Skip to main content
Top
Published in: Rheumatology International 9/2018

Open Access 01-09-2018 | Observational Research

Non-obese visceral adiposity is associated with the risk of atherosclerosis in Japanese patients with rheumatoid arthritis: a cross-sectional study

Authors: Tamami Yoshida, Motomu Hashimoto, Rie Kawahara, Hiroko Yamamoto, Masao Tanaka, Hiromu Ito, Izuru Masuda, Kiminori Hosoda, Wataru Yamamoto, Ryuji Uozumi, Satoshi Morita, Yasutomo Fujii, Tsuneyo Mimori, Kazuko Nin

Published in: Rheumatology International | Issue 9/2018

Login to get access

Abstract

Rheumatoid arthritis (RA) patients often have altered body composition including reduced muscle mass and increased fat mass. Some RA patients are likely to increase visceral fat without obesity [Body Mass Index (BMI) ≥ 25]. The objective of the study was to determine the association between obesity and/or visceral adiposity and the risk for atherosclerosis in Japanese RA patients. Obesity was evaluated using the BMI, with visceral adiposity evaluated using the visceral fat area (VFA) and the visceral/subcutaneous fat ratio (V/S ratio), quantified using the dual bioelectrical impedance method. Atherosclerosis was evaluated based on the intima–media thickness (IMT) and Plaque score (PS) of the carotid artery, measured using ultrasonography. Multivariate analysis was performed to determine the factors associated with IMT and PS. IMT and PS were compared among groups of patients sub-classified according to BMI and VFA levels. The V/S ratio was higher in RA patients than healthy controls, after adjustment for age, BMI, and waist circumference. On multivariate analysis, the V/S ratio, but not the BMI, was independently associated with the IMT and PS. Among the sub-classifications for BMI and VFA, non-obese patients with a high visceral adiposity (18.5 ≤ BMI < 25 kg/m2 and VFA ≥ 100 cm2) had the highest IMT (mean IMT, 0.93 ± 0.29 mm; maximum IMT, 1.44 ± 0.71 mm) and PS (1.43 ± 0.61), compared to all other BMI and VFA subgroups. RA patients have increased visceral adiposity, which is associated with a high prevalence of atherosclerotic of plaques. Non-obese RA patients who have visceral adiposity have a specifically higher risk for atherosclerosis.
Literature
1.
go back to reference Kim YJ, Shim JS, Choi CB, Bea SC (2012) Mortality and incidence of malignancy in Korean patients with rheumatoid arthritis. J Rheumatol 39:226–232CrossRefPubMed Kim YJ, Shim JS, Choi CB, Bea SC (2012) Mortality and incidence of malignancy in Korean patients with rheumatoid arthritis. J Rheumatol 39:226–232CrossRefPubMed
2.
go back to reference Radovits BJ, Fransen J, Al Shamma S, Eijsbouts AM, van Riel PLCM, Laan RFJM (2010) Excess mortality emerges after 10 years in an inception cohort of early rheumatoid arthritis. Arthritis Care Res (Hoboken) 62:362–370CrossRef Radovits BJ, Fransen J, Al Shamma S, Eijsbouts AM, van Riel PLCM, Laan RFJM (2010) Excess mortality emerges after 10 years in an inception cohort of early rheumatoid arthritis. Arthritis Care Res (Hoboken) 62:362–370CrossRef
3.
go back to reference Avina-Zubieta JA, Choi HK, Sadatsafavi M, Etminan M, Esdaile JM, Lacaille D (2008) Risk of cardiovascular mortality in patients with rheumatoid arthritis: a meta-analysis of observational studies. Arthritis Rheumatol 59:1690–1697CrossRef Avina-Zubieta JA, Choi HK, Sadatsafavi M, Etminan M, Esdaile JM, Lacaille D (2008) Risk of cardiovascular mortality in patients with rheumatoid arthritis: a meta-analysis of observational studies. Arthritis Rheumatol 59:1690–1697CrossRef
4.
go back to reference Solomon DH, Karlson EW, Rimm EB, Cannuscio CC, Mandl LA, Manson JE, Stampfer MJ, Curhan GC (2003) Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation 107:1303–1307CrossRefPubMed Solomon DH, Karlson EW, Rimm EB, Cannuscio CC, Mandl LA, Manson JE, Stampfer MJ, Curhan GC (2003) Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation 107:1303–1307CrossRefPubMed
5.
go back to reference Young A, Koduri G, Batley M, Kulinskaya E, Gough A, Norton S, Dixey J, Early Rheumatoid Arthritis Study (ERAS) Group (2007) Mortality in rheumatoid arthritis. Increased in the early course of disease, in ischaemic heart disease and in pulmonary fibrosis. Rheumatology (Oxford) 46:350–357CrossRef Young A, Koduri G, Batley M, Kulinskaya E, Gough A, Norton S, Dixey J, Early Rheumatoid Arthritis Study (ERAS) Group (2007) Mortality in rheumatoid arthritis. Increased in the early course of disease, in ischaemic heart disease and in pulmonary fibrosis. Rheumatology (Oxford) 46:350–357CrossRef
6.
go back to reference Mason JC, Libby P (2015) Cardiovascular disease in patients with chronic inflammation: mechanisms underlying premature cardiovascular events in rheumatologic conditions. Eur Heart J 36:482–489cCrossRefPubMed Mason JC, Libby P (2015) Cardiovascular disease in patients with chronic inflammation: mechanisms underlying premature cardiovascular events in rheumatologic conditions. Eur Heart J 36:482–489cCrossRefPubMed
7.
go back to reference Twig G, Yaniv G, Levine H, Leiba A, Goldberg N, Derazne E, Ben-Ami Shor D, Tzur D, Afek A, Shamiss A, Haklai Z, Kark JD (2016) Body Mass Index in 2.3 million adolescents and cardiovascular death in adulthood. N Engl J Med 374:2430–2440CrossRefPubMed Twig G, Yaniv G, Levine H, Leiba A, Goldberg N, Derazne E, Ben-Ami Shor D, Tzur D, Afek A, Shamiss A, Haklai Z, Kark JD (2016) Body Mass Index in 2.3 million adolescents and cardiovascular death in adulthood. N Engl J Med 374:2430–2440CrossRefPubMed
8.
go back to reference Kremers HM, Nicola PJ, Crowson CS, Therneau TM, Roger VL, Gabriel SE (2004) Prognostic importance of low Body Mass Index in relation to cardiovascular mortality in rheumatoid arthritis. Arthritis Rheumatol 50:3450–3457CrossRef Kremers HM, Nicola PJ, Crowson CS, Therneau TM, Roger VL, Gabriel SE (2004) Prognostic importance of low Body Mass Index in relation to cardiovascular mortality in rheumatoid arthritis. Arthritis Rheumatol 50:3450–3457CrossRef
9.
go back to reference Kremers HM, Crowson CS, Therneau TM, Roger VL, Gabriel SE (2008) High ten-year risk of cardiovascular disease in newly diagnosed rheumatoid arthritis patients: a population-based cohort study. Arthritis Rheumatol 58:2268–2274CrossRef Kremers HM, Crowson CS, Therneau TM, Roger VL, Gabriel SE (2008) High ten-year risk of cardiovascular disease in newly diagnosed rheumatoid arthritis patients: a population-based cohort study. Arthritis Rheumatol 58:2268–2274CrossRef
10.
11.
go back to reference Engvall IL, Elkan AC, Tengstrand B, Cederholm T, Brismar K, Hafstrom I (2008) Cachexia in rheumatoid arthritis is associated with inflammatory activity, physical disability, and low bioavailable insulin-like growth factor. Scand J Rheumatol 37:321–328CrossRefPubMed Engvall IL, Elkan AC, Tengstrand B, Cederholm T, Brismar K, Hafstrom I (2008) Cachexia in rheumatoid arthritis is associated with inflammatory activity, physical disability, and low bioavailable insulin-like growth factor. Scand J Rheumatol 37:321–328CrossRefPubMed
12.
go back to reference Elkan AC (2008) Malnutrition in women with rheumatoid arthritis is not revealed by clinical anthropometrical measurements or nutritional evaluation tools. Eur J Clin Nutr 62:1239–1247CrossRefPubMed Elkan AC (2008) Malnutrition in women with rheumatoid arthritis is not revealed by clinical anthropometrical measurements or nutritional evaluation tools. Eur J Clin Nutr 62:1239–1247CrossRefPubMed
13.
go back to reference Summers GD, Metsios GS, Stavropoulos-Kalinoglou A, Kitas GD (2010) Rheumatoid cachexia and cardiovascular disease. Nat Rev Rheumatol 6:445–451CrossRefPubMed Summers GD, Metsios GS, Stavropoulos-Kalinoglou A, Kitas GD (2010) Rheumatoid cachexia and cardiovascular disease. Nat Rev Rheumatol 6:445–451CrossRefPubMed
14.
go back to reference Britton KA, Massaro JM, Murabito JM, Kreger BE, Hoffmann U, Fox CS (2013) Body fat distribution, incident cardiovascular disease, cancer, and all-cause mortality. J Am Coll Cardiol 62:921–925CrossRefPubMedPubMedCentral Britton KA, Massaro JM, Murabito JM, Kreger BE, Hoffmann U, Fox CS (2013) Body fat distribution, incident cardiovascular disease, cancer, and all-cause mortality. J Am Coll Cardiol 62:921–925CrossRefPubMedPubMedCentral
15.
go back to reference Fujimoto WY, Bergstrom RW, Boyko EJ, Chen KW, Leonetti DL, Newell-Morris L, Shofer JB, Wahl PW (1999) Visceral adiposity and incident coronary heart disease in Japanese-American men. The 10-year follow-up results of the Seattle Japanese-American Community Diabetes Study. Diabetes Care 22:1808–1812CrossRefPubMed Fujimoto WY, Bergstrom RW, Boyko EJ, Chen KW, Leonetti DL, Newell-Morris L, Shofer JB, Wahl PW (1999) Visceral adiposity and incident coronary heart disease in Japanese-American men. The 10-year follow-up results of the Seattle Japanese-American Community Diabetes Study. Diabetes Care 22:1808–1812CrossRefPubMed
16.
go back to reference Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M (2007) Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation 115:459–467CrossRefPubMed Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M (2007) Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation 115:459–467CrossRefPubMed
17.
go back to reference Stein JH, Korcarz CE, Hurst RT, Lonn E, Kendall CB, Mohler ER et al (2008) 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 21:93–111 quiz 89–90.CrossRefPubMed Stein JH, Korcarz CE, Hurst RT, Lonn E, Kendall CB, Mohler ER et al (2008) 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 21:93–111 quiz 89–90.CrossRefPubMed
18.
go back to reference Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO III et al (2010) Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheumatol 62:2569–2581CrossRef Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO III et al (2010) Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheumatol 62:2569–2581CrossRef
19.
go back to reference Yanase T, Nasu S, Mukuta Y, Shimizu Y, Nishihara T, Okabe T, Nomura M, Inoguchi T, Nawata H (2006) Evaluation of a new carotid intima-media thickness measurement by B-mode ultrasonography using an innovative measurement software, intimascope. Am J Hypertens 19:1206–1212CrossRefPubMed Yanase T, Nasu S, Mukuta Y, Shimizu Y, Nishihara T, Okabe T, Nomura M, Inoguchi T, Nawata H (2006) Evaluation of a new carotid intima-media thickness measurement by B-mode ultrasonography using an innovative measurement software, intimascope. Am J Hypertens 19:1206–1212CrossRefPubMed
20.
go back to reference Terminology and Diagnostic Criteria Committee, Japan Society of Ultrasonics in Medicine (2001) Standard method for ultrasound evaluation of carotid artery lesions. J Med Ultrason 36:219–226CrossRef Terminology and Diagnostic Criteria Committee, Japan Society of Ultrasonics in Medicine (2001) Standard method for ultrasound evaluation of carotid artery lesions. J Med Ultrason 36:219–226CrossRef
21.
go back to reference Oshima Y, Shiga T, Namba H, Kuno S (2010) Estimation of whole-body skeletal muscle mass by bioelectrical impedance analysis in the standing position. Obes Res Clin Pract 4:e1–e82CrossRefPubMed Oshima Y, Shiga T, Namba H, Kuno S (2010) Estimation of whole-body skeletal muscle mass by bioelectrical impedance analysis in the standing position. Obes Res Clin Pract 4:e1–e82CrossRefPubMed
22.
go back to reference Shiga T, Hamaguchi T, Oshima Y, Kanai H, Hirata M, Hosoda K et al (2009) A new simple measurement system of visceral fat accumulation by bioelectrical impedance analysis. In: Dössel O, Schlegel WC (eds) Proceedings of the world congress on medical physics and biomedical engineering. Springer, Berlin, pp 338–341 Shiga T, Hamaguchi T, Oshima Y, Kanai H, Hirata M, Hosoda K et al (2009) A new simple measurement system of visceral fat accumulation by bioelectrical impedance analysis. In: Dössel O, Schlegel WC (eds) Proceedings of the world congress on medical physics and biomedical engineering. Springer, Berlin, pp 338–341
23.
go back to reference Examination Committee of Criteria for ‘Obesity Disease’ in Japan; Japan Society for the Study of Obesity (2002) New criteria for ‘obesity disease’ in Japan. Circulation 66:987–992CrossRef Examination Committee of Criteria for ‘Obesity Disease’ in Japan; Japan Society for the Study of Obesity (2002) New criteria for ‘obesity disease’ in Japan. Circulation 66:987–992CrossRef
24.
go back to reference Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE, Pratt M, Ekelund U, Yngve A, Sallis JF, Oja P (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35:1381–1395CrossRefPubMed Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE, Pratt M, Ekelund U, Yngve A, Sallis JF, Oja P (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35:1381–1395CrossRefPubMed
25.
go back to reference Giles JT (2010) Abdominal adiposity in rheumatoid arthritis: association with cardiometabolic risk factors and disease characteristics. Arthritis Rheumatol 62:3173–3182CrossRef Giles JT (2010) Abdominal adiposity in rheumatoid arthritis: association with cardiometabolic risk factors and disease characteristics. Arthritis Rheumatol 62:3173–3182CrossRef
26.
go back to reference Inaba M (2007) Independent association of increased trunk fat with increased arterial stiffening in postmenopausal patients with rheumatoid arthritis. J Rheumatol 34:290–295PubMed Inaba M (2007) Independent association of increased trunk fat with increased arterial stiffening in postmenopausal patients with rheumatoid arthritis. J Rheumatol 34:290–295PubMed
28.
go back to reference Matsuzawa Y, Funahashi T, Nakamura T (2011) The concept of metabolic syndrome: contribution of visceral fat accumulation and its molecular mechanism. J Atheroscler Thromb 18:629–639CrossRefPubMed Matsuzawa Y, Funahashi T, Nakamura T (2011) The concept of metabolic syndrome: contribution of visceral fat accumulation and its molecular mechanism. J Atheroscler Thromb 18:629–639CrossRefPubMed
29.
go back to reference Muscaritoli M (2010) Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by Special Interest Groups (SIG) “cachexia–anorexia in chronic wasting diseases” and “nutrition in geriatrics”. Clin Nutr 29:154–159CrossRefPubMed Muscaritoli M (2010) Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by Special Interest Groups (SIG) “cachexia–anorexia in chronic wasting diseases” and “nutrition in geriatrics”. Clin Nutr 29:154–159CrossRefPubMed
30.
31.
go back to reference Schrager MA (2007) Sarcopenic obesity and inflammation in the InCHIANTI study. J Appl Physiol 102:919–925CrossRefPubMed Schrager MA (2007) Sarcopenic obesity and inflammation in the InCHIANTI study. J Appl Physiol 102:919–925CrossRefPubMed
32.
go back to reference Baker JF, Cannon GW, Ibrahim S, Haroldsen C, Caplan L, Mikuls TR (2015) Predictors of long term changes in Body Mass Index in rheumatoid arthritis. J Rheumatol 42:920–927CrossRefPubMedPubMedCentral Baker JF, Cannon GW, Ibrahim S, Haroldsen C, Caplan L, Mikuls TR (2015) Predictors of long term changes in Body Mass Index in rheumatoid arthritis. J Rheumatol 42:920–927CrossRefPubMedPubMedCentral
33.
go back to reference Peters MJ, Symmons DP, McCarey D, Dijkmans BA, Nicola P, Kvienn TK et al (2010) EULAR evidence-based recommendations for cardiovascular risk management in patients with rheumatoid arthritis and other forms of inflammatory arthritis. Ann Rheum Dis 69:325–331CrossRefPubMed Peters MJ, Symmons DP, McCarey D, Dijkmans BA, Nicola P, Kvienn TK et al (2010) EULAR evidence-based recommendations for cardiovascular risk management in patients with rheumatoid arthritis and other forms of inflammatory arthritis. Ann Rheum Dis 69:325–331CrossRefPubMed
34.
go back to reference Agca R, Heslinga SC, Rollefstad S, Heslinga M, McInnes IB, Peters MJ et al (2017) EULAR recommendations for cardiovascular disease risk management in patients with rheumatoid arthritis and other forms of inflammatory joint disorders: 2015/2016 update. Ann Rheum Dis 76:17–28CrossRefPubMed Agca R, Heslinga SC, Rollefstad S, Heslinga M, McInnes IB, Peters MJ et al (2017) EULAR recommendations for cardiovascular disease risk management in patients with rheumatoid arthritis and other forms of inflammatory joint disorders: 2015/2016 update. Ann Rheum Dis 76:17–28CrossRefPubMed
Metadata
Title
Non-obese visceral adiposity is associated with the risk of atherosclerosis in Japanese patients with rheumatoid arthritis: a cross-sectional study
Authors
Tamami Yoshida
Motomu Hashimoto
Rie Kawahara
Hiroko Yamamoto
Masao Tanaka
Hiromu Ito
Izuru Masuda
Kiminori Hosoda
Wataru Yamamoto
Ryuji Uozumi
Satoshi Morita
Yasutomo Fujii
Tsuneyo Mimori
Kazuko Nin
Publication date
01-09-2018
Publisher
Springer Berlin Heidelberg
Published in
Rheumatology International / Issue 9/2018
Print ISSN: 0172-8172
Electronic ISSN: 1437-160X
DOI
https://doi.org/10.1007/s00296-018-4095-0

Other articles of this Issue 9/2018

Rheumatology International 9/2018 Go to the issue