Utility of maternal A1c measurement in the second trimester for the diagnosis of gestational diabetes mellitus

doi:10.21203/rs.3.rs-5313206/v1

Background: The aim of this study was to investigate the impact of changes in diagnostic processes and criteria for gestational diabetes mellitus (GDM) on adverse obstetric outcomes associated with GDM.

Methods: A total of 3000 pregnant women between 24 and 28 weeks of gestation were included in the study. Screening for gestational diabetes was performed using hemoglobin A1c (HbA1c) in 1200 pregnant women who either refused or could not tolerate the oral glucose tolerance test (OGTT). The HbA1c cut-off value for the diagnosis of GDM was set at ≥5.7% in accordance with ameta-analysis by Paula B. Renz et al. A total of 154 pregnant women with HbA1c ≥5.7% were diagnosed with gestational diabetes, and their data were recorded prospectively. These data were compared with obstetric outcomes in 250 pregnant women diagnosed with diabetes by performing a 100-g OGTT after a 50-g glucose challenge test (GCT).

Results: There were no significant differences between two groups in terms of maternal age, gestational age at diagnosis, gravidity, and parity. Body mass index (BMI) was found to be significantly higher in pregnant women with HbA1c levels ≥5.7% (p<0.001). Polyhydramnios was more common in the HbA1c ≥5.7% group and oligohydramnios was more common in the OGTT group (p<0.001). Neonatal hypoglycemia was found to be significantly higher in the OGTT group (p<0.05). The median HbA1c value were different in each group (OGTT group 5.6%, HbA1c group 5.8% ; p< 0.001).

Conclusion: As treatment plays an important role in the management of GDM, it was found that HbA1c levels are not sufficient to detect some obstetric consequences of GDM in the second trimester. It was concluded that evaluations that synchronize HbA1c and OGTT results are necessary for the diagnosis of GDM in the second trimester.

Gestational diabetes mellitus

HbA1c

oral glucose tolerance test

poor obstetric outcome

Gestational diabetes mellitus (GDM) is one of the most common medical complications during pregnancy (1). GDM is a condition characterized by carbohydrate intolerance that either begins or is diagnosed during pregnancy. It is known that complications involving any type of diabetes mellitus occur in 7% of pregnancies, with 86% of these cases being attributed to GDM (1). Poor obstetric outcomes in GDM can be both maternal and fetal. Screening for GDM is typically recommended between the 24th and 28th weeks of gestation (2). In the United States, a two-step approach is commonly used for screening purposes, involving the consumption of 50 grams of glucose followed by venous glucose measurement one hour later (3). In 2017, the American Diabetes Association (ADA) included HbA1c levels ≥5.7% (39 mmol/mol) in early screening strategies for gestational diabetes, but it currently does not recommend the use of HbA1c for the diagnosis of GDM in its guidelines (4,5). However, during the COVID-19 pandemic, many countries worldwide, including the United Kingdom, Canada, Australia, and New Zealand, actively incorporated and utilized HbA1c in their guidelines in second trimester to expedite hospital stays (6-8).

In the literature, high HbA1c levels in early pregnancy have been found to be associated with an increased risk of GDM (9). It has been shown that as the HbA1c level approaches 6.5% (48 mmol/mol) in early pregnancy, particularly at levels ≥5.7% (39 mmol/mol), the likelihood of developing GDM increases (9).

This study aimed to compare poor obstetric outcomes of GDM according to HbA1c value among pregnant women in our hospital who refused to undergo the 50-gram glucose test for GDM screening between the 24th and 28th gestational weeks. For those who consented to the screening, either a 50-gram glucose challenge test or, if necessary, a 100-gram OGTT were conducted to diagnose GDM. Our aim was to assess the obstetric consequences of GDM by selecting an HbA1c cut-off of ≥5.7% (39 mmol/mol) in the second trimester.

This study was conducted prospectively at Etlik Zübeyde Hanım Women's Health Training and Research Hospital from july 2021 and july 2023 . Ethical approval was obtained by the institutional review board from Ankara Etlik Zübeyde Hanım Women's Health Training and Research Hospital on 09.06.2021 # 2021/63 . The study complied with the ethical principles for medical research of the Declaration of Helsinki (10) . Pregnant women who presented to our hospital between the 24th and 28th weeks of gestation were informed about the study as well as provided with relevant details. In this study, 1471 pregnant women who met the study criteria were screened by 100 gr OGTT after a 50 g GCT, while 1200 pregnant women were screened by HbA1c (Figure 1). A total of 154 pregnant women with HbA1c levels ≥5.7% (39 mmol/mol) were diagnosed with GDM (7). Their outcomes were compared with those of 250 pregnant women who underwent 100-g OGTT after 50-g GCT according to American College of Obstetric and Gynecology (ACOG) guidelines and diagnosed with diabetes (3). Patients with HbA1c levels ≥5.7% (39 mmol/mol) and those with values ≥140 mg/dL after a 50-g GCT were considered to have GDM if they exhibited dual elevations in values following a 100-g OGTT. Accordingly, 250 patients in the OGTT group and 154 patients in the HbA1c group who were considered to have GDM were included in the study and their data were prospectively recorded. The inclusion criteria for the study were defined as pregnant individuals between the 24th and 28th gestational weeks with singleton pregnancies, those who received a diagnosis of diabetes through a 100-g OGTT after a 50-g GCT, and those who either refused or could not tolerate the 50-g OGTT. Pregnant women with pre-existing type 1 or type 2 diabetes, those with a history of diabetes in a previous pregnancy, pregnant individuals diagnosed with preeclampsia before the 24th week of gestation, multiple pregnancies, pregnancies with fetal anomalies, and pregnancies diagnosed with fetal growth restriction (FGR) were excluded from the study.

Maternal age, gravidity, parity, BMI, abdominal circumference (AC) and estimated fetal weight (EFW) on ultrasound percentile in the fetus, presence or absence of preeclampsia during pregnancy monitoring, gestational age at delivery, mode of delivery, shoulder dystocia, newborn weight, APGAR scores at 1 and 5 minutes, neonatal hypoglycemia, and adverse obstetric outcomes were recorded for both groups. In the study, all pregnant individuals diagnosed with gestational diabetes were followed-up in a multidisciplinary manner throughout pregnancy by a team consisting of a dietitian, obstetrician, and internal medicine specialist. Following the diagnosis of GDM, dietary treatment was initiated initially. In cases where blood sugar levels could not be regulated despite dietary measures, insulin therapy was initiated. Poor obstetric outcomes in gestational diabetes were defined as the development of preeclampsia during pregnancy monitoring (diagnosed having a blood pressure measurement of ≥ 140/90 mmHg on two separate occasions with a 15-minute rest, accompanied by proteinuria or systemic signs suggesting preeclampsia) (11), preterm birth (delivery before 37 weeks), cesarean delivery, newborn 5-minute APGAR score of <7 (12), and the presence of shoulder dystocia requiring maneuvers (McRoberts maneuver, episiotomy after fetal head delivery, suprapubic pressure, delivery of the posterior shoulder by oblique angle, and 180-degree rotation of the baby). Newborn weight ≥ 4000 grams (macrosomia) and the presence of neonatal hypoglycemia (defined as blood glucose level < 2.2 mmol/dl during the first two days based on laboratory tests) were also considered as poor obstetric outcomes (13). Obstetric care was performed according to ACOG 2018 guideline (3).

Statistical Analysis

Data were analyzed using the statistical program SPSS 22.0. Descriptive data were presented as number, percentage, mean, standard deviation, median and range. According to the normality of the data, parametric and nonparametric methods were used to compare the independent variables. Post hoc analysis were used with Bonferroni correciton. Spearman correlation analysis was used to determine correlation. Results were analyzed with a significance level p<0.05 and a confidence interval of 95%.

Intergroup comparison of sociodemographic, general health and obstetric characteristics during pregnancy period is given in the Table 1. The rate of treatment with insulin were statistically significantly higher in the group diagnosed with GDM by OGTT test. BMI value and AC, percentile of AC, EFW, percentile of EFW values were statistically significantly higher in the group diagnosed with GDM by HbA1c test.

There was no difference between the groups in terms of birth week, birth weight, APGAR scores, delivery type, maturity, preeclampsia, newborn intensive care unit (NICU) requirement, NICU stay (day), neonatal macrosomia and shoulder dystocia (p>0.05). When the groups were compared with amnion fluid index (AFI), a difference was detected between the groups. In Bonferroni corrected pairwise comparisons, the rate of polyhydramnios was found to be high in the group diagnosed with the HbA1c test, while the rate of oligohydramnios was found to be high in the group diagnosed with the OGTT test (p˂0.001). Neonatal hypoglycemia was more common in the OGTT group (p˂0.05 ,Table 2).

Table 3 includes laboratory findings. The HbA1c value of the group diagnosed with the HbA1c test was statistically significantly higher than the group diagnosed with the OGTT test.

Not stated in the table, while a statistically significant correlation was determined between HbA1c and OGTT 100 g (fasting blood sugar) and random blood test value (respectively ρ=223, ρ=847; p˂0.001), there was no correlation between other OGTT test values.

When comparing HbA1c levels by groups (below 5.6% (38 mmol/mol), between 5.6-5.7%, 38-39 mmol/mol) between 5.7-5.8% (39-40 mmol/mol), above 5.8% (40 mmol/mol), a difference in the incidence of pre-eclampsia (χ2 = 12.401, p=0.006) and neonatal hypoglycemia (χ2=11.123 p=0.011) was found. A higher rate of pre-eclampsia was observed in the group with a score above 5.8% (40 mmol/mol) compared to the groups with 5.7% (39 mmol/mol) and 5.8% (40 mmol/mol) (χ2=9.876 p=0.002). No significant difference was observed in the subgroup comparison of neonatal hypoglycemia.

OGTT is considered as the gold standard method for GDM screening; however, a significant portion of pregnant individuals may have difficulty tolerating glucose solutions (14). As previously mentioned, it has been shown that increasing HbA1c levels may be associated with GDM. Numerous studies have mentioned that high HbA1c levels may be associated with adverse obstetric outcomes related to GDM (8). Studies have shown that HbA1c levels ≥ 5.7% (39 mmol/mol) have a specificity of 96% (95% confidence interval: 86-99) and a sensitivity of 25% (95% confidence interval: 10-49) for the diagnosis of GDM (7). The revised UK and Canada guidelines set the HbA1c threshold at 5.7% (39 mmol/mol) (7,8).

In the present study, maternal characteristics such as age, gravidity, and parity were similar between the groups, but BMI was found to be significantly higher in the HbA1c ≥5.7% (39 mmol/mol) group. In addition, the AC and EFW percentile were found to be significantly higher in the HbA1c ≥5.7% (39 mmol/mol) group. This may be attributed to high HbA1c levels as well as to high maternal BMI. Several studies have shown that the fetuses and neonates of obese women tend to have higher measurements compared to those of non-obese women (15,16). In the present study, maternal random blood glucose levels were found to be significantly higher in the HbA1c ≥5.7% (39 mmol/mol) group. This finding highlights the fact that fetal macrosomia is an important indicator of hyperglycemia in pregnancy and the known relationship between macrosomia, excessive adiposity, and fetal hyperinsulinemia (17,18). Hyperglycemia during pregnancy is associated with maternal and perinatal adverse outcomes (17).

In our study, it was found that neonatal hypoglycemia and oligohydramnios was more common in the OGTT group (p˂0.05, p<0.001, respectively), and polyhydramnios was more common in the HbA1c ≥5.7% (39 mmol/mol) group (p<0.001), but there was no significant difference in other poor obstetric outcomes (p>0.05). Several studies have demonstrated that high HbA1c levels increase adverse obstetric outcomes related to GDM (19,20). An HbA1c level >5.9% (41 mmol/mol) in early pregnancy has been associated with at least a twofold increase in the relative risk of preeclampsia, shoulder dystocia, congenital anomalies, and perinatal death (20). In this study, the incidence of pre-eclampsia was higher in the group with an HbA1c value above 5.8% (40 mmol/mol).

Other studies have found that elevated HbA1c levels may be associated with large-for-gestational-age (LGA) and preterm labor (21). In second trimester McIntyre et al. evaluated cases diagnosed with GDM using the routine two-step 75-g OGTT accepted in the UK and considered non-diagnosed cases according to modified GDM (HbA1c ≥5.7% (39 mmol/mol) and/or fasting plasma glucose ≥5.6 mmol/L as "missed GDM cases" (8). Statistically significant higher rates of preterm birth, LGA infants, neonatal hypoglycemia, increased neonatal adipose tissue, and hypertension during pregnancy were observed in these cases (8). This finding in the present study can be interpreted as follows. This may indicate that the follow-up and treatment of patients diagnosed with GDM are well managed. Falavigna et al. conducted a systematic study at different locations to estimate the effectiveness of treating GDM, encompassing various adverse outcomes associated with GDM (22). In a systematic review incorporating 7 randomized controlled trials conducted in different countries, a decrease in relative risks for macrosomia, LGA, and shoulder dystocia was observed following GDM treatment (22). The prognostic value of HbA1c for adverse obstetric outcomes of GDM needs to be further evaluated through prospective studies .

In a meta-analysis conducted by Paula B. Renz et al., it was shown that when using an HbA1c cutoff value of ≥5.7% (39 mmol/mol) to diagnose GDM in the second trimester across five studies, the ROC curve had an AUC of 0.741 (95% CI 0.675-0.807), with a sensitivity range of 9-73% and specificity of 76-100% (6). Accordingly, an HbA1c level of ≥5.7% (39 mmol/mol) was chosen for the diagnosis of GDM in the present study. The median HbA1c value in pregnant women diagnosed with GDM by OGTT was found to be 5.6% (38 mmol/mol), which was significantly different from the median value of 5.8% (40 mmol/mol) in the HbA1c ≥5.7% (39 mmol/mol) group (p<0.001). The significant difference observed when compared with the 100 g OGTT, the gold standard test, suggests that HbA1c ≥5.7% (39 mmol/mol) may be underestimate to diagnosis of GDM. The finding that the HbA1C value of pregnant women diagnosed with OGTT was less than 5.7% (39 mmol/mol) showed that taking this cut-off value (HbA1c ≥5.7% (39 mmol/mol)) as a diagnostic criterion would cause some patients diagnosed with GDM to be overlooked. However, there is a need for further studies in which both methods are evaluated in the same patient groups.

Limitations of this study include that the results could not be compared with fetal-maternal outcomes of patients not diagnosed with GDM. In addition, the treatment and follow-up of diagnosed patients is likely to influence poor obstetric outcomes. The strengths of this study are that it was a single-center study, the results reflect the same patient group, and the sample size was large.

In the study, we tried to explain the role of HbA1c measurement in the diagnosis of GDM. Developments in diagnostic and treatment methods prevent poor obstetric outcomes in GDM. The results of the current study suggest that an HbA1c level of ≥5.7% (39 mmol/mol) may not be a suitable alternative to OGTT for the diagnosis of GDM, as pregnant women with GDM may be missed and this may pose additional risks to the pregnant women. Further studies are needed to evaluate HbA1c values synchronized with OGTT results in the same patient group.

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Table1. Intergroup comparison of sociodemographic general health and obstetric characteristics during pregnancy period

	Diagnosed with HbA1c ≥5.7 Group		Diagnosed with OGTT Group		Total		Analysis
	n	Mean ±SD Med (min-max)/ Mean R.	n	Mean ±SD Med (min-max)/ Mean R.	n	Mean ±SD Med (min-max)
Maternal Age (years)	154	32.58±5.69	250	33.59±5.69	404	33.17±5.64	t=-1.647 p=0.100
BMI (kg/m²⁾	151	32 (22-54)/223.84	250	31 (21-44)/187.21	401	31 (21-54)	z=-3.074 p=0.002
Gastasional week	154	27.2 (22.1-30.4)	250	27.2 (24.1-29.6)	404	27.2 (22.1-30.4)	z=-0.389 p=0.697
Gravidity	154	3 (1-9)/ 193.57	250	3 (1-13)/ 208.00	404	3 (1-13)	z=-1.231 p=0.218
Paritiy	154	1 (0-5)/ 200.41	250	2 (0-5)/ 203.79	404	1 (0-5)	z=-0.292 p=0.770
AC (milimeter)	154	240 (169-323)/ 220.93	250	234 (185-296)/ 191.15	404	236 (169-323)	z=-2.490 p=0.013
Percentil AC	154	64.4 (10.4-99.3)/ 227.57	250	52.9 (10.0-99.9)/ 187.05	404	58.7 (10.0- 99.9)	z=-3.389 p=0.001
EFW	154	1216.5 (505.0-2323.0)/ 225.76	250	1166.0 (593.0-1914.0)/ 188.17	404	1189.0 (505.0- 23230)	z=-3.143 p=0.002
Percentil EFW	154	80 (12-100)/ 235.53	250	58 (10-100)/ 182.16	404	65 (1-100)	z=-4.467 p=0.000
	n	%	n	%	n	%
GDM treatment
Diet	127	82.5	185	74	312	77.2	χ²=3.885 p=0.049
Insulin	27	17.5	65	26	92	22.8	χ²=3.885 p=0.049
Obstetric history
Primiparite	46	29.9	81	32.4	127	31.4	χ²=0.335 p=0.846
Previous CS	52	33.8	79	31.6	131	32.4
Previous VD	56	36.4	90	36	146	36.1

t= Student T Test; z= Mann-Whitney U Test; χ²= Chi Square Test; Abbreviations:HbA1C: Hemoglobin A1c, OGTT: Oral Glucose Tolerance Test; BMI: Body Mass Index; AC: Abdominal Circumference; EFW: Estimated Fetal Weight; GDM: Gestational diabetes mellitus CS: Cesarean section; VD: Vaginal delivery

Table 2. Intergroup comparison of data on obstetric outcomes

	Diagnosed with HbA1c ≥5.7 Group		Diagnosed with OGTT Group		Total		Analysis
	n	Mean ±SD Med (min-max)/ Mean R.	n	Mean ±SD Med (min-max)/ Mean R.	n	Mean ±SD Med (min-max)
Birth week	154	38.20 (32.5-41.5)/ 214.60	250	38.1 (31-41.4)/ 195.04	404	38.1 (31-41.5)	z=-1.637 p=0.102
Birth weight (gram)	154	3240(1320-4740)/215.34	250	3135 1220-4465)/ 187.21/194.59	404	3165 (1220-4465)	z=-1.735 p=0.083
APGAR score 1	154	9 (5-9) /204.48	250	9 (6-9) /201.28	404	9 (5-9)	z=-0.712 p=0.476
APGAR score 2	154	10(7-10) /203.06	250	10 (7-10) /202.16	404	10 (7-10)	z=-0.217 p=0.828
NICU stay (day)	16	2 (1-19) /22.81	35	4 (1-20) /27.46	51	3 (1-20)	z=-1.048 p=0.295
	n	%	n	%	n	%
Delivery type
CS delivery	108	70.1	167	66.8	275	68.1	χ²=0.486 p=0.486
Vaginal delivery	56	29.9	83	33.2	129	31.9	χ²=0.486 p=0.486
Maturity
Preterm	46	29.9	56	22.4	102	25.2	χ²=2.818 p=0.093
Term	108	70.1	194	77.6	302	74.8	χ²=2.818 p=0.093
AFI
Polyhydramnios ^x	28	18.2	14	5.6	42	10.4	χ²=22.36 p=0.000 (x-y), (x-z), (y-z)
Oligohydramnios ^y	3	4.5	34	13.6	41	10.1
Normal ^z	119	77.3	202	80.8	321	79.5
Preeclampsia
No	125	81.2	208	83.2	333	82.4	χ²=0.271 p=0.602
Yes	29	18.8	42	16.8	71	17.6	χ²=0.271 p=0.602
NICU requirement
No	138	89.6	215	86.0	353	87.4	χ²=1.126 p=0.289
Yes	16	10.4	35	14.0	51	12.6	χ²=1.126 p=0.289
Neonatal hypoglycemia
No	149	98	232	92.8	381	94.8	χ2=5.215 p=0.022
Yes	3	2	18	7.2	21	5.2	χ2=5.215 p=0.022
Neonatal macrosomia
<4000 gr	142	92.2	238	95.2	380	94.1	χ²=1.527 p=0.217
4000 gr	12	7.8	12	4.8	24	5.9	χ²=1.527 p=0.217
Shoulder Dystocia
No	154	100.0	249	99.6	403	99.8	Fisher's Exact T. p=0.289
Yes	0	0.0	1	0.4	1	0.2	Fisher's Exact T. p=0.289

t= Student T Test; z= Mann-Whitney U Test; χ²= Chi Square Test; Fisher's Exact T: Fisher's Exact Test

Abbreviations: HbA1C: Hemoglobin A1c, OGTT: Oral Glucose Tolerance Test; AFI: Amnion fluid index, NICU: Neonatal intensive care unit. CS: Cesarean section

Table 3. Laboratory findings

	Diagnosed with HbA1c ≥5.7 Group		Diagnosed with OGTT Group		Total		Analysis
	n	Mean ±SD Med (min-max)/ Mean R.	n	Mean ±SD Med (min-max)/ Mean R.	n	Mean ±SD Med (min-max)
HbA1c (%)	154	5.8 (5.7-6.5)/ 272.12	250	5.6 (4.5-7.9)/ 159.61	404	5.7 (4.50- 7.9)	z=-9.502 p=0.000
Random blood glucose (mg/dl)	154	120 (115-234)			154	120(115-234)
OGTT 100 g (fasting blood sugar mg/dl)			250	88.5 (33-204)	250	88.5 (33-204)
OGTT 100 g (1st hour mg/dl)			250	199 (84-309)	250	199 (84-309)
OGTT 100 g (2st hour mg /dl)			250	167 (54-261	250	167 (54-261
OGTT 100 g (3st hour mg /dl)			250	133 (47-241)	250	133 (47-241)

z= Mann-Whitney U Test

Abbreviations: HbA1C: Hemoglobin A1c, OGTT: Oral Glucose Tolerance Test. g: Gram, mg/dl: miligram /deciliter

No competing interests reported.

Utility of maternal A1c measurement in the second trimester for the diagnosis of gestational diabetes mellitus

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Abstract

Figures

INTRODUCTION

MATERIALS AND METHODS

RESULTS

DISCUSSION

CONCLUSION

References

Tables

Additional Declarations

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