Abstract
Background
The aim of this study was to evaluate the presence of subclinical cardiovascular disease (CVD) and its relation to risk factors, particularly hypertension in juvenile-onset systemic lupus erythematosus (SLE).
Methods
A total of 24 patients with normal renal function were examined for subclinical CVD by using non-invasive methods, including the measurement of carotid intima-media thickness (IMT), carotid distensibility, aortic pulse wave velocity (PWV) and left ventricular mass (LVM). Blood pressure (BP) pattern and the presence of hypertension were assessed by 24-h ambulatory blood pressure monitoring (ABPM).
Results
The patients had higher aortic PWV than the controls (p = 0.011). Increased carotid IMT was present in 48 % of the patients and reduced carotid distensibility in 17 %. Left ventricular hypertrophy (LVH) was present in 22 % of the patients. Eight patients were hypertensive; hypertensive patients had a significantly lower distensibility coefficient (DC)-SDS, higher aortic PWV and higher LVM index than the normotensive patients (p = 0.008, p = 0.023 and p = 0.001, respectively). Higher carotid IMT-standard deviation score (SDS) significantly correlated with higher nighttime diastolic BP-SDS (R 2 = 0.204, p = 0.046); lower DC-SDS correlated with higher nighttime systolic BP-SDS (R 2 = 0.290, p = 0.014). Increased aortic PWV was significantly associated with higher daytime systolic BP-SDS and elevated erythrocyte sedimentation rate (R 2 = 0.607, p = 0.003 and p = 0.010, respectively). PWV was the only independent predictor of LVM index (R 2 = 0.396, p = 0.004).
Conclusion
These results provide additional evidence for the presence of subclinical CVD and its relation to hypertension in juvenile-onset SLE. They also indicate a significant relation between LVH and increased arterial stiffness. It is also important to note that our findings reveal significant relationships between ambulatory BP and cardiovascular changes and underline the importance of ABPM to predict CVD.
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References
Ward MM (1999) Premature morbidity from cardiovascular and cerebrovascular disease in women with systemic lupus erythematosus. Arthritis Rheum 42:338–346
Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Gladman DD, Urowitz M, Fortin PR, Petri M, Barr S, Gordon C, Bae SC, Isenberg D, Zoma A, Aranow C, Dooley MA, Nived O, Sturfelt G, Steinsson K, Alarcón G, Senécal JL, Zummer M, Hanly J, Ensworth S, Pope J, Edworthy S, Rahman A, Sibley J, El-Gabalawy H, McCarthy T, St Pierre Y, Clarke A, Ramsey-Goldman R (2006) Mortality in systemic lupus erythematosus. Arthritis Rheum 54:2550–2557
Esdaile JM, Abrahamowicz M, Grodzicky T, Li Y, Panaritis C, du Berger R, Côte R, Grover SA, Fortin PR, Clarke AE, Senécal JL (2001) Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 44:2331–2337
Roman MJ, Devereux RB, Schwartz JE, Lockshin MD, Paget SA, Davis A, Crow MK, Sammaritano L, Levine DM, Shankar BA, Moeller E, Salmon JE (2005) Arterial stiffness in chronic inflammatory diseases. Hypertension 46:1–6
Schanberg LE, Sandborg C, Barnhart HX, Ardoin SP, Yow E, Evans GW, Mieszkalski KL, Ilowite NT, Eberhard A, Levy DM, Kimura Y, von Scheven E, Silverman E, Bowyer SL, Punaro L, Singer NG, Sherry DD, McCurdy D, Klein-Gitelman M, Wallace C, Silver R, Wagner-Weiner L, Higgins GC, Brunner HI, Jung L, Soep JB, Reed A, Atherosclerosis Prevention in Pediatric Lupus Erythematosus Investigators (2009) Premature atherosclerosis in pediatric systemic lupus erythematosus. Arthritis Rheum 60:1496–1507
Petri M, Lakatta C, Magder L, Goldman (1994) Effect of prednisone and hydroxychloroquine on coronary artery disease risk factors in systemic lupus erythematosus: a longitudinal data analysis. Am J Med 96:254–259
Boros CA, Bradley TJ, Cheung MM, Bargman JM, Russell JL, McCrindle BW, Adeli K, Hamilton J, Silverman ED (2011) Early determinants of atherosclerosis in pediatric systemic lupus erythematosus. Clin Exp Rhematol 29:575–581
Bessant R, Duncan R, Ambler G, Swanton J, Isenberg DA, Gordon C, Rahman A (2006) Prevalence of conventional and lupus-specific risk factors for cardiovascular disease in patients with systemic lupus erythematosus: a case control study. Arthritis Rheum 55:892–899
Berenson GS, Srinivasan SR, Bao W, Newman WP 3rd, Tracy RE, Wattigney WA (1998) Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults. N Eng J Med 338:1650–1666
Davis PH, Dawson JD, Riley WA, Lauer RM (2001) Carotid intimal medial thickness is related to cardiovascular risk factors measured from childhood through middle age: The Muscatine study. Circulation 104:2815–2819
Flynn JS (2011) Ambulatory blood pressure monitoring in children: imperfect yet essential. Pediatr Nephrol 26:2089–2094
Mitsnefes M, Flynn J, Cohn S, Samuels J, Blydt-Hansen T, Saland J, Kimball T, Furth S, Warady B, CiKD Study Group (2010) Masked hypertension associates with left ventricular hypertrophy in children with CKD. J Am Soc Nephrol 21:137–144
Lurbe E, Sorof JM, Daniels SR (2004) Clinical and research aspects of ambulatory blood pressure monitoring in children. J Pediatr 144:7–16
Falaschi F, Ravelli A, Martignoni A, Migliavacca D, Sartori M, Pistorio A, Perani G, Martini A (2000) Nephrotic range proteinuria, the major risk factor for early atherosclerosis in juvenile onset systemic lupus erythematosus. Arthritis Rheum 43:1405–1409
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 60:3766–3775
Nascif AK, Hilário MO, Terreri MT, Ajzen SA, D’Almeida V, Plavnik FL, de Jesus Christofalo DM (2007) Endothelial function analysis and atherosclerotic risk factors in adolescents with systemic lupus erythematosus. Int J Adolesc Med Health 19:497–505
Soep JB, Mietus-Snyder M, Malloy MJ, Witztum JL, Scheven EV (2004) Assessment of atherosclerotic risk factors and endothelial function in children and young adults with pediatric-onset systemic lupus erythematosus. Arthritis Rheum 51:451–457
Schwartz GJ, Gauthier B (1985) A simple estimate of glomerular filtration rate in adolescent boys. J Pediatr 106:522–526
Hochberg MC, for the Diagnostic and Therapeutic Criteria Committee of the American College of Rheumatology (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40:1725
Bundak R, Furman A, Gunoz H, Darendeliler F, Bas F, Neyzi O (2006) Body mass index references for Turkish children. Acta Pediatr 95:194–198
Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 35:630–640
Gladman D, Ginzler E, Goldsmith C, Fortin P, Liang M, Urowitz M, Bacon P, Bombardieri S, Hanly J, Hay E, Isenberg D, Jones J, Kalunian K, Maddison P, Nived O, Petri M, Richter M, Sanchez-Guerrero J, Snaith M, Sturfelt G, Symmons D, Zoma A (1996) The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erithematosus. Arthritis Rheum 39:363–369
Soergel M, Kirschstein M, Busch C, Danne T, Gellermann JJ, Holl R, Krull F, Reichert H, Reusz GS, Rascher W (1997) Oscillometric twenty-four-hour ambulatory blood pressure values in healthy children and adolescents: a multicenter trial including 1141 subjects. J Pediatr 130:178–184
Wuhl E, Witte K, Soergel M, Mehls O, Schaefer F (2002) Distribution of 24-h ambulatory blood pressure in children: normalized reference values and role of body dimensions. Germany Working Group on Pediatric Hypertension. J Hypertens 20:1995–2007
Urbina E, Alpert B, Flynn J, Hayman L, Harshfield GA, Jacobson M, Mahoney L, McCrindle B, Mietus-Snyder M, Steinberger J, Daniels S (2008) Ambulatory blood pressure monitoring in children and adolescents: recommendations for standard assessment: a scientific statement from the American Heart Association Atherosclerosis, Hypertension, and Obesity in Youth Committee of the Council on Cardiovascular Disease in the Young and the Council for High Blood Pressure Research. Hypertension 52:433–451
Stein JH, Korcarz CE, Hurst RT, Lonn E, Kendall CB, Mohler ER, Najjar SS, Rembold CM, Post WS, American Society of Echocardiography Carotid Intima-Media Thickness Task Force (2008) Use of carotid ultrasound to identify subclinical vascular disease and evaluate cardiovascular disease risk: a consensus statement from the American Society of Echocardiography Carotid Intima-Media Thickness Task Force. Endorsed by the Society for Vascular Medicine. J Am Soc Echocardiogr 21:93–111
Jourdan C, Wühl E, Litwin M, Fahr K, Trelewicz J, Jobs K, Schenk JP, Grenda R, Mehls O, Tröger J, Schaefer F (2005) Normative values for intima-media thickness and distensibility of large arteries in healthy adolescents. J Hypertens 23:1707–1715
Hickson SS, Butlin M, Broad J, Avolio AP, Wilkinson IB, McEniery CM (2009) Validity and repeatability of the Vicorder apparatus: a comparison with the SyphygmoCor device. Hypertens Res 32:1079–1085
Sahn DJ, De Maria A, Kisslo J, Weyman A (1978) Recommendations regarding quantification in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58:1072–1083
Devereux RB, Reichek N (1977) Echocardiographic determination of left ventricular mass in man: anatomic validation of the method. Circulation 55:613–618
De Simone G, Daniels SR, Devereux RB, Meyer RA, Roman MJ, de Diviitis O, Alderman MH (1992) Left ventricular mass and body size in normotensive children and adults: assessment of allometric relations and impact of overweight. J Am Coll Cardiol 20:1251–1260
Khoury PR, Mitsnefes M, Daniels SR, Kimball TR (2009) Age-specific reference intervals for indexed left ventricular mass in children. J Am Soc Echocardiogr 22:709–714
Sarkissian T, Beyenne J, Feldman B, McCrindle BW, Silverman ED (2007) Longitudinal examination of lipid profiles in pediatric systemic lupus erythematosus. Arthritis Rheum 56:631–638
Sorof JM, Poffenbarger T, Portman R (2000) Abnormal 24-hour blood pressure patterns in children after renal transplantation. Am J Kidney Dis 35:681–686
Ohkubo T, Hozawa A, Yamaguchi J, Kikuya M, Ohmori K, Michimata M, Matsubara M, Hashimoto J, Hoshi H, Araki T, Tsuji I, Satoh H, Hisamichi S, Imai Y (2002) Prognostic significance of the nocturnal decline in blood pressure in individuals with and without high 24-h blood pressure: the Ohasama study. J Hypertens 20:2183–2189
Routledge FS, McFetridge-Durdle JA, Dean CR, Canadian Hypertension Society (2007) Night-time blood pressure patterns and target organ damage: a review. Can J Cardiol 23:132–138
Sorof JM, Alexandrov AV, Cardwell G, Portman RJ (2003) Carotid artery intimal-medial thickness and left ventricular hypertrophy in children with elevated blood pressure. Pediatrics 111:61–66
Stabouli S, Kotsis V, Papamichael C, Constantopoulos A, Zakopoulos N (2005) Adolescent obesity is associated with high ambulatory blood pressure and increased carotid intimal-medial thickness. J Pediatr 147:651–656
Lande MB, Carson NL, Roy J, Meagher CC (2006) Effects of childhood primary hypertension on carotid intima media thickness: a matched controlled study. Hypertension 48:40–44
Tsioufis C, Stefanadis C, Antoniadis D, Kallikazaros I, Zambaras P, Pitsavos C, Tsiamis E, Toutouzas P (2000) Absence of any significant effects of circadian blood pressure variations on carotid artery elastic properties in essential hypertensive subjects. J Hum Hypertens 14:813–818
Lekakis JP, Zakopoulos NA, Protogerou AD, Papaioannou TG, Kotsis VT, Pitiriga VC, Tsitsirikos MD, Stamatelopoulos KS, Papamichael CM, Mavrikakis ME (2005) Arterial stiffness assessed by pulse wave analysis in essential hypertension: relation to 24-h blood pressure profile. Int J Cardiol 102:391–395
Mitsnefes MM, Kimball TR, Witt SA, Glascock BJ, Khoury PR, Daniels SR (2004) Abnormal carotid artery structure and function in children and adolescents with successful renal transplantation. Circulation 110:97–101
Shang Q, Tam LS, Li EKM, Yip GKW, Yu CM (2008) Increased arterial stiffness correlated with disease activity in systemic lupus erythematosus. Lupus 17:1096–1102
Cypiene A, Kovaite M, Venalis A, Dadoniene J, Rugiene R, Petrulioniene Z, Ryliskyte L, Laucevicius A (2009) Arterial wall dysfunction in systemic lupus erythematosus. Lupus 18:522–529
Bjarnegrad N, Bengtsson C, Brodziski J, Sturfelt G, Nived O, Lanne T (2006) Increased aortic pulse wave velocity in middle aged women with systemic lupus erythematosus. Lupus 15:644–650
Cervera R, Font J, Paré C, Azqueta M, Pérez-Villa F, López-Soto A, Ingelmo M (1992) Cardiac disease in systemic lupus erythematosus: prospective study of 70 patients. Ann Rheum Dis 51:151–159
Shi B, Ni Z, Cai H, Zhang M, Mou S, Wang Q, Cao L, Yu Z, Yan Y, Qian J (2010) High sensitive C-reactive protein: an independent risk factor for left ventricular hypertrophy in patients with lupus nephritis. J Biomed Biotechnol 2010:373426
Pieretti J, Roman MJ, Devereux RB, Lockshin MD, Crow MK, Paget SA, Schwartz JE, Sammaritano L, Levine DM, Salmon JE (2007) Systemic lupus erythematosus predicts increased left ventricular mass. Circulation 116:419–426
Chow PC, Ho MH, Lee TL, Cheung YF (2007) Relation of arterial stiffness to left ventriculare structure and function in adolescents and young adults with pediatric-onset systemic lupus erythematosus. J Rheumatol 34:1345–1352
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This study was presented as an oral presentation at the 18th European Pediatric Rheumatology Congress (PReS2011) and also as a poster presentation at the ESPN 2011.
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Canpolat, N., Kasapcopur, O., Caliskan, S. et al. Ambulatory blood pressure and subclinical cardiovascular disease in patients with juvenile-onset systemic lupus erythematosus. Pediatr Nephrol 28, 305–313 (2013). https://doi.org/10.1007/s00467-012-2317-3
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DOI: https://doi.org/10.1007/s00467-012-2317-3