Associations of childhood adiposity with adult intima-media thickness and inflammation: a 20-year longitudinal population-based cohort.


Journal

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

Informations de publication

Date de publication:
01 03 2023
Historique:
pubmed: 3 2 2023
medline: 25 3 2023
entrez: 2 2 2023
Statut: ppublish

Résumé

The associations between childhood adiposity and adult increased carotid intima-media thickness (cIMT) have been well established, which might be corroborated by the association between adiposity in children and inflammation in adults. However, longitudinal data regarding biological pathways associated with childhood adiposity are lacking. The current study included participants from the STANISLAS cohort who had adiposity measurements at age 5-18 years [ N  = 519, mean (SD) age, 13.0 (2.9) years; 46.4% male], and who were measured with cIMT, vascular-related and metabolic-related proteins at a median follow-up of 19 ± 2 years. BMI, waist-to-height ratio and waist circumference were converted to age-specific and sex-specific z -scores. A minority of children were overweight/obese (16.2% overweight-BMI z -score >1; 1.3% obesity- z -score >2). Higher BMI, waist-height ratio and waist circumference in children were significantly associated with greater adult cIMT in univariable analysis, although not after adjusting for C-reactive protein. These associations were more pronounced in those with consistently high adiposity status from childhood to middle adulthood. Participants with higher adiposity during childhood (BMI or waist-height ratio) had higher levels of insulin-like growth factor-binding protein-1, protein-2, matrix metalloproteinase-3, osteopontin, hemoglobin and C-reactive protein in adulthood. Network analysis showed that IL-6, insulin-like growth factor-1 and fibronectin were the key proteins associated with childhood adiposity. In a population-based cohort followed for 20 years, higher BMI or waist-to-height ratio in childhood was significantly associated with greater cIMT and enhanced levels of proteins reflective of inflammation, supporting the importance of inflammation as progressive atherosclerosis in childhood adiposity.

Sections du résumé

BACKGROUND
The associations between childhood adiposity and adult increased carotid intima-media thickness (cIMT) have been well established, which might be corroborated by the association between adiposity in children and inflammation in adults. However, longitudinal data regarding biological pathways associated with childhood adiposity are lacking.
METHODS
The current study included participants from the STANISLAS cohort who had adiposity measurements at age 5-18 years [ N  = 519, mean (SD) age, 13.0 (2.9) years; 46.4% male], and who were measured with cIMT, vascular-related and metabolic-related proteins at a median follow-up of 19 ± 2 years. BMI, waist-to-height ratio and waist circumference were converted to age-specific and sex-specific z -scores.
RESULTS
A minority of children were overweight/obese (16.2% overweight-BMI z -score >1; 1.3% obesity- z -score >2). Higher BMI, waist-height ratio and waist circumference in children were significantly associated with greater adult cIMT in univariable analysis, although not after adjusting for C-reactive protein. These associations were more pronounced in those with consistently high adiposity status from childhood to middle adulthood. Participants with higher adiposity during childhood (BMI or waist-height ratio) had higher levels of insulin-like growth factor-binding protein-1, protein-2, matrix metalloproteinase-3, osteopontin, hemoglobin and C-reactive protein in adulthood. Network analysis showed that IL-6, insulin-like growth factor-1 and fibronectin were the key proteins associated with childhood adiposity.
CONCLUSION
In a population-based cohort followed for 20 years, higher BMI or waist-to-height ratio in childhood was significantly associated with greater cIMT and enhanced levels of proteins reflective of inflammation, supporting the importance of inflammation as progressive atherosclerosis in childhood adiposity.

Identifiants

pubmed: 36728849
doi: 10.1097/HJH.0000000000003343
pii: 00004872-990000000-00160
doi:

Substances chimiques

C-Reactive Protein 9007-41-4

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

402-410

Informations de copyright

Copyright © 2022 Wolters Kluwer Health, Inc. All rights reserved.

Références

Wang Y, Lobstein T. Worldwide trends in childhood overweight and obesity. Int J Pediatr Obes 2006; 1:11–25.
Koskinen J, Kähönen M, Viikari JS, Taittonen L, Laitinen T, Rönnemaa T, et al. Conventional cardiovascular risk factors and metabolic syndrome in predicting carotid intima–media thickness progression in young adults: the cardiovascular risk in young Finns study. Circulation 2009; 120:229–236.
Juonala M, Magnussen CG, Berenson GS, Venn A, Burns TL, Sabin MA, et al. Childhood adiposity, adult adiposity, and cardiovascular risk factors. N Engl J Med 2011; 365:1876–1885.
Rocha VZ, Libby P. Obesity, inflammation, and atherosclerosis. Nat Rev Cardiol 2009; 6:399–409.
Kotsis VT, Stabouli SV, Papamichael CM, Zakopoulos NA. Impact of obesity in intima–media thickness of carotid arteries. Obesity (Silver Spring, Md) 2006; 14:1708–1715.
Stabouli S, Kotsis V, Papamichael C, Constantopoulos A, Zakopoulos N. Adolescent obesity is associated with high ambulatory blood pressure and increased carotid intimal–medial thickness. J Pediatr 2005; 147:651–656.
Girerd N, Bresso E, Devignes MD, Rossignol P. Insulin-like growth factor binding protein 2: a prognostic biomarker for heart failure hardly redundant with natriuretic peptides. Int J Cardiol 2020; 300:252–254.
Ferreira JP, Verdonschot J, Wang P, Pizard A, Collier T, Ahmed FZ, et al. Proteomic and mechanistic analysis of spironolactone in patients at risk for HF. JACC Heart Fail 2021; 9:268–277.
Ferreira JP, Girerd N, Bozec E, Merckle L, Pizard A, Bouali S, et al. Cohort profile: rationale and design of the fourth visit of the STANISLAS cohort: a familial longitudinal population-based cohort from the Nancy region of France. Int J Epidemiol 2018; 47:395–1395.
Ferreira JP, Girerd N, Bozec E, Mercklé L, Pizard A, Bouali S, et al. Cohort profile: rationale and design of the fourth visit of the STANISLAS cohort: a familial longitudinal population-based cohort from the Nancy region of France. Int J Epidemiol 2017; 47:395–1395.
Schwartz GJ, Haycock GB, Edelmann CM Jr, Spitzer A. A simple estimate of glomerular filtration rate in children derived from body length and plasma creatinine. Pediatrics 1976; 58:259–263.
Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, et al. A new equation to estimate glomerular filtration rate. Ann Intern Med 2009; 150:604–612.
National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) Final Report. Circulation 2002; 106:3143–13143.
Cole TJ, Lobstein T. Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatr Obes 2012; 7:284–294.
Sharma AK, Metzger DL, Daymont C, Hadjiyannakis S, Rodd CJ. LMS tables for waist-circumference and waist-height ratio Z -scores in children aged 5–19 y in NHANES III: association with cardio-metabolic risks. Pediatr Res 2015; 78:723–729.
Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ (Clinical Research ed) 2000; 320:1240–1243.
Laurent S, Cockcroft J, Van Bortel L, Boutouyrie P, Giannattasio C, Hayoz D, et al. Struijker-Boudier H and European Network for Noninvasive Investigation of Large A. Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J 2006; 27:2588–2605.
Goncalves N, Gomes-Ferreira C, Moura C, Roncon-Albuquerque R Jr, Leite-Moreira AF, Falcao-Pires I. Worse cardiac remodeling in response to pressure overload in type 2 diabetes mellitus. Int J Cardiol 2016; 217:195–204.
Tzemos N, Lyseggen E, Silversides C, Jamorski M, Tong JH, Harvey P, et al. Endothelial function, carotid-femoral stiffness, and plasma matrix metalloproteinase-2 in men with bicuspid aortic valve and dilated aorta. J Am Coll Cardiol 2010; 55:660–668.
Peeters SA, Engelen L, Buijs J, Chaturvedi N, Fuller JH, Jorsal A, et al. Circulating matrix metalloproteinases are associated with arterial stiffness in patients with type 1 diabetes: pooled analysis of three cohort studies. Cardiovasc Diabetol 2017; 16:139.
Yasmin, McEniery CM, Wallace S, Dakham Z, Pulsalkar P, Maki-Petaja K, Ashby MJ, 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.
Skrypnik D, Mostowska A, Jagodziński PP, Bogdański P. Association of rs699947 (−2578 C/A) and rs2010963 (−634 G/C) single nucleotide polymorphisms of the VEGF gene, VEGF-A and leptin serum level, and cardiovascular risk in patients with excess body mass: a case–control study. J Clin Med 2020; 9:469.
Hassanisaber H, Rouleau L, Faucheux N. Effect of BMP-9 on endothelial cells and its role in atherosclerosis. Front Biosci (Landmark edition) 2019; 24:994–1023.
Wang J, Razuvaev A, Folkersen L, Hedin E, Roy J, Brismar K, et al. The expression of IGFs and IGF binding proteins in human carotid atherosclerosis, and the possible role of IGF binding protein-1 in the regulation of smooth muscle cell proliferation. Atherosclerosis 2012; 220:102–109.
Bazzichi L, Ghiadoni L, Rossi A, Bernardini M, Lanza M, De Feo F, et al. Osteopontin is associated with increased arterial stiffness in rheumatoid arthritis. Mol Med (Cambridge, Mass) 2009; 15:402–406.
Bui AL, Katz R, Kestenbaum B, de Boer IH, Fried LF, Polak JF, et al. Cystatin C and carotid intima-media thickness in asymptomatic adults: the Multi-Ethnic Study of Atherosclerosis (MESA). Am J Kidney Dis 2009; 53:389–398.
Aleksandrova K, Mozaffarian D, Pischon T. Addressing the perfect storm: biomarkers in obesity and pathophysiology of cardiometabolic risk. Clin Chem 2018; 64:142–153.
Bayes-Genis A, Cediel G, Domingo M, Codina P, Santiago E, Lupón J. Biomarkers in heart failure with preserved ejection fraction. Cardiac Fail Rev 2022; 8:e20.
Nimptsch K, Konigorski S, Pischon T. Diagnosis of obesity and use of obesity biomarkers in science and clinical medicine. Metab Clin Exp 2019; 92:61–70.
Enroth S, Maturi V, Berggrund M, Enroth SB, Moustakas A, Johansson A, et al. Systemic and specific effects of antihypertensive and lipid-lowering medication on plasma protein biomarkers for cardiovascular diseases. Sci Rep 2018; 8:5531.
Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucl Acids Res 2019; 47:D607–d613.
Fabregat A, Korninger F, Viteri G, Sidiropoulos K, Marin-Garcia P, Ping P. Reactome graph database: efficient access to complex pathway data. PLoS Comput Biol 2018; 14:e1005968.
Grundy SM, Brewer HB, Cleeman JI, Smith SC, Lenfant C. Definition of metabolic syndrome. Circulation 2004; 109:433–438.
Charakida M, Jones A, Falaschetti E, Khan T, Finer N, Sattar N, et al. Childhood obesity and vascular phenotypes: a population study. J Am Coll Cardiol 2012; 60:2643–2650.
Aatola H, Hutri-Kähönen N, Juonala M, Laitinen TT, Pahkala K, Mikkilä V, et al. Prospective relationship of change in ideal cardiovascular health status and arterial stiffness: the Cardiovascular Risk in Young Finns Study. J Am Heart Assoc 2014; 3:e000532.
Buscot MJ, Thomson RJ, Juonala M, Sabin MA, Burgner DP, Lehtimäki T, et al. Distinct child-to-adult body mass index trajectories are associated with different levels of adult cardiometabolic risk. Eur Heart J 2018; 39:2263–2270.
Charakida M, Khan T, Johnson W, Finer N, Woodside J, Whincup PH, et al. Lifelong patterns of BMI and cardiovascular phenotype in individuals aged 60–64 years in the 1946 British birth cohort study: an epidemiological study. Lancet Diabetes Endocrinol 2014; 2:648–654.
de Divitiis O, Fazio S, Petitto M, Maddalena G, Contaldo F, Mancini M. Obesity and cardiac function. Circulation 1981; 64:477–482.
Kasper EK, Hruban RH, Baughman KL. Cardiomyopathy of obesity: a clinicopathologic evaluation of 43 obese patients with heart failure. Am J Cardiol 1992; 70:921–924.
Smulyan H, Marchais SJ, Pannier B, Guerin AP, Safar ME, London GM. Influence of body height on pulsatile arterial hemodynamic data. J Am Coll Cardiol 1998; 31:1103–1109.
Zore T, Palafox M, Reue K. Sex differences in obesity, lipid metabolism, and inflammation-A role for the sex chromosomes? Mol Metab 2018; 15:35–44.
Goossens GH, Jocken JWE, Blaak EE. Sexual dimorphism in cardiometabolic health: the role of adipose tissue, muscle and liver. Nat Rev Endocrinol 2021; 17:47–66.
Davis PH, Dawson JD, Riley WA, Lauer RM. Carotid intimal-medial thickness is related to cardiovascular risk factors measured from childhood through middle age: the Muscatine Study. Circulation 2001; 104:2815–2819.
Chau K, Girerd N, Bozec E, Ferreira JP, Duarte K, Nazare JA, et al. Association between abdominal adiposity and 20-year subsequent aortic stiffness in an initially healthy population-based cohort. J Hypertens 2018; 36:2077–2084.
Lischka J, Schanzer A, Hojreh A, Ba-Ssalamah A, de Gier C, Valent I, et al. Circulating microRNAs 34a, 122, and 192 are linked to obesity-associated inflammation and metabolic disease in pediatric patients. Int J Obes 2021; 45:1763–1772.
Ferrante AW Jr. Obesity-induced inflammation: a metabolic dialogue in the language of inflammation. J Intern Med 2007; 262:408–414.
Ridker PM, Rane M. Interleukin-6 signaling and anti-interleukin-6 therapeutics in cardiovascular disease. Circ Res 2021; 128:1728–1746.
Dinarello CA. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 2011; 117:3720–3732.
Dinarello CA, Simon A, van der Meer JW. Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat Rev Drug Discov 2012; 11:633–652.
Amar J, Fauvel J, Drouet L, Ruidavets JB, Perret B, Chamontin B, et al. Interleukin 6 is associated with subclinical atherosclerosis: a link with soluble intercellular adhesion molecule 1. J Hypertens 2006; 24:1083–1088.
Lee WY, Allison MA, Kim DJ, Song CH, Barrett-Connor E. Association of interleukin-6 and C-reactive protein with subclinical carotid atherosclerosis (the Rancho Bernardo Study). Am J Cardiol 2007; 99:99–102.
Wolters TLC, Netea MG, Hermus A, Smit JWA, Netea-Maier RT. IGF1 potentiates the pro-inflammatory response in human peripheral blood mononuclear cells via MAPK. J Mol Endocrinol 2017; 59:129–139.
Maffei P, Dassie F, Wennberg A, Parolin M, Vettor R. The endothelium in acromegaly. Front Endocrinol 2019; 10:437.
Budatha M, Zhang J, Schwartz MA. Fibronectin-mediated inflammatory signaling through integrin α5 in vascular remodeling. J Am Heart Assoc 2021; 10:e021160.
Chambless LE, Heiss G, Folsom AR, Rosamond W, Szklo M, Sharrett AR, et al. Association of coronary heart disease incidence with carotid arterial wall thickness and major risk factors: the Atherosclerosis Risk in Communities (ARIC) Study, 1987–1993. Am J Epidemiol 1997; 146:483–494.
Salonen JT, Salonen R. Ultrasonographically assessed carotid morphology and the risk of coronary heart disease. Arterioscler Thromb 1991; 11:1245–1249.
Powell-Wiley TM, Poirier P, Burke LE, Després JP, Gordon-Larsen P, Lavie CJ, et al. A scientific statement from the American Heart Association. Circulation 2021; 143:e984–e1010.
Hettwer J, Hinterdobler J, Miritsch B, Deutsch MA, Li X, Mauersberger C, et al. Interleukin-1β suppression dampens inflammatory leukocyte production and uptake in atherosclerosis. Cardiovasc Res 2022; 118:2778–2791.
Ridker PM, Everett BM, Thuren T, MacFadyen JG, Chang WH, Ballantyne C, et al. Antiinflammatory therapy with canakinumab for atherosclerotic disease. N Engl J Med 2017; 377:1119–1131.

Auteurs

Tomona Fujikawa (T)

Centre d'Investigations Cliniques Plurithématique 1433, Université de Lorraine, INSERM 1116, CHRU de Nancy.
F-CRIN INI-CRCT Cardiovascular and Renal Clinical Trialists Network, Nancy.

Masatake Kobayashi (M)

Centre d'Investigations Cliniques Plurithématique 1433, Université de Lorraine, INSERM 1116, CHRU de Nancy.
F-CRIN INI-CRCT Cardiovascular and Renal Clinical Trialists Network, Nancy.

Sandra Wagner (S)

Centre d'Investigations Cliniques Plurithématique 1433, Université de Lorraine, INSERM 1116, CHRU de Nancy.
F-CRIN INI-CRCT Cardiovascular and Renal Clinical Trialists Network, Nancy.

Kevin Duarte (K)

Centre d'Investigations Cliniques Plurithématique 1433, Université de Lorraine, INSERM 1116, CHRU de Nancy.
F-CRIN INI-CRCT Cardiovascular and Renal Clinical Trialists Network, Nancy.

Pauline Scherdel (P)

INSERM, UMR1153 Epidemiology and Biostatistics Sorbonne Paris Cité Center (CRESS), Early Determinants of the Child's Health and Development Team (ORCHAD), Paris.

Barbara Heude (B)

INSERM, UMR1153 Epidemiology and Biostatistics Sorbonne Paris Cité Center (CRESS), Early Determinants of the Child's Health and Development Team (ORCHAD), Paris.

Vincent Dupont (V)

Departement of Nephrology, Centre Hospitalier Universitaire de Reims.
French Clinical Research Infrastructure Network, Investigation Network Initiative - Cardiovascular and Renal Clinical Trialists (F-CRIN INI-CRCT), Reims, France.

Erwan Bozec (E)

Centre d'Investigations Cliniques Plurithématique 1433, Université de Lorraine, INSERM 1116, CHRU de Nancy.
F-CRIN INI-CRCT Cardiovascular and Renal Clinical Trialists Network, Nancy.

Emmanuel Bresso (E)

Centre d'Investigations Cliniques Plurithématique 1433, Université de Lorraine, INSERM 1116, CHRU de Nancy.
F-CRIN INI-CRCT Cardiovascular and Renal Clinical Trialists Network, Nancy.

Faiez Zannad (F)

Centre d'Investigations Cliniques Plurithématique 1433, Université de Lorraine, INSERM 1116, CHRU de Nancy.
F-CRIN INI-CRCT Cardiovascular and Renal Clinical Trialists Network, Nancy.

Patrick Rossignol (P)

Centre d'Investigations Cliniques Plurithématique 1433, Université de Lorraine, INSERM 1116, CHRU de Nancy.
F-CRIN INI-CRCT Cardiovascular and Renal Clinical Trialists Network, Nancy.

Nicolas Girerd (N)

Centre d'Investigations Cliniques Plurithématique 1433, Université de Lorraine, INSERM 1116, CHRU de Nancy.
F-CRIN INI-CRCT Cardiovascular and Renal Clinical Trialists Network, Nancy.

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