Abstract
Purpose
Metabolic syndrome (MetS), regardless of the presence of obesity, is known as a risk of diabetes and cardiovascular disease. Weight gain after age 20 reported to be associated with these diseases. Impact of the difference between the body mass index (BMI) at examination and BMI at age 20 (ΔBMIexa−20y) on MetS, especially in non-overweight individuals, remains to be elucidated.
Methods
We analyzed the data of 24,363 individuals (14,301 men and 10,062 women) in this cross-sectional study. The diagnosis of MetS was diagnosed when three or more of the following criteria were present: hypertension, hyperglycemia, hypertriglyceridemia, low HDL-cholesterol level, and abdominal obesity. Logistic regression was performed to calculate odds ratios (ORs) and 95% confidence intervals (CIs) adjusting for age, alcohol, smoking, exercise, and BMI at examination.
Results
Compared to the lowest ΔBMIexa−20y tertile (ΔBMIexa−20y < 1.2 kg/m2 in men and ≤0 kg/m2 in women), the highest tertile (ΔBMIexa−20y ≥ 3.2 kg/m2 in men and ≥2.0 kg/m2 in women) was associated with the risk of the presence of MetS (multivariate OR = 1.80, 95%CI 1.53–2.11, p < 0.001 in men and OR = 3.27, 95%CI 2.22–4.96, p < 0.001 in women). This result was also applicable in non-overweight individuals (multivariate OR = 2.06, 95%CI 1.46–2.92, p < 0.001 in men and OR = 2.49, 95%CI 1.40–4.64, p < 0.001 in women).
Conclusions
Our analyses showed that ΔBMIexa−20y is associated with the risk of the presence of MetS, even in non-overweight individuals. It is thus important to check weight changes from early adulthood, even in non-overweight individuals.
Similar content being viewed by others
References
M. Hamaguchi, T. Kojima, N. Takeda, T. Nakagawa, H. Taniguchi, K. Fujii, T. Omatsu, T. Nakajima, H. Sarui, M. Shimazaki, T. Kato, J. Okuda, K. Ida, The metabolic syndrome as a predictor of nonalcoholic fatty liver disease. Ann. Intern. Med. 143, 722–728 (2005)
C. Lorenzo, M. Okoloise, K. Williams, M.P. Stern, S.M. Haffner; San Antonio Heart Study, The metabolic syndrome as predictor of type 2 diabetes: the San Antonio heart study. Diabetes Care 26, 3153–3159 (2003)
G. Thomas, A.R. Sehgal, S.R. Kashyap, T.R. Srinivas, J.P. Kirwan, S.D. Navaneethan, Metabolic syndrome and kidney disease: a systematic review and meta-analysis. Clin. J. Am. Soc. Nephrol. 6, 2364–2373 (2011)
S. Mottillo, K.B. Filion, J. Genest, L. Joseph, L. Pilote, P. Poirier, S. Rinfret, E.L. Schiffrin, M.J. Eisenberg, The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J. Am. Coll. Cardiol. 56, 1113–1132 (2010)
World Health Organization. Obesity: Preventing and Managing the Global Epidemic: Report of a WHO Consultation. (World Health Organization, Geneva, 2000). WHO technical report series 894
Y. Hashimoto, M. Tanaka, H. Okada, T. Senmaru, M. Hamaguchi, M. Asano, M. Yamazaki, Y. Oda, G. Hasegawa, H. Toda, N. Nakamura, M. Fukui, Metabolically healthy obesity and risk of incident CKD. Clin. J. Am. Soc. Nephrol. 10, 578–583 (2015)
H. Mathew, O.M. Farr, C.S. Mantzoros, Metabolic health and weight: understanding metabolically unhealthy normal weight or metabolically healthy obese patients. Metabolism 65, 73–80 (2016)
Y. Heianza, Y. Arase, H. Tsuji, K. Fujihara, K. Saito, S.D. Hsieh, S. Tanaka, S. Kodama, S. Hara, H. Sone, Metabolically healthy obesity, presence or absence of fatty liver, and risk of type 2 diabetes in Japanese individuals: toranomon hospital health management center study 20 (TOPICS 20). J. Clin. Endocrinol. Metab. 99, 2952–2960 (2014)
C.K. Kramer, B. Zinman, R. Retnakaran, Are metabolically healthy overweight and obesity benign conditions?: a systematic review and meta-analysis. Ann. Intern. Med. 159, 758–769 (2013)
J. Zhang, H. Jiang, J. Chen, Combined effect of body mass index and metabolic status on the risk of prevalent and incident chronic kidney disease: a systematic review and meta-analysis. Oncotarget 8, 35619–35629 (2017)
E.J. Rhee, M.K. Lee, J.D. Kim, W.S. Jeon, J.C. Bae, S.E. Park, C.Y. Park, K.W. Oh, S.W. Park, W.Y. Lee, Metabolic health is a more important determinant for diabetes development than simple obesity: a 4-year retrospective longitudinal study. PLoS One 9, e98369 (2014)
Y. Hashimoto, M. Tanaka, T. Senmaru, M. Asano, M. Yamazaki, Y. Oda, H. Tods, N. Nakamura, M. Fukui, Maintaining metabolically healthy overweight and risk of incident type 2 diabetes or cardiovascular disease. Int. J. Diabetol. Vasc. Dis. Res. S3, 1–6 (2015)
L. Di Renzo, E. Tyndall, P. Gualtieri, C. Carboni, R. Valente, A.S. Ciani, M.G. Tonini, A. De Lorenzo, Association of body composition and eating behavior in the normal weight obese syndrome. Eat. Weight Disord. 21, 99–106 (2016)
A. De Lorenzo, V. Del Gobbo, M.G. Premrov, M. Bigioni, F. Galvano, L. Di Renzo, Normal-weight obese syndrome: early inflammation? Am. J. Clin. Nutr. 85, 40–45 (2007)
R. de Mutsert, Q. Sun, W.C. Willett, F.B. Hu, R.M. van Dam, Overweight in early adulthood, adult weight change, and risk of type 2 diabetes, cardiovascular diseases, and certain cancers in men: a cohort study. Am. J. Epidemiol. 179, 1353–1365 (2014)
Y. Heianza, S. Kodama, Y. Arase, S.D. Hsieh, S. Yoshizawa, H. Tsuji, K. Saito, S. Tanaka, S. Hara, H. Sone, Role of body mass index history in predicting risk of the development of hypertension in Japanese individuals: toranomon hospital health management center study 18 (TOPICS 18). Hypertens 64, 247–252 (2014)
Y. Hashimoto, M. Hamaguchi, T. Fukuda, N. Nakamura, A. Ohbora, T. Kojima, M. Fukui, BMI history and risk of incident fatty liver: a population-based large-scale cohort study. Eur. J. Gastroenterol. Hepatol. 28, 1188–1193 (2016)
C.L. Chei, H. Iso, K. Yamagishi, M. Inoue, S. Tsugane, Body mass index and weight change since 20 years of age and risk of coronary heart disease among Japanese: the Japan public health center-based study. Int. J. Obes. 32, 144–151 (2008)
A. Suzuki, R. Akamatsu, Long-term weight gain is related to risk of metabolic syndrome even in the non-obese. Diabetes Metab. Syndr. 8, 177–183 (2014)
Y. Hashimoto, M. Hamaguchi, T. Kojima, Y. Ohshima, A. Ohbora, T. Kato, N. Nakamura, M. Fukui, The modest alcohol consumption reduces the incidence of fatty liver in men; a population based large scale cohort study. J. Gastroenterol. Hepatol. 30, 546–552 (2015)
T. Fukuda, M. Hamaguchi, T. Kojima, Y. Hashimoto, A. Ohbora, T. Kato, N. Nakamura, M. Fukui, The impact of nonalcoholic fatty liver disease on incident type 2 diabetes mellitus in non-overweight individuals. Liver. Int. 36, 275–283 (2016)
Y. Fukuda, Y. Hashimoto, M. Hamaguchi, T. Fukuda, N. Nakamura, A. Ohbora, T. Kato, T. Kojima, M. Fukui, Triglycerides to high-density lipoprotein cholesterol ratio is an independent predictor of incident fatty liver; a population-based cohort study. Liver. Int. 36, 713–720 (2016)
S. Ryu, Y. Chang, D.I. Kim, W.S. Kim, B.S. Suh, γ-Glutamyltransferase as a predictor of chronic kidney disease in nonhypertensive and nondiabetic Korean men. Clin. Chem. 53, 71–77 (2007)
R.C. Weisell, Body mass index as an indicator of obesity. Asia Pac. J. Clin. Nutr. 11(Suppl 8), S681–S684 (2002)
Y. Hashimoto, M. Tanaka, T. Kimura, N. Kitagawa, M. Hamaguchi, M. Asano, M. Yamazaki, Y. Oda, H. Toda, N. Nakamura, M. Fukui, Hemoglobin concentration and incident metabolic syndrome: a population-based large-scale cohort study. Endocrine 50, 390–396 (2015)
K.G. Alberti, R.H. Eckel, S.M. Grundy, P.Z. Zimmet, J.I. Cleeman, K.A. Donato, J.C. Fruchart, W.P. James, C.M. Loria, S.C. Smith Jr.; International Diabetes Federation Task Force on Epidemiology and Prevention.; Hational Heart, Lung, and Blood Institute.; American Heart Association.; World Heart Federation.; International Atherosclerosis Society.; International Association for the Study of Obesity., Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International. Circulation 120, 1640–1645 (2009)
J.P. Després, I. Lemieux, Abdominal obesity and metabolic syndrome. Nature 444, 881–887 (2006)
S.A. Porter, J.M. Massaro, U. Hoffmann, R.S. Vasan, C.J. O’Donnel, C.S. Fox, Abdominal subcutaneous adipose tissue: a protective fat depot? Diabetes Care 32, 1068–1075 (2009)
B.M. Kaess, A. Pedley, J.M. Massaro, J. Murabito, U. Hoffmann, C.S. Fox, The ratio of visceral to subcutaneous fat, a metric of body fat distribution, is a unique correlate of cardiometabolic risk. Diabetologia 55, 2622–2630 (2012)
K.L. Spalding, E. Arner, P.O. Westermark, S. Bernard, B.A. Buchholz, O. Bergmann, L. Blomqvist, J. Hoffstedt, E. Näslund, T. Britton, H. Concha, M. Hassan, M. Rydén, J. Frisén, P. Arner, Dynamics of fat cell turnover in humans. Nature 453, 783–787 (2008)
S. Virtue, A. Vidal-Puig, It’s not how fat you are, it’s what you do with it that counts. PLoS Biol. 6, e237 (2008)
R.M. Mancina, M.A. Burza, C. Maglio, C. Pirazzi, F. Sentinelli, M. Incani, T. Montalcini, A. Pujia, T. Congiu, S. Loche, S. Pilia, O. Wiklund, J. Borén, S. Romeo, M.G. Baroni, The COBLL1 C allele is associated with lower serum insulin levels and lower insulin resistance in overweight and obese children. Diabetes Metab. Res. Rev. 29, 413–416 (2013)
F. Sentinelli, L. Bertoccini, I. Barchetta, D. Capoccia, M. Incani, M.G. Pani, S. Loche, F. Angelico, M. Arca, S. Morini, E. Manconi, A. Lenzi, E. Cossu, F. Leonetti, M.G. Baroni, M.G. Cavallo, The vitamin D receptor (VDR) gene rs11568820 variant is associated with type 2 diabetes and impaired insulin secretion in Italian adult subjects, and associates with increased cardio-metabolic risk in children. Nutr. Metab. Cardiovasc. Dis. 26, 407–413 (2016)
R.M. Mancina, F. Sentinelli, M. Incani, L. Bertoccini, C. Russo, S. Romeo, M.G. Baroni, Transmembrane-6 superfamily member 2 (TM6SF2) E167K variant increases susceptibility to hepatic steatosis in obese children. Dig. Liver. Dis. 48, 100–101 (2016)
Y. Hashimoto, T. Fukuda, C. Oyabu, M. Tanaka, M. Asano, M. Yamazaki, M. Fukui, Impact of low-carbohydrate diet on body composition: meta-analysis of randomized controlled studies. Obes. Rev. 17, 499–509 (2016)
Y. Hashimoto, T. Osaka, T. Fukuda, M. Tanaka, M. Yamazaki, M. Fukui, The relationship between hepatic steatosis and skeletal muscle mass index in men with type 2 diabetes. Endocr. J. 63, 877–884 (2016)
E. Han, Y.H. Lee, G. Kim, S.R. Kim, B.W. Lee, E.S. Kang, C.W. Ahn, B.S. Cha, Sarcopenia is associated with albuminuria independently of hypertension and diabetes: KNHANES 2008–2011. Metabolism 65, 1531–1540 (2016)
B.B. Rasmussen, S. Fujita, R.R. Wolfe, B. Mittendorfer, M. Roy, V.L. Rowe, E. Volpi, Insulin resistance of muscle protein metabolism in aging. FASEB J. 20, 768–769 (2006)
N. Di Daniele, L. Petramala, L. Di Renzo, F. Sarlo, D.G. Della Rocca, M. Rizzo, V. Fondacaro, L. Iacopino, C.J. Pepine, A. De Lorenzo, Body composition changes and cardiometabolic benefits of a balanced Italian Mediterranean Diet in obese patients with metabolic syndrome. Acta. Diabetol. 50, 409–416 (2013)
G. Merra, S. Gratteri, A. De Lorenzo, S. Barrucco, M.A. Perrone, E. Avolio, S. Bernardini, M. Marchetti, L. Di Renzo, Effects of very-low-calorie diet on body composition, metabolic state, and genes expression: a randomized double-blind placebo-controlled trial. Eur. Rev. Med. Pharmacol. Sci. 21, 329–345 (2017)
V.A. Casey, J.T. Dwyer, C.S. Berkey, K.A. Coleman, J. Gardner, I. Valadian, Long-term memory of body weight and past weight satisfaction: a longitudinal follow-up study. Am. J. Clin. Nutr. 53, 1493–1498 (1991)
S.S. Bassuk, J.E. Manson, The timing hypothesis: do coronary risks of menopausal hormone therapy vary by age or time since menopause onset? Metabolism 65, 794–803 (2016)
Acknowledgements
We thank all of the staff members in the medical health checkup center at Murakami Memorial Hospital.
Author contributions
Y.H. designed and conducted the study, researched, analyzed, and interpreted the data, and wrote the manuscript; M.H. designed and conducted the study, researched and interpreted the data, and reviewed and edited the manuscript. T.F., A.O., and T.K. researched and interpreted the data, and reviewed the manuscript. M.F. designed and conducted the study, researched and interpreted the data, and reviewed the manuscript. All authors have approved the final draft submitted.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
M. Fukui has received grant and research support from AstraZeneca plc, Astellas Pharma Inc., Bristol–Myers Squibb K.K., Daiichi Sankyo Co., Ltd., Eli Lilly Japan K.K., Kyowa Hakko Kirin Company Ltd., Kowa Pharmaceutical Co., Ltd., Kissei Pharmaceutical Co., Ltd., MSD K.K., Mitsubishi Tanabe Pharma Corporation, Novo Nordisk Pharma Ltd., Nippon Chemiphar Company Ltd., Sanwa Kagaku Kenkyusho Co., Ltd., Sanofi K.K., Taisho Toyama Pharmaceutical Co., Ltd., Takeda Pharmaceutical Co., Ltd., Terumo Co. The sponsors were not involved in the study design; in the collection, analysis, interpretation of data; in the writing of this manuscript; or in the decision to submit the article for publication. M. Fukui, his immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article. M. Fukui received no current funding for this study and this does not alter their adherence to all of the journal policies on sharing data and materials. The other authors declare that they have no competing interests.
Ethical Approval
The study was conducted in accordance with the Declaration of Helsinki, and an independent ethics committee.
Informed Consent
Informed consent was obtained from all individual participants included in the study.
Rights and permissions
About this article
Cite this article
Hashimoto, Y., Hamaguchi, M., Fukuda, T. et al. Weight gain since age of 20 as risk of metabolic syndrome even in non-overweight individuals. Endocrine 58, 253–261 (2017). https://doi.org/10.1007/s12020-017-1411-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12020-017-1411-5