DIABETICMedicine DOI: 10.1111/dme.12532
Research: Epidemiology Obesity index and the risk of diabetes among Chinese women with prior gestational diabetes L. Wang1, H. Liu1, S. Zhang1, J. Leng1, G. Liu1, C. Zhang1, W. Q. Li1,2, N. Li1, W. Li1, Y. Li1, S. Sun1, Z. Yu3, X. Yang4 and G. Hu2 1 Tianjin Women’s and Children’s Health Center, China, 2Pennington Biomedical Research Center, Baton Rouge, LA, USA, 3Population Cancer Research Program, Dalhousie University, Halifax, NS, Canada and 4Department of Epidemiology and Biostatistics, Tianjin Medical University, China
Accepted 20 June 2014
Abstract Aims There is some confusion regarding which anthropometric measurement of adiposity should be used to indicate diabetes, especially for Asians. The present study was to evaluate different indicators of adiposity (BMI, waist circumference and body fat) with Type 2 diabetes risk among women with prior gestational diabetes mellitus. Methods We performed a cross-sectional survey in 1263 women with gestational diabetes at 1–5 years after delivery. Logistic regression models were used to estimate the association of BMI, waist circumference and body fat with Type 2 diabetes risk.
BMI, waist circumference and body fat were all associated with an increased risk of Type 2 diabetes among women with prior gestational diabetes (all Ptrend < 0.001). After adjustment for waist circumference and body fat, the positive association of BMI with Type 2 diabetes risk became non-significant and reversed. There was a significantly positive association of waist circumference with Type 2 diabetes risk after adjustment for BMI, and a significantly positive association of body fat with Type 2 diabetes risk after adjustment for both BMI and waist circumference. When the joint effects were examined, the significantly positive associations of waist circumference or body fat with Type 2 diabetes risk were consistent among women with different levels of BMI, and the positive association of BMI and Type 2 diabetes risk was significant among women with gestational diabetes with a waist circumference of ≥ 50% or body fat ≥ 50%. Results
Conclusions BMI, waist circumference and body fat were all associated with an increased risk of Type 2 diabetes, and waist circumference and body fat were better indicators than BMI for Type 2 diabetes risk among Chinese women with prior gestational diabetes.
Diabet. Med. 31, 1368–1377 (2014)
Introduction With the fast economic development over the past three decades, the Chinese population has been experiencing a rapid lifestyle change, tending towards a more sedentary and high-energy/high-fat diet [1]. This change has resulted in a marked increase of diabetes prevalence among adult Chinese aged ≥ 20 years, from 1% in 1980 [2] to 11.6% in 2010 [3]. This lifestyle change has also caused dramatic increases of overweight (from 20.0% in 1992 to 29.9% in 2002 in Chinese aged ≥ 18 years) [4,5] and gestational diabetes mellitus (from 2.4% in 1999 to 8.2% in 2012 in urban Chinese women aged ≥ 20 years) [6], both of which will further increase diabetes prevalence. A systematic review has Correspondence to: Gang Hu. E-mail: [email protected]
1368
indicated that 20–50% of women with a history of gestational diabetes will develop Type 2 diabetes within 3– 5 years after delivery, and 70% will develop Type 2 diabetes if followed for ≥ 10 years [7]. Thus, how to define obesity and how to measure it among women with a history of gestational diabetes are of paramount importance for controlling Type 2 diabetes. Various measures of obesity, particularly BMI, have been widely used to define obesity. However, specific BMI values can reflect different body compositions across genders and races and, in some Asian populations, a given BMI value indicates a higher percentage of body fat than in European populations [8]. Body fat is used as the gold standard in receiver operating characteristic curve analyses examining the indicative value of various anthropometrics [9]. However, a prior investigation of body compositions with health
ª 2014 The Authors. Diabetic Medicine ª 2014 Diabetes UK
Research article
What’s new? • There is some confusion regarding which anthropometric measurement of adiposity should be used to indicate diabetes, especially for Asians. The present study evaluated different indicators of adiposity (BMI, waist circumference and body fat) with Type 2 diabetes risk among women with prior gestational diabetes mellitus in China and concluded that waist circumference and body fat were better indicators than BMI, and that body fat might be the best indicator for risk of Type 2 diabetes among Chinese women with prior gestational diabetes.
DIABETICMedicine
≥ 7.8 mmol/l were invited to undergo a 2-h 75-g oral glucose tolerance test at Tianjin Women’s and Children’s Health Center [6]. Gestational diabetes was defined using the 2005 criteria of the American Diabetes Association [15]. Women with a 75-g glucose 2-h oral glucose tolerance test result confirming either diabetes (fasting glucose ≥ 7 mmol/l or 2-h glucose ≥ 11.1 mmol/l) or impaired glucose tolerance (2-h glucose ≥ 7.8 and < 11.1 mmol/l) were regarded as having gestational diabetes. From December 1998 to December 2009, in total 128 125 pregnant women participated in the gestational diabetes screening programme and 6247 were diagnosed with gestational diabetes [16].
Study population
risk found that the percentage of fat did not perform better than BMI or waist circumference [10]. In 2001, waist circumference was included in obesity definition by the National Cholesterol Education Program (NCEP) Adult Treatment Panel III (ATP III) [11] because it has been widely used to define central obesity. Although some studies emphasized waist circumference as being more reflective of high risk of Type 2 diabetes than knowledge of BMI [12], a meta-analysis in 2007 indicated that waist circumference and BMI can be used interchangeably as they have same abilities to indicate future Type 2 diabetes risk [13]. Until now, there is still confusion as to which anthropometric measurement of adiposity should be used to indicate diabetes, especially for Asians or Asian Americans who have lower BMI but similar or even higher prevalence of diabetes and gestational diabetes than white people in western countries [14]. Moreover, the above studies were all performed among the general population, and few studies have compared the associations of different indexes of obesity with Type 2 diabetes risk among women with a history of gestational diabetes. The aim of the present study was to investigate the association of BMI, waist circumference and body fat with the risk of Type 2 diabetes, and to determine which of these is the stronger risk factor for Type 2 diabetes among Chinese women with prior gestational diabetes.
Patients and methods Tianjin gestational diabetes screening project
Tianjin is the fourth largest city in Northern China, consisting of 16 county-level administrative areas. In 2010, 4.3 million residents lived in six central urban districts among the 13 million residents. Since 1999, all pregnant women living in six urban districts have participated in the universal screening for gestational diabetes, and the average proportion of screened pregnancies from 1999 to 2008 was over 91% [6]. All pregnant women at 26–30 gestational weeks participated in a 1-h 50-g glucose screening test (glucose challenge test). Women who had a glucose reading
ª 2014 The Authors. Diabetic Medicine ª 2014 Diabetes UK
We used the data based on the participants of the Tianjin Gestational Diabetes Mellitus Prevention Program, who were recruited as described previously [16]. As we had set up a good healthcare registration system for health and contact information for mothers with gestational diabetes, all pregnant women diagnosed with gestational diabetes between 2005 and 2009 in six urban districts (n = 4644) were invited to participate in a post-partum baseline survey for the Tianjin Gestational Diabetes Mellitus Prevention Program [16] from August 2009 to July 2011. Ultimately, 1263 women with gestational diabetes (participation rate 27%) aged > 24 years finished the baseline survey (Fig. 1). There were no differences in the oral glucose tolerance test at 26–30 gestational weeks in age (28.9 vs. 28.7 years), 2-h glucose (9.23 vs. 9.16 mmol/l), fasting glucose (5.34 vs. 5.34 mmol/l), and the prevalence of impaired glucose tolerance (90.9% vs. 91.8%) and diabetes (9.1% vs. 8.2%) between the women with gestational diabetes who returned and those who did not. The study was approved by the Human Subjects Committee of the Tianjin Women’s and Children’s Health Center and informed consent was obtained from each participant.
Examinations
All study participants filled in a questionnaire about their socio-demographics (age, marital status, education, income and occupation), history of gestational diabetes, family history (diabetes, coronary heart disease, stroke, cancer and hypertension), medical history (hypertension, diabetes and hypercholesterolaemia), pregnancy outcomes (pre-pregnancy weight, weight gain in pregnancy and number of children), dietary habits (a self-administered food frequency questionnaire to measure the frequency and quantity of intake of 33 major food groups and beverages during the past year) [17], alcohol intake, smoking habits, passive smoking and physical activity (the frequency and duration of leisure-time and sedentary activities) at the post-partum baseline survey. They also completed the 3-day 24-h food records using methods for dietary record collections taught by a dietician. The
1369
Obesity index and post-partum diabetes L. Wang et al.
DIABETICMedicine
4644 women with GDM from 2005 to 2009 were invited to participate in OGTT Excluded 2,956 Could not be contacted 1,623 Move out 113 Not interested 747 Rejected 441 Diabetes 15 Fetal death 17 1688 GDM women were willing to make an appointment Excluded 385 Could not be contacted 85 Could not meet study criteria 250 Unwilling to participate 19 Have no time to participated 31
1,303 (28.1%) eligible finished baseline survey Excluded 40 Could not be contacted 9 Unwilling to participate 31
1,263 (27.2%) eligible finished baseline survey FIGURE 1 Participant flow chart.
performance of 3-day 24-h food records [17], the food frequency questionnaire [17] and the above questionnaire on assessing physical activity [18] have been validated in the China National Nutrition and Health Survey in 2002. Body weight, height, waist circumference and body fat were measured for all women using the standardized protocol by specially trained research doctors. Height was measured without shoes and with light clothing. The measurement of height was rounded to the nearest centimetre. Weight and body fat were measured by Body Composition Analyser (SC-240, Tanita, Tokyo, Japan). The Tanita SC-240 has been validated as having acceptable accuracy for estimating present body fat when compared with dual-energy X-ray absorptiometry (DXA) [19]. Waist circumference was measured midway between the lower rib margin and the iliac crest. The waist measurement was rounded to the nearest half centimetre. BMI was calculated
1370
by dividing current weight in kilograms by the square of height in metres. Blood samples were collected in all participants after an overnight fast of at least 12 h. Participants were given a standard 75-g glucose solution and plasma glucose was measured on an automatic analyser (TBA-120FR, Toshiba, Tokyo, Japan) at 0 and 2 h after administration during the oral glucose tolerance test.
Definition of Type 2 diabetes and pre-diabetes after delivery
According to the 2005 criteria of the American Diabetes Association [15], Type 2 diabetes was defined as fasting glucose ≥ 7.0 mmol/l or 2-h glucose ≥ 11.1 mmol/l, and pre-diabetes was defined as either impaired fasting glucose (fasting glucose ≥ 5.6 mmol/l and < 7.0 mmol/l) or impaired glucose tolerance (2-h glucose ≥ 7.8 mmol/l and
ª 2014 The Authors. Diabetic Medicine ª 2014 Diabetes UK
Research article
DIABETICMedicine
< 11.1 mmol/l). Hyperglycaemia included both Type 2 diabetes and pre-diabetes.
Statistical analyses
Logistic regression models were used to estimate the association of BMI, waist circumference and body fat with the risks of Type 2 diabetes, pre-diabetes and hyperglycaemia. BMI, waist circumference and body fat were evaluated in the following two ways: (1) as categories [BMI < 24 kg/m2 (reference group), 24–27.9 kg/m2 and ≥ 28 kg/ m2; waist circumference and body fat as quartiles] and (2) as a continuous variable. All analyses were adjusted for age (model 1) and further for education, family history of diabetes, smoking, passive smoking, alcohol drinking, leisure-time physical activity, sitting time, dietary fibre, total energy intake, energy per cent of monounsaturated fat, energy per cent of polyunsaturated fat and energy per cent of saturated fat (model 2) and, additionally, for waist circumference (in BMI and body fat analyses) and BMI (in waist circumference analysis) (model 3), and finally adjusted for variables in model 2 and also waist circumference and body fat (in BMI analysis), BMI and body fat (in waist circumference analysis), BMI and waist circumference (in body fat analysis) (model 4). Different levels of BMI,
waist circumference or body fat were included in the models as dummy variables, and the significance of the trends over different categories were tested in models with the median of each category as a continuous variable. As some studies concluded that odds ratios estimated by logistic regression tended to overestimate the risk ratio when the outcome events were common (especially if more than 20%) [20], log–binomial regression was used for hyperglycaemia analyses [21]. Statistical significance was considered to be P < 0.05. All statistical analyses were performed with Predictive Analytics Software (PASW) for Windows, version 20.0 (IBM SPSS, Chicago, IL, USA) and Statistical Analysis System (SAS) for Windows, version 9.3 (SAS Institute, Cary, NC, USA).
Results General characteristics of the study population are presented in Table 1. Compared with women with normal glucose, women who were diagnosed with pre-diabetes and Type 2 diabetes had significantly higher BMI, larger waist circumference and body fat, had lower education level and family income, and more often had a family history of diabetes. Age-adjusted partial correlations were 0.89 (P < 0.001) for BMI and waist circumference, 0.97 (P < 0.001) for BMI and
Table 1 Baseline characteristics of women with a history of gestational diabetes Characteristic No. of subjects Age (years) BMI (kg/m2) Waist circumference (cm) Body fat (%) Family history of diabetes (%) Current smoking (%) Passive smoking (%) Current alcohol drinkers (%) Education (%) < 13 years 13–16 years ≥ 16 years Income (%) < 5000 yuan/month 5000–7999 yuan/month ≥ 8000 yuan/month Sitting time at home (h/day) Leisure-time physical activity (%) 0 min/day 1–29 min/day ≥ 30 min/day Dietary intake* Energy consumption (kcal/day) Fibre (g/day) Fat (% energy) Saturated fat (% energy) Monounsaturated fat (% energy) Polyunsaturated fat (% energy)
Normal glucose 779 32.3 23.2 78.3 31.6 31.7 2.05 52.8 21.3
3.5 3.4 8.2 5.3
Pre-diabetes 401 32.5 25.4 83.4 35.0 39.2 1.75 54.4 21.9
3.5 4.1 10.0 5.8
Diabetes 83 32.7 27.3 88.7 37.9 59.0 2.41 61.4 25.3
P-value
3.8 4.0 9.6 5.2
< < <
0.1) (model 4). There were significant and positive associations across quartiles of body fat with the risks of Type 2 diabetes (Ptrend < 0.001), pre-diabetes (Ptrend < 0.001) and hyperglycaemia (Ptrend < 0.001). These positive associations remained significant after adjustment for waist circumference and BMI (models 3 and 4). When using log–binomial regression in hyperglycaemia analyses, the odds ratios of hyperglycaemia associated with BMI, waist circumference and body fat became smaller, but the trend of odds ratios was similar compared with the odds
Table 2 Odds ratios of diabetes by different levels of BMI, waist circumference and body fat
No. of subjects BMI categories (kg/m2) < 24 682 24–27.9 383 ≥ 28 198 P for trend BMI as a continuous variable (1-unit increase) Waist circumference categories* Quartile 1 306 Quartile 2 327 Quartile 3 293 Quartile 4 337 P for trend Waist circumference as a continuous variable (1-unit increase) Body fat categories* Quartile 1 312 Quartile 2 324 Quartile 3 312 Quartile 4 315 P for trend Body fat as a continuous variable (1-unit increase)
Crude prevalence (%)
Odds ratios (95% confidence intervals)
No. of cases
Model 1†
Model 2‡
Model 3§
Model 4¶
18 32 33
2.64 8.36 16.7
1.00 3.35 (1.85–6.06) 7.50 (4.12–13.7) < 0.001 1.20 (1.14–1.27)
1.00 2.77 (1.50–5.08) 6.88 (3.66–13.0) < 0.001 1.20 (1.13–1.27)
1.00 1.53 (0.76–3.09) 1.80 (0.64–5.04) 0.255 1.04 (0.93–1.17)
1.00 1.10 (0.48–2.52) 0.97 (0.25–3.71) 0.956 0.59 (0.41–0.85)
4 9 22 48
1.31 2.75 7.51 14.2
1.00 2.14 (0.65–7.02) 6.13 (2.08–18.0) 12.5 (4.46–35.2)
Research: Epidemiology Obesity index and the risk of diabetes among Chinese women with prior gestational diabetes L. Wang1, H. Liu1, S. Zhang1, J. Leng1, G. Liu1, C. Zhang1, W. Q. Li1,2, N. Li1, W. Li1, Y. Li1, S. Sun1, Z. Yu3, X. Yang4 and G. Hu2 1 Tianjin Women’s and Children’s Health Center, China, 2Pennington Biomedical Research Center, Baton Rouge, LA, USA, 3Population Cancer Research Program, Dalhousie University, Halifax, NS, Canada and 4Department of Epidemiology and Biostatistics, Tianjin Medical University, China
Accepted 20 June 2014
Abstract Aims There is some confusion regarding which anthropometric measurement of adiposity should be used to indicate diabetes, especially for Asians. The present study was to evaluate different indicators of adiposity (BMI, waist circumference and body fat) with Type 2 diabetes risk among women with prior gestational diabetes mellitus. Methods We performed a cross-sectional survey in 1263 women with gestational diabetes at 1–5 years after delivery. Logistic regression models were used to estimate the association of BMI, waist circumference and body fat with Type 2 diabetes risk.
BMI, waist circumference and body fat were all associated with an increased risk of Type 2 diabetes among women with prior gestational diabetes (all Ptrend < 0.001). After adjustment for waist circumference and body fat, the positive association of BMI with Type 2 diabetes risk became non-significant and reversed. There was a significantly positive association of waist circumference with Type 2 diabetes risk after adjustment for BMI, and a significantly positive association of body fat with Type 2 diabetes risk after adjustment for both BMI and waist circumference. When the joint effects were examined, the significantly positive associations of waist circumference or body fat with Type 2 diabetes risk were consistent among women with different levels of BMI, and the positive association of BMI and Type 2 diabetes risk was significant among women with gestational diabetes with a waist circumference of ≥ 50% or body fat ≥ 50%. Results
Conclusions BMI, waist circumference and body fat were all associated with an increased risk of Type 2 diabetes, and waist circumference and body fat were better indicators than BMI for Type 2 diabetes risk among Chinese women with prior gestational diabetes.
Diabet. Med. 31, 1368–1377 (2014)
Introduction With the fast economic development over the past three decades, the Chinese population has been experiencing a rapid lifestyle change, tending towards a more sedentary and high-energy/high-fat diet [1]. This change has resulted in a marked increase of diabetes prevalence among adult Chinese aged ≥ 20 years, from 1% in 1980 [2] to 11.6% in 2010 [3]. This lifestyle change has also caused dramatic increases of overweight (from 20.0% in 1992 to 29.9% in 2002 in Chinese aged ≥ 18 years) [4,5] and gestational diabetes mellitus (from 2.4% in 1999 to 8.2% in 2012 in urban Chinese women aged ≥ 20 years) [6], both of which will further increase diabetes prevalence. A systematic review has Correspondence to: Gang Hu. E-mail: [email protected]
1368
indicated that 20–50% of women with a history of gestational diabetes will develop Type 2 diabetes within 3– 5 years after delivery, and 70% will develop Type 2 diabetes if followed for ≥ 10 years [7]. Thus, how to define obesity and how to measure it among women with a history of gestational diabetes are of paramount importance for controlling Type 2 diabetes. Various measures of obesity, particularly BMI, have been widely used to define obesity. However, specific BMI values can reflect different body compositions across genders and races and, in some Asian populations, a given BMI value indicates a higher percentage of body fat than in European populations [8]. Body fat is used as the gold standard in receiver operating characteristic curve analyses examining the indicative value of various anthropometrics [9]. However, a prior investigation of body compositions with health
ª 2014 The Authors. Diabetic Medicine ª 2014 Diabetes UK
Research article
What’s new? • There is some confusion regarding which anthropometric measurement of adiposity should be used to indicate diabetes, especially for Asians. The present study evaluated different indicators of adiposity (BMI, waist circumference and body fat) with Type 2 diabetes risk among women with prior gestational diabetes mellitus in China and concluded that waist circumference and body fat were better indicators than BMI, and that body fat might be the best indicator for risk of Type 2 diabetes among Chinese women with prior gestational diabetes.
DIABETICMedicine
≥ 7.8 mmol/l were invited to undergo a 2-h 75-g oral glucose tolerance test at Tianjin Women’s and Children’s Health Center [6]. Gestational diabetes was defined using the 2005 criteria of the American Diabetes Association [15]. Women with a 75-g glucose 2-h oral glucose tolerance test result confirming either diabetes (fasting glucose ≥ 7 mmol/l or 2-h glucose ≥ 11.1 mmol/l) or impaired glucose tolerance (2-h glucose ≥ 7.8 and < 11.1 mmol/l) were regarded as having gestational diabetes. From December 1998 to December 2009, in total 128 125 pregnant women participated in the gestational diabetes screening programme and 6247 were diagnosed with gestational diabetes [16].
Study population
risk found that the percentage of fat did not perform better than BMI or waist circumference [10]. In 2001, waist circumference was included in obesity definition by the National Cholesterol Education Program (NCEP) Adult Treatment Panel III (ATP III) [11] because it has been widely used to define central obesity. Although some studies emphasized waist circumference as being more reflective of high risk of Type 2 diabetes than knowledge of BMI [12], a meta-analysis in 2007 indicated that waist circumference and BMI can be used interchangeably as they have same abilities to indicate future Type 2 diabetes risk [13]. Until now, there is still confusion as to which anthropometric measurement of adiposity should be used to indicate diabetes, especially for Asians or Asian Americans who have lower BMI but similar or even higher prevalence of diabetes and gestational diabetes than white people in western countries [14]. Moreover, the above studies were all performed among the general population, and few studies have compared the associations of different indexes of obesity with Type 2 diabetes risk among women with a history of gestational diabetes. The aim of the present study was to investigate the association of BMI, waist circumference and body fat with the risk of Type 2 diabetes, and to determine which of these is the stronger risk factor for Type 2 diabetes among Chinese women with prior gestational diabetes.
Patients and methods Tianjin gestational diabetes screening project
Tianjin is the fourth largest city in Northern China, consisting of 16 county-level administrative areas. In 2010, 4.3 million residents lived in six central urban districts among the 13 million residents. Since 1999, all pregnant women living in six urban districts have participated in the universal screening for gestational diabetes, and the average proportion of screened pregnancies from 1999 to 2008 was over 91% [6]. All pregnant women at 26–30 gestational weeks participated in a 1-h 50-g glucose screening test (glucose challenge test). Women who had a glucose reading
ª 2014 The Authors. Diabetic Medicine ª 2014 Diabetes UK
We used the data based on the participants of the Tianjin Gestational Diabetes Mellitus Prevention Program, who were recruited as described previously [16]. As we had set up a good healthcare registration system for health and contact information for mothers with gestational diabetes, all pregnant women diagnosed with gestational diabetes between 2005 and 2009 in six urban districts (n = 4644) were invited to participate in a post-partum baseline survey for the Tianjin Gestational Diabetes Mellitus Prevention Program [16] from August 2009 to July 2011. Ultimately, 1263 women with gestational diabetes (participation rate 27%) aged > 24 years finished the baseline survey (Fig. 1). There were no differences in the oral glucose tolerance test at 26–30 gestational weeks in age (28.9 vs. 28.7 years), 2-h glucose (9.23 vs. 9.16 mmol/l), fasting glucose (5.34 vs. 5.34 mmol/l), and the prevalence of impaired glucose tolerance (90.9% vs. 91.8%) and diabetes (9.1% vs. 8.2%) between the women with gestational diabetes who returned and those who did not. The study was approved by the Human Subjects Committee of the Tianjin Women’s and Children’s Health Center and informed consent was obtained from each participant.
Examinations
All study participants filled in a questionnaire about their socio-demographics (age, marital status, education, income and occupation), history of gestational diabetes, family history (diabetes, coronary heart disease, stroke, cancer and hypertension), medical history (hypertension, diabetes and hypercholesterolaemia), pregnancy outcomes (pre-pregnancy weight, weight gain in pregnancy and number of children), dietary habits (a self-administered food frequency questionnaire to measure the frequency and quantity of intake of 33 major food groups and beverages during the past year) [17], alcohol intake, smoking habits, passive smoking and physical activity (the frequency and duration of leisure-time and sedentary activities) at the post-partum baseline survey. They also completed the 3-day 24-h food records using methods for dietary record collections taught by a dietician. The
1369
Obesity index and post-partum diabetes L. Wang et al.
DIABETICMedicine
4644 women with GDM from 2005 to 2009 were invited to participate in OGTT Excluded 2,956 Could not be contacted 1,623 Move out 113 Not interested 747 Rejected 441 Diabetes 15 Fetal death 17 1688 GDM women were willing to make an appointment Excluded 385 Could not be contacted 85 Could not meet study criteria 250 Unwilling to participate 19 Have no time to participated 31
1,303 (28.1%) eligible finished baseline survey Excluded 40 Could not be contacted 9 Unwilling to participate 31
1,263 (27.2%) eligible finished baseline survey FIGURE 1 Participant flow chart.
performance of 3-day 24-h food records [17], the food frequency questionnaire [17] and the above questionnaire on assessing physical activity [18] have been validated in the China National Nutrition and Health Survey in 2002. Body weight, height, waist circumference and body fat were measured for all women using the standardized protocol by specially trained research doctors. Height was measured without shoes and with light clothing. The measurement of height was rounded to the nearest centimetre. Weight and body fat were measured by Body Composition Analyser (SC-240, Tanita, Tokyo, Japan). The Tanita SC-240 has been validated as having acceptable accuracy for estimating present body fat when compared with dual-energy X-ray absorptiometry (DXA) [19]. Waist circumference was measured midway between the lower rib margin and the iliac crest. The waist measurement was rounded to the nearest half centimetre. BMI was calculated
1370
by dividing current weight in kilograms by the square of height in metres. Blood samples were collected in all participants after an overnight fast of at least 12 h. Participants were given a standard 75-g glucose solution and plasma glucose was measured on an automatic analyser (TBA-120FR, Toshiba, Tokyo, Japan) at 0 and 2 h after administration during the oral glucose tolerance test.
Definition of Type 2 diabetes and pre-diabetes after delivery
According to the 2005 criteria of the American Diabetes Association [15], Type 2 diabetes was defined as fasting glucose ≥ 7.0 mmol/l or 2-h glucose ≥ 11.1 mmol/l, and pre-diabetes was defined as either impaired fasting glucose (fasting glucose ≥ 5.6 mmol/l and < 7.0 mmol/l) or impaired glucose tolerance (2-h glucose ≥ 7.8 mmol/l and
ª 2014 The Authors. Diabetic Medicine ª 2014 Diabetes UK
Research article
DIABETICMedicine
< 11.1 mmol/l). Hyperglycaemia included both Type 2 diabetes and pre-diabetes.
Statistical analyses
Logistic regression models were used to estimate the association of BMI, waist circumference and body fat with the risks of Type 2 diabetes, pre-diabetes and hyperglycaemia. BMI, waist circumference and body fat were evaluated in the following two ways: (1) as categories [BMI < 24 kg/m2 (reference group), 24–27.9 kg/m2 and ≥ 28 kg/ m2; waist circumference and body fat as quartiles] and (2) as a continuous variable. All analyses were adjusted for age (model 1) and further for education, family history of diabetes, smoking, passive smoking, alcohol drinking, leisure-time physical activity, sitting time, dietary fibre, total energy intake, energy per cent of monounsaturated fat, energy per cent of polyunsaturated fat and energy per cent of saturated fat (model 2) and, additionally, for waist circumference (in BMI and body fat analyses) and BMI (in waist circumference analysis) (model 3), and finally adjusted for variables in model 2 and also waist circumference and body fat (in BMI analysis), BMI and body fat (in waist circumference analysis), BMI and waist circumference (in body fat analysis) (model 4). Different levels of BMI,
waist circumference or body fat were included in the models as dummy variables, and the significance of the trends over different categories were tested in models with the median of each category as a continuous variable. As some studies concluded that odds ratios estimated by logistic regression tended to overestimate the risk ratio when the outcome events were common (especially if more than 20%) [20], log–binomial regression was used for hyperglycaemia analyses [21]. Statistical significance was considered to be P < 0.05. All statistical analyses were performed with Predictive Analytics Software (PASW) for Windows, version 20.0 (IBM SPSS, Chicago, IL, USA) and Statistical Analysis System (SAS) for Windows, version 9.3 (SAS Institute, Cary, NC, USA).
Results General characteristics of the study population are presented in Table 1. Compared with women with normal glucose, women who were diagnosed with pre-diabetes and Type 2 diabetes had significantly higher BMI, larger waist circumference and body fat, had lower education level and family income, and more often had a family history of diabetes. Age-adjusted partial correlations were 0.89 (P < 0.001) for BMI and waist circumference, 0.97 (P < 0.001) for BMI and
Table 1 Baseline characteristics of women with a history of gestational diabetes Characteristic No. of subjects Age (years) BMI (kg/m2) Waist circumference (cm) Body fat (%) Family history of diabetes (%) Current smoking (%) Passive smoking (%) Current alcohol drinkers (%) Education (%) < 13 years 13–16 years ≥ 16 years Income (%) < 5000 yuan/month 5000–7999 yuan/month ≥ 8000 yuan/month Sitting time at home (h/day) Leisure-time physical activity (%) 0 min/day 1–29 min/day ≥ 30 min/day Dietary intake* Energy consumption (kcal/day) Fibre (g/day) Fat (% energy) Saturated fat (% energy) Monounsaturated fat (% energy) Polyunsaturated fat (% energy)
Normal glucose 779 32.3 23.2 78.3 31.6 31.7 2.05 52.8 21.3
3.5 3.4 8.2 5.3
Pre-diabetes 401 32.5 25.4 83.4 35.0 39.2 1.75 54.4 21.9
3.5 4.1 10.0 5.8
Diabetes 83 32.7 27.3 88.7 37.9 59.0 2.41 61.4 25.3
P-value
3.8 4.0 9.6 5.2
< < <
0.1) (model 4). There were significant and positive associations across quartiles of body fat with the risks of Type 2 diabetes (Ptrend < 0.001), pre-diabetes (Ptrend < 0.001) and hyperglycaemia (Ptrend < 0.001). These positive associations remained significant after adjustment for waist circumference and BMI (models 3 and 4). When using log–binomial regression in hyperglycaemia analyses, the odds ratios of hyperglycaemia associated with BMI, waist circumference and body fat became smaller, but the trend of odds ratios was similar compared with the odds
Table 2 Odds ratios of diabetes by different levels of BMI, waist circumference and body fat
No. of subjects BMI categories (kg/m2) < 24 682 24–27.9 383 ≥ 28 198 P for trend BMI as a continuous variable (1-unit increase) Waist circumference categories* Quartile 1 306 Quartile 2 327 Quartile 3 293 Quartile 4 337 P for trend Waist circumference as a continuous variable (1-unit increase) Body fat categories* Quartile 1 312 Quartile 2 324 Quartile 3 312 Quartile 4 315 P for trend Body fat as a continuous variable (1-unit increase)
Crude prevalence (%)
Odds ratios (95% confidence intervals)
No. of cases
Model 1†
Model 2‡
Model 3§
Model 4¶
18 32 33
2.64 8.36 16.7
1.00 3.35 (1.85–6.06) 7.50 (4.12–13.7) < 0.001 1.20 (1.14–1.27)
1.00 2.77 (1.50–5.08) 6.88 (3.66–13.0) < 0.001 1.20 (1.13–1.27)
1.00 1.53 (0.76–3.09) 1.80 (0.64–5.04) 0.255 1.04 (0.93–1.17)
1.00 1.10 (0.48–2.52) 0.97 (0.25–3.71) 0.956 0.59 (0.41–0.85)
4 9 22 48
1.31 2.75 7.51 14.2
1.00 2.14 (0.65–7.02) 6.13 (2.08–18.0) 12.5 (4.46–35.2)
