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Published in: Heart and Vessels 1/2020

01-01-2020 | Arterial Occlusive Disease | Original Article

Effect of cigarette smoking on carotid artery atherosclerosis: a community-based cohort study

Authors: Hiroyuki Kiriyama, Hidehiro Kaneko, Hidetaka Itoh, Yuriko Yoshida, Koki Nakanishi, Yoshiko Mizuno, Masao Daimon, Hiroyuki Morita, Nobutake Yamamichi, Issei Komuro

Published in: Heart and Vessels | Issue 1/2020

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Abstract

Cigarette smoking is closely associated with the development of cardiovascular diseases. However, the relationship between cigarette smoking and subclinical atherosclerosis has not been fully studied. We sought to clarify the association between cigarette smoking and carotid intima-media thickness (cIMT) in a general Japanese population. Among 1,209 participants who received a medical check-up with cardiovascular examination at our institution, 450 participants (37.2%) were smokers (including both past and current smokers). We evaluated cIMT as a marker of subclinical atherosclerosis. The value of cIMT and rate of carotid plaque defined as IMT ≥ 1.1 mm did not differ between smokers and never smokers. However, the rate of carotid high-risk atheroma, defined as carotid artery atheroma including hypoechoic dominant and ulceration, was significantly higher among smokers than never smokers (30.4%, vs 23.6%, p = 0.009). Even after adjustment for covariates, cigarette smoking was independently associated with high-risk atheroma formation (odds ratio 1.384, 95% CI 1.019–1.880; p = 0.038). The value of cIMT and the rate of high-risk atheroma were significantly higher in smokers than never smokers in the subgroup of participants aged ≥ 60 years, whereas the rate of high-risk atheroma only was higher in smokers than never smokers in the subgroup of participants aged < 60 years. In conclusion, the development of high-risk carotid artery atheroma may precede the thickening of cIMT in cigarette smokers, which suggests the novel insight for the pathological mechanism underlying cardiovascular events and cigarette smoking.
Literature
1.
go back to reference GBD Risk Factors Collaborators (2015) Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks in 188 countries, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 386:2287–2323CrossRef GBD Risk Factors Collaborators (2015) Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks in 188 countries, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 386:2287–2323CrossRef
2.
go back to reference Thun MJ, Carter BD, Feskanich D, Freedman ND, Prentice R, Lopez AD, Hartge P, Gapstur SM (2013) 50-year trends in smoking-related mortality in the United States. N Engl J Med 368:351–64CrossRef Thun MJ, Carter BD, Feskanich D, Freedman ND, Prentice R, Lopez AD, Hartge P, Gapstur SM (2013) 50-year trends in smoking-related mortality in the United States. N Engl J Med 368:351–64​CrossRef
3.
go back to reference Ng M, Freeman MK, Fleming TD, Robinson M, Dwyer-Lindgren L, Thomson B, Wollum A, Sanman E, Wulf S, Lopez AD, Murray CJL, Gakidou E (2014) Smoking prevalence and cigarette consumption in 187 countries, 1980–2012. JAMA 311:183–192CrossRef Ng M, Freeman MK, Fleming TD, Robinson M, Dwyer-Lindgren L, Thomson B, Wollum A, Sanman E, Wulf S, Lopez AD, Murray CJL, Gakidou E (2014) Smoking prevalence and cigarette consumption in 187 countries, 1980–2012. JAMA 311:183–192CrossRef
4.
go back to reference Jonas MA, Oates JA, Ockene JK, Hennekens CH (1992) Statement on smoking and cardiovascular disease for health care professionals: American Heart Association. Circulation 86:1664–1669CrossRef Jonas MA, Oates JA, Ockene JK, Hennekens CH (1992) Statement on smoking and cardiovascular disease for health care professionals: American Heart Association. Circulation 86:1664–1669CrossRef
5.
go back to reference Leng GC, Lee AJ, Fowkes FG, Lowe GD, Housley E (1995) The relationship between cigarette smoking and cardiovascular risk factors in peripheral arterial disease compared with ischemic heart disease. The Edinburgh Artery Study. Eur Heart J 16:1542–1548CrossRef Leng GC, Lee AJ, Fowkes FG, Lowe GD, Housley E (1995) The relationship between cigarette smoking and cardiovascular risk factors in peripheral arterial disease compared with ischemic heart disease. The Edinburgh Artery Study. Eur Heart J 16:1542–1548CrossRef
6.
go back to reference Burns DM (2003) Epidemiology of smoking-induced cardiovascular disease. Prog Cardiovasc Dis 46:11–29CrossRef Burns DM (2003) Epidemiology of smoking-induced cardiovascular disease. Prog Cardiovasc Dis 46:11–29CrossRef
7.
go back to reference Witteman JCM, Grobbee DE, Valkenburg HA, Vanhemert AM, Stijnen T, Hofman A (1993) Cigarette-smoking and the development and progression of aortic atherosclerosis—a 9-year population-based follow-up-study in women. Circulation 88:2156–2162CrossRef Witteman JCM, Grobbee DE, Valkenburg HA, Vanhemert AM, Stijnen T, Hofman A (1993) Cigarette-smoking and the development and progression of aortic atherosclerosis—a 9-year population-based follow-up-study in women. Circulation 88:2156–2162CrossRef
8.
go back to reference Waters D, Lesperance J, Gladstone P, Boccuzzi SJ, Cook T, Hudgin R, Krip G, Higginson L (1996) Effects of cigarette smoking on the angiographic evolution of coronary atherosclerosis. A Canadian Coronary Atherosclerosis Intervention Trial (CCAIT) Substudy. Circulation 94:614–621CrossRef Waters D, Lesperance J, Gladstone P, Boccuzzi SJ, Cook T, Hudgin R, Krip G, Higginson L (1996) Effects of cigarette smoking on the angiographic evolution of coronary atherosclerosis. A Canadian Coronary Atherosclerosis Intervention Trial (CCAIT) Substudy. Circulation 94:614–621CrossRef
9.
go back to reference Inoue T, Oku K, Kimoto K, Takao M, Nomoto J, Handa K, Kono S, Arakawa K (1995) Relationship of cigarette-smoking to the severity of coronary and thoracic aortic atherosclerosis. Cardiology 86:374–379CrossRef Inoue T, Oku K, Kimoto K, Takao M, Nomoto J, Handa K, Kono S, Arakawa K (1995) Relationship of cigarette-smoking to the severity of coronary and thoracic aortic atherosclerosis. Cardiology 86:374–379CrossRef
10.
go back to reference Peters SAE, Grobbee DE, Bots ML (2011) Carotid intima-media thickness: a suitable alternative for cardiovascular risk as outcome? Eur J Cardiovasc Prev Rehabil 18:167–174CrossRef Peters SAE, Grobbee DE, Bots ML (2011) Carotid intima-media thickness: a suitable alternative for cardiovascular risk as outcome? Eur J Cardiovasc Prev Rehabil 18:167–174CrossRef
11.
go back to reference Lorenz MW, von Kegler S, Steinmetz H, Markus HS, Sitzer M (2006) Carotid intima-media thickening indicates a higher vascular risk across a wide age range: prospective data from the Carotid Atherosclerosis Progression Study (CAPS). Stroke 37:87–92CrossRef Lorenz MW, von Kegler S, Steinmetz H, Markus HS, Sitzer M (2006) Carotid intima-media thickening indicates a higher vascular risk across a wide age range: prospective data from the Carotid Atherosclerosis Progression Study (CAPS). Stroke 37:87–92CrossRef
12.
go back to reference Sinning C, Wild PS, Echevarria FM, Wilde S, Schnabel R, Lubos E, Herkenhoff S, Bickel C, Klimpe S, Gori T, Munzel TF, Blankenberg S, Espinola-Klein C (2011) Sex differences in early carotid atherosclerosis (from the community-based Gutenberg-Heart Study). Am J Cardiol 107:1841–1847CrossRef Sinning C, Wild PS, Echevarria FM, Wilde S, Schnabel R, Lubos E, Herkenhoff S, Bickel C, Klimpe S, Gori T, Munzel TF, Blankenberg S, Espinola-Klein C (2011) Sex differences in early carotid atherosclerosis (from the community-based Gutenberg-Heart Study). Am J Cardiol 107:1841–1847​CrossRef
13.
go back to reference Herder M, Johnsen SH, Arntzen KA, Mathiesen EB (2012) Risk factors for progression of carotid intima-media thickness and total plaque area: a 13-year follow-up study: the Tromso Study. Stroke 43:1818–1823CrossRef Herder M, Johnsen SH, Arntzen KA, Mathiesen EB (2012) Risk factors for progression of carotid intima-media thickness and total plaque area: a 13-year follow-up study: the Tromso Study. Stroke 43:1818–1823CrossRef
14.
go back to reference Jashari F, Ibrahimi P, Bajraktari G, Gronlund C, Wester P, Henein MY (2016) Carotid plaque echogenicity predicts cerebrovascular symptoms: a systematic review and meta-analysis. Eur J Neurol 23:1241–1247CrossRef Jashari F, Ibrahimi P, Bajraktari G, Gronlund C, Wester P, Henein MY (2016) Carotid plaque echogenicity predicts cerebrovascular symptoms: a systematic review and meta-analysis. Eur J Neurol 23:1241–1247CrossRef
15.
go back to reference Yuan J, Usman A, Das T, Patterson AJ, Gillard JH, Graves MJ (2017) Imaging carotid atherosclerosis plaque ulceration: comparison of advanced imaging modalities and recent developments. Am J Neuroradiol 38:664–671CrossRef Yuan J, Usman A, Das T, Patterson AJ, Gillard JH, Graves MJ (2017) Imaging carotid atherosclerosis plaque ulceration: comparison of advanced imaging modalities and recent developments. Am J Neuroradiol 38:664–671CrossRef
16.
go back to reference Salonen R, Salonen JT (1990) Progression of carotid atherosclerosis and its determinants: a population-based ultrasonography study. Atherosclerosis 81:33–40CrossRef Salonen R, Salonen JT (1990) Progression of carotid atherosclerosis and its determinants: a population-based ultrasonography study. Atherosclerosis 81:33–40CrossRef
18.
go back to reference Itoh H, Kaneko H, Kiriyama H, Yoshida Y, Nakanishi K, Mizuno Y, Daimon M, Morita H, Yatomi Y, Yamamichi N, Komuro I (2019) Effect of metabolically healthy obesity on the development of carotid plaque in general population: a community-based cohort study. J Atheroscler Thromb. https://doi.org/10.5551/jat.48728 Itoh H, Kaneko H, Kiriyama H, Yoshida Y, Nakanishi K, Mizuno Y, Daimon M, Morita H, Yatomi Y, Yamamichi N, Komuro I (2019) Effect of metabolically healthy obesity on the development of carotid plaque in general population: a community-based cohort study. J Atheroscler Thromb. https://​doi.​org/​10.​5551/​jat.​48728
19.
go back to reference Gray-Weale AC, Graham JC, Burnett JR, Byrne K, Lusby RJ (1988) Carotid artery atheroma: comparison of preoperative B-mode ultrasound appearance with carotid endarterectomy specimen pathology. J Cardiovasc Surg 29:676–681 Gray-Weale AC, Graham JC, Burnett JR, Byrne K, Lusby RJ (1988) Carotid artery atheroma: comparison of preoperative B-mode ultrasound appearance with carotid endarterectomy specimen pathology. J Cardiovasc Surg 29:676–681
20.
go back to reference Hiramatsu K, Shima T, Toyota A, Yokota A (2003) Usefulness of ultrasonologic examinations on microemboli and hemodynamics for the prevention of complications associated with carotid endarterectomy. J Stroke Cerebrovasc Dis 12:51–58CrossRef Hiramatsu K, Shima T, Toyota A, Yokota A (2003) Usefulness of ultrasonologic examinations on microemboli and hemodynamics for the prevention of complications associated with carotid endarterectomy. J Stroke Cerebrovasc Dis 12:51–58CrossRef
21.
go back to reference Ikeda N, Saito E, Kondo N, Inoue M, Ikeda S, Satoh T, Wada K, Stickley A, Katanoda K, Mizoue T, Noda M, Iso H, Fujino Y, Sobue T, Tsugane S, Naghavi M, Ezzati M, Shibuya K (2011) Japan: Universal Health Care at 50 years 1 What has made the population of Japan healthy? Lancet 378:1094–1105CrossRef Ikeda N, Saito E, Kondo N, Inoue M, Ikeda S, Satoh T, Wada K, Stickley A, Katanoda K, Mizoue T, Noda M, Iso H, Fujino Y, Sobue T, Tsugane S, Naghavi M, Ezzati M, Shibuya K (2011) Japan: Universal Health Care at 50 years 1 What has made the population of Japan healthy? Lancet 378:1094–1105CrossRef
22.
go back to reference Gariepy J, Denarie N, Chironi G, Salomon J, Levenson J, Simon A (2000) Gender difference in the influence of smoking on arterial wall thickness. Atherosclerosis 153:139–145CrossRef Gariepy J, Denarie N, Chironi G, Salomon J, Levenson J, Simon A (2000) Gender difference in the influence of smoking on arterial wall thickness. Atherosclerosis 153:139–145CrossRef
23.
go back to reference Liang YL, Shiel LM, Teede H, Kotsopoulos D, McNeil J, Cameron JD, McGrath BP (2001) Effects of blood pressure, smoking, and their interaction on carotid artery structure and function. Hypertension 37:6–11CrossRef Liang YL, Shiel LM, Teede H, Kotsopoulos D, McNeil J, Cameron JD, McGrath BP (2001) Effects of blood pressure, smoking, and their interaction on carotid artery structure and function. Hypertension 37:6–11CrossRef
24.
go back to reference Raitakari OT, Juonala M, Kahonen M, Taittonen L, Laitinen T, Maki-Torkko N, Jarvisalo MJ, Uhari M, Jokisen E, Ronnemaa T, Akerblom HK, Viikari JS (2003) Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the Cardiovascular Risk in Young Finns Study. JAMA 290:2277–2283CrossRef Raitakari OT, Juonala M, Kahonen M, Taittonen L, Laitinen T, Maki-Torkko N, Jarvisalo MJ, Uhari M, Jokisen E, Ronnemaa T, Akerblom HK, Viikari JS (2003) Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the Cardiovascular Risk in Young Finns Study. JAMA 290:2277–2283CrossRef
25.
go back to reference Karim R, Buchanan TA, Hodis HN, Li Y, Mack WJ (2005) The association of smoking and subclinical atherosclerosis in type 2 diabetes: modification by duration of diabetes. Diabet Med. 22:81–87CrossRef Karim R, Buchanan TA, Hodis HN, Li Y, Mack WJ (2005) The association of smoking and subclinical atherosclerosis in type 2 diabetes: modification by duration of diabetes. Diabet Med. 22:81–87CrossRef
26.
go back to reference Sacco RL, Roberts JK, Boden-Albala B, Gu Q, Lin IF, Kargman DE, Berglund L, Hauser WA, Shea S, Paik MC (1997) Race-ethnicity and determinants of carotid atherosclerosis in a multiethnic population: The Northern Manhattan Stroke Study. Stroke 28:929–935CrossRef Sacco RL, Roberts JK, Boden-Albala B, Gu Q, Lin IF, Kargman DE, Berglund L, Hauser WA, Shea S, Paik MC (1997) Race-ethnicity and determinants of carotid atherosclerosis in a multiethnic population: The Northern Manhattan Stroke Study. Stroke 28:929–935CrossRef
27.
go back to reference Jones DL, Rodriguez VJ, Alcaide ML, Barylski N, Cabral D, Rundek T, Weiss SM, Kumar M (2017) Subclinical atherosclerosis among young and middle-aged adults using carotid intima-media thickness measurements. South Med J 110:733–737CrossRef Jones DL, Rodriguez VJ, Alcaide ML, Barylski N, Cabral D, Rundek T, Weiss SM, Kumar M (2017) Subclinical atherosclerosis among young and middle-aged adults using carotid intima-media thickness measurements. South Med J 110:733–737CrossRef
28.
go back to reference Redgrave JN, Lovett JK, Rothwell PM (2010) Histological features of symptomatic carotid plaques in relation to age and smoking: the oxford plaque study. Stroke 41:2288–2294CrossRef Redgrave JN, Lovett JK, Rothwell PM (2010) Histological features of symptomatic carotid plaques in relation to age and smoking: the oxford plaque study. Stroke 41:2288–2294CrossRef
30.
go back to reference Ambrose JA, Barua RS (2004) The pathophysiology of cigarette smoking and cardiovascular disease: an update. J Am Coll Cardiol 43:1731–1737CrossRef Ambrose JA, Barua RS (2004) The pathophysiology of cigarette smoking and cardiovascular disease: an update. J Am Coll Cardiol 43:1731–1737CrossRef
31.
go back to reference Hisamatsu T, Miura K, Arima H, Kadota A, Kadowaki S, Torii S, Suzuki S, Miyagawa N, Sato A, Yamazoe M, Fujiyoshi A, Ohkubo T, Yamamoto T, Murata K, Abbott RD, Sekikawa A, Horie M, Ueshima H (2016) Smoking, smoking cessation, and measures of subclinical atherosclerosis in multiple vascular beds in Japanese men. J Am Heart Assoc 5(9):e003738CrossRef Hisamatsu T, Miura K, Arima H, Kadota A, Kadowaki S, Torii S, Suzuki S, Miyagawa N, Sato A, Yamazoe M, Fujiyoshi A, Ohkubo T, Yamamoto T, Murata K, Abbott RD, Sekikawa A, Horie M, Ueshima H (2016) Smoking, smoking cessation, and measures of subclinical atherosclerosis in multiple vascular beds in Japanese men. J Am Heart Assoc 5(9):e003738CrossRef
32.
go back to reference Baldassarre D, Castelnuovo S, Frigerio B, Amato M, Werba JP, De Jong A, Ravani AL, Tremoli E, Sirtori CR (2009) Effects of timing and extent of smoking, type of cigarettes, and concomitant risk factors on the association between smoking and subclinical atherosclerosis. Stroke 40:1991–1998CrossRef Baldassarre D, Castelnuovo S, Frigerio B, Amato M, Werba JP, De Jong A, Ravani AL, Tremoli E, Sirtori CR (2009) Effects of timing and extent of smoking, type of cigarettes, and concomitant risk factors on the association between smoking and subclinical atherosclerosis. Stroke 40:1991–1998CrossRef
33.
go back to reference Shephard RJ (2003) Limits to the measurement of habitual physical activity by questionnaires. Br J Sports Med 37:197–206CrossRef Shephard RJ (2003) Limits to the measurement of habitual physical activity by questionnaires. Br J Sports Med 37:197–206CrossRef
34.
go back to reference Cires-Drouet RS, Mozafarian M, Ali A, Sikdar S, Lal BK (2017) Imaging of high-risk carotid plaques: ultrasound. Semin Vasc Surg 30:44–53CrossRef Cires-Drouet RS, Mozafarian M, Ali A, Sikdar S, Lal BK (2017) Imaging of high-risk carotid plaques: ultrasound. Semin Vasc Surg 30:44–53CrossRef
35.
go back to reference Saam T, Hetterich H, Hoffmann V, Yuan C, Dichgans M, Poppert H, Koeppel T, Hoffmann U, Reiser MF, Bamberg F (2013) Meta-analysis and systematic review of the predictive value of carotid plaque hemorrhage on cerebrovascular events by magnetic resonance imaging. J Am Coll Cardiol 62:1081–1091CrossRef Saam T, Hetterich H, Hoffmann V, Yuan C, Dichgans M, Poppert H, Koeppel T, Hoffmann U, Reiser MF, Bamberg F (2013) Meta-analysis and systematic review of the predictive value of carotid plaque hemorrhage on cerebrovascular events by magnetic resonance imaging. J Am Coll Cardiol 62:1081–1091CrossRef
36.
go back to reference Singh N, Moody AR, Roifman I, Bluemke DA, Zavodni AE (2016) Advanced MRI for carotid plaque imaging. Int J Cardiovasc Imaging 32:83–89CrossRef Singh N, Moody AR, Roifman I, Bluemke DA, Zavodni AE (2016) Advanced MRI for carotid plaque imaging. Int J Cardiovasc Imaging 32:83–89CrossRef
Metadata
Title
Effect of cigarette smoking on carotid artery atherosclerosis: a community-based cohort study
Authors
Hiroyuki Kiriyama
Hidehiro Kaneko
Hidetaka Itoh
Yuriko Yoshida
Koki Nakanishi
Yoshiko Mizuno
Masao Daimon
Hiroyuki Morita
Nobutake Yamamichi
Issei Komuro
Publication date
01-01-2020
Publisher
Springer Japan
Published in
Heart and Vessels / Issue 1/2020
Print ISSN: 0910-8327
Electronic ISSN: 1615-2573
DOI
https://doi.org/10.1007/s00380-019-01455-5

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