DIABETES/METABOLISM RESEARCH AND REVIEWS RESEARCH ARTICLE

Diabetes Metab Res Rev 2007; 23: 485–489.

Published online 4 April 2007 in Wiley InterScience (www.interscience.wiley.com) DOI: 10.1002/dmrr.741

Progression to impaired glucose regulation,

diabetes and metabolic syndrome in Chinese
women with a past history of gestational diabetes

Wing Hung Tam1 * Abstract

Xi Lin Yang2
Juliana C. N. Chan2 Background To examine the risk of developing impaired glucose regulation
Gary T. C. Ko3 (IGR), diabetes mellitus (DM) and metabolic syndrome (MetS) in Chinese
Peter C. Y. Tong2 women with history of gestational diabetes.
Ronald C. W. Ma2
Methods 203 Chinese women enrolled in a previous study were followed
Clive S. Cockram2
up at a median of 8 (range 7–10) years of whom 136 had normal glucose
Daljit Sahota1 tolerance (NGT) and 68 had gestational diabetes mellitus (GDM) and
Michael S. Rogers1 gestational impaired glucose tolerance (GIGT).
1
Department of Obstetrics and
Results In women with a history of gestational diabetes (n = 4), GIGT
Gynaecology, The Chinese University
of Hong Kong, Hong Kong SAR (n = 63) and NGT (n = 136), 2 (50%), 19 (30.2%) and 21 (15.4%) developed
2
IGR while 2 (50%), 4 (6.3%), 3 (2.2%) developed DM respectively. Most
Department of Medicine and
women developed IGR (86%, n = 36) or DM (78%, n = 7) were undiagnosed.
Therapeutics, The Chinese University
MetS occurred in 16 (7.9%) women with similar rates between those with
of Hong Kong, Hong Kong SAR
3
and those without a history of gestational diabetes (7.5% vs 8.1%; p = 0.85).
Department of Medicine, Alice Ho History of gestational diabetes [OR: 3.8 (95% CI 1.9–7.8)] and body mass
Miu Ling Nethersole Hospital, Hong
index (BMI) ≥23 kg/m2 [OR: 3.4 (95% CI 1.7–6.8)] at first antenatal
Kong SAR
visit were predictors for IGR or DM. Family history of DM [OR: 5.0 (95%
*Correspondence to: CI 1.5–16.4)] and BMI ≥23 kg/m2 [OR: 28.3 (95% CI 3.6–223)] at first
Wing Hung Tam, Department of antenatal visit were predictors for MetS.
Obstetrics and Gynaecology, The
Chinese University of Hong Kong, Conclusions Chinese women with a history of gestational diabetes have a
1st floor, E Block, The Prince of high risk of IGR or DM. Overweight at the first antenatal visit is a common
Wales Hospital, Shatin, New
risk factor for IGR, DM and MetS. A prior history of gestational diabetes was
Territories Hong Kong SAR.
predictive of IGR and DM while a positive family history of DM was predictive
E-mail: [email protected]
of MetS. Copyright  2007 John Wiley & Sons, Ltd.

Keywords gestational diabetes mellitus; impaired glucose regulation; diabetes;

metabolic syndrome; Chinese

Introduction
Type 2 diabetes mellitus (DM) and metabolic syndrome (MetS) are major
public health challenges worldwide. The World Health Organization (WHO)
predicts that globally the number of people with diabetes will increase from
171 million in 2005 to 366 million in 2030, with the majority of new patients
coming from Asia and Africa [1]. Owing to the silent nature of diabetes,
Received: 17 January 2007 diagnosis is often delayed with many patients presenting complications such
Accepted: 5 February 2007 as myocardial infarction [2]. Although screening for DM may allow early
detection and intervention, the cost-effectiveness and psychological impact

Copyright  2007 John Wiley & Sons, Ltd.

486 W. H. Tam et al.

of screening program remain controversial [3]. On the test (non-fasting) at first antenatal clinic visit followed by
basis of modelling, screening of non-Caucasians and a 75 g oral glucose tolerance test (OGTT) administered
young subjects with risk factors is considered cost effective between 24 and 28 weeks of gestation. None of these
due to high detection rates and potentially long disease women had a known history of DM.
duration faced by these subjects [4]. Of these 1032 women, 942 had complete data collection
According to the WHO, gestational diabetes is defined during their index pregnancies and were eligible for
as the joint category of gestational diabetes mellitus reassessment in this study. On the basis of their 75 g
(GDM) [fasting plasma glucose (FPG) ≥7.0 mmol/L OGTT results at the index pregnancy, these women were
and/or 2-h plasma glucose (PG) ≥11.1 mmol/L] and re-classified into normal glucose tolerance (NGT) (i.e. FPG
gestational impaired glucose tolerance (GIGT) (FPG <7.0 mmol/L and 2-h PG <7.8 mmol/L; n = 808), GIGT
<7.0 mmol/L and 2-h PG ≥7.8–11.1 mmol/L) first (i.e. FPG <7.0 mmol/L and 2-h PG ≥7.8–11.1 mmol/L;
detected in pregnancy [5]. In a systematic review of n = 127) and gestational diabetes (i.e. FPG ≥7.0 mmol/L
28 studies, the cumulative incidence of type 2 DM in and/or 2-h PG ≥11.1 mmol/L; n = 7) groups according
women with history of gestational diabetes was 2.6% to the 1999 WHO criteria [5]. All 134 women with
at 6 weeks and 70% at 28 years post-delivery [6]. A gestational diabetes and a random cohort of age-matched
recent meta-analysis of six prospective studies also shows 268 women with NGT selected by a computer program
that gestational diabetes conferred a 6-fold increased risk from the original cohort were invited for follow up study
of DM and that 10–30% of women with diabetes had in 2002.
a previous history of gestational diabetes [7]. On the Contact details including telephone numbers and
other hand, MetS is associated with 2 to 3 fold increased addresses were retrieved from medical records supple-
risk of DM and premature cardiovascular disease [8]. mented by updated information from the outpatient
Despite some overlaps between DM, impaired glucose computer registry. All relevant medical information was
regulation (IGR) and MetS [9], the differential risk obtained by review of case notes. Women, who agreed
associations between gestational diabetes and these high were asked to undergo repeat assessment including a 75 g
risk conditions remain to be clarified. While Lauenborg OGTT after at least 8 h of overnight fast. Body weight,
and colleagues have shown that a history of gestational height, hip and waist circumferences were measured in
diabetes confers a 3-fold increased risk of MetS [10], light clothing. Blood pressure (BP) was measured in the
Albareda and colleagues showed risk association with non-dominant arm with the Dinamap PRO-100 device
only some components of the MetS [11]. (Critikon, Milwaukee, WI) thrice, 1 min apart, and after
In a retrospective analysis, 23% of Chinese women with at least 5 min of rest. The mean BP reading was used for
a history of gestational diabetes had IGT and 13% had analysis. Advanced maternal age was defined as ≥35 years
DM at 6 weeks postpartum [12]. These women also had at delivery of the index pregnancy. Maternal overweight
higher frequencies of other cardiovascular risk factors was defined as BMI ≥23 kg/m2 at booking according to
such as hypertension, obesity and dyslipidemia than the Asian criteria [16]. No information regarding BP, BMI
their age-matched healthy counterparts [12]. In a survey and waist circumference before the index pregnancies was
conducted in mid 1990s, the incidence of gestational available. Family history of DM was defined as having at
diabetes was 14.2% in Hong Kong Chinese women with least one affected first degree relative. The latest Amer-
the majority having GIGT (96.2%) [13]. ican Diabetes Association diagnostic criteria were used
Despite the high prevalence of DM in young Chinese to define glycemic status, i.e. diabetes was defined as a
[14], there is a paucity of prospective data on the risks FPG ≥7.0 mmol/L or a 2-h PG ≥11.1 mmol/L; IGT was
of IGR, DM or MetS in Chinese women with history of defined as a FPG <7.0 mmol/L and a 2-h PG ≥7.8 and
gestational diabetes. In this prospective study, we recalled <11.1 mmol/L; and impaired fasting glycaemia (IFG) as
women previously recruited for a study on gestational a FPG ≥5.6 mmol/L and <7.0 mmol/L [17].
diabetes in the early 1990s for repeat clinical assessments Using the International Diabetes Federation (IDF) def-
after a median follow up period of 8 years [7]. inition [18] modified from the latest American Diabetes
Association criteria for IFG [17] and Asian-specific def-
inition of central obesity, MetS was defined as three or
Materials and methods more of five risk factors: (1) waist circumference ≥80 cm,
(2) FPG ≥5.6 mmol/L, (3) systolic BP ≥130 mmHg or
Research design and methods diastolic BP ≥85 mmHg, (4) fasting plasma triglyceride
≥1.7 mmol/L and (5) high density lipoprotein cholesterol
Subjects were identified from a cohort of 1032 women (HDL-C) <1.3 mmol/L.
recruited consecutively between 1992 and 1994 at the Plasma triglyceride and HDL-C were measured by
Prince of Wales Hospital. This is a regional hospital with enzymatic methods with DP Modular Analytics (Roche
8000 deliveries per annum at that time and the purpose Diagnostics, Indianapolis, IN, USA) while PG was
of the study was to define the optimal screening method measured by the hexokinase method. The study was
and diagnostic criteria for gestational diabetes or GIGT in approved by the Chinese University of Hong Kong Clinical
Chinese [15]. In the original study conducted in 1990s, Research Ethics Committee. Written informed consent
all women underwent a 50-g 1-h oral glucose challenge was obtained from all participants.

Copyright  2007 John Wiley & Sons, Ltd. Diabetes Metab Res Rev 2007; 23: 485–489.
DOI: 10.1002/dmrr
Progression to IGR 487

Statistical methods pregnancies. The mean age, BMI, nulliparity and family
history of DM for non-responders (28.2 ± 4.7 years,
Statistical analysis was performed using the SPSS 13.0 24.5 ± 3.1 kg/m2 , 60.9 and 16.8%) and responders
(SPSS Inc., Chicago, IL) program. All data are expressed (27.8 ± 4.4 years, 24.5 ± 3.1 kg/m2 , 56.2 and 15.3%)
as mean ± SD or percentage (%). Between-group were similar (p-values: all >0.05).
comparisons were made using the Chi-square tests, The median follow up period was 8 years (range:
Fisher’s exact tests or Student’s t-tests as appropriate. 7–10 years) and, of the 203 study participants, 94
Multivariate logistic regression analysis was used to obtain had further pregnancies, following the index pregnancy.
adjusted OR with 95% confidence intervals (CI), with Table 1 shows the baseline and 8-year clinical and
forced entry of age, BMI ≥23 kg/m2 , family history of DM glycemic parameters of these women stratified by their
and gestational diabetes status during index pregnancy glycaemic status in the original study. Both groups of
(GDM and GIGT) as independent variables. Stepwise women had similar age, BMI at first antenatal visit,
algorithm (p = 0.10 for entry and 0.05 for removal) was parity and number of subsequent pregnancies. A total
used to select other variables. Model fit was assessed of 51 (25%) women developed IGR (IGT or IFG) or
using the Hosmer and Lemeshow Goodness-of-Fit test. A DM. In women with NGT during the index pregnancy,
p-value <0.05 for two-tailed statistical tests was used to 21 (15.4%) developed IGR and 3 (2.2%) developed
indicate significance. DM. In the GIGT group, the respective figures were 19
(30.2%) and 4 (6.3%) and in the gestational diabetes
group 2 (50%) and 2 (50%). Women with gestational
diabetes had higher frequencies of IGR (OR: 2.8; 95%
Results CI 1.4–5.7; p = 0.003) and DM (OR: 4.4; 95% CI
1.1–18; p = 0.017) than women with NGT; 86% of
Amongst the 402 women selected from the original women with IGR (n = 36) and 78% of those with
cohort, 203 (50.5%) women could be contacted who also DM (n = 7) were undiagnosed prior to the present
agreed for reassessment. Of these, 136, 63 and 4 women study. Women with history of gestational diabetes had
had NGT, GIGT and GDM respectively during their index higher BP and lower HDL-C than women with NGT

Table 1. Clinical and glycaemic parameters of 203 Chinese women at their first antenatal booking and 8 years later, stratified by
their status of a past history of gestational diabetes (incluing GDM and GIGT)

Total Gestational NGT

Number (n = 203) diabetes (n = 67) (n = 136) a p-values

Index pregnancy
Age at index pregnancy (years) 27.8 ± 4.4 28.6 ± 4.3 27.4 ± 4.3 0.07
Body weight (kg) 54.7 ± 8.8 55.3 ± 8.8 54.4 ± 8.3 0.48
Body mass index (kg/m2 ) 24.5 ± 3.1 24.8 ± 3.6 24.4 ± 2.7 0.20
Family history of diabetes (%) 31 (15.3%) 13 (19.4%) 18 (13.2%) 0.25
50 g GCT, 1 h PG (mmol/L) 7.0 ± 1.7 7.9 ± 1.8 6.5 ± 1.5 <0.001
75 g OGTT, fasting PG (mmol/L) 4.2 ± 0.6 4.5 ± 0.6 4.0 ± 0.6 <0.001
75 g OGTT, 2 h PG (mmol/L) 6.8 ± 1.8 8.8 ± 1.3 5.8 ± 1.0 <0.001
Mean PG profile (mmol/L) 5.2 ± 0.8 5.67 ± 1.1 4.96 ± 0.5 <0.001
Nulliparity during index pregnancy 115 (56.2%) 40 (59.7%) 74 (54.4%) 0.39
Neonatal birth weight (g) 3259 ± 447 3230 ± 485 3272 ± 429 0.26
Gestational week at delivery 39.4 ± 1.8 39.3 ± 2.1 39.5 ± 1.6 0.54
Lifebirth with 5 min Apgar score <7 1 (0.5%) 1 (1.5%) 0 0.32†
Stillbirth 1 (0.5%) 1 (1.5%) 0 0.32†
At 8-year follow up – – – –
Age 36.5 ± 4.6 36.9 ± 4.4 36.3 ± 4.7 0.40
Subsequent pregnancies: 1 82 (40.2%) 26 (38.2%) 59 (50.0%) 0.32
≥2 12 (5.9%) 2 (2.9%) 10 (41.9%) 0.15
Subsequent pregnancies with GDM/GIGT 8 (3.9%) 5 (7.4%) 3 (2.2%) 0.074†
Family history of diabetes (%) 63 (30.9%) 28 (41.2%) 35 (25.7%) 0.04
Body mass index (kg/m2 ) 23.9 ± 3.9 24.4 ± 4.6 23.7 ± 3.5 0.24
Glycemic status:
IGR (IFG and/or IGT) 42 (20.7%) 21 (31.3%) 21 (15.4%) 0.003
DM 9 (4.4%) 6 (9.0%) 3 (2.2%) 0.017†
Triglyceride ≥1.7 mmol/L 18 (8.9%) 8 (11.9%) 10 (7.4%) 0.28
HDL-C <1.3 mmol/L 42 (20.7%) 21 (31.3%) 21 (15.4%) 0.009
Systolic BP ≥130 mmHg 26 (12.8%) 15 (22.4%) 11 (8.1%) 0.004
Diastolic BP ≥85 mmHg 22 (10.8%) 12 (17.9%) 10 (7.4%) 0.023
Waist circumference ≥80 cm (%) 46 (22.7%) 14 (20.9%) 32 (23.5%) 0.64
Metabolic syndrome (IDF criterion) (%) 16 (7.9%) 5 (7.5%) 11 (8.1%) 0.85

a p-values comparing those with NGT or GDM/GIGT using the Student’s t-test, Chi-square or
† Fisher exact test where appropriate.
DM, diabetes mellitus; IGR, impaired glucose regulation, IGT, impaired glucose tolerance; IFG, impaired fasting glycaemia; GDM, gestational DM;
GIGT, gestational IGT; NGT, normal glucose tolerance; GCT, glucose challenge test; PG, plasma glucose; OGTT, oral glucose tolerance test.

Copyright  2007 John Wiley & Sons, Ltd. Diabetes Metab Res Rev 2007; 23: 485–489.
DOI: 10.1002/dmrr
488 W. H. Tam et al.

Table 2. Pregnancy-related variables in women who developed impaired glucose regulation (IGR) or diabetes and metabolic syndrome
(MetS) at 8 years follow up

Glycaemic status Metabolic Syndrome Status

Variables Adjusted Non-MetS Adjusted

of index pregnancy NGT (n = 152) IGR/DM (n = 51) OR (n = 187) MetS (n = 16) OR

Gestational diabetes 40 (26.3%) 27 (52.9%) 3.8 (1.9–7.8) 62 (33.5%) 5 (31.3%) 0.9 (0.3–2.7)
Advanced maternal age 8 (5.3%) 8 (15.7%) 2.9 (1.0–8.7) 13 (7.1%) 3 (18.8%) 3.0 (0.7–12.0)
Family history of DM 21 (13.9%) 10 (19.6%) 1.5 (0.7–3.5) 24 (13.0%) 7 (43.8%) 5.0 (1.5–16.4)
BMI at booking ≥23 kg/m2 49 (33.1%) 30 (58.8%) 3.4 (1.7–6.8) 62 (34.3%) 15 (93.8%) 28.3 (3.6–223)

but the rates of MetS were similar between the 2 developed IGR/DM reported a higher frequency at 8 years
groups. later.
In the multivariate model, gestational diabetes and Despite some overlap between IGR and MetS, we found
BMI ≥23 kg/m2 at booking increased the odds of later different risk factors for these conditions in our Chinese
developing IGR by 3.8 (95% CI 1.9–7.8) and DM by 3.4 women. In agreement with other workers [11], a history
(95% CI 1.7–6.8) respectively. Family history of DM and of gestational diabetes was associated with increased
BMI ≥23 kg/m2 at booking were significant predictors of risk of some components of MetS, namely hypertension
MetS with ORs of 5.0 (95% CI 1.5–16.4) and 28.3 (95% and low HDL-C, but was not predictive of an increased
CI 3.6–223) respectively (Table 2). frequency of MetS. On the other hand, being overweight
at booking and family history of DM were predictors
of MetS in our cohort. These findings may be either
Discussion due to chance or inadequate sample size. Given the
heterogeneity of IFG, IGT, DM and MetS, more studies
are required to clarify their natural history, phenotypes
In this first prospective study to examine the effects
and aetiologies. From a preventive perspective, given
of gestational diabetes in Chinese women, we have
the high risk nature of these conditions for premature
demonstrated high rates and increased risk of DM, IGR
cardiovascular diseases [8] and that randomized clinical
and MetS in subjects with a family history of DM,
studies have confirmed that lifestyle modification and
overweight at booking and history of gestational diabetes
drug treatment with metformin, acarbose, PPARγ agonist
as main risk factors. Despite only a 50% recall rate,
and orlistat can prevent progression to DM in 30–60%
our findings are in agreement with data from Caucasians
of subjects with IGT or gestational diabetes [32–34], our
[6,7]. There were no major differences in the demographic
findings can be used to develop a strategy to select high
data between responders and non-responders, making
risk women for surveillance and possible intervention.
major selection bias unlikely.
In conclusion, in this 8-year prospective study, we
In unselected population-based cohort and subjects
observed high rates of IGR, DM and MetS in relatively
with known risk factors, Chinese women with IGT or IFG
young Chinese women, most of whom would have
have annual conversion rates to DM of 4–10%, with waist-
remained undiagnosed if they had not participated in
hip ratio and 2-h post OGTT PG as the main predictors
the study. In addition to having family history of DM
[19–26]. Although we encourage women with history of
and being overweight at their first antenatal visit, history
gestational diabetes to visit their family doctors for repeat
of gestational diabetes increases the odds of IGR/DM by
OGTT 6 weeks after delivery, we do not have a system to
four-fold.
ensure compliance with this recommendation. Majority
of women with DM or IGR were undiagnosed at the time
of the present study. Given their young age and long
disease duration if affected, missed diagnosis of diabetes
Acknowledgements
can have major consequences [27]. Thus, our prospective We thank our research nurses, Delanda Wong, Yee-Mui
data further emphasize the need to target these high risk Lee, Cherry Chiu and Cecilia Fung for their dedication and
women for regular screening and surveillance. professionalism in conducting this survey. We thank all mothers
In agreement with most findings [5,28–30], a history and children for participating in this study. This study was
of gestational diabetes and overweight at booking were supported by the CUHK Direct Research Grant.
predictors for IGR or DM in these women. However,
contrary to other findings [29,31], advanced maternal age
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Copyright  2007 John Wiley & Sons, Ltd. Diabetes Metab Res Rev 2007; 23: 485–489.
DOI: 10.1002/dmrr