Abstract
Aims
To investigate the prevalence and risk factors of diabetes and impaired fasting glucose among urban university applicants in Eastern China.
Method
The study uses data from the annual health examination among all students finishing high school who applied for university entrance in Changzhou City in 2012. In total, 6716 students aged 17–19 years had fasting blood glucose, alanine transaminase, height, weight and blood pressure measured. Impaired fasting glucose and diabetes were defined as fasting blood glucose ≥ 5.6 mmol/l (but < 7 mmol/l) and ≥ 7 mmol/l, respectively.
Results
The overall prevalence of impaired fasting glucose and diabetes was 2.40% and 0.13%, respectively (3.67% and 0.09% in boys; 1.09% and 0.18% in girls). In total, 20.9% of boys and 10.6% of girls were overweight/obese. High socio-economic status was associated with an increased risk of diabetes / impaired fasting glucose, but the association was significant only among boys (adjusted odds ratio 1.94, 95% CI 1.26–2.98). Alanine transaminase levels were significantly and positively related to diabetes / impaired fasting glucose risk. Overweight / obesity was significantly associated with increased risk of impaired fasting glucose/diabetes in girls, but not in boys. Moreover, the number of the above-mentioned risk factors (i.e. overweight/obesity, elevated alanine transaminase, pre-hypertension) was significantly and positively related to diabetes / impaired fasting glucose among both boys and girls.
Conclusions
Impaired fasting glucose was prevalent among urban university applicants, in particular boys and those of high socio-economic status in eastern China. Elevated levels of liver function enzyme appear to be the strongest risk factor for diabetes / impaired fasting glucose.
Introduction
Parallel to the escalating burden of diabetes in adults, the prevalence of diabetes increases in adolescents globally [1–3], including in developing countries adopting a westernized lifestyle such as China. Data from 14 medical centres in China suggest that the prevalence of diabetes in children has increased dramatically, with Type 2 diabetes exceeding Type 1 diabetes [4]. Studies on the prevalence and risk factors of diabetes / impaired fasting glucose among adolescents are still limited in China [5–7].
Many factors may contribute to the rise of diabetes in adolescents. Among them, obesity is a significant risk factor [8]. In the past, the Chinese population was lean but over the last three decades there has been an increase in obesity [9]. Accompanying the obesity epidemic, the burden of other metabolic disorders is increasing, including non-alcoholic fatty liver disease [6,10].
This study aims to investigate the prevalence of diabetes / impaired fasting glucose, as well as risk factors, among students completing high school in Changzhou City, an affluent city in eastern China.
Research design and methods
In China, when a student finishes high school, they are required to undertake a health check prior to the National University Entrance Examination. This is part of the university enrolment application process and there are no exceptions. The current study uses such annual health examination data from students living in Changzhou City, China. Changzhou is close to Shanghai and is one of the most affluent cities in China, with a population of 3.6 million [11].
In March 2012, 6927 year 12 students attended the health check. Of these, 211 (3.1%) students were aged < 17 years or ≥ 20 years (out of the normal range of age for completing high school) and were thus excluded. The final sample size included in the analysis was 6716.
A morning blood sample was collected after an overnight fast. Fasting plasma glucose was measured using an enzymatic (hexokinase) colorimetric test. Impaired fasting glucose and diabetes were defined as fasting blood glucose ≥ 5.6 mmol/l (but < 7 mmol/l) and ≥ 7 mmol/l, respectively[12]. Alanine transaminase (ALT) was measured using an Olympus AU640 (Olympus, Tokyo, Japan). Elevated ALT was defined as ALT ≥ 40 IU/l. Students were asked about their major disease history, but not specifically about diabetes.
Height, weight and blood pressure of the students were measured according to standardized protocol. Pre-hypertension was defined as systolic blood pressure ≥ 120 mmHg and/or diastolic blood pressure ≥ 80 mmHg [13]. Overweight, obesity and underweight were defined using International Obesity Task Force (IOTF) criteria [14,15]. The criteria used BMI cut-offs corresponding to 25, 30 and 18.5 kg/m2 in adults to define overweight, obesity and underweight, respectively.
A school socio-economic status variable was constructed based on real estate / property prices near each school: low (< 5000 Yuan/m2), medium (5000– 10 000 Yuan/m2) and high (≥ 10 000 Yuan/m2). The real estate / property prices were extracted from a local website in June 2012 [16]. Overall, 43.9%, 26.1% and 30.0% of the students were from low, medium and high socio-economic status schools, respectively.
As this study was based on secondary data using anonymous information, written consent was not gained from the students.
Data analysis
Chi-square tests were used to compare differences between categorical variables, and analysis of variance (ANOVA) was used to compare differences in continuous variables between groups. ALT levels were categorized into sex-specific tertiles. A metabolic risk factor score was calculated based on three conditions, including overweight / obesity, the highest tertile of ALT, and pre-hypertension / hypertension (each scored 1). Logistic regression was performed to assess the association between socio-demographic factors and diabetes / impaired fasting glucose.
Results
In the present study, nine of the students had diabetes (three boys and six girls) and 161 had impaired fasting glucose (125 boys and 36 girls). The prevalences of diabetes and impaired fasting glucose were 0.09% and 3.67%, respectively, in boys; 0.18% and 1.09%, respectively, in girls; and 0.13% and 2.40% in both genders combined. However, no students reported having a history of diabetes.
In total, 20.9% of boys and 10.6% of girls were overweight / obese. The prevalence of pre-hypertension was 68.0% in boys and 36.4% in girls. More boys had elevated ALT than girls (9.4% vs 1.7%). Overall, 12.9% of the boys had all three metabolic risk factors.
Among those being overweight or obese, the prevalences of diabetes and impaired fasting glucose were 0.66% (0.42% in boys, 1.14% in girls) and 3.86% (4.49% in boys, 2.57% in girls), respectively. The prevalence of diabetes / impaired fasting glucose was positively associated with the increase of ALT. Those with diabetes / impaired fasting glucose had higher BMI and were more likely to have high ALT than those without the condition (Table 1).
Table 1.
Characteristics of high school university applicants by diabetes and impaired glucose tolerance status, Changzhou, China, 2012 (n = 6716)*
| Boys (n = 3408) |
P-value | Girls (n = 3308) |
P-value | |||
|---|---|---|---|---|---|---|
| Normal (n = 3280) |
Diabetes/impaired fasting glucose (n = 128) |
Normal (n = 3266) |
Diabetes/impaired fasting glucose (n = 42) |
|||
| Age (years) | 18.1 (0.5) | 18.1 (0.5) | 0.590 | 18.0 (0.4) | 18.0 (0.5) | 0.740 |
| Height (cm) | 174.7 (5.9) | 174.6 (6.2) | 0.900 | 161.5 (5.4) | 162.4 (5.7) | 0.250 |
| Weight (kg) | 68.3 (12.8) | 71.1 (14.3) | 0.016 | 55.2 (8.7) | 62.3 (17.7) | <0.001 |
| School socio-economic status (%) | ||||||
| Low | 45.5 | 31.0 | 0.005 | 42.9 | 37.5 | 0.049 |
| Medium | 25.6 | 30.2 | 26.6 | 15.0 | ||
| High | 28.9 | 38.9 | 30.4 | 47.5 | ||
| BMI (kg/m2) | 22.4 (3.9) | 23.3 (4.4) | 0.008 | 21.2 (3.0) | 23.5 (5.9) | <0.001 |
| BMI (%) | ||||||
| Underweight | 9.7 | 10.2 | 0.170 | 15.0 | 16.7 | <0.001 |
| Normal | 69.6 | 62.5 | 74.7 | 52.4 | ||
| Overweight/obesity | 20.7 | 27.3 | 10.3 | 31.0 | ||
| ALT (IU/l) | 21.3 (19.4) | 27.6 (25.8) | <0.001 | 13.1 (8.6) | 23.6 (27.5) | <0.001 |
| ALT > 40 IU/l (%) | 9.1 | 16.4 | 0.005 | 1.6 | 14.3 | <0.001 |
| Tertiles of ALT (%) | ||||||
| T1: 10.5 (9–11.8) in boys; 8.4 (7.4–9.1) in girls† | 33.8 | 28.1 | 0.013 | 34.0 | 23.8 | 0.060 |
| T2: 15.7 (14.4–17.5) in boys; 11.4 (10.6–12.1) in girls† | 33.3 | 26.6 | 33.3 | 26.2 | ||
| T3: 29.1 (23.3–42.2) in boys; 16.5 (14.4–20.6) in girls† | 32.9 | 45.3 | 32.8 | 50.0 | ||
| Pre-hypertension/hypertension (%) | 67.8 | 74.2 | 0.130 | 36.2 | 54.8 | 0.013 |
| Glucose (mmol/l) | 4.8 (0.4) | 6.0 (0.6) | <0.001 | 4.7 (0.4) | 6.4 (1.3) | <0.001 |
| Number of metabolic risk factors (%)‡ | ||||||
| 0 | 24.2 | 14.8 | 0.020 | 42.8 | 31.0 | <0.001 |
| 1 | 43.0 | 40.6 | 39.0 | 31.0 | ||
| 2 | 20.0 | 27.3 | 14.3 | 9.5 | ||
| 3 | 12.8 | 17.2 | 3.9 | 28.6 | ||
Values are mean (sd) unless otherwise specified.
Values median (interquartile range).
Including overweight/obesity, third tertile of alanine transaminase (ALT) and pre-hypertension/hypertension.
Boys from high socio-economic status schools had a higher risk of having diabetes / impaired fasting glucose (odds ratio 1.94, 95% CI 1.26–2.98) than those from low socio-economic status (Table 2). A similar association was found in girls, although it was not statistically significant. In both boys and girls, a high ALT level (third tertile) was associated with an increased risk of diabetes / impaired fasting glucose. In comparison with those with normal ALT, those with elevated ALT had a significantly higher risk of having diabetes / impaired fasting glucose (odds ratio 1.76 (1.03–3.01) in boys and 6.29 (2.21–17.87) in girls) (data not shown). Among girls, both prehypertension and overweight / obesity were related to an increased risk of diabetes / impaired fasting glucose. Among boys, both pre-hypertension and overweight / obesity were marginally associated with diabetes / impaired fasting glucose in univariate analyses. However, neither pre-hypertension nor overweight / obesity was associated with diabetes / impaired fasting glucose in multivariable models in boys.
Table 2.
Odds ratios (95% CI) for characteristics associated with diabetes/impaired fasting glucose among high school university applicants in Changzhou, China (n = 6716)
| Boys | Girls | |||||||
|---|---|---|---|---|---|---|---|---|
| Odds ratio (95% CI) | Odds ratio (95% CI) | |||||||
| Model 1‡ | Model 2§ | Model 1‡ | Model 2§ | |||||
| School socio-economic status | ||||||||
| Low | 1.00 | Reference | 1.00 | Reference | 1.00 | Reference | 1.00 | Reference |
| Medium | 1.73* | (1.10–2.73) | 1.68* | (1.07–2.66) | 0.65 | (0.25–1.68) | 0.63 | (0.24–1.63) |
| High | 1.98** | (1.29–3.03) | 1.94** | (1.26–2.98) | 1.80 | (0.91–3.56) | 1.70 | (0.86–3.38) |
| BMI status | ||||||||
| Normal | 1.00 | Reference | 1.00 | Reference | 1.00 | Reference | 1.00 | Reference |
| Underweight | 1.16 | (0.64–2.12) | 1.42 | (0.77–2.62) | 1.59 | (0.67–3.73) | 1.82 | (0.76–4.37) |
| Overweight/obesity | 1.47 | (0.98–2.21) | 1.12 | (0.71–1.76) | 4.27** | (2.13–8.55) | 3.49** | (1.63–7.45) |
| Blood pressure | ||||||||
| Normal | 1.00 | Reference | 1.00 | Reference | 1.00 | Reference | 1.00 | Reference |
| Pre-hypertension/hypertension | 1.37 | (0.92–2.05) | 1.29 | (0.85–1.98) | 2.14* | (1.16–3.94) | 1.69 | (0.87–3.29) |
| Tertiles of ALT | ||||||||
| T1: 10.5 (9–11.8) in boys; 8.4 (7.4–9.1) in girls† | 1.00 | Reference | 1.00 | Reference | 1.00 | Reference | 1.00 | Reference |
| T2: 15.7 (14.4–17.5) in boys; 11.4 (10.6–12.1) in girls† | 0.96 | (0.60–1.54) | 1.01 | (0.62–1.65) | 1.13 | (0.48–2.67) | 0.94 | (0.39–2.28) |
| T3: 29.1 (23.3–42.2) in boys; 16.5 (14.4–20.6) in girls† | 1.67* | (1.09–2.55) | 1.63* | (1.01–2.64) | 2.19* | (1.02–4.67) | 1.53 | (0.69–3.40) |
| Number of metabolic risk factors ‖ | ||||||||
| 0 | 1.00 | Reference | 1.00 | Reference | 1.00 | Reference | 1.00 | Reference |
| 1 | 1.55 | (0.91–2.63) | 1.60 | (0.93–2.75) | 1.10 | (0.51–2.38) | 1.18 | (0.54–2.60) |
| 2 | 2.25** | (1.27–3.98) | 2.30** | (1.29–4.11) | 0.93 | (0.30–2.85) | 0.74 | (0.21–2.63) |
| 3 | 2.20* | (1.18–4.12) | 2.21* | (1.17–4.18) | 10.07** | (4.50–22.53) | 10.88** | (4.76–24.88) |
P < 0.05,
P < 0.01.
Values are median (interquartile range).
Model 1: adjusted for age.
Model 2: adjusted for age, school socio-economic status, BMI status, pre-hypertension/hypertension and tertiles of alanine transaminase (ALT). For number of metabolic risk factors, model 2 only adjusted for age and school socio-economic status.
Including overweight/obesity, third tertile of ALT and pre-hypertension/hypertension.
The coexistence of multiple risk factors was associated with an increased risk of diabetes/ impaired fasting glucose. Girls with all three metabolic risk factors were 10 times more likely to have diabetes / impaired fasting glucose than those without the conditions.
Discussion
In this population-based study among high socio-economic status urban university applicants in China, we observed that diabetes / impaired fasting glucose was prevalent among boys and those from high socio-economic status. Elevated ALT was significantly associated with an increased risk of diabetes / impaired fasting glucose in both genders. Overweight and pre-hypertension were related to an increased risk of diabetes / impaired fasting glucose in girls.
A study in the 1990s showed that the prevalence of Type 1 diabetes among Chinese children (< 15 years) was very low (incident rate of 0.51 per 100 000), with large regional variation[17]. Results from the 2002 Chinese National Nutrition Survey (household based) show that the prevalence of diabetes was 0.4% among adolescents aged 12–18 years [6]. However, data from China Nutrition and Health Survey 2009 (household based) found that 0.9% and 8.4% of adolescents aged 12–17 years had diabetes or impaired fasting glucose, respectively [7]. The prevalence of impaired fasting glucose and diabetes among overweight/obese university applicants in our data was similar to the findings from other school-based studies in Tianjin, China [5], Iran[18] and Germany[19]. The prevalence of impaired fasting glucose in the study was much lower than in US adolescents from the National Health and Nutrition Examination Survey (NHANES) 2005–2006 (13.1%) [20]. These differences may be partly attributable to the different sampling methods and the study population. The gender difference in the prevalence of diabetes / impaired fasting glucose was consistent with previous findings [5]. A high prevalence of diabetes / impaired fasting glucose was found in schools with high socio-economic status. This association is in line with mainstream findings on the socio-economic distribution of diabetes in adults [21] and obesity in Chinese adolescents [22].
Consistent with other studies, overweight/obesity was positively associated with diabetes / impaired fasting glucose risk [5]. However, in multivariable analysis, the association between overweight/obesity and diabetes / impaired fasting glucose was not statistically significant in boys. In the study, we defined overweight/obesity based on BMI, which may not be able to differentiate fat mass from lean mass, especially in boys. It suggests that screening for diabetes / impaired fasting glucose may not be efficient if we only focus on overweight / obesity using BMI.
ALT has been suggested to be a useful surrogate measure of non-alcoholic fatty liver disease [23]. An elevated ALT level was related to the risk of incident diabetes [24– 27]. Consistent with current knowledge, we found a positive association between ALT and diabetes / impaired fasting glucose. In our study, the prevalence of elevated ALT was similar in girls, but higher in boys (9.8% vs 4.8%) compared with another study in China [28].
A high prevalence of pre-hypertension is of concern and needs further study. Although pre-hypertension itself is not significantly associated with diabetes / impaired fasting glucose, the combined three metabolic risk factors are significantly related to diabetes / impaired fasting glucose. Because of the low prevalence of diabetes / impaired fasting glucose in children, general population screening is not a cost-effective option. As ALT is a widely used measurement in routine health checks in China, clustering of overweight / obesity, pre-hypertension / hypertension and elevated ALT can be served as an indicator for further tests of abnormal glucose metabolism.
The strength of the study includes its large sample size, with anthropometrics and fasting blood profiles measured. The study has several potential limitations. It focused only on those who wanted to apply for university entrance, not those planning to apply to vocational schools (which is approximately half of the population). An oral glucose tolerance test was not performed, which may lead to an underestimation of the burden of Type 2 diabetes. We were not able to distinguish between Type 1 and Type 2 diabetes. We did not have information on lifestyle factors and family history of diabetes.
In conclusion, among high socio-economic status urban high school students in China, overweight / obesity and impaired fasting glucose are common, especially among boys. Different from adults, elevated level of liver function enzyme appears to be the strongest risk factor for diabetes / impaired fasting glucose than other factors, including overweight/obesity, which may merit particular attention in the identification of high-risk population for diabetes / impaired fasting glucose among university applicants.
What’s new?
The study is based on population data from the annual health examination among all students finishing high school who applied for university entrance in Changzhou City in 2012.
Impaired fasting glucose was prevalent among urban high school university applicants, in particular boys and those of high socio-economic status in eastern China. Elevated levels of liver function enzyme appear to be the strongest risk factor for diabetes / impaired fasting glucose.
Acknowledgements
CZ was supported by the Intramural Research Program of the Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health.
Funding sources
None.
Footnotes
Competing interests
None declared.
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