Serum neutrophil gelatinase-associated lipocalin and cystatin C is associated with blood pressure in ex-preterm children and adolescents.


Journal

Journal of hypertension
ISSN: 1473-5598
Titre abrégé: J Hypertens
Pays: Netherlands
ID NLM: 8306882

Informations de publication

Date de publication:
06 Sep 2024
Historique:
medline: 9 9 2024
pubmed: 9 9 2024
entrez: 9 9 2024
Statut: aheadofprint

Résumé

As preterm birth is a risk factor for hypertension (HTN), biomarkers for early prediction of HTN in childhood is an emerging need. The aims of the study were to evaluate serum biomarkers in ex-preterm children and examine for associations with office peripheral and central SBP (cSBP), ambulatory BP parameters and pulse wave velocity (PWV). This case-control study included children and adolescents born prematurely (ex-preterms) and at full term (controls). All participants underwent office and ambulatory BP monitoring, assessment of cSBP, PWV and serum biomarkers at the same visit. Neutrophil gelatinase-associated lipocalin (NGAL), matrix metalloproteinase-2, metalloproteinase-9 (MMP-2, MMP-9) and Cystatin C (CysC) were measured using ELISA. The study population included 52 ex-preterm individuals and 26 controls. Mean age was 10.7 ± 3.6 years. NGAL, MMP-2, MMP-9, and CysC levels were similar between the ex-preterm and the control group. In the ex-preterm group, NGAL is associated with office SBP z score (β = 1.007, 95% CI 1.001-0.014, P = 0.049), CysC with office DBP z score (β = 1.003, 95% CI 1.001-0.005, P = 0.018) and cSBP z score (β = 1.003, 95% CI 1.001-0.005, P = 0.006) independently of age, sex and BMI z score. Among ex-preterm children and adolescents 17% had ambulatory HTN and 31% had white-coat HTN. NGAL levels were higher in ex-preterm children with WCH compared with children with normal BP [57.9 (IQR 50.8) versus 34.6 (IQR 46.2)], P = 0.018]. WCH is common in ex-preterm children and adolescents and is associated with higher NGAL levels and CysC presents positive association with cSBP. The findings in this study provides preliminary evidence that NGAL and CysC may have a role in predicting the risk of developing hypertension later in life. Further studies are warranted.

Sections du résumé

BACKGROUND BACKGROUND
As preterm birth is a risk factor for hypertension (HTN), biomarkers for early prediction of HTN in childhood is an emerging need. The aims of the study were to evaluate serum biomarkers in ex-preterm children and examine for associations with office peripheral and central SBP (cSBP), ambulatory BP parameters and pulse wave velocity (PWV).
METHODS METHODS
This case-control study included children and adolescents born prematurely (ex-preterms) and at full term (controls). All participants underwent office and ambulatory BP monitoring, assessment of cSBP, PWV and serum biomarkers at the same visit. Neutrophil gelatinase-associated lipocalin (NGAL), matrix metalloproteinase-2, metalloproteinase-9 (MMP-2, MMP-9) and Cystatin C (CysC) were measured using ELISA.
RESULTS RESULTS
The study population included 52 ex-preterm individuals and 26 controls. Mean age was 10.7 ± 3.6 years. NGAL, MMP-2, MMP-9, and CysC levels were similar between the ex-preterm and the control group. In the ex-preterm group, NGAL is associated with office SBP z score (β = 1.007, 95% CI 1.001-0.014, P = 0.049), CysC with office DBP z score (β = 1.003, 95% CI 1.001-0.005, P = 0.018) and cSBP z score (β = 1.003, 95% CI 1.001-0.005, P = 0.006) independently of age, sex and BMI z score. Among ex-preterm children and adolescents 17% had ambulatory HTN and 31% had white-coat HTN. NGAL levels were higher in ex-preterm children with WCH compared with children with normal BP [57.9 (IQR 50.8) versus 34.6 (IQR 46.2)], P = 0.018].
CONCLUSION CONCLUSIONS
WCH is common in ex-preterm children and adolescents and is associated with higher NGAL levels and CysC presents positive association with cSBP. The findings in this study provides preliminary evidence that NGAL and CysC may have a role in predicting the risk of developing hypertension later in life. Further studies are warranted.

Identifiants

pubmed: 39248130
doi: 10.1097/HJH.0000000000003868
pii: 00004872-990000000-00540
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 Wolters Kluwer Health, Inc. All rights reserved.

Références

Song P, Zhang Y, Yu J, Zha M, Zhu Y, Rahimi K, Rudan I. Global prevalence of hypertension in children: a systematic review and meta-analysis. JAMA Pediatr 2019; 173:1154–1163.
Chen X, Wang Y. Tracking of blood pressure from childhood to adulthood: a systematic review and meta-regression analysis. Circulation 2008; 117:3171–3180.
Toschke AM, Kohl L, Mansmann U, von Kries R. Meta-analysis of blood pressure tracking from childhood to adulthood and implications for the design of intervention trials. Acta Paediatr 2010; 99:24–29.
Erlingsdottir A, Indridason OS, Thorvaldsson O, Edvardsson VO. Blood pressure in children and target-organ damage later in life. Pediatr Nephrol 2010; 25:323–328.
LBWaNNW Group The impact of kidney development on the life course: a consensus document for action. Nephron 2017; 136:3–49.
Brenner BM, Garcia DL, Anderson S. Glomeruli and blood pressure. Less of one, more the other? Am J Hypertens 1988; 1 (4 Pt 1):335–347.
Heo JS, Lee JM. The long-term effect of preterm birth on renal function: a meta-analysis. Int J Environ Res Public Health 2021; 18:2951.
Chainoglou A, Chrysaidou K, Kotsis V, Stabouli S. Preterm birth, kidney function and cardiovascular disease in children and adolescents. Children (Basel) 2022; 9:1130.
KDIGO CKD Work Group. KDIGO 2012 Clinical practice guideline for the evaluation and management of chronic kidney disease. 2013.
Lopez-Giacoman S, Madero M. Biomarkers in chronic kidney disease, from kidney function to kidney damage. World J Nephrol 2015; 4:57–73.
Raffetto JD, Khalil RA. Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem Pharmacol 2008; 75:346–359.
Atzori L, Mussap M, Noto A, Barberini L, Puddu M, Coni E, et al. Clinical metabolomics and urinary NGAL for the early prediction of chronic kidney disease in healthy adults born ELBW. J Matern Fetal Neonatal Med 2011; 24 Suppl 2:40–43.
Buonafine M, Martinez-Martinez E, Jaisser F. More than a simple biomarker: the role of NGAL in cardiovascular and renal diseases. Clin Sci (Lond) 2018; 132:909–923.
Salgado JV, França AK, Cabral NA, Lages J, Ribeiro VS, Santos AM, et al. Cystatin C, kidney function, and cardiovascular risk factors in primary hypertension. Rev Assoc Med Bras 19922013; 59:21–27.
Akhabue E, Montag S, Reis JP, Pool LR, Mehta R, Yancy CW, et al. FGF23 (fibroblast growth factor-23) and incident hypertension in young and middle-aged adults: the CARDIA Study. Hypertension 2018; 72:70–76.
Chainoglou A, Sarafidis K, Chrysaidou K, Farmaki E, Kolios K, Economou M, et al. Hypertension and arterial stiffness in preterm children and adolescents. J Hypertens 2022; 40:e156.
March of Dimes, PMNCH, Save the children, WHO. Howson CP, Kinney MV, Je Lawn, editors. Born too soon: the global action report on preterm birth. Geneva: World Health Organization; 2012.
Schlaudecker EP, Munoz FM, Bardají A, Boghossian NS, Khalil A, Mousa H, et al. Brighton Collaboration Small for Gestational Age Working Group Small for gestational age: case definition & guidelines for data collection, analysis, and presentation of maternal immunisation safety data. Vaccine 2017; 35 (48 Pt a):6518–6528.
Cole TJ, Lobstein T. Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatric Obes 2012; 7:284–294.
Schwartz GJ, Haycock GB, Edelmann CM, Spitzer A. A simple estimate of glomerular filtration rate in children derived from body length and plasma creatinine. Pediatrics 1976; 58:259–263.
Schwartz GJ, Schneider MF, Maier PS, Moxey-Mims M, Dharnidharka VR, Warady BA, et al. Improved equations estimating GFR in children with chronic kidney disease using an immunonephelometric determination of cystatin C. Kidney Int 2012; 82:445–453.
Lurbe E, Agabiti-Rosei E, Cruickshank JK, Dominiczak A, Erdine S, Hirth A, et al. 2016 European Society of Hypertension guidelines for the management of high blood pressure in children and adolescents. J Hypertens 2016; 34:1887–1920.
Stabouli S, Papakatsika S, Kotronis G, Papadopoulou-Legbelou K, Rizos Z, Kotsis V. Arterial stiffness and SBP variability in children and adolescents. J Hypertens 2015; 33:88–95.
Wuhl E, Witte K, Soergel M, Mehls O, Schaefer F. German Working Group on Pediatric Hypertension Distribution of 24-h ambulatory blood pressure in children: normalized reference values and role of body dimensions. J Hypertens 2002; 20:1995–2007.
Stabouli S, Printza N, Zervas C, Dotis J, Chrysaidou K, Maliahova O, et al. Comparison of the SphygmoCor XCEL device with applanation tonometry for pulse wave velocity and central blood pressure assessment in youth. J Hypertens 2019; 37:30–36.
Elmenhorst J, Hulpke-Wette M, Barta C, Dalla Pozza R, Springer S, Oberhoffer R. Percentiles for central blood pressure and pulse wave velocity in children and adolescents recorded with an oscillometric device. Atherosclerosis 2015; 238:9–16.
Filho LT, Grande AJ, Colonetti T, Della É, da Rosa MI. Accuracy of neutrophil gelatinase-associated lipocalin for acute kidney injury diagnosis in children: systematic review and meta-analysis. Pediatr Nephrol 2017; 32:1979–1988.
Mishra J, Dent C, Tarabishi R, Mitsnefes MM, Ma Q, Kelly C, et al. Neutrophil gelatinase-associated lipocalin (NGAL) as a biomarker for acute renal injury after cardiac surgery. Lancet 2005; 365:1231–1238.
Mitsnefes MM, Kathman TS, Mishra J, Kartal J, Khoury PR, Nickolas TL, et al. Serum neutrophil gelatinase-associated lipocalin as a marker of renal function in children with chronic kidney disease. Pediatr Nephrol 2007; 22:101–108.
Hasegawa M, Ishii J, Kitagawa F, Takahashi H, Sugiyama K, Tada M, et al. Plasma neutrophil gelatinase-associated lipocalin as a predictor of cardiovascular events in patients with chronic kidney disease. Biomed Res Int 2016; 2016:8761475.
Solak Y, Yilmaz MI, Siriopol D, Saglam M, Unal HU, Yaman H, et al. Serum neutrophil gelatinase-associated lipocalin is associated with cardiovascular events in patients with chronic kidney disease. Int Urol Nephrol 2015; 47:1993–2001.
Daniels LB, Barrett-Connor E, Clopton P, Laughlin GA, Ix JH, Maisel AS. Plasma neutrophil gelatinase-associated lipocalin is independently associated with cardiovascular disease and mortality in community-dwelling older adults: the Rancho Bernardo Study. J Am Coll Cardiol 2012; 59:1101–1109.
Katagiri M, Takahashi M, Doi K, Myojo M, Kiyosue A, Ando J, et al. Serum neutrophil gelatinase-associated lipocalin concentration reflects severity of coronary artery disease in patients without heart failure and chronic kidney disease. Heart Vessels 2016; 31:1595–1602.
Park CG, Choi KM. Lipocalin-2, A-FABP and inflammatory markers in relation to flow-mediated vasodilatation in patients with essential hypertension. Clin Exp Hypertens 2014; 36:478–483.
Malyszko J, Bachorzewska-Gajewska H, Malyszko JS, Pawlak K, Dobrzycki S. Serum neutrophil gelatinase-associated lipocalin as a marker of renal function in hypertensive and normotensive patients with coronary artery disease. Nephrology (Carlton) 2008; 13:153–156.
Staub E, Urfer-Maurer N, Lemola S, Risch L, Evers KS, Welzel T, et al. Comparison of blood pressure and kidney markers between adolescent former preterm infants and term controls. Children (Basel) 2020; 7:E141.
Bassareo PP, Fanos V, Mussap M, Flore G, Noto A, Puddu M, et al. Urinary NGAL and hematic ADMA levels: an early sign of cardio-renal syndrome in young adults born preterm? J Matern Fetal Neonatal Med 2013; 26 Suppl 2:80–83.
Helanova K, Spinar J, Parenica J. Diagnostic and prognostic utility of neutrophil gelatinase-associated lipocalin (NGAL) in patients with cardiovascular diseases--review. Kidney Blood Press Res 2014; 39:623–629.
Bisogni V, Cerasari A, Pucci G, Vaudo G. Matrix metalloproteinases and hypertension-mediated organ damage: current insights. Integr Blood Press Control 2020; 13:157–169.
Parente J, Castro M. Matrix metalloproteinase in the cardiovascular remodeling of hypertension: current insights and therapeutic potential. Metalloproteinases Med 2018; 5:1–11.
Stabouli S, Kotsis V, Maliachova O, Printza N, Chainoglou A, Christoforidis A, et al. Matrix metalloproteinase -2, -9 and arterial stiffness in children and adolescents: the role of chronic kidney disease, diabetes, and hypertension. Int J Cardiol Hypertens 2020; 4:100025.
Tayebjee MH, Nadar S, Blann AD, Gareth Beevers D, MacFadyen RJ, Lip GY. Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 in hypertension and their relationship to cardiovascular risk and treatment: a substudy of the Anglo-Scandinavian Cardiac Outcomes Trial (ASCOT). Am J Hypertens 2004; 17:764–769.
Onal IK, Altun B, Onal ED, Kirkpantur A, Gul Oz S, Turgan C. Serum levels of MMP-9 and TIMP-1 in primary hypertension and effect of antihypertensive treatment. Eur J Intern Med 2009; 20:369–372.
Yasmin, McEniery CM, Wallace S, Dakham Z, Pulsalkar P, Pusalkar P, et al. Matrix metalloproteinase-9 (MMP-9), MMP-2, and serum elastase activity are associated with systolic hypertension and arterial stiffness. Arterioscler Thromb Vasc Biol 2005; 25:372.
Sesso R, Franco MC. Abnormalities in metalloproteinase pathways and IGF-I axis: a link between birth weight, hypertension, and vascular damage in childhood. Am J Hypertens 2010; 23:6–11.
den Bakker E, Gemke RJBJ, Bökenkamp A. Endogenous markers for kidney function in children: a review. Crit Rev Clin Lab Sci 2018; 55:163–183.
Roos JF, Doust J, Tett SE, Kirkpatrick CM. Diagnostic accuracy of cystatin C compared to serum creatinine for the estimation of renal dysfunction in adults and children--a meta-analysis. Clin Biochem 2007; 40:383–391.
Dönmez O, Korkmaz HA, Yıldız N, Ediz B. Comparison of serum cystatin C and creatinine levels in determining glomerular filtration rate in children with stage I to III chronic renal disease. Ren Fail 2015; 37:784–790.
Carballo-Magdaleno D, Guízar-Mendoza JM, Amador-Licona N, Domínguez-Domínguez V. Renal function, renal volume, and blood pressure in infants with antecedent of antenatal steroids. Pediatr Nephrol 2011; 26:1851–1856.
Yamamura-Miyazaki N, Yamamoto K, Fujiwara K, Santo Y, Michigami T, Kitajima H, et al. Risk factors associated with a decreased estimated glomerular filtration rate based on cystatin C levels in school-age children with extremely low birthweight. Nephrology (Carlton) 2017; 22:463–469.
Kwinta P, Klimek M, Drozdz D, Grudzień A, Jagła M, Zasada M, Pietrzyk JJ. Assessment of long-term renal complications in extremely low birth weight children. Pediatr Nephrol 2011; 26:1095–1103.
Raaijmakers A, Zhang ZY, Claessens J, Cauwenberghs N, van Tienoven TP, Wei FF, et al. Does extremely low birth weight predispose to low-renin hypertension? Hypertension 2017; 69:443–449.
Gilarska M, Raaijmakers A, Zhang ZY, Staessen JA, Levtchenko E, Klimek M, et al. Extremely low birth weight predisposes to impaired renal health: a pooled analysis. Kidney Blood Press Res 2019; 44:897–906.
Starzec K, Klimek M, Grudzień A, Jagła M, Kwinta P. Longitudinal assessment of renal size and function in extremely low birth weight children at 7 and 11 years of age. Pediatr Nephrol 2016; 31:2119–2126.
Shlipak MG, Sarnak MJ, Katz R, Fried LF, Seliger SL, Newman AB, et al. Cystatin C and the risk of death and cardiovascular events among elderly persons. N Engl J Med 2005; 352:2049–2060.
Koenig W, Twardella D, Brenner H, Rothenbacher D. Plasma concentrations of cystatin C in patients with coronary heart disease and risk for secondary cardiovascular events: more than simply a marker of glomerular filtration rate. Clin Chem 2005; 51:321–327.
Ix JH, Shlipak MG, Chertow GM, Whooley MA. Association of cystatin C with mortality, cardiovascular events, and incident heart failure among persons with coronary heart disease: data from the Heart and Soul Study. Circulation 2007; 115:173–179.
Kestenbaum B, Rudser KD, de Boer IH, Peralta CA, Fried LF, Shlipak MG, et al. Differences in kidney function and incident hypertension: the multiethnic study of atherosclerosis. Ann Intern Med 2008; 148:501–508.
Laurent S, Boutouyrie P. Can we learn about the hypertension-induced decline in renal function from noninvasive haemodynamics? J Hypertens 2014; 32:26–27.
Mancia G, Bombelli M, Facchetti R, Madotto F, Quarti-Trevano F, Polo Friz H, et al. Long-term risk of sustained hypertension in white-coat or masked hypertension. Hypertension 2009; 54:226–232.
Grandi AM, Solbiati F, Laurita E, Cassinerio E, Marchesi C, Piperno F, et al. Isolated office hypertension: a 3-year follow-up study. Blood Press 2005; 14:298–305.
Ugajin T, Hozawa A, Ohkubo T, Asayama K, Kikuya M, Obara T, et al. White-coat hypertension as a risk factor for the development of home hypertension: the Ohasama study. Arch Intern Med 2005; 165:1541–1546.
Lurbe E, Torró MI, Alvarez J. Ambulatory blood pressure monitoring in children and adolescents: coming of age? Curr Hypertens Rep 2013; 15:143–149.
Miyashita Y, Hanevold C, Faino A, Scher J, Lande M, Yamaguchi I, et al. White coat hypertension persistence in children and adolescents: the Pediatric Nephrology Research Consortium Study. J Pediatr 2022; 246:154.e1–160.e1.
Stabouli S, Kotsis V, Toumanidis S, Papamichael C, Constantopoulos A, Zakopoulos N. White-coat and masked hypertension in children: association with target-organ damage. Pediatr Nephrol 2005; 20:1151–1155.
Androulakis E, Papageorgiou N, Lioudaki E, Chatzistamatiou E, Zacharia E, Kallikazaros I, Tousoulis D. Subclinical organ damage in white-coat hypertension: the possible role of cystatin C. J Clin Hypertens (Greenwich) 2017; 19:190–197.

Auteurs

Athanasia Chainoglou (A)

Department of Pediatrics, School of Medicine, Faculty of Health Sciences, Aristotle University Thessaloniki, Hippokratio Hospital.

Kosmas Sarafidis (K)

Department of Neonatology, School of Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki.

Anna Taparkou (A)

Department of Pediatrics, School of Medicine, Faculty of Health Sciences, Aristotle University Thessaloniki, Hippokratio Hospital.

Evangelia Farmaki (E)

Department of Pediatrics, School of Medicine, Faculty of Health Sciences, Aristotle University Thessaloniki, Hippokratio Hospital.

Katerina Chrysaidou (K)

Department of Pediatrics, School of Medicine, Faculty of Health Sciences, Aristotle University Thessaloniki, Hippokratio Hospital.

Dimos Gidaris (D)

Department of Pediatrics, School of Medicine, Faculty of Health Sciences, Aristotle University Thessaloniki, Hippokratio Hospital.

Konstantinos Kollios (K)

Department of Pediatrics, School of Medicine, Faculty of Health Sciences, Aristotle University Thessaloniki, Hippokratio Hospital.

Vasilios Kotsis (V)

3 Department of Internal Medicine, School of Medicine, Faculty of Health Sciences, Aristotle University Thessaloniki, Papageorgiou Hospital, Thessaloniki, Greece.

Stella Stabouli (S)

Department of Pediatrics, School of Medicine, Faculty of Health Sciences, Aristotle University Thessaloniki, Hippokratio Hospital.

Classifications MeSH