-Frøslie K, Holven KB, Førre O (2007) Body composition, lipid and lipoprotein levels in childhood-onset systemic lupus erythematosus. Scand J Rheumatol 36:40–47CrossRefPubMed Lilleby V, Haugen M, Mørkrid L, Frey-Frøslie K, Holven KB, Førre O (2007) Body composition, lipid and lipoprotein levels in childhood-onset systemic lupus erythematosus. Scand J Rheumatol 36:40–47CrossRefPubMed
12.
go back to reference Boros CA, Bradley TJ, Cheung MM, Bargman JM, Russell JL, McCrindle BW et al (2011) Early determinants of atherosclerosis in paediatric systemic lupus erythematosus. Clin Exp Rheumatol 29:575–581PubMed Boros CA, Bradley TJ, Cheung MM, Bargman JM, Russell JL, McCrindle BW et al (2011) Early determinants of atherosclerosis in paediatric systemic lupus erythematosus. Clin Exp Rheumatol 29:575–581PubMed
13.
go back to reference (1999) The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42(4):599–608 (1999) The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42(4):599–608
14.
go back to reference Gladman DD, Ibañez D, Urowitz MB (2002) Systemic lupus erythematosus disease activity index 2000. J Rheumatol 29:288–291PubMed Gladman DD, Ibañez D, Urowitz MB (2002) Systemic lupus erythematosus disease activity index 2000. J Rheumatol 29:288–291PubMed
15.
go back to reference Gladman D, Ginzler E, Goldsmith C, Fortin P, Liang M, Urowitz M et al (1996) The development and initial validation of systemic lupus international collaborating clinics/American College of Rheumatology Damage Index for systemic lupus erythematosus. Arthritis Rheum 39:363–369CrossRefPubMed Gladman D, Ginzler E, Goldsmith C, Fortin P, Liang M, Urowitz M et al (1996) The development and initial validation of systemic lupus international collaborating clinics/American College of Rheumatology Damage Index for systemic lupus erythematosus. Arthritis Rheum 39:363–369CrossRefPubMed
16.
go back to reference World Health Organization (1995) Physical status: the use and interpretation of anthropometry: report of a WHO Expert Committee, vol 854. Geneva, pp 1–452 (Technical Report Series, 854) World Health Organization (1995) Physical status: the use and interpretation of anthropometry: report of a WHO Expert Committee, vol 854. Geneva, pp 1–452 (Technical Report Series, 854)
17.
go back to reference Frisancho AR (1974) Triceps skin fold and upper arm muscle size norms for assessment of nutritional status. Am J Clin Nutr 27:1052–1058PubMed Frisancho AR (1974) Triceps skin fold and upper arm muscle size norms for assessment of nutritional status. Am J Clin Nutr 27:1052–1058PubMed
18.
go back to reference Frisancho AR (1991) Anthropometric standards for the assessments of growth and nutritional status. University of Michigan Press, Ann Arbor Frisancho AR (1991) Anthropometric standards for the assessments of growth and nutritional status. University of Michigan Press, Ann Arbor
19.
go back to reference de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J (2007) Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 85:660–667CrossRefPubMedPubMedCentral de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J (2007) Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 85:660–667CrossRefPubMedPubMedCentral
21.
go back to reference TACO (2011) Tabela Brasileira de Composição de Alimentos [Brazilian table of food consumption], 4th edn. Ed. Nepa-Unicamp, Campinas TACO (2011) Tabela Brasileira de Composição de Alimentos [Brazilian table of food consumption], 4th edn. Ed. Nepa-Unicamp, Campinas
22.
go back to reference Institute of Medicine (2003) Dietary reference intakes: applications in dietary assessment. National Academy Press, Washington Institute of Medicine (2003) Dietary reference intakes: applications in dietary assessment. National Academy Press, Washington
23.
go back to reference De Geest B, Stengel D, Landeloos M, Lox M, Le Gat L, Collen D et al (2000) Effect of overexpression of human apo A-I in C57BL/6 and C57BL/6 apo E-deficient mice on 2 lipoprotein-associated enzymes, platelet-activating factor acetylhydrolase and paraoxonase. Comparison of adenovirus-mediated human apo A-I gene transfer and human apo A-I transgenesis. Arterioscler Thromb Vasc Biol 20:E68–E75CrossRefPubMed De Geest B, Stengel D, Landeloos M, Lox M, Le Gat L, Collen D et al (2000) Effect of overexpression of human apo A-I in C57BL/6 and C57BL/6 apo E-deficient mice on 2 lipoprotein-associated enzymes, platelet-activating factor acetylhydrolase and paraoxonase. Comparison of adenovirus-mediated human apo A-I gene transfer and human apo A-I transgenesis. Arterioscler Thromb Vasc Biol 20:E68–E75CrossRefPubMed
24.
go back to reference Daniels SR, Greer FR, Committee on Nutrition (2008) Lipid screening and cardiovascular health in childhood. Pediatrics 122:198–208CrossRefPubMed Daniels SR, Greer FR, Committee on Nutrition (2008) Lipid screening and cardiovascular health in childhood. Pediatrics 122:198–208CrossRefPubMed
25.
go back to reference Srinivasan SR, Frontini MG, Xu J, Berenson GS (2006) Utility of childhood non-high-density lipoprotein cholesterol levels in predicting adult dyslipidemia and other cardiovascular risks: the Bogalusa Heart Study. Pediatrics 118:201–206CrossRefPubMed Srinivasan SR, Frontini MG, Xu J, Berenson GS (2006) Utility of childhood non-high-density lipoprotein cholesterol levels in predicting adult dyslipidemia and other cardiovascular risks: the Bogalusa Heart Study. Pediatrics 118:201–206CrossRefPubMed
26.
go back to reference Millán J, Pintó X, Muñoz A, Zúñiga M, Rubiés-Prat J, Pallardo LF et al (2009) Lipoprotein ratios: physiological significance and clinical usefulness in cardiovascular prevention. Vasc Health Risk Manag 5:757–765PubMedPubMedCentral Millán J, Pintó X, Muñoz A, Zúñiga M, Rubiés-Prat J, Pallardo LF et al (2009) Lipoprotein ratios: physiological significance and clinical usefulness in cardiovascular prevention. Vasc Health Risk Manag 5:757–765PubMedPubMedCentral
27.
go back to reference Davidson MH (2009) Apolipoprotein measurements: is more widespread use clinically indicated? Clin Cardiol 32:482–486CrossRefPubMed Davidson MH (2009) Apolipoprotein measurements: is more widespread use clinically indicated? Clin Cardiol 32:482–486CrossRefPubMed
28.
go back to reference Radwan MM, El-Lebedy D, Fouda R, Elsorougy E, Fakhry D (2014) Anti-apolipoprotein A-1 antibodies and carotid intima-media thickness in Egyptian woman with systemic lupus erythematosus. Clin Rheumatol 33:493–498CrossRefPubMed Radwan MM, El-Lebedy D, Fouda R, Elsorougy E, Fakhry D (2014) Anti-apolipoprotein A-1 antibodies and carotid intima-media thickness in Egyptian woman with systemic lupus erythematosus. Clin Rheumatol 33:493–498CrossRefPubMed
29.
go back to reference Radwan MM, El-Lebedy D, Fouda R, Elsorougy E, Fakhry D (2007) Management of dyslipidemia in children and adolescents with systemic lupus erythematosus. Lupus 16:618–626CrossRef Radwan MM, El-Lebedy D, Fouda R, Elsorougy E, Fakhry D (2007) Management of dyslipidemia in children and adolescents with systemic lupus erythematosus. Lupus 16:618–626CrossRef
30.
go back to reference Ortiz TT, Terreri MT, Caetano M, Souza FI, D’Almeida V, Sarni RO et al (2013) Dyslipidemia in pediatric systemic lupus erythematosus: the relationship with disease activity and plasma homocysteine and cysteine concentrations. Ann Nutr Metab 63:77–82CrossRefPubMed Ortiz TT, Terreri MT, Caetano M, Souza FI, D’Almeida V, Sarni RO et al (2013) Dyslipidemia in pediatric systemic lupus erythematosus: the relationship with disease activity and plasma homocysteine and cysteine concentrations. Ann Nutr Metab 63:77–82CrossRefPubMed
31.
go back to reference Hayata AL, Borba EF, Bonfá E, Kochen JA, Goldenstein-Schainberg C (2005) The frequency of high/moderate lipoprotein risk factor for coronary artery disease is significant in juvenile-onset systemic lupus erythematosus. Lupus 14:613–617CrossRefPubMed Hayata AL, Borba EF, Bonfá E, Kochen JA, Goldenstein-Schainberg C (2005) The frequency of high/moderate lipoprotein risk factor for coronary artery disease is significant in juvenile-onset systemic lupus erythematosus. Lupus 14:613–617CrossRefPubMed
32.
go back to reference Nascif AK, Hilário MO, Terreri MT, Ajzen SA, D’Almeida V, Plavnik FL et al (2007) Endothelial function analysis and atherosclerotic risk factors in adolescents with systemic lupus erythematosus. Int J Adolesc Med Health 19:497–505CrossRefPubMed Nascif AK, Hilário MO, Terreri MT, Ajzen SA, D’Almeida V, Plavnik FL et al (2007) Endothelial function analysis and atherosclerotic risk factors in adolescents with systemic lupus erythematosus. Int J Adolesc Med Health 19:497–505CrossRefPubMed
33.
go back to reference Tyrrell PN, Beyene J, Benseler SM, Sarkissian T, Silverman ED (2007) Predictors of lipid abnormalities in children with new-onset systemic lupus erythematosus. J Rheumatol 34:2112–2118PubMed Tyrrell PN, Beyene J, Benseler SM, Sarkissian T, Silverman ED (2007) Predictors of lipid abnormalities in children with new-onset systemic lupus erythematosus. J Rheumatol 34:2112–2118PubMed
34.
go back to reference Benatti FB, Miossi R, Passareli M, Nakandakare ER, Perandini L, Lima FR et al (2015) The effects of exercise on lipid profile in systemic lupus erythematosus and healthy individual: a randomized trial. Rheumatol Int 35:61–69CrossRefPubMed Benatti FB, Miossi R, Passareli M, Nakandakare ER, Perandini L, Lima FR et al (2015) The effects of exercise on lipid profile in systemic lupus erythematosus and healthy individual: a randomized trial. Rheumatol Int 35:61–69CrossRefPubMed
35.
go back to reference McMahon M, Skaggs BJ, Grossman JM, Sahakian L, Fitzgerald J, Wong WK et al (2014) A panel of biomarkers is associated with increased risk of the presence and progression of atherosclerosis in women with systemic lupus erythematosus. Arthritis Rheumatol 66:130–139CrossRefPubMedPubMedCentral McMahon M, Skaggs BJ, Grossman JM, Sahakian L, Fitzgerald J, Wong WK et al (2014) A panel of biomarkers is associated with increased risk of the presence and progression of atherosclerosis in women with systemic lupus erythematosus. Arthritis Rheumatol 66:130–139CrossRefPubMedPubMedCentral
36.
go back to reference McMahon M, Skaggs B (2014) Pathogenesis and treatment of atherosclerosis in lupus. Rheum Dis Clin N Am 40:475–495CrossRef McMahon M, Skaggs B (2014) Pathogenesis and treatment of atherosclerosis in lupus. Rheum Dis Clin N Am 40:475–495CrossRef
37.
go back to reference Caetano MC, Ortiz TT, Terreri MT, Sarni RO, Silva SG, Souza FI et al (2009) Inadequate dietary intake of children and adolescents with juvenile idiopathic arthritis and systemic lupus erythematosus. J Pediatr (Rio J) 85:509–515CrossRef Caetano MC, Ortiz TT, Terreri MT, Sarni RO, Silva SG, Souza FI et al (2009) Inadequate dietary intake of children and adolescents with juvenile idiopathic arthritis and systemic lupus erythematosus. J Pediatr (Rio J) 85:509–515CrossRef
38.
go back to reference dos Santos FM, Borges MC, Correia MI, Telles RW, Lanna CC (2010) Assessment of nutritional status and physical activity in systemic lupus erythematosus patients. Rev Bras Reumatol 50:631–638CrossRef dos Santos FM, Borges MC, Correia MI, Telles RW, Lanna CC (2010) Assessment of nutritional status and physical activity in systemic lupus erythematosus patients. Rev Bras Reumatol 50:631–638CrossRef
39.
go back to reference Borges MC, dos Santos FM, Telles RW, Lanna CC, Correia MI (2012) Nutritional status and food intake in patients with systemic lupus erythematosus. Nutrition 28:1098–1103CrossRefPubMed Borges MC, dos Santos FM, Telles RW, Lanna CC, Correia MI (2012) Nutritional status and food intake in patients with systemic lupus erythematosus. Nutrition 28:1098–1103CrossRefPubMed
Metadata
Title
Lipid profile among girls with systemic lupus erythematosus
Authors
Daniele Machado
Roseli O. S. Sarni
Thaís T. O. Abad
Simone G. L. Silva
Eugênia J. B. Khazaal
Sonia Hix
Milena S. G. Correia
Fabíola I. Suano-Souza
Claudio A. Len
Maria Teresa R. A. Terreri
Publication date
01-01-2017
Publisher
Springer Berlin Heidelberg
Published in
Rheumatology International / Issue 1/2017
Print ISSN: 0172-8172
Electronic ISSN: 1437-160X
DOI
https://doi.org/10.1007/s00296-015-3393-z

Other articles of this Issue 1/2017

Rheumatology International 1/2017 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.