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Published in: BMC Cardiovascular Disorders 1/2020

Open Access 01-12-2020 | Obesity | Research article

The association between anthropometric measures of adiposity and the progression of carotid atherosclerosis

Authors: Yume Imahori, Ellisiv B. Mathiesen, Katy E. Morgan, Chris Frost, Alun D. Hughes, Laila A. Hopstock, Stein Harald Johnsen, Nina Emaus, David A. Leon

Published in: BMC Cardiovascular Disorders | Issue 1/2020

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Abstract

Background

Few reports are available on the contribution of general and abdominal obesity to the progression of carotid atherosclerosis in late adulthood. This study investigated the impact of four simple anthropometric measures of general and abdominal obesity on the progression of carotid atherosclerosis and the extent to which the association between adiposity and the progression of plaque burden is mediated by cardiometabolic markers.

Methods

Four thousand three hundred forty-five adults (median age 60) from the population-based Tromsø Study were followed over 7 years from the first carotid ultrasound screening to the next. The progression of carotid atherosclerosis was measured in three ways: incidence of plaques in previously plaque-free participants; change in the number of plaques; and total plaque area (TPA). We used generalised linear models to investigate the association between each adiposity measure – body mass index (BMI), waist circumference (WC), waist-to-hip ratio (WHR), and waist-to-height ratio (WHtR) – and each outcome. Models were adjusted for potential confounders (age, sex, smoking, education, physical activity). The pathways through which any associations observed might operate were investigated by further adjusting for cardiometabolic mediators (systolic blood pressure, cholesterol, and HbA1c).

Results

There was little evidence that adiposity was related to the formation of new plaques during follow-up. However, abdominal adiposity was associated with TPA progression. WHtR showed the largest effect size (mean change in TPA per one standard deviation (SD) increase in WHtR of 0.665 mm2, 95% confidence interval 0.198, 1.133) while BMI showed the smallest. Effect sizes were substantially reduced after the adjustment for potential mediators.

Conclusions

Abdominal obesity indirectly measured with WC seems more strongly associated with the progression of TPA than general obesity. These associations appear to be largely mediated by known cardiometabolic markers.
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Literature
2.
go back to reference Moran AE, Forouzanfar MH, Roth GA, Mensah GA, Ezzati M, Murray CJ, et al. Temporal trends in ischemic heart disease mortality in 21 world regions, 1980 to 2010: the global burden of disease 2010 study. Circulation. 2014;129(14):1483–92.CrossRef Moran AE, Forouzanfar MH, Roth GA, Mensah GA, Ezzati M, Murray CJ, et al. Temporal trends in ischemic heart disease mortality in 21 world regions, 1980 to 2010: the global burden of disease 2010 study. Circulation. 2014;129(14):1483–92.CrossRef
3.
go back to reference Mensah GA, Wei GS, Sorlie PD, Fine LJ, Rosenberg Y, Kaufmann PG, et al. Decline in cardiovascular mortality: possible causes and implications. Circ Res. 2017;120(2):366–80.CrossRef Mensah GA, Wei GS, Sorlie PD, Fine LJ, Rosenberg Y, Kaufmann PG, et al. Decline in cardiovascular mortality: possible causes and implications. Circ Res. 2017;120(2):366–80.CrossRef
4.
go back to reference Preston SH, Vierboom YC, Stokes A. The role of obesity in exceptionally slow US mortality improvement. Proc Natl Acad Sci U S A. 2018;115(5):957–61.CrossRef Preston SH, Vierboom YC, Stokes A. The role of obesity in exceptionally slow US mortality improvement. Proc Natl Acad Sci U S A. 2018;115(5):957–61.CrossRef
5.
go back to reference Lloyd-Jones DM. Slowing Progress in cardiovascular mortality rates: you reap what you sow. JAMA Cardiol. 2016;1(5):599–600.CrossRef Lloyd-Jones DM. Slowing Progress in cardiovascular mortality rates: you reap what you sow. JAMA Cardiol. 2016;1(5):599–600.CrossRef
6.
go back to reference Inaba Y, Chen JA, Bergmann SR. Carotid plaque, compared with carotid intima-media thickness, more accurately predicts coronary artery disease events: a meta-analysis. Atherosclerosis. 2012;220(1):128–33.CrossRef Inaba Y, Chen JA, Bergmann SR. Carotid plaque, compared with carotid intima-media thickness, more accurately predicts coronary artery disease events: a meta-analysis. Atherosclerosis. 2012;220(1):128–33.CrossRef
7.
go back to reference 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(8):648–54.CrossRef 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(8):648–54.CrossRef
8.
go back to reference Herder M, Johnsen SH, Arntzen KA, Mathiesen EB. Risk factors for progression of carotid intima-media thickness and total plaque area: a 13-year follow-up study: the Tromso study. Stroke. 2012;43(7):1818–23.CrossRef Herder M, Johnsen SH, Arntzen KA, Mathiesen EB. Risk factors for progression of carotid intima-media thickness and total plaque area: a 13-year follow-up study: the Tromso study. Stroke. 2012;43(7):1818–23.CrossRef
9.
go back to reference van der Meer IM, Iglesias del Sol A, Hak AE, Bots ML, Hofman A, Witteman JC. Risk factors for progression of atherosclerosis measured at multiple sites in the arterial tree: the Rotterdam study. Stroke. 2003;34(10):2374–9.CrossRef van der Meer IM, Iglesias del Sol A, Hak AE, Bots ML, Hofman A, Witteman JC. Risk factors for progression of atherosclerosis measured at multiple sites in the arterial tree: the Rotterdam study. Stroke. 2003;34(10):2374–9.CrossRef
10.
go back to reference Molino-Lova R, Macchi C, Gori AM, Marcucci R, Polcaro P, Cecchi F, et al. High sensitivity C-reactive protein predicts the development of new carotid artery plaques in older persons. Nutr Metab Cardiovasc Dis. 2011;21(10):776–82.CrossRef Molino-Lova R, Macchi C, Gori AM, Marcucci R, Polcaro P, Cecchi F, et al. High sensitivity C-reactive protein predicts the development of new carotid artery plaques in older persons. Nutr Metab Cardiovasc Dis. 2011;21(10):776–82.CrossRef
11.
go back to reference Sturlaugsdottir R, Aspelund T, Bjornsdottir G, Sigurdsson S, Thorsson B, Eiriksdottir G, et al. Predictors of carotid plaque progression over a 4-year follow-up in the Reykjavik REFINE-study. Atherosclerosis. 2018;269:57–62.CrossRef Sturlaugsdottir R, Aspelund T, Bjornsdottir G, Sigurdsson S, Thorsson B, Eiriksdottir G, et al. Predictors of carotid plaque progression over a 4-year follow-up in the Reykjavik REFINE-study. Atherosclerosis. 2018;269:57–62.CrossRef
12.
go back to reference Tchernof A, Despres JP. Pathophysiology of human visceral obesity: an update. Physiol Rev. 2013;93(1):359–404.CrossRef Tchernof A, Despres JP. Pathophysiology of human visceral obesity: an update. Physiol Rev. 2013;93(1):359–404.CrossRef
13.
go back to reference Imahori Y, Mathiesen EB, Leon DA, Hopstock LA, Hughes AD, Johnsen SH, et al. The contribution of obesity to carotid atherosclerotic plaque burden in a general population sample in Norway: the Tromso study. Atherosclerosis. 2018;273:15–20.CrossRef Imahori Y, Mathiesen EB, Leon DA, Hopstock LA, Hughes AD, Johnsen SH, et al. The contribution of obesity to carotid atherosclerotic plaque burden in a general population sample in Norway: the Tromso study. Atherosclerosis. 2018;273:15–20.CrossRef
14.
go back to reference Jacobsen BK, Eggen AE, Mathiesen EB, Wilsgaard T, Njolstad I. Cohort profile: the Tromso study. Int J Epidemiol. 2012;41(4):961–7.CrossRef Jacobsen BK, Eggen AE, Mathiesen EB, Wilsgaard T, Njolstad I. Cohort profile: the Tromso study. Int J Epidemiol. 2012;41(4):961–7.CrossRef
17.
go back to reference Joakimsen O, Bonaa KH, Stensland-Bugge E. Reproducibility of ultrasound assessment of carotid plaque occurrence, thickness, and morphology. Tromso Study. Stroke. 1997;28(11):2201–7.CrossRef Joakimsen O, Bonaa KH, Stensland-Bugge E. Reproducibility of ultrasound assessment of carotid plaque occurrence, thickness, and morphology. Tromso Study. Stroke. 1997;28(11):2201–7.CrossRef
18.
go back to reference Fosse E, Johnsen SH, Stensland-Bugge E, Joakimsen O, Mathiesen EB, Arnesen E, et al. Repeated visual and computer-assisted carotid plaque characterization in a longitudinal population-based ultrasound study: the Tromso study. Ultrasound Med Biol. 2006;32(1):3–11.CrossRef Fosse E, Johnsen SH, Stensland-Bugge E, Joakimsen O, Mathiesen EB, Arnesen E, et al. Repeated visual and computer-assisted carotid plaque characterization in a longitudinal population-based ultrasound study: the Tromso study. Ultrasound Med Biol. 2006;32(1):3–11.CrossRef
19.
go back to reference Ceponiene I, Klumbiene J, Tamuleviciute-Prasciene E, Motiejunaite J, Sakyte E, Ceponis J, et al. Associations between risk factors in childhood (12–13 years) and adulthood (48–49 years) and subclinical atherosclerosis: The Kaunas Cardiovascular Risk Cohort Study. BMC Cardiovascular Disorders. 2015;15 (1) (no pagination)(89). Ceponiene I, Klumbiene J, Tamuleviciute-Prasciene E, Motiejunaite J, Sakyte E, Ceponis J, et al. Associations between risk factors in childhood (12–13 years) and adulthood (48–49 years) and subclinical atherosclerosis: The Kaunas Cardiovascular Risk Cohort Study. BMC Cardiovascular Disorders. 2015;15 (1) (no pagination)(89).
20.
go back to reference Ferreira I, Twisk JWR, Van Mechelen W, Kemper HCG, Seidell JC, Stehouwer CDA. Current and adolescent body fatness and fat distribution: relationships with carotid intima-media thickness and large artery stiffness at the age of 36 years. J Hypertens. 2004;22(1):145–55.CrossRef Ferreira I, Twisk JWR, Van Mechelen W, Kemper HCG, Seidell JC, Stehouwer CDA. Current and adolescent body fatness and fat distribution: relationships with carotid intima-media thickness and large artery stiffness at the age of 36 years. J Hypertens. 2004;22(1):145–55.CrossRef
21.
go back to reference Freedman DS, Dietz WH, Tang R, Mensah GA, Bond MG, Urbina EM, et al. The relation of obesity throughout life to carotid intima-media thickness in adulthood: the Bogalusa heart study. Int J Obes. 2004;28(1):159–66.CrossRef Freedman DS, Dietz WH, Tang R, Mensah GA, Bond MG, Urbina EM, et al. The relation of obesity throughout life to carotid intima-media thickness in adulthood: the Bogalusa heart study. Int J Obes. 2004;28(1):159–66.CrossRef
22.
go back to reference Freedman DS, Patel DA, Srinivasan SR, Chen W, Tang R, Bond MG, et al. The contribution of childhood obesity to adult carotid intima-media thickness: the Bogalusa heart study. Int J Obes. 2008;32(5):749–56.CrossRef Freedman DS, Patel DA, Srinivasan SR, Chen W, Tang R, Bond MG, et al. The contribution of childhood obesity to adult carotid intima-media thickness: the Bogalusa heart study. Int J Obes. 2008;32(5):749–56.CrossRef
23.
go back to reference Huynh Q, Blizzard L, Sharman J, Magnussen C, Schmidt M, Dwyer T, et al. Relative contributions of adiposity in childhood and adulthood to vascular health of young adults. Atherosclerosis. 2013;228(1):259–64.CrossRef Huynh Q, Blizzard L, Sharman J, Magnussen C, Schmidt M, Dwyer T, et al. Relative contributions of adiposity in childhood and adulthood to vascular health of young adults. Atherosclerosis. 2013;228(1):259–64.CrossRef
24.
go back to reference Raitakari OT, Juonala M, Kahonen M, Taittonen L, Laitinen T, Maki-Torkko N, et al. Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the cardiovascular risk in young Finns study. JAMA. 2003;290(17):2277–83.CrossRef Raitakari OT, Juonala M, Kahonen M, Taittonen L, Laitinen T, Maki-Torkko N, et al. Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the cardiovascular risk in young Finns study. JAMA. 2003;290(17):2277–83.CrossRef
25.
go back to reference Global BMIMC, Di Angelantonio E, Bhupathiraju Sh N, Wormser D, Gao P, Kaptoge S, et al. Body-mass index and all-cause mortality: individual-participant-data meta-analysis of 239 prospective studies in four continents. Lancet. 2016;388(10046):776–86.CrossRef Global BMIMC, Di Angelantonio E, Bhupathiraju Sh N, Wormser D, Gao P, Kaptoge S, et al. Body-mass index and all-cause mortality: individual-participant-data meta-analysis of 239 prospective studies in four continents. Lancet. 2016;388(10046):776–86.CrossRef
26.
go back to reference Yusuf S, Hawken S, Ounpuu S, Dans T, Avezum A, Lanas F, et al. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet. 2004;364(9438):937–52.CrossRef Yusuf S, Hawken S, Ounpuu S, Dans T, Avezum A, Lanas F, et al. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet. 2004;364(9438):937–52.CrossRef
27.
go back to reference O'Donnell MJ, Chin SL, Rangarajan S, Xavier D, Liu L, Zhang H, et al. Global and regional effects of potentially modifiable risk factors associated with acute stroke in 32 countries (INTERSTROKE): a case-control study. Lancet. 2016;388(10046):761–75.CrossRef O'Donnell MJ, Chin SL, Rangarajan S, Xavier D, Liu L, Zhang H, et al. Global and regional effects of potentially modifiable risk factors associated with acute stroke in 32 countries (INTERSTROKE): a case-control study. Lancet. 2016;388(10046):761–75.CrossRef
28.
go back to reference Emdin CA, Khera AV, Natarajan P, Klarin D, Zekavat SM, Hsiao AJ, et al. Genetic Association of Waist-to-hip Ratio with Cardiometabolic Traits, type 2 diabetes, and coronary heart disease. JAMA. 2017;317(6):626–34.CrossRef Emdin CA, Khera AV, Natarajan P, Klarin D, Zekavat SM, Hsiao AJ, et al. Genetic Association of Waist-to-hip Ratio with Cardiometabolic Traits, type 2 diabetes, and coronary heart disease. JAMA. 2017;317(6):626–34.CrossRef
29.
go back to reference Dale CE, Fatemifar G, Palmer TM, White J, Prieto-Merino D, Zabaneh D, et al. Causal associations of adiposity and body fat distribution with coronary heart disease, stroke subtypes, and type 2 diabetes mellitus: a Mendelian randomization analysis. Circulation. 2017;135(24):2373–88.CrossRef Dale CE, Fatemifar G, Palmer TM, White J, Prieto-Merino D, Zabaneh D, et al. Causal associations of adiposity and body fat distribution with coronary heart disease, stroke subtypes, and type 2 diabetes mellitus: a Mendelian randomization analysis. Circulation. 2017;135(24):2373–88.CrossRef
30.
go back to reference Finn AV, Kolodgie FD, Virmani R. Correlation between carotid intimal/medial thickness and atherosclerosis: a point of view from pathology. Arterioscler Thromb Vasc Biol. 2010;30(2):177–81.CrossRef Finn AV, Kolodgie FD, Virmani R. Correlation between carotid intimal/medial thickness and atherosclerosis: a point of view from pathology. Arterioscler Thromb Vasc Biol. 2010;30(2):177–81.CrossRef
31.
go back to reference Wannarong T, Parraga G, Buchanan D, Fenster A, House AA, Hackam DG, et al. Progression of carotid plaque volume predicts cardiovascular events. Stroke. 2013;44(7):1859–65.CrossRef Wannarong T, Parraga G, Buchanan D, Fenster A, House AA, Hackam DG, et al. Progression of carotid plaque volume predicts cardiovascular events. Stroke. 2013;44(7):1859–65.CrossRef
32.
go back to reference Global Burden of Metabolic Risk Factors for Chronic Diseases C, Lu Y, Hajifathalian K, Ezzati M, Woodward M, Rimm EB, et al. Metabolic mediators of the effects of body-mass index, overweight, and obesity on coronary heart disease and stroke: a pooled analysis of 97 prospective cohorts with 1.8 million participants. Lancet. 2014;383(9921):970–83.CrossRef Global Burden of Metabolic Risk Factors for Chronic Diseases C, Lu Y, Hajifathalian K, Ezzati M, Woodward M, Rimm EB, et al. Metabolic mediators of the effects of body-mass index, overweight, and obesity on coronary heart disease and stroke: a pooled analysis of 97 prospective cohorts with 1.8 million participants. Lancet. 2014;383(9921):970–83.CrossRef
34.
go back to reference Dombrowski SU, Knittle K, Avenell A, Araujo-Soares V, Sniehotta FF. Long term maintenance of weight loss with non-surgical interventions in obese adults: systematic review and meta-analyses of randomised controlled trials. BMJ. 2014;348:g2646.CrossRef Dombrowski SU, Knittle K, Avenell A, Araujo-Soares V, Sniehotta FF. Long term maintenance of weight loss with non-surgical interventions in obese adults: systematic review and meta-analyses of randomised controlled trials. BMJ. 2014;348:g2646.CrossRef
35.
go back to reference Franz MJ, VanWormer JJ, Crain AL, Boucher JL, Histon T, Caplan W, et al. Weight-loss outcomes: a systematic review and meta-analysis of weight-loss clinical trials with a minimum 1-year follow-up. J Am Diet Assoc. 2007;107(10):1755–67.CrossRef Franz MJ, VanWormer JJ, Crain AL, Boucher JL, Histon T, Caplan W, et al. Weight-loss outcomes: a systematic review and meta-analysis of weight-loss clinical trials with a minimum 1-year follow-up. J Am Diet Assoc. 2007;107(10):1755–67.CrossRef
36.
go back to reference Bays HE. Adiposopathy is "sick fat" a cardiovascular disease? J Am Coll Cardiol. 2011;57(25):2461–73.CrossRef Bays HE. Adiposopathy is "sick fat" a cardiovascular disease? J Am Coll Cardiol. 2011;57(25):2461–73.CrossRef
37.
go back to reference Mons U, Muezzinler A, Gellert C, Schottker B, Abnet CC, Bobak M, et al. Impact of smoking and smoking cessation on cardiovascular events and mortality among older adults: meta-analysis of individual participant data from prospective cohort studies of the CHANCES consortium. BMJ. 2015;350:h1551.CrossRef Mons U, Muezzinler A, Gellert C, Schottker B, Abnet CC, Bobak M, et al. Impact of smoking and smoking cessation on cardiovascular events and mortality among older adults: meta-analysis of individual participant data from prospective cohort studies of the CHANCES consortium. BMJ. 2015;350:h1551.CrossRef
38.
go back to reference Lavie CJ, De Schutter A, Patel DA, Romero-Corral A, Artham SM, Milani RV. Body composition and survival in stable coronary heart disease: impact of lean mass index and body fat in the "obesity paradox". J Am Coll Cardiol. 2012;60(15):1374–80.CrossRef Lavie CJ, De Schutter A, Patel DA, Romero-Corral A, Artham SM, Milani RV. Body composition and survival in stable coronary heart disease: impact of lean mass index and body fat in the "obesity paradox". J Am Coll Cardiol. 2012;60(15):1374–80.CrossRef
39.
go back to reference Srikanthan P, Horwich TB, Tseng CH. Relation of muscle mass and fat mass to cardiovascular disease mortality. Am J Cardiol. 2016;117(8):1355–60.CrossRef Srikanthan P, Horwich TB, Tseng CH. Relation of muscle mass and fat mass to cardiovascular disease mortality. Am J Cardiol. 2016;117(8):1355–60.CrossRef
40.
go back to reference Ko BJ, Chang Y, Jung HS, Yun KE, Kim CW, Park HS, et al. Relationship between low relative muscle mass and coronary artery calcification in healthy adults. Arterioscler Thromb Vasc Biol. 2016;36(5):1016–21.CrossRef Ko BJ, Chang Y, Jung HS, Yun KE, Kim CW, Park HS, et al. Relationship between low relative muscle mass and coronary artery calcification in healthy adults. Arterioscler Thromb Vasc Biol. 2016;36(5):1016–21.CrossRef
41.
go back to reference Mason C, Katzmarzyk PT. Variability in waist circumference measurements according to anatomic measurement site. Obesity (Silver Spring). 2009;17(9):1789–95.CrossRef Mason C, Katzmarzyk PT. Variability in waist circumference measurements according to anatomic measurement site. Obesity (Silver Spring). 2009;17(9):1789–95.CrossRef
42.
go back to reference Ross R, Berentzen T, Bradshaw AJ, Janssen I, Kahn HS, Katzmarzyk PT, et al. Does the relationship between waist circumference, morbidity and mortality depend on measurement protocol for waist circumference? Obes Rev. 2008;9(4):312–25.CrossRef Ross R, Berentzen T, Bradshaw AJ, Janssen I, Kahn HS, Katzmarzyk PT, et al. Does the relationship between waist circumference, morbidity and mortality depend on measurement protocol for waist circumference? Obes Rev. 2008;9(4):312–25.CrossRef
Metadata
Title
The association between anthropometric measures of adiposity and the progression of carotid atherosclerosis
Authors
Yume Imahori
Ellisiv B. Mathiesen
Katy E. Morgan
Chris Frost
Alun D. Hughes
Laila A. Hopstock
Stein Harald Johnsen
Nina Emaus
David A. Leon
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Cardiovascular Disorders / Issue 1/2020
Electronic ISSN: 1471-2261
DOI
https://doi.org/10.1186/s12872-020-01417-0

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