Use of Glycated Hemoglobin and Waist Circumference for Diabetic Screening in Women With a History of Gestational Diabetes

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1 WOMEN S HEALTH Use of Glycated Hemoglobin and Waist Circumference for Diabetic Screening in Women With a History of Gestational Diabetes Véronique Gingras, RD, 1,2 André Tchernof, PhD, 1,2,3 S. John Weisnagel, MD, 1,2,3 Julie Robitaille, RD, PhD 1,2 1 Department of Food Science and Nutrition, Laval University, Quebec City QC 2 Institute of Nutrition and Functional Foods, Laval University, Quebec City QC 3 Endocrinology and Nephrology, Laval University Medical Research Centre, Quebec City QC Abstract Objective: Although their risk of type 2 diabetes is markedly increased, women with prior gestational diabetes mellitus (GDM) do not receive appropriate testing following their pregnancy. Identifying a less burdensome testing method might increase postpartum testing rates. Our objective was to examine the adequacy of glycated hemoglobin (A1C) and waist circumference (WC) measurements to detect impaired glucose metabolism among women with prior GDM. Methods: The analysis included 178 women who had GDM between 2003 and WC and A1C were measured, and a 75g 2h-OGTT was performed. Pre-diabetes was defined as a fasting plasma glucose (FPG) 5.6 and < 7.0 mmol/l or a 2-hour plasma glucose (2h-PG) 7.8 and < 11.0 mmol/l, and type 2 diabetes was defined as a FPG 7.0 mmol/l and/or a 2h-PG 11.1 mmol/l. Sensitivity and specificity analyses were performed. Results: The mean age of subjects was 36.4 ± 4.8 years, and testing occurred at a mean 3.5 ± 1.9 years following delivery. Combining A1C 5.7 and WC 88 cm to detect pre-diabetes had a sensitivity of 76 and specificity of 62, and to detect type 2 diabetes it had a sensitivity of 91 and specificity of 34. Compared with women who had A1C and WC within the normal range, women with A1C 5.7 and WC 88 cm were more likely to have type 2 diabetes (OR 4.4; 95 CI 2.0 to 9.9). Conclusion: These analyses suggest that the combination of A1C and WC could represent a sensitive test for pre-diabetes and type 2 diabetes in the years following a pregnancy complicated by GDM. Further validation of this testing method is required. Key Words: A1C, waist circumference, gestational diabetes, testing Competing Interests: None declared. Received on March 13, 2013 Accepted on June 20, 2013 Résumé Objectif : Bien que leur risque de présenter un diabète de type 2 connaisse une hausse considérable, les femmes ayant déjà connu un diabète sucré gestationnel (DSG) ne bénéficient pas de services de dépistage adéquats à la suite de leur grossesse. L identification d une méthode de dépistage moins lourde pourrait accroître les taux de dépistage postpartum. Nous avions pour objectif d examiner le caractère adéquat des mesures du taux d hémoglobine glyquée (A1C) et du tour de taille (TT) pour ce qui est de la détection de l altération du métabolisme du glucose chez les femmes ayant déjà connu un DSG. Méthodes : L analyse portait sur 178 femmes ayant connu un DSG entre 2003 et Le TT et le taux d A1C ont été mesurés, et une épreuve d hyperglycémie provoquée par voie orale (75 g, 2 h) a été menée. Le prédiabète a été défini comme étant une glycémie à jeun (GJ) 5,6 et < 7,0 mmol/l ou une glycémie à 2 heures (G-2 h) 7,8 et < 11,0 mmol/l, tandis que le diabète de type 2 a été défini comme étant une GJ 7,0 mmol/l et/ou une G-2 h 11,1 mmol/l. Des analyses de sensibilité et de spécificité ont été menées. Résultats : L âge moyen des sujets était de 36,4 ± 4,8 ans et le dépistage s est déroulé, en moyenne, 3,5 ± 1,9 ans à la suite de l accouchement. La combinaison d un taux de A1C 5,7 et d un TT 88 cm pour détecter le prédiabète comptait une sensibilité de 76 et une spécificité de 62 ; pour ce qui est de la détection du diabète de type 2, cette combinaison comptait une sensibilité de 91 et une spécificité de 34. Par comparaison avec les femmes qui présentaient un taux d A1C et un TT se situant dans la plage normale, les femmes qui présentaient un taux d A1C 5,7 et un TT 88 cm étaient plus susceptibles de connaître un diabète de type 2 (RC, 4,4; IC à 95, 2,0-9,9). Conclusion : Ces analyses semblent indiquer que la combinaison du taux d A1C et de la mesure du TT pourrait constituer un test sensible pour le dépistage du prédiabète et du diabète de type 2 au cours des années qui suivent une grossesse ayant été compliquée par la présence d un DSG. La tenue d autres études permettant de valider cette méthode de dépistage s avère requise. J Obstet Gynaecol Can 2013;35(9): SEPTEMBER JOGC SEPTEMBRE 2013

2 Use of Glycated Hemoglobin and Waist Circumference for Diabetic Screening in Women With a History of Gestational Diabetes INTRODUCTION Gestational diabetes mellitus, defined as glucose intolerance with first onset or recognition during pregnancy, 1 is associated with adverse metabolic outcomes in the years following delivery. 2 5 Women with prior GDM are at greater risk to develop type 2 diabetes than women with a normoglycemic pregnancy. 2,3 Therefore, it is recommended that women with a history of GDM undergo a 2-hour oral glucose tolerance test within six months following pregnancy, and, if this is normal, assay of fasting plasma glucose or OGTT should be performed every three years. 1,6 However, few women with GDM appear to receive adequate follow-up and testing after pregnancy. 7 9 OGTTs are time consuming and expensive, and the identification of simpler and equally effective postpartum testing methods may facilitate and increase life-long testing among this population. FPG alone is not a consistently sensitive test for type 2 diabetes in women with prior GDM. 10,11 Only a few studies have examined use of A1C as a marker for metabolic risk among women with prior GDM, and these studies report only moderate or fair agreement of A1C with plasma glucose. 12 The current cut-off for A1C (5.7 to 6.4 for pre-diabetes and 6.5 for type 2 diabetes) appears to be inappropriate for postpartum glucose tolerance evaluation in women with prior GDM. 13,14 Women with prior GDM have also been reported to have a larger waist circumference than women with a past normoglycemic pregnancy. 15,16 Increasing waist circumference has been associated with insulin resistance in women, 17,18 and waist circumference is a standardized and undemanding measure. 19 Our objective was to examine the adequacy of two simple and inexpensive measurements, A1C and waist circumference, to identify and predict abnormal glucose metabolism in women with prior GDM in long-term follow-up. We hypothesized that the combined use of these two measures adequately identifies women with prior GDM who have abnormal glucose metabolism. METHODS We recruited women for this study using databanks from the Régie de l assurance maladie du Québec, the provincial health plan registry. Women aged 18 years from the greater ABBREVIATIONS A1C FPG GDM OGTT PG glycated hemoglobin fasting plasma glucose gestational diabetes mellitus oral glucose tolerance test plasma glucose Quebec City area, with a diagnosis of GDM made between April 2003 and June 2010, who were not pregnant at the time of the study, and who did not have type 1 diabetes, were invited to participate. 20 The study sample consisted of 215 women recruited between October 2009 and August 2011 who were tested at the clinical investigation unit of the Institute of Nutrition and Functional Foods. Women were tested at a mean 3.5 ± 1.9 years after their most recent pregnancy. In 5 of the women, the most recent pregnancy had not been complicated by GDM. There was no significant difference in age, BMI, or insulin sensitivity between these women and women who did have GDM in their most recent pregnancy (P > 0.05). Participants on medication for type 2 diabetes or dyslipidemia (n = 8), with previous bariatric surgery (n = 1), or with missing laboratory measurements from the OGTT (n = 21) were excluded from analyses. Women who were tested less than six months after their most recent pregnancy (n = 7) were excluded to avoid any bias due to glycemic control during pregnancy on A1C measures. Therefore, 178 participants were included in the analyses. All subjects gave their written consent to participate in this study. Height was measured to the nearest millimetre with a stadiometer and body weight was measured to the nearest 0.1 kg on a calibrated balance. BMI was calculated for each participant. Waist circumference, using a standardized procedure, 21 was measured to the nearest 0.1 cm in standing subjects at the midpoint between the iliac crest and the lateral lowest rib, and was measured twice by a trained professional. In the case of a discrepancy of > 1 cm between the two measures, a third measurement was taken. The average of the measures was used for analyses. A waist circumference 88 cm was used as the cut-off for risk stratification in analyses. 6,22 A 2-hour 75 g OGTT was performed in the morning after an overnight fast. Blood samples were collected in EDTA-containing tubes (Becton Dickinson, Franklin Lakes, NJ) through a venous catheter from an antecubital vein at 15, 0, 15, 30, 60, 90, and 120 minutes. Plasma glucose and insulin were measured enzymatically 23 and by radioimmunoassay, 24 respectively. A1C was determined using Cobas Integra 800 (Integra; Roche, Switzerland) and standardized to the National Glycated Haemoglobin Standardization Program. In accordance with the United States 1 and Canadian 6 criteria, type 2 diabetes was defined as having a FPG 7.0 mmol/l and/or a 2h-PG 11.1 mmol/l. Impaired fasting glycemia and impaired glucose tolerance were defined as a FPG 5.6 mmol/l and < 7.0 mmol/l and as a 2h-PG 7.8 mmol/l and < 11.0 mmol/l, respectively. SEPTEMBER JOGC SEPTEMBRE

3 Women s Health Table 1. Characteristics of participants according to A1C concentrations Overall n = 178 A1C < 5.7 n = 104 A1C 5.7 n = 74 P* Age, years 36.4 ± ± ± Time since latest pregnancy, years 3.5 ± ± ± Ethnicity (n = 165) 0.52 Non-Hispanic white 156 (94.6) 91 (94.8) 65 (94.2) Other 9 (5.4) 5 (5.2) 4 (5.8) Waist circumference, cm 91.4 ± ± ± BMI, kg/m ± ± ± 7.7 < 0.01 Fasting glycemia, mmol/l 5.9 ± ± ± 0.8 < h post-ogtt glycemia, mmol/l 8.2 ± ± ± 2.7 < 0.01 Fasting insulinemia, pmol/l 85.8 ± ± ± h post-ogtt insulinemia, pmol/l ± ± ± Pre-diabetes 109 (61.2) 62 (59.6) 47 (63.5) < 0.01 Type 2 diabetes 32 (18.0) 11 (10.6) 21 (28.4) 0.02 Any glucose intolerance 141 (79.2) 73 (70.2) 68 (91.9) < Data are presented as means ± SD for continuous variables and as n () for categorical variables. *P value for the difference between participants with A1C < 5.7 and participants with A1C 5.7 Pre-diabetes was defined as impaired fasting glycemia or impaired glucose tolerance. 1 Any glucose intolerance included pre-diabetes and type 2 diabetes. An A1C level 5.7 was used as the cut-off for sensitivity and specificity analyses since this level is the cut-off for prediabetes according to the American Diabetes Association s criteria. 1 Standardized questionnaires were used to obtain self-reported data on personal medical history, ethnicity, and medication. Continuous variables were tested for normality of distribution, and log transformations of skewed variables were used in subsequent analyses, where necessary. Differences in characteristics of the participants, categorized by A1C concentration (< 5.7 or 5.7), were tested for statistical significance using one-way ANOVA. Logistic regression analyses were performed to examine the relative odds of having type 2 diabetes according to A1C concentration (< 5.7 or 5.7) and waist circumference (< 88 cm or 88 cm). We evaluated the sensitivity and specificity of A1C 5.7 and/or waist circumference 88 cm to detect pre-diabetes, type 2 diabetes, or any glucose intolerance. Analyses were conducted using SAS statistical software, version 9.2 (SAS Institute Inc, Cary, NC). Statistical significance was defined as P Ethics approval for the study was provided by the Medical Ethics Committee of Laval University. RESULTS As shown in Table 1, the mean age of participants was 36.4 ± 4.8 years. Most were non-hispanic white (94.6) and were tested at a mean 3.5 ± 1.9 years after their most recent pregnancy. Women were tested at between six and 94 months after delivery. These variables did not differ between groups stratified by A1C. Women with A1C 5.7 had larger waist circumference, higher BMI, and higher FPG and 2h-PG levels than women with A1C < 5.7 (P < 0.05). No difference was observed between these groups in fasting and 2h-insulinemia (P > 0.05). More than one half of the participants (61.2) had prediabetes, and 18.0 of women had type 2 diabetes. Women with A1C 5.7 were more likely to have prediabetes (OR 3.9; 95 CI 1.5 to 10.2) and type 2 diabetes (OR 3.4; 95 CI 1.5 to 7.5) than women with A1C < 5.7. However, despite high specificity (84), an A1C level 5.7 had 43 sensitivity to detect pre-diabetes and 66 sensitivity and 64 specificity to detect type 2 diabetes. Finally, A1C 5.7 had 48 sensitivity and 84 specificity to detect any glucose intolerance (Table 2). The A1C cut-offs recommended in the most recent Canadian guidelines for pre-diabetes (6) and type 2 diabetes (6.5) had lower sensitivity and higher specificity. An A1C level 6 had 14 sensitivity and 97 specificity to detect pre-diabetes and A1C 6.5 had 9 sensitivity and 99 specificity to detect type 2 diabetes. If FPG 6.0 mmol/l 812 SEPTEMBER JOGC SEPTEMBRE 2013

4 Use of Glycated Hemoglobin and Waist Circumference for Diabetic Screening in Women With a History of Gestational Diabetes Table 2. Sensitivity and specificity of A1C, waist circumference (WC), and the combination of the two measures (A1C and waist circumference) to detect impaired glucose metabolism Sensitivity A1C 5.7 Specificity Sensitivity WC 88 cm Specificity A1C 5.7 and/or WC 88 cm Sensitivity Specificity Impaired fasting glucose Impaired glucose tolerance Pre-diabetes only Type 2 diabetes only Any glucose intolerance had been used to define pre-diabetes instead of FPG 5.6 mmol/l, as suggested in the Canadian guidelines, A1C 5.7 would have had a slightly higher sensitivity and lower specificity to detect pre-diabetes. The relative odds of having type 2 diabetes according to A1C (< 5.7 or 5.7) and waist circumference (< 88 cm or 88 cm) were examined; women with A1C 5.7 and waist circumference 88 cm were approximately 11 times more likely to have pre-diabetes (OR 11.3; 95 CI 1.5 to 86.3) and four times more likely to have type 2 diabetes (OR 4.4; 95 CI 2.0 to 9.9) than women with one or neither of these criteria. As shown in Table 2, the combination of A1C 5.7 and/or waist circumference 88 cm had 76 sensitivity and 62 specificity to detect pre-diabetes and 91 sensitivity and 34 specificity to detect type 2 diabetes. Finally, this combination had 79 sensitivity and 62 specificity to detect any glucose intolerance. The timing of the testing did not seem to influence these results significantly. For example, in women tested before or after the median time of testing, differences < 10 were observed for sensitivity and specificity. DISCUSSION Results from the present study showed an association between elevated A1C levels and abnormal glucose metabolism. However, A1C alone did not appear to be a sensitive test to detect pre-diabetes in women with prior GDM. The combination of A1C 5.7 with waist circumference 88 cm had the strongest association with pre-diabetes and type 2 diabetes, with 11.3 and 4.4-fold increased risk, respectively. This combination of A1C and waist circumference also had relatively high sensitivity to detect pre-diabetes and type 2 diabetes. Few studies have examined the association between A1C and metabolic complications and its sensitivity to detect abnormal glucose metabolism in women with prior GDM. A study of 54 women with prior GDM conducted by Kim et al. showed that A1C 5.7 had 65 sensitivity and 68 specificity for any glucose intolerance. 12 The results of the present study showed 48 sensitivity and 84 specificity for the same outcome. However, when A1C 5.7 was combined with waist circumference 88 cm in the present study, a greater sensitivity (79) was obtained with a similar specificity (62). García de Guadiana Romualdo et al. also showed that the same cut-off for A1C is inappropriate for postpartum glucose tolerance evaluation in women with prior GDM. 14 Megia et al. showed that the combination of A1C ( 5.5) and FPG had an appropriate sensitivity for abnormal glucose metabolism in a cohort of 364 Spanish women in the first year postpartum. 25 This combination was suggested as a means of selecting candidates for OGTTs. However, this proposed combination of testing methods requires a fasting period, which makes it less useful than A1C alone or in combination with waist circumference, for which no fasting period is required. In addition, Picón et al. showed in a similar sample (231 Spanish women with prior GDM at one year after delivery) that A1C, alone or in combination with FPG, was not a sensitive and specific test for abnormal glucose metabolism in women with prior GDM. 13 In our study, the large sample size and the high proportion of women with type 2 diabetes allowed us to evaluate the sensitivity and specificity of A1C 5.7 alone or the combination of A1C 5.7 and waist circumference 88 cm to detect type 2 diabetes. Our results indicated that the two measures combined had a higher sensitivity (91 vs. 66) and a lower specificity (34 vs. 64) for the ability to detect type 2 diabetes than A1C alone. Since with the proposed testing method women may have an abnormal A1C, an abnormal waist circumference, or both, a greater number of women were identified as potentially at risk, and therefore a lower specificity was expected. Consequently, our results suggest that the combined use of A1C and waist circumference could detect women at increased risk; SEPTEMBER JOGC SEPTEMBRE

5 Women s Health nevertheless, the low specificity suggests that this testing method alone is insufficient considering the high number of false positives identified. Thus, the combination of measures could potentially be used as a primary detecting tool to increase testing rates because of its simplicity and its low cost. Women identified by this combination of measures could then undergo an OGTT to complete the diagnosis; but if the A1C is already higher than 6.5 (cutoff for diabetes diagnosis) or higher than 6 (Canadian cutoff for pre-diabetes), then the diagnosis could be established directly. This testing could reduce the number of OGTTs performed in women with prior GDM. For example, for the identification of type 2 diabetes in our study sample, the use of A1C and waist circumference would have required a subsequent OGTT in 126 women, 30 fewer than if the entire group of women required OGTT, and 91 of the cases of type 2 diabetes would have been identified. This reduction may not be seen as substantial; however, the objective was not necessarily to reduce the number of tests performed, but rather to increase the long-term rates of testing of women with prior GDM using simpler and less expensive methods. Using the combination of A1C and waist circumference rather than OGTT, 9 of women who developed type 2 diabetes following delivery would have been missed. This number seems fairly high; yet, considering the low testing rates of women with prior GDM, we can assume that a high proportion of women who develop type 2 diabetes following delivery are already being missed. In addition, the acceptability of the proposed testing method compared with the acceptability of the OGTT should be further explored. Testing rates of women with prior GDM have appeared to increase over the last decade, but remain insufficient. 8,9 This indicates the need to find adequate strategies to ensure women with prior GDM return for testing following their pregnancy. The use of a simpler testing method may help increase adherence to postpartum testing. A1C testing is a standardized measure that may be more representative of overall glycemic exposure and risk for long-term complications than FPG or 2h-PG. 26 A1C is also more convenient because there is no fasting period needed and it is a simple and rapid testing measure. 27 Some factors such as hemoglobinopathies, iron deficiency, hemolytic anemia, severe hepatic and renal disease, ethnicity, and age could affect A1C values. 26,27 In the present study, 10 women had hemoglobin values lower than 120 g/l, and when these women were excluded from the analyses, results remained unchanged (data not shown). Waist circumference is also a simple and standardized measure that is higher in women with prior GDM 15,16 and has been associated with insulin resistance. 17,18 Yet no study to date has evaluated the combined use of these two measures, which are much simpler, less time consuming, and less expensive than oral glucose challenges to detect and predict abnormal glucose metabolism in women with prior GDM. On the other hand, the necessity to test women for abnormal glucose metabolism in longterm follow-up can be argued. The proposed method of testing (combining A1C and waist circumference) would identify 76 of women with pre-diabetes. In clinical settings, these women would be encouraged to improve their lifestyle and lose weight if necessary, and they would be monitored more closely. However, our results showed that within an average of 3.5 years, 61 of women with prior GDM had developed pre-diabetes, and 79 of women had developed some form of glucose intolerance, which suggests that virtually all women with prior GDM could benefit from a lifestyle intervention. Although all women with prior GDM should adopt a healthy lifestyle following delivery, we know that their lifestyle is not optimal. 20 The simple testing we propose could be an additional measure to ensure adequate follow-up of these women. The cost-effectiveness of the testing method versus a lifestyle program for all women needs to be examined. The strengths of this study include the use of an OGTT to measure glucose and insulin concentrations as well as to detect glucose intolerance, pre-diabetes, and type 2 diabetes in women with prior GDM. Confounding factors such as ethnicity, age, time since most recent pregnancy, and hemoglobin levels were also considered in the present study. Indeed, adjustments of the statistical analyses for these confounding variables did not alter the results. Our study sample was mainly composed of white women, and racial disparities in A1C values among individuals with impaired glucose tolerance have been documented. 28 However, no race-specific diagnostic values have been established, 26 and recent results from the ORIGIN trial showed that the relationship between A1C and FPG is not significantly affected by ethnic or geographic differences. 29 The cut-off used for waist circumference (88 cm) was selected according to recommendations from the Canadian Diabetes Association 6 and NCEP-ATP III 22 ; nevertheless, the International Diabetes Federation recommends ethnicspecific cut-offs for waist circumference measures. 30 Repeated testing and outcome-based studies are also needed to validate the use of these two measures as a screening tool in women with prior GDM. CONCLUSION Results from the present study suggest that the combination of A1C and waist circumference, two simple measures, could offer a sensitive test for the detection of pre-diabetes 814 SEPTEMBER JOGC SEPTEMBRE 2013

6 Use of Glycated Hemoglobin and Waist Circumference for Diabetic Screening in Women With a History of Gestational Diabetes and type 2 diabetes in the years following a pregnancy complicated by GDM. However, repeated testing in larger cohorts with a more ethnically diverse population will be necessary to validate this testing method. ACKNOWLEDGEMENTS We thank all the participants of this study. We would also like to express our gratitude to Geneviève Faucher, MSc, RD, Véronique Garneau, MSc, RD, and Ann-Marie Paradis, PhD, RD, from Laval University, for their assistance and technical support throughout the study. This work is supported by the Canadian Institute for Health Research (CIHR) and by the Fonds de la recherche en santé du Québec (FRSQ). André Tchernof is the recipient of a senior scholarship from the FRSQ. Julie Robitaille is the recipient of a Junior Investigator scholarship from the FRSQ. REFERENCES 1. American Diabetes Association. 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