Epidemiology/Health Services/Psychosocial Research ORIGINAL ARTICLE

Impaired Fasting and Impaired Glucose Tolerance in Women With Prior Gestational Are Associated With a Different Cardiovascular Profile

1 1 LUIS FELIPE PALLARDO, MD TERESA GARCIA-INGELMO, MD of abnormalities is associated with 1 2 LUCRECIA HERRANZ, MD CRISTINA GRANDE, SCD resistance even in situations of normal 1 3 PILAR MARTIN-VAQUERO, BM MERCEDES JANEZ˜ , BM glucose tolerance (8,9). On the other hand, the establishment of two intermediate categories between normal glucose homeostasis and diabetes (impaired glucose tolerance [IGT] and OBJECTIVE — The purpose of this study was to investigate the association of cardiovascular impaired fasting glucose [IFG]) (10) has risk factors to impaired glucose tolerance (IGT) and to impaired fasting glucose (IFG) in women raised concern in which of these distur- with prior mellitus (GDM). bances has a major role in predicting the RESEARCH DESIGN AND METHODS — We studied 838 women with prior GDM. development of or cardio- Postpartum glucose tolerance status was classified as normal, IFG, IGT, IFG plus IGT, and vascular disease. diabetes according to the World Health Organization criteria. Postpartum BMI, waist circum- The aim of this study was to investi- ference, blood pressure, triglyceride, cholesterol, and HDL cholesterol were assessed. gate the association of cardiovascular risk factors to IGT and IFG in the postpartum RESULTS — BMI and blood pressure were significantly higher in women with IFG than in evaluation of women with GDM. women with normal glucose status. BMI and waist circumference were significantly higher in women with IFG plus IGT than in women with normal glucose status. No differences were observed between women with IGT and normal glucose status. The prevalence of hypertension RESEARCH DESIGN AND and obesity was significantly increased in IFG compared with normal glucose status. The prev- METHODS — This research was con- alence of obesity and abnormal lipids was significantly increased in IFG plus IGT compared with ducted in the normal glucose status. IGT showed no increased prevalence of cardiovascular risk factors. Unit at the University Hospital La Paz in Madrid between 1992 and 2000. We CONCLUSIONS — Traditional cardiovascular risk factors have a stronger association with isolated IFG than with isolated IGT in women with prior GDM. studied 838 Caucasian women (mean age 32.4 Ϯ 4.6 years; mean parity 1.8 Ϯ 0.9) Diabetes Care 26:2318–2322, 2003 with singleton gestations complicated by GDM and who attended the initial post- partum assessment (3–6 months after de- livery) when lactation was concluded. omen with gestational diabetes creased LDL cholesterol and triglyceride The total number of women with single- mellitus (GDM) are at an in- levels and decreased HDL cholesterol lev- ton gestations who had a diagnosis of creased risk for the development els (2–4). Furthermore, changes in endo- W GDM during this period was 1,350. of diabetes (usually type 2) after preg- thelial function (5) and increased levels of Women who did not participate in the nancy (1). Likewise, women with prior adhesion molecules (6), together with a postpartum examination (37.9%) were GDM, when compared with women with higher prevalence of microalbuminuria similar to those who attended with regard no history of GDM, are found to have (7), abnormal electrocardiograms, and to age, parity, prepregnancy BMI, and de- higher BMI (2), higher blood pressure cardiovascular events (3) are observed in gree of glucose intolerance during preg- (3,4), and an altered lipid profile with in- women with prior GDM. This spectrum nancy. Ethical permission for the study ●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●● was received from the hospital ethical From the 1Department of Endocrinology, Division of Diabetes, Hospital Universitario La Paz, Madrid, Spain; committee, and informed consent was 2the Department of Biochemistry, Hospital Universitario La Paz, Madrid, Spain; and 3the Department of obtained from all subjects. Obstetrics and Gynecology, Hospital Universitario La Paz, Madrid, Spain. The diagnosis of GDM was made us- Address correspondence and reprint requests to Dr. L.F. Pallardo, Jefe de Servicio de Endocrinologı´a y ing the criteria of the National Diabetes Nutricio´n, Unidad de Diabetes, Hospital Universitario La Paz, Paseo de la Castellana 261, 28046 Madrid, Spain. E-mail: [email protected]. Data Group (11) after performing a fast- Received for publication 29 October 2002 and accepted in revised form 16 April 2003. ing 3-h, 100-g oral Abbreviations: dBP, diastolic blood pressure; GDM, gestational diabetes mellitus; IFG, impaired fasting (OGTT) in all pregnant women with a glucose; IGT, impaired glucose tolerance; OGTT, oral glucose tolerance test; sBP, systolic blood pressure; screening test (50-g oral glucose chal- WHR, waist-to-hip ratio. Ն A table elsewhere in this issue shows conventional and Syste`me International (SI) units and conversion lenge) showing a 1-h glucose value 140 factors for many substances. mg/dl (7.8 mmol/l). The screening test © 2003 by the American Diabetes Association. was performed at the first prenatal visit if

2318 DIABETES CARE, VOLUME 26, NUMBER 8, AUGUST 2003 Pallardo and Associates

Table 1—Potential cardiovascular risk factors by postpartum glucose tolerance status

Parameter Normal IFG IGT IFG plus IGT Diabetes P n 681 40 62 25 30 BMI (kg/m2) 25.3 Ϯ 4.1*†‡ 27.9 Ϯ 6.0* 25.4 Ϯ 4.5§ 29.0 Ϯ 5.4†§ 29.3 Ϯ 7.5‡ Ͻ0.001 Waist circumference (cm) 79.7 Ϯ 9.5†‡ 83.8 Ϯ 12.9 79.9 Ϯ 9.5§ 88.8 Ϯ 12.1†§ 88.8 Ϯ 16.1‡ Ͻ0.001 Triglyceride (mmol/l) 1.00 Ϯ 0.57‡ 1.08 Ϯ 0.62 1.20 Ϯ 0.69 1.37 Ϯ 0.86 1.39 Ϯ 1.15‡ Ͻ0.001 Cholesterol (mmol/l) 4.96 Ϯ 1.00 4.93 Ϯ 0.98 5.06 Ϯ 0.99 5.04 Ϯ 0.65 4.68 Ϯ 1.13 0.560 HDL cholesterol (mmol/l) 1.44 Ϯ 0.32 1.39 Ϯ 0.32 1.42 Ϯ 0.31 1.21 Ϯ 0.25 1.35 Ϯ 0.39 0.064 sBP (mmHg) 112.0 Ϯ 14.7* 118.4 Ϯ 16.8* 113.9 Ϯ 14.7 112.9 Ϯ 16.9 118.7 Ϯ 15.5 0.017 dBP (mmHg) 69.5 Ϯ 10.5*‡ 74.3 Ϯ 11.1* 71.3 Ϯ 11.2 68.9 Ϯ 12.5 75.5 Ϯ 11.0‡ 0.002 Data are means Ϯ SD. Significance of differences among pairs of group means (P Ͻ 0.05): *Normal versus IFG; †normal versus IFG plus IGT; ‡normal versus diabetes; §IGT versus IFG plus IGT; IGT versus diabetes. clinical characteristics were consistent els. Systolic (sBP) and diastolic (dBP) one-way ANOVA was used (F test) and with a high risk of GDM (obesity, family blood pressures were recorded with the post hoc tests were performed using the , personal history of patient in a sitting position after at least 5 Bonferroni method. Categorical variables GDM, or poor obstetric outcome) or at min of rest, using a sphyngomanometer. were compared using ␹2 and Fisher’s ex- 24–28 weeks of gestation when these The average of two blood pressure mea- act tests of significance. Multiple-variable characteristics were not present. surements was used for the analysis. An- logistic regression models were used to All women with a diagnosis of GDM thropometric measurements included estimate adjusted ORs. Association be- received nutrition counseling with indi- weight, height, and waist and hip circum- tween variables was evaluated using lin- vidualized caloric intake and providing ferences (13). BMI (kg/m2) was computed ear correlation coefficients and stepwise 50% of calories from carbohydrates, 30% from current weight and height, and multiple linear regression analysis. A P from fat, and 20% from protein. Self- waist-to-hip ratio (WHR) was computed value Ͻ0.05 was considered significant. glucose monitoring was performed by the from waist and hip circumferences. patients on alternate days. Insulin ther- Postpartum area under the glucose apy, given on the basis of a fasting blood curve was calculated by the trapezoidal RESULTS — At postpartum assess- glucose Ն105 mg/dl (5.8 mmol/l) or a 2-h method. A woman was classified as hav- ment of the 838 women with GDM, 681 postprandial blood glucose Ն120 mg/dl ing abnormal lipids if she had any of the women (81.3%) had a normal glycemic (6.7 mmol/l) on two or more occasions, following characteristics: triglyceride lev- status, 30 (3.5%) had diabetes, 40 (4.8%) was needed in 386 women (46.1%). els Ն150 mg/dl (1.69 mmol/l), HDL cho- had IFG, 62 (7.4%) had IGT, and 25 (3%) At postpartum assessment, a standard lesterol levels Յ39 mg/dl (1.01 mmol/l), had IFG plus IGT. Mean age was 32.5 Ϯ 75-g OGTT was given to 834 women (4 or total cholesterol levels Ն200 mg/dl 4.2 years for women with normal glyce- women had fasting glucose values that (5.17 mmol/l). Obesity was defined as the mic status, 32.6 Ϯ 4.8 years for women were diagnostic of diabetes). Reclassifica- presence of BMI Ն30 kg/m2 and/or WHR with diabetes, 32.8 Ϯ 5.1 years for tion of glycemic status was done accord- Ն0.85. Hypertension was defined as the women with IFG, 32.7 Ϯ 4.7 years for ing to the criteria of the World Health presence of sBP Ն140 mmHg and/or dBP women with IGT, and 32.8 Ϯ 4.8 years Organization (12) with the following Ն90 mmHg. for women with IFG plus IGT. modification: diabetes, fasting glucose Plasma glucose was enzymatically Potential cardiovascular risk factors Ն126 mg/dl (7.0 mmol/l) or 2-h glucose measured on an automated analyzer by postpartum categories of glucose tol- Ն200 mg/dl (11.1 mmol/l); IFG (isolated (Hitachi 704; Boehringer-Mannheim, In- erance are presented in Table 1. Mean IFG), fasting glucose Ն110 mg/dl (6.1 dianapolis, IN). Cholesterol and triglycer- BMI, sBP, and dBP were significantly mmol/l) and Ͻ126 mg/dl (7.0 mmol/l) ide levels were determined using higher in women with IFG than in women and 2-h glucose Ͻ140 mg/dl (7.8 mmol/ enzymatic assays (Kit CHOL-PAP and Kit with normal glucose status; these differ- l); IGT (isolated IGT), fasting glucose GPO-PAP; Boehringer-Mannheim, India- ences were not observed for women with Ͻ110 mg/dl (6.1 mmol/l) and 2-h glu- napolis, IN). HDL cholesterol levels were IGT. Women with IFG plus IGT had sig- cose Ն140 mg/dl (7.8 mmol/l) and Ͻ200 measured using an enzymatic assay after nificantly higher mean BMI and waist cir- mg/dl (11.1 mmol/l); IFG plus IGT, fast- precipitation of LDLs and VLDLs with cumference than women with normal ing glucose Ն110 mg/dl (6.1 mmol/l) and dextran sulfate (Kit CHOL-HDL; Sclavo glucose status or with IGT. Mean sBP and Ͻ126 mg/dl (7.0 mmol/l) and 2-h glu- Diagnostici, Sienna, Italy). dBP in women with IFG plus IGT were cose Ն140 mg/dl (7.8 mmol/l) and Ͻ200 Statistical analyses were conducted not significantly different from women mg/dl (11.1 mmol/l); and normal, fasting using SPSS version 8.0 statistical software with normal glucose status, women with glucose Ͻ110 mg/dl (6.1 mmol/l) and (SPSS, Chicago, IL). Values are reported IFG, or women with IGT. Mean BMI, 2-h glucose Ͻ140 mg/dl (7.8 mmol/l). At as means Ϯ SD or as percentages. Data waist circumference, dBP, and triglycer- the same time, a fasting blood sample was were tested for normal distribution using ide were significantly higher in women drawn for the measurement of triglycer- the Kolmogorov-Smirnov test. To com- with diabetes than in women with normal ide, cholesterol, and HDL cholesterol lev- pare continuous variables among groups, glucose status. Mean cholesterol and HDL

DIABETES CARE, VOLUME 26, NUMBER 8, AUGUST 2003 2319 Cardiovascular profile after GDM

Table 2—Linear correlation coefficients be- Table 3—OR and 95% CI for hypertension, obesity, and abnormal lipids by postpartum tween potential cardiovascular risk factors glucose tolerance categories, adjusted for age, parity, and family history of diabetes and postpartum fasting glucose and area un- der the glucose curve Adjusted OR Risk factors n % (95% CI) P Fasting Hypertension glucose AUC Normal 56 8.2 (n ϭ 838) (n ϭ 834) IFG 10 25.0 3.4 (1.6–7.4) 0.002 BMI 0.232* 0.236* IGT 8 12.9 1.7 (0.7–4.0) 0.233 Waist circumference 0.236* 0.255* IFG plus IGT 3 12.0 1.3 (0.3–5.7) 0.768 Trygliceride 0.140* 0.276* Diabetes 5 16.7 2.3 (0.8–6.4) 0.102 Cholesterol Ϫ0.030 0.032 Obesity HDL cholesterol Ϫ0.129* Ϫ0.146* Normal 121 17.8 sBP 0.155* 0.135* IFG 14 35.0 2.4 (1.2–4.9) 0.016 dBP 0.167* 0.155* IGT 11 17.7 1.0 (0.5–2.1) 0.942 *P Ͻ 0.0001. AUC, area under the glucose curve. IFG plus IGT 10 40.0 2.9 (1.2–7.0) 0.015 Diabetes 12 40.0 3.2 (1.4–7.1) 0.004 Abnormal lipids cholesterol did not differ by postpartum Normal 89 13.1 glucose tolerance categories. IFG 8 20.0 1.6 (0.7–3.8) 0.273 Table 2 shows linear correlation coef- IGT 13 21.0 1.7 (0.8–3.4) 0.147 ficients between potential cardiovascular IFG plus IGT 8 32.0 3.2 (1.1–9.6) 0.036 risk factors and postpartum fasting glu- Diabetes 10 33.3 3.5 (1.6–7.8) 0.002 cose and area under the glucose curve. BMI, waist circumference, trygliceride, HDL cholesterol, and sBP and dBP were among the different postpartum catego- CONCLUSIONS — At postpartum significantly related to both fasting glu- ries of glucose tolerance (Fig. 1). Only the glycemic assessment using an OGTT, cose and area under the glucose curve. To IFG and diabetes categories showed a sig- ϳ20% of the women with prior GDM had test the independent associations, multi- nificantly increased prevalence; women impaired glucose metabolism, and ϳ4% ple linear regression analysis was used. with IFG had an OR of 3.7 (95% CI 1.6– had diabetes, in agreement with previous Variables independently associated with 8.9) and women with diabetes had an OR data (14). the area under the glucose curve were of 5.7 (95% CI 2.3–14) for two or more According to the 1997 American Di- ␤ϭ ϭ waist circumference ( 0.236; P cardiovascular risk factors. abetes Association criteria (10), impaired 0.0001) and triglycerides (␤ϭ0.172; P ϭ 0.0001). Variables independently as- sociated with fasting glucose were BMI (␤ϭ0.227; P ϭ 0.0001), dBP (␤ϭ 0.121; P ϭ 0.007), and HDL cholesterol (␤ϭϪ0.084; P ϭ 0.049). The prevalence of cardiovascular risk factors among the different postpartum categories of glucose tolerance is pro- vided in Table 3. The odds ratio for hy- pertension (3.7; P Ͻ 0.0001) and obesity (2.4; P ϭ 0.009) was significantly in- creased in IFG compared with normal glucose status, whereas IGT showed no increased prevalence of cardiovascular risk factors. The IFG plus IGT category showed a significantly higher odds ratio for abnormal lipids (3; P ϭ 0.036) and obesity (2.9; P ϭ 0.024) compared with normal glucose status. The prevalence of obesity (OR 3.1; P ϭ 0.003) and abnor- mal lipids (OR 3.3; P ϭ 0.002) was sig- nificantly increased in diabetes compared with normal glucose status. Finally, we estimated the prevalence of two or more Figure 1—Prevalence of two or more of the cardiovascular risk factors assessed (obesity, hyper- of the cardiovascular risk factors assessed tension, abnormal lipids) by postpartum categories of glucose tolerance. *P ϭ 0.005; †P ϭ 0.001.

2320 DIABETES CARE, VOLUME 26, NUMBER 8, AUGUST 2003 Pallardo and Associates glucose metabolism comprises two cate- When cardiovascular risk factors 3. Meyer-Seifer CH, Vohr BR: Lipid levels in gories: IFG and IGT. Since the establish- have been analyzed across the categories former gestational diabetic mothers. Dia- ment of these two intermediate metabolic of impaired glucose metabolism, the re- betes Care 19:1351–1356, 1996 stages, their identity with future diabetes sults have not been so conclusive. De Pab- 4. O’Sullivan JB: Subsequent morbidity los-Velasco et al. (19) showed that in a among gestational diabetic women. In and with cardiovascular risk has been put Carbohydrate Metabolism in Pregnancy and forward. A modification in the criteria Caucasian population, both IFG and IGT the Newborn. Sutherland HW, Stowers JM, used to ascertain these two intermediate had higher prevalence of certain cardio- Eds. Edinburgh, Churchill Livingstone, categories is required for an accurate eval- vascular risk factors compared with nor- 1984, p. 174–180 uation of the consequences of fasting mal glucose tolerance; and at the same 5. Anastasiou E, Lekakis J, Alevizaki M, Pa- and postprandial hyper- time, IFG was associated with higher pamichael CM, Megas J, Souvatzoglou A, glycemia. Hence, it is necessary to take total-to-HDL cholesterol ratio than IGT. Stamatelopoulos SF: Impaired endotheli- Among a Swedish population, Larsson et um-dependent vasodilatation in women into account isolated IFG with normal with previous gestational diabetes. Diabe- glucose tolerance, isolated IGT with nor- al. (20) did not find differences between IFG and IGT, whereas IFG plus IGT tes Care 21:2111–2115, 1998 mal fasting glucose, and the occurrence of showed higher BMI, cholesterol, and tri- 6. Wagner OF, Jilma B: Putative role of ad- both IFG and IGT (IFG plus IGT). Finally, hesion molecules in metabolic disorders. glyceride values than IGT and higher tri- it must be remembered that the limited Horm Metab Res 29:627–630, 1997 glyceride values than IFG. To date, 7. Friedman S, Rabinerson D, Bar J, Erman repeat test reproducibility of fasting and combined IFG plus IGT seems to be asso- 2-h glucose levels can lead to different A, Kaplan B, Boner G, Ovadia J: Mi- ciated with the highest cardiovascular risk croalbuminuira following gestational dia- classifications of an individual when (21). Our data showed that BMI and waist betes. Acta Obstet Gynecol Scand 74:356– tested more than once (15). circumference in the IFG plus IGT cate- 360, 1995 With the scheme proposed, women gory were higher than in the normal glu- 8. Ward K, Johnston CLW, Beard JC, with IFG and IGT at the postpartum eval- cose tolerance and in the IGT categories. Benedetti TS, Halter JS, Porte Jr D: Insulin uation showed similar lipid levels, blood Given the small number of women (n ϭ resistance and impaired insulin secretion pressure values, BMI, and waist circum- 25) in the IFG plus IGT group in our in subjects with histories of gestational ference, whereas women with IFG plus diabetes mellitus. Diabetes 34:861–869, study, it is possible that differences in the 1995 IGT had higher mean BMI and waist cir- prevalence of two or more cardiovascular 9. Osei K, Gaillard TR, Schuster DP: History cumference than women with IGT. Com- factors compared with the normal toler- of gestational diabetes leads to distinct parison of women with impaired glucose ance group were not detected. metabolic alterations in nondiabetic Afri- metabolism with women with normal gly- Apart from the above discussion on can-American women with a parental his- cemic status disclosed that only women the cardiovascular consequences of fast- tory of type 2 diabetes. Diabetes Care 21: with IFG and women with IFG plus IGT ing or postprandial hyperglycemia, the 1250–1256, 1998 were different in relation to potential car- overall degree of impaired glucose metab- 10. Expert Committee on the Diagnosis and Classification of Diabetes Mellitus: Report diovascular risk factors. Regarding the olism (assessed as the area under the glu- cose curve) was significantly associated of the expert committee on the diagnosis prevalence of each cardiovascular risk and classification of diabetes mellitus. Di- factor, obesity and abnormal lipids were with all the cardiovascular risk factors an- abetes Care 20:1183–1197, 1997 more common in women with diabetes alyzed in this study (BMI, waist circum- 11. National Diabetes Data Group: Classifica- than in women with normal glucose sta- ference, triglyceride, HDL-cholesterol, tion and diagnosis of diabetes mellitus tus. As for the intermediate metabolic sBP, and dBP), except cholesterol. and other categories of glucose intoler- stages, IGT showed no increased preva- In conclusion, our data indicate that ance. Diabetes 28:1039–1057, 1979 lence of cardiovascular risk factors, IFG has a stronger association than IGT 12. World Health Organization: Definition, with traditional cardiovascular risk fac- Diagnosis and Classification of Diabetes whereas obesity and hypertension were Mellitus and Its Complications: Report of more frequent in IFG, and obesity and tors in women with prior GDM, although the underlying determinant of the rela- a WHO Consultation: Part I. Diagnosis abnormal lipids occurred more often in tion may well be the overall degree of im- and Classification of Diabetes Mellitus. IFG plus IGT. In a similar way, IFG but World Health Organization, Geneve, 1999 paired glucose metabolism. Further data not IGT had a higher prevalence of two or 13. 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