Natural Course of Metabolically Healthy Overweight/Obese Subjects and the Impact of Weight Change
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nutrients Article Natural Course of Metabolically Healthy Overweight/Obese Subjects and the Impact of Weight Change Ruizhi Zheng 1,†, Chengguo Liu 2,†, Chunmei Wang 3,†, Biao Zhou 4, Yi Liu 1, Feixia Pan 1, Ronghua Zhang 4,* and Yimin Zhu 1,* 1 Department of Epidemiology & Biostatistics, School of Public Health, Zhejiang University, Hangzhou 310058, Zhejiang, China; [email protected] (R.Z.); [email protected] (Y.L.); [email protected] (F.P.) 2 Department of Endocrinology and Institute of Cardiovascular Diseases, Zhejiang Putuo Hospital, Zhoushan 316100, Zhejiang, China; [email protected] 3 Tongxiang Center for Disease Control and Prevention, Tongxiang 314500, Zhejiang, China; [email protected] 4 Institute of Nutrition and Food Safety, Zhejiang Center for Disease Control and Prevention, Hangzhou 310000, Zhejiang, China; [email protected] * Correspondence: [email protected] (R.Z.); [email protected] (Y.Z.); Tel.: +86-571-8711-5111 (R.Z.); +86-571-8820-8138 (Y.Z.); Fax: +86-571-8711-5111 (R.Z.); +86-571-8820-8198 (Y.Z.) † These authors contributed equally to this work. Received: 19 May 2016; Accepted: 11 July 2016; Published: 15 July 2016 Abstract: Few studies have described the characteristics of metabolically healthy individuals with excess fat in the Chinese population. This study aimed to prospectively investigate the natural course of metabolically healthy overweight/obese (MH-OW/OB) adults, and to assess the impact of weight change on developing metabolic abnormalities. During 2009–2010, 525 subjects without any metabolic abnormalities or other obesity-related diseases were evaluated and reevaluated after 5 years. The subjects were categorized into two groups of overweight/obese and normal weight based on the criteria of BMI by 24.0 at baseline. At follow-up, the MH-OW/OB subjects had a significantly increased risk of developing metabolically abnormalities compared with metabolically healthy normal-weight (MH-NW) individuals (risk ratio: 1.35, 95% confidence interval: 1.17–1.49, p value < 0.001). In the groups of weight gain and weight maintenance, the MH-OW/OB subjects was associated with a larger increase in fasting glucose, triglycerides, systolic blood pressure, diastolic blood pressure and decrease in high-density lipoprotein cholesterol comparing with MH-NW subjects. In the weight loss group, no significant difference of changes of metabolic parameters was observed between MH-OW/OB and MH-NW adults. This study verifies that MH-OW/OB are different from MH-NW subjects. Weight management is needed for all individuals since weight change has a significant effect on metabolic health without considering the impact of weight change according to weight status. Keywords: metabolically healthy; overweight and obese; weight change 1. Introduction Obesity is a key risk factor for various diseases, including type 2 diabetes, cardiovascular disease (CVD), certain cancers, and musculoskeletal diseases [1]. However, it has been appreciated for many years that about 20% to 30% of obese adults exhibit fewer of these complications and do not meet all the criteria for metabolic syndrome [2]. Intense interest surrounds the “healthy” obese phenotype, which is defined as being obesity in the absence of metabolic syndrome (MetS), termed as metabolically healthy obesity (MHO) [3]. Despite the fact that there is no consensus on which criteria is preferable Nutrients 2016, 8, 430; doi:10.3390/nu8070430 www.mdpi.com/journal/nutrients Nutrients 2016, 8, 430 2 of 12 for defining MHO phenotype, longitudinal studies have suggested that this subtype of obesity are still at increased risk of diabetes and cardiovascular diseases [4–7]. Additionally, several studies have reported that MHO is not a permanent state and almost 30% to 50% of these individuals will convert to metabolically unhealthy status, with resultant increased cardiovascular risk [8,9]. Therefore, it has been speculated that the MHO subjects are not protected, but simply require additional time to develop adverse metabolic outcomes. Weight change has a strong impact on metabolic status; however, several studies investigating the effects of weight loss by lifestyle intervention on metabolic status in the MHO subjects have yielded inconsistent results [10–12]. Most of these studies find that the MHO individuals obtain smaller improvements in MetS components from weight loss, compared with the metabolically abnormal obese (MAO) patients. Furthermore, it has been suggested that weight loss in postmenopausal MHO women may be unnecessary and paradoxically harmful given their favorable metabolic profiles [12]. Fabbrini et al. have evaluated the effect of a high-calorie diet on the metabolic status between the MHO and the MAO subjects [13]. The results demonstrate distinct differences in the response to weight gain. The MAO patients are predisposed to adverse metabolic effects of moderate weight gain, but not in the MHO subjects [13]. According to their conclusion, it can be speculated that the MHO subjects may maintain a healthy status in weight maintenance or even a little weight gain. China has been experiencing an epidemic of obesity and metabolic disease in the last few decades; it has been estimated that almost 70% of Chinese adults are in the overweight and obesity category [14]. Furthermore, the Chinese population tend to accumulate fat intra-abdominally, and thus even lean subjects may have ectopic fat deposition and intra-abdominal obesity, accompanied with increasing cardiometabolic problems in overweight and obese subjects [15]. Our previous study found that 27.9% of obese participants are in metabolic health in the Chinese population [16]. However, little is known regarding the impact of weight changes on the metabolic profile for metabolically healthy overweight/obese subjects in Chinese population. Given this background, the aim of this study was to assess the metabolic response to 5-year weight change for metabolically healthy overweight/obese (MH-OW/OB) adults. 2. Materials and Methods 2.1. Subjects During 2009–2010, the population aged over 30 and residing in the city of Tongxiang and Zhoushan in the Zhejiang province, China, were invited to participate in a health survey aimed at identifying risk factors for non-communicable diseases. A total of 3603 subjects participated in the prospective study, and data collected in 2009–2010 were used as the baseline for the present study. A clinical assessment was repeated 5 years later. This study was conducted according to the guidelines laid down in the Declaration of Helsinki and all procedures involving human subjects were approved by the Institutional Review Board of School of Medicine, Zhejiang University, Zhejiang, China (ethic approval code: ZGL201304-3). Written informed consents were obtained from all participants. According to the objective for the current study, those with a history of chronic diseases were excluded (e.g., diabetes, cardiovascular disease, dyslipidemia, cancer, hypertension) (n = 719). After exclusion of those with body mass index (BMI) < 18.5 kg/m2 (n = 150), and those who had missing anthropometric, metabolic detection data and questionnaire information (n = 30), 2704 participants were remained. Of these subjects, we selected those who had healthy metabolic status at baseline. Namely, all of the selected subjects had no metabolic abnormality of MetS definition of the International Diabetes Federation (IDF) criteria (waist circumference was not included in the definition of metabolic health because of collinearity with BMI), including elevated triglycerides (TG) (¥1.7 mmol/L), low high-density lipoprotein cholesterol (HDL-C) (men < 1.03 mmol/L, women < 1.29 mmol/L), elevated systolic blood pressure (SBP) (¥130 mm¨ Hg) or diastolic blood pressure (DBP) (¥85 mm¨ Hg), elevated fasting plasma glucose (FPG) (¥5.6 mmol/L) [17]. The selection yielded 630 subjects in metabolic Nutrients 2016, 8, 430 3 of 12 Nutrients 2016, 8, 430 3 of 12 health. After starting the study, 105 subjects (16.7%) were excluded for not attending a follow-up visit. Ultimately,in metabolic 525 subjects health. After were starting included the in study, the analysis 105 subjects (Figure (16.7%)1). General were excluded obesity for was not defined attending by a BMI, whichfollow was‐up recommended visit. Ultimately, by 525 the subjects Working were Group included on in Obesity the analysis in China (Figure (WGOC) 1). General [18 obesity]. There was were defined by BMI, which was recommended by the Working Group on Obesity in China (WGOC) [18]. 392 subjects in the normal weight category (BMI < 24.0 kg/m2), 98 in the overweight category There were 392 subjects in the normal weight category (BMI < 24.0 kg/m2), 98 in the overweight 2 ¥ 2 (BMIcategory 24 textasciitilde (BMI 24 ~ 28 28 kg/m kg/m2) )and and 35 35 in in the the obesity obesity category category (BMI (BMI ≥ 28 kg/m282). kg/m ). 3603 subjects recruited from Zhejiang Metabolic Syndrome cohort in 2009‐2010 Exclusions (n = 2973) ‐ With history of diabetes, CVD, dyslipidemia, cancer, hypertension (n = 719) ‐ Missing data on anthropometric measures or covariates (n = 30) ‐ Body mass index < 18.5 kg/m2 (n = 150) ‐ Presenting at least one abnormal metabolic component (n = 2074) 630 eligible subjects for the study Missed in follow‐up n = 105 525 metabolically healthy participants with complete data for final analysis Figure 1. The flowchart of including subjects in the analysis. Figure 1. The flowchart of including subjects in the analysis. 2.2. Clinical Measurements at Baseline and Follow‐up 2.2. Clinical Measurements at Baseline and Follow-up Follow‐up measurements took place 5 years after baseline examination. Both at baseline and Follow-upfollow‐up investigation, measurements the same took measurements place 5 years were after conducted. baseline examination.Nurses collected Both anthropometric at baseline and follow-updata (weight, investigation, height) the and same blood measurements pressure using were standard conducted. protocols. Nurses Height collected and weight anthropometric were data (weight,measured height) on a scale, and with blood the pressuresubjects wearing using standard light clothing protocols. and without Height shoes.