Advertisement

Vascular aging in the young: New carotid stiffness centiles and association with general and abdominal obesity – The KIGGS cohort

  • J. Büschges
    Correspondence
    Corresponding author. Robert Koch Institute, Department of Epidemiology and Health Monitoring, General Pape Str. 62-66, D-12101, Berlin, Germany.
    Affiliations
    Robert Koch Institute, Department of Epidemiology and Health Monitoring, Berlin, Germany

    DZHK (German Centre for Cardiovascular Research), Partner Site Berlin, Germany
    Search for articles by this author
  • A. Schaffrath Rosario
    Affiliations
    Robert Koch Institute, Department of Epidemiology and Health Monitoring, Berlin, Germany
    Search for articles by this author
  • A. Schienkiewitz
    Affiliations
    Robert Koch Institute, Department of Epidemiology and Health Monitoring, Berlin, Germany
    Search for articles by this author
  • K. Königstein
    Affiliations
    DZHK (German Centre for Cardiovascular Research), Partner Site Berlin, Germany

    Department of Sport, Exercise and Health, Division Sports and Exercise Medicine, University of Basel, Switzerland
    Search for articles by this author
  • G. Sarganas
    Affiliations
    Robert Koch Institute, Department of Epidemiology and Health Monitoring, Berlin, Germany

    DZHK (German Centre for Cardiovascular Research), Partner Site Berlin, Germany
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this work.
    A. Schmidt-Trucksäss
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    Department of Sport, Exercise and Health, Division Sports and Exercise Medicine, University of Basel, Switzerland
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this work.
    H. Neuhauser
    Correspondence
    Corresponding author. Robert Koch Institute, Department of Epidemiology and Health Monitoring, General Pape Str. 62-66, D-12101, Berlin, Germany.
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    Robert Koch Institute, Department of Epidemiology and Health Monitoring, Berlin, Germany

    DZHK (German Centre for Cardiovascular Research), Partner Site Berlin, Germany
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this work.

      Highlights

      • Carotid vascular aging in adolescents to young adults is measured in a large cohort.
      • Sex-, age- and height-specific reference centiles are presented for carotid stiffness.
      • From the age of 14, young men have stiffer arteries than young women.
      • Carotid stiffness increases with age in both sexes.
      • Cross-sectionally and longitudinally adverse effects of obesity on carotid stiffness are observed.

      Abstract

      Background and aims

      The evidence for an association between obesity and increased carotid intima-media thickness (CIMT) and carotid stiffness (CS) in the young has been limited by methodological challenges related to study populations, measurements, methods of percentile derivation and comprehensiveness of obesity markers investigated. This nationwide general population study developed new CS and CIMT centiles in the young and used them to study associations with body mass index, waist circumference, waist-to-height-ratio, bioimpedance-derived absolute and relative fat mass, fat-free mass, subscapular skinfold thickness and blood pressure.

      Methods

      In its 11-year follow-up, the KiGGS cohort, which is based on a nationally representative sample, included semi-automated state-of-the-art sonographic CIMT and CS measurements in 4,709 participants aged 14 to 28. Distensibility coefficient (DC), stiffness index β, Young's elastic modulus (YEM) and Peterson's elastic modulus (Ep) centiles were modelled by sex, age and height simultaneously.

      Results

      CS increased with age in both sexes, and young men had stiffer arteries than young women at all ages. All obesity measures at baseline and at follow-up, except for subscapular skinfold thickness, were positively associated with several CS parameters with moderate relative risks (RR), e.g. cross-sectional RR 2.23 (95% CI 1.26–3.93) for DC ≥ 90th percentile when waist circumference ≥90th percentile; RR 5.98 (3.38–10.56) for elevated DC associated with simultaneously elevated waist circumference and BP.

      Conclusions

      These new state-of-the-art CS percentiles show consistent associations of obesity with CS in the young and support primary prevention efforts starting at a young age.

      Graphical abstract

      keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Atherosclerosis
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Laurent S.
        Defining vascular aging and cardiovascular risk.
        J. Hypertens. 2012; 30: S3-S8
        • de Groot E.
        • Hovingh G.K.
        • Wiegman A.
        • Duriez P.
        • Smit A.J.
        • Fruchart J.C.
        • et al.
        Measurement of arterial wall thickness as a surrogate marker for atherosclerosis.
        Circulation. 2004; 109: III33-I38
        • Dalla Pozza R.
        • Ehringer-Schetitska D.
        • Fritsch P.
        • Jokinen E.
        • Petropoulos A.
        • Oberhoffer R.
        • et al.
        Intima media thickness measurement in children: a statement from the association for European paediatric cardiology (AEPC) working group on cardiovascular prevention endorsed by the association for European paediatric cardiology.
        Atherosclerosis. 2015; 238: 380-387
        • Urbina E.M.
        • Srinivasan S.R.
        • Kieltyka R.L.
        • Tang R.
        • Bond M.G.
        • Chen W.
        • et al.
        Correlates of carotid artery stiffness in young adults: the Bogalusa Heart Study.
        Atherosclerosis. 2004; 176: 157-164
        • Caviezel S.
        • Dratva J.
        • Schaffner E.
        • Teynor A.
        • Baumstark M.W.
        • Schindler C.
        • et al.
        Variability and reproducibility of carotid structural and functional parameters assessed with transcutaneous ultrasound - results from the SAPALDIA Cohort Study.
        Atherosclerosis. 2013; 231: 448-455
        • Juonala M.
        • Viikari J.S.
        • Kahonen M.
        • Taittonen L.
        • Laitinen T.
        • Hutri-Kahonen N.
        • et al.
        Life-time risk factors and progression of carotid atherosclerosis in young adults: the Cardiovascular Risk in Young Finns study.
        Eur. Heart J. 2010; 31: 1745-1751
        • Yan Y.
        • Hou D.
        • Liang Y.
        • Zhao X.
        • Hu Y.
        • Liu J.
        • et al.
        Tracking body mass index from childhood to adulthood for subclinical cardiovascular diseases at adulthood.
        J. Am. Coll. Cardiol. 2016; 67: 1006-1007
        • Koskinen J.S.
        • Kyto V.
        • Juonala M.
        • Viikari J.S.A.
        • Nevalainen J.
        • Kahonen M.
        • et al.
        Childhood risk factors and carotid atherosclerotic plaque in adulthood: the Cardiovascular Risk in Young Finns Study.
        Atherosclerosis. 2020; 293: 18-25
        • Buscot M.J.
        • Thomson R.J.
        • Juonala M.
        • Sabin M.A.
        • Burgner D.P.
        • Lehtimaki 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
        • Sanchez A.
        • Barth J.D.
        • Zhang L.
        The carotid artery wall thickness in teenagers is related to their diet and the typical risk factors of heart disease among adults.
        Atherosclerosis. 2000; 152: 265-266
        • Shah A.S.
        • Dolan L.M.
        • Khoury P.R.
        • Gao Z.
        • Kimball T.R.
        • Urbina E.M.
        Severe obesity in adolescents and young adults is associated with subclinical cardiac and vascular changes.
        J. Clin. Endocrinol. Metab. 2015; 100: 2751-2757
        • Geerts C.C.
        • Evelein A.M.
        • Bots M.L.
        • van der Ent C.K.
        • Grobbee D.E.
        • Uiterwaal C.S.
        Body fat distribution and early arterial changes in healthy 5-year-old children.
        Ann. Med. 2012; 44: 350-359
        • Kollias A.
        • Psilopatis I.
        • Karagiaouri E.
        • Glaraki M.
        • Grammatikos E.
        • Grammatikos E.E.
        • et al.
        Adiposity, blood pressure, and carotid intima-media thickness in Greek adolescents.
        Obesity. 2013; 21: 1013-1017
        • Konigstein K.
        • von Schenck U.
        • Buschges J.C.
        • Schweizer D.
        • Vogelgesang F.
        • Damerow S.
        • et al.
        Carotid IMT and stiffness in the KiGGS 2 national survey: third-generation measurement, quality algorithms and determinants of completeness.
        Ultrasound Med. Biol. 2021; 47: 296-308
        • Doyon A.
        • Kracht D.
        • Bayazit A.K.
        • Deveci M.
        • Duzova A.
        • Krmar R.T.
        • et al.
        Carotid artery intima-media thickness and distensibility in children and adolescents: reference values and role of body dimensions.
        Hypertension. 2013; 62: 550-556
        • Jourdan C.
        • Wuhl E.
        • Litwin M.
        • Fahr K.
        • Trelewicz J.
        • Jobs K.
        • et al.
        Normative values for intima-media thickness and distensibility of large arteries in healthy adolescents.
        J. Hypertens. 2005; 23: 1707-1715
        • Weberruss H.
        • Pirzer R.
        • Bohm B.
        • Elmenhorst J.
        • Pozza R.D.
        • Netz H.
        • et al.
        Increased intima-media thickness is not associated with stiffer arteries in children.
        Atherosclerosis. 2015; 242: 48-55
        • Davis P.H.
        • Dawson J.D.
        • Riley W.A.
        • Lauer R.M.
        Carotid intimal-medial thickness is related to cardiovascular risk factors measured from childhood through middle age: the Muscatine Study.
        Circulation. 2001; 104: 2815-2819
        • Recio-Rodriguez J.I.
        • Gomez-Marcos M.A.
        • Patino-Alonso M.C.
        • Agudo-Conde C.
        • Rodriguez-Sanchez E.
        • Garcia-Ortiz L.
        • et al.
        Abdominal obesity vs general obesity for identifying arterial stiffness, subclinical atherosclerosis and wave reflection in healthy, diabetics and hypertensive.
        Bmc Cardiovasc. Disor. 2012; 12
        • Chiesa S.T.
        • Charakida M.
        • Georgiopoulos G.
        • Dangardt F.
        • Wade K.H.
        • Rapala A.
        • et al.
        Determinants of Intima-Media Thickness in the Young: the ALSPAC Study.
        JACC Cardiovasc Imaging, 2019
        • Park M.H.
        • Skow A.
        • De Matteis S.
        • Kessel A.S.
        • Saxena S.
        • Viner R.M.
        • et al.
        Adiposity and carotid-intima media thickness in children and adolescents: a systematic review.
        BMC Pediatr. 2015; 15: 161
        • Urbina E.M.
        • Kimball T.R.
        • Khoury P.R.
        • Daniels S.R.
        • Dolan L.M.
        Increased arterial stiffness is found in adolescents with obesity or obesity-related type 2 diabetes mellitus.
        J. Hypertens. 2010; 28: 1692-1698
        • Weberruss H.
        • Pirzer R.
        • Bohm B.
        • Dalla Pozza R.
        • Netz H.
        • Oberhoffer R.
        Intima-media thickness and arterial function in obese and non-obese children.
        BMC Obes. 2015; 3: 2
        • Mauz E.
        • Lange M.
        • Houben R.
        • Hoffmann R.
        • Allen J.
        • Gößwald A.
        • et al.
        Cohort Profile: KiGGS Cohort - longitudinal study on the health of children, adolescents, and young adults in Germany.
        Int. J. Epidemiol. 2019; (accepted. Int J Epidemiol. 2019 (accepted))
        • Stein J.H.
        • Korcarz C.E.
        • Hurst R.T.
        • Lonn E.
        • Kendall C.B.
        • Mohler E.R.
        • et al.
        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. 2008; 21 (quiz 89-90): 93-111
        • Touboul P.J.
        • Hennerici M.G.
        • Meairs S.
        • Adams H.
        • Amarenco P.
        • Bornstein N.
        • et al.
        Mannheim carotid intima-media thickness consensus (2004-2006). An update on behalf of the advisory board of the 3rd and 4th watching the risk symposium, 13th and 15th European stroke conferences, mannheim, Germany, 2004, and brussels, Belgium, 2006.
        Cerebrovasc. Dis. 2007; 23: 75-80
        • Kromeyer-Hauschild K.
        • Wabitsch M.
        • Kunze D.
        • Geller F.
        • Geiß H.
        • Hesse V.
        • et al.
        Perzentile für den Body-mass-Index für das Kindes- und Jugendalter unter Heranziehung verschiedener deutscher Stichproben.
        Monatsschr. Kinderheilkd. 2001; 149: 807-818
        • Consultation W.
        Obesity: preventing and managing the global epidemic - Introduction.
        WHO Tech. Rep. Ser. 2000; 894: 1-253
        • Kromeyer-Hauschild K.
        • Dortschy R.
        • Stolzenberg H.
        • Neuhauser H.
        • Rosario A.S.
        Nationally representative waist circumference percentiles in German adolescents aged 11.0-18.0 years.
        Int. J. Pediatr. Obes. 2011; 6: E129-E137
        • Kromeyer-Hauschild K.
        • Neuhauser H.
        • Schaffrath Rosario A.
        • Schienkiewitz A.
        Abdominal obesity in German adolescents defined by waist-to-height ratio and its association to elevated blood pressure: the KiGGS study.
        Obes Facts. 2013; 6: 165-175
        • Bosy-Westphal A.
        • Schautz B.
        • Later W.
        • Kehayias J.J.
        • Gallagher D.
        • Muller M.J.
        What makes a BIA equation unique? Validity of eight-electrode multifrequency BIA to estimate body composition in a healthy adult population.
        Eur. J. Clin. Nutr. 2013; 67: S14-S21
        • Neuhauser H.
        • Thamm M.
        [Blood pressure measurement in the German health interview and examination survey for children and adolescents (KiGGS). Methodology and initial results].
        Bundesgesundheitsblatt - Gesundheitsforsch. - Gesundheitsschutz. 2007; 50: 728-735
        • Neuhauser H.K.
        • Thamm M.
        • Ellert U.
        • Hense H.W.
        • Rosario A.S.
        Blood pressure percentiles by age and height from nonoverweight children and adolescents in Germany.
        Pediatrics. 2011; 127: e978-e988
        • Andersen L.B.
        • Harro M.
        • Sardinha L.B.
        • Froberg K.
        • Ekelund U.
        • Brage S.
        • et al.
        Physical activity and clustered cardiovascular risk in children: a cross-sectional study (The European Youth Heart Study).
        Lancet. 2006; 368: 299-304
        • Brauns H.S.
        • Susanne
        Educational reform in France, West-Germany and the United Kingdom: updating the CASMIN educational classification.
        ZUMA Nachrichten. 1999; 44: 7-44
        • Rigby R.A.
        • Stasinopoulos D.M.
        Generalized additive models for location, scale and shape.
        J. R. Stat. Soc. C-Appl. 2005; 54: 507-544
        • Royston P.
        • Wright E.M.
        Goodness-of-fit statistics for age-specific reference intervals.
        Stat. Med. 2000; 19: 2943-2962
        • van Buuren S.
        • Fredriks M.
        Worm plot: a simple diagnostic device for modelling growth reference curves.
        Stat. Med. 2001; 20: 1259-1277
        • Neuhauser H.
        • Büschges J.
        • Schaffrath Rosario A.
        • Königstein K.
        • Schweizer D.
        • Damerow S.
        • et al.
        Carotid Artery Intima-Media Thickness in Adolescents and Young Adults: Population-Based Reference Percentiles and Predictive Value of Obesity and Elevated Blood Pressure.
        Manuscript submitted for publication, 2020
        • Zhao M.
        • Lopez-Bermejo A.
        • Caserta C.A.
        • Medeiros C.C.M.
        • Kollias A.
        • Bassols J.
        • et al.
        Metabolically healthy obesity and high carotid intima-media thickness in children and adolescents: international childhood vascular structure evaluation consortium.
        Diabetes Care. 2019; 42: 119-125
        • McNutt L.A.
        • Wu C.T.
        • Xue X.N.
        • Hafner J.P.
        Estimating the relative risk in cohort studies and clinical trials of common outcomes.
        Am. J. Epidemiol. 2003; 157: 940-943
        • Lash T.L.
        Heuristic thinking and inference from observational epidemiology.
        Epidemiology. 2007; 18: 67-72
        • Sterne J.A.C.
        • Smith G.D.
        Sifting the evidence - what's wrong with significance tests?.
        BMJ Br. Med. J. (Clin. Res. Ed.). 2001; 322: 226-+
        • Büschges J.
        • Schaffrath Rosario A.
        • Königstein K.
        • Schmidt-Trucksäss A.
        • Neuhauser H.
        Reference Centile Data for Carotid Stiffness in Adolescents and Young Adults – Based on the Nationwide KIGGS Cohort from Germany.
        2022 (Data in brief (submitted))
        • Weberruss H.
        • Pirzer R.
        • Dalla Pozza R.
        • Netz H.
        • Oberhoffer R.
        Intima-media thickness does not differ between two common carotid artery segments in children.
        PLoS One. 2016; 11e0149057
        • DuPont J.J.
        • Kenney R.M.
        • Patel A.R.
        • Jaffe I.Z.
        Sex differences in mechanisms of arterial stiffness.
        Br. J. Pharmacol. 2019; 176: 4208-4225
        • Aroor A.R.
        • Jia G.
        • Sowers J.R.
        Cellular mechanisms underlying obesity-induced arterial stiffness.
        Am. J. Physiol. Regul. Integr. Comp. Physiol. 2018; 314: R387-R398
        • Menezes A.M.B.
        • da Silva C.T.B.
        • Wehrmeister F.C.
        • Oliveira P.D.
        • Oliveira I.O.
        • Goncalves H.
        • et al.
        Adiposity during adolescence and carotid intima-media thickness in adulthood: results from the 1993 Pelotas Birth Cohort.
        Atherosclerosis. 2016; 255: 25-30
        • Freedman D.S.
        • Dietz W.H.
        • Tang R.
        • Mensah G.A.
        • Bond M.G.
        • Urbina E.M.
        • et al.
        The relation of obesity throughout life to carotid intima-media thickness in adulthood: the Bogalusa Heart Study.
        Int. J. Obes. Relat. Metab. Disord. 2004; 28: 159-166
        • Elkiran O.
        • Yilmaz E.
        • Koc M.
        • Kamanli A.
        • Ustundag B.
        • Ilhan N.
        The association between intima media thickness, central obesity and diastolic blood pressure in obese and overweight children: a cross-sectional school-based study.
        Int. J. Cardiol. 2013; 165: 528-532
        • Al-Shorman A.
        • Al-Domi H.
        • Al-Atoum M.
        The associations of body composition and anthropometric measures with carotid intima-media thickness in obese and non-obese schoolchildren: a possible predictor for cardiovascular diseases.
        Vascular. 2018; 26: 285-290
        • Akbari-Sedigh A.
        • Asghari G.
        • Yuzbashian E.
        • Dehghan P.
        • Imani H.
        • Mirmiran P.
        Association of dietary pattern with carotid intima media thickness among children with overweight or obesity.
        Diabetol. Metab. Syndrome. 2019; 11: 77
        • Juonala M.
        • Magnussen C.G.
        • Venn A.
        • Dwyer T.
        • Burns T.L.
        • Davis P.H.
        • et al.
        Influence of age on associations between childhood risk factors and carotid intima-media thickness in adulthood: the cardiovascular risk in young Finns study, the childhood determinants of adult health study, the Bogalusa heart study, and the muscatine study for the international childhood cardiovascular cohort (i3C) consortium.
        Circulation. 2010; 122: 2514-2520
        • De Michele M.
        • Panico S.
        • Iannuzzi A.
        • Celentano E.
        • Ciardullo A.V.
        • Galasso R.
        • et al.
        Association of obesity and central fat distribution with carotid artery wall thickening in middle-aged women.
        Stroke. 2002; 33: 2923-2928
        • Yan R.T.
        • Yan A.T.
        • Anderson T.J.
        • Buithieu J.
        • Charbonneau F.
        • Title L.
        • et al.
        The differential association between various anthropometric indices of obesity and subclinical atherosclerosis.
        Atherosclerosis. 2009; 207: 232-238