The association between an oral glucose tolerance test performed at term pregnancy and obstetric outcomes

Abstract

Aims

Assessing the value of oral glucose tolerance test performed at term pregnancy in identifying obstetric complications.

Methods

Retrospective cohort study of women with a normal 50 g glucose challenge test who also had an oral glucose tolerance test at term (defined as at or after 37 weeks of gestation). Comparison between the pathological and normal oral glucose tolerance test groups was performed.

Results

The mean glucose in the glucose challenge test of women in the normal oral glucose tolerance test (n = 256) group was lower than that in the pathological oral glucose tolerance test (N = 16) group (105 ± 17 mg/dl (5.8 ± 0.9 mmol/l) vs 117 ± 13 mg/dl (6.5 ± 0.7 mmol/l), p = 0.007). Relevant obstetrical complications did not differ significantly between the groups. Of note, in the pathological oral glucose tolerance test group only one woman delivered a macrosomic infant.

Conclusions

A pathological oral glucose tolerance test performed at term was unable to identify women at risk for impaired glucose metabolism-related obstetric complications and is therefore of limited clinical value and seems to be unjustified.

Keywords

Diabetes gestational impaired glucose metabolism oral glucose tolerance test macrosomia

Introduction

A missed diagnosis of impaired glucose metabolism may have major consequences on the parturient and her neonate, as glucose is one of the important drivers for fetal growth. Imbalanced maternal glucose metabolism, as seen in gestational diabetes mellitus (GDM), is thought to be a key factor in excessive fetal growth, contributing to the increased risk of obstetric complications.^1,2 At any given fetal weight, the presence of GDM increases the risk for maternal and neonatal complications, and to a greater extent when birth weight is greater than 4000 g, also known as macrosomia.^3,4

Delivery of a macrosomic baby may result in maternal and neonatal complications such as prolonged labor, instrumental or caesarean deliveries, high-degree perineal tears, postpartum hemorrhage (PPH), shoulder dystocia (SD), brachial plexus injury, fracture of the clavicle, neonatal intensive care unit admission and low 5 min APGAR score.^5,6 An impaired glucose metabolism at term is suspected in cases of high fetal weight estimation or newly diagnosed polyhydramnios.

According to the American College of Obstetrician and Gynecologist (ACOG) guidelines,⁴ GDM screening can be performed by a two-step approach, using a 50 g glucose challenge test (GCT) at 24 to 28 weeks of gestation followed by a 3 h 100 g oral glucose tolerance test (OGTT) performed when the GCT value is higher than institutional cut-off (commonly, 130–140 mg/dl (7.2–7.8 mmol/l)). GDM is diagnosed when two or more test values in the OGTT exceeds the Carpenter and Coustan cutoffs.⁷ However, which test needs to be used to diagnose GDM in late pregnancy and the value of a late diagnosis on pregnancy outcomes is not clear. Few studies have examined the use of OGTT in the third trimester and its association with pregnancy complications,^8–11 yet, its effect on clinical-making decisions and pregnancy outcomes when performed at term has not been studied extensively. The aim of this study was to assess the clinical value of using an OGTT at term to identify complications related to the late or missed diagnosis of GDM in women with an earlier normal GCT.

Materials and methods

Study population

This was a retrospective cohort study of women insured in the central district of ‘CLALIT’ health services, which is the largest health care provider in Israel, and delivered at Kaplan Medical Center, Rehovot, Israel, between June 2010 and June 2018 and had an OGTT performed at term. The inclusion criteria were: (1) a documented normal GDM screening earlier in pregnancy; (2) an OGTT performed between 37 and 42 completed weeks of gestation; women were excluded if they had a multifetal pregnancy, a non-vertex presentation, or if they had a previous diagnosis of gestational or pre-gestational diabetes. The local Institutional Review Board approved the study protocol and the use of demographical and clinical women's data for research purposes.

Definitions

A normal GCT was defined as a test result lower than 140 mg/dl (7.8 mmol/l). A pathological OGTT was defined when at least two out of four test results exceeded the Carpenter and Coustan cutoffs: fasting over 95 mg/dl (5.3 mmol/l), 1 h over 180 mg/dl (10 mmol/l), 2 h over 155 mg/dl (8.6 mmol/l) and 3 h over 140 mg/dl (7.8 mmol/l). Macrosomia was defined as a birth weight of 4000 g or more. Large for gestational age (LGA) was defined as birth weight greater than the 90th percentile for gestational age and neonatal sex.¹² Polyhydramnios was considered as amniotic fluid index higher than 250 mm. 5 min APGAR score below 7 was considered low. Severe neonatal hypoglycemia was defined as a plasma glucose concentration below 37 mg/dl (2.1 mmol/l).¹³ Gestational age was determined according to the last menstrual period if this had been confirmed by a first-trimester ultrasound examination, or by ultrasound if the sonographic determination of gestational age during the first trimester differed from the menstrual dating by more than 1 week.

Study procedures

A search in the electronic database of the central district of “CLALIT” health care provider and our institution for women that underwent a 100 g OGTT between 37 and 42 completed weeks of gestation. After exclusion of women who did not have an earlier documented GCT or who had a GCT result above 139 mg/dl (7.7 mmol/l), we used the women identification number and the last menstrual period date to cross-match the results with our labor ward database in order to identify the women that gave birth at our hospital in the corresponding pregnancy. The study population was classified into two groups according to the OGTT results: the normal OGTT (N-OGTT) group and the pathological OGTT (P-OGTT) group. A comparison was done between the two groups regarding birthweight (mean), and incidence of the following: macrosomia, caesarean delivery (CD), high degree perineal tears, PPH, SD low 5 min APGAR scores and severe neonatal hypoglycemia.

Statistical analyses

Continuous variables were compared between groups using either Student's t-test or the Mann–Whitney U-test, depending on data distribution evaluated using the Kolmogorov–Smirnov test. Chi-square or Fisher's exact tests were used for comparisons of proportions. The statistical software package used was PASW statistics version 18.0 (SPSS Inc., Chicago, IL, USA). A p-value of <0.05 was considered statistically significant.

Results

During the study period, 348 women had an OGTT at term, of whom 272 (78.2%) met the inclusion criteria. Sixteen women (5.9%) were included in the P-OGTT group and 256 (94.1%) in the N-OGTT group. Twenty-three women had a single abnormal value in the OGTT and were considered in the analysis as part of the N-OGTT group. As recently some studies showed that women with a single abnormal value have higher risk of obstetric complications, a secondary analysis with these women as part of the P-OGTT was performed.^4,14 The demographic and clinical characteristics of the two groups are shown in Table 1.

Table 1.

Demographic and clinical characteristics of women with normal and pathological term oral glucose tolerance test (OGTT).

	Normal OGTT (n = 256)^a	Pathological OGTT (n = 16)^a	p-value
Maternal age (years)	30.9 ± 4.8	32.2 ± 4.7	0.9
Parity	1 (0–6)	1 (0–3)	0.6
Pre-pregnancy BMI (kg/m²)	24.4 ± 4.3	22.0 ± 3.5	0.04
BMI at delivery (kg/m²)	29.7 ± 4.6	27.6 ± 3.3	0.08
Gestational age at delivery (weeks)	40.2 ± 0.9	39.5 ± 1	0.01
Gestational age at GCT (weeks)	25.4 ± 1	25.3 ± 4	0.9
GCT (mg/dl; mmol/l)	105 ± 17; 5.8 ± 0.9	117 ± 13; 6.5 ± 0.7	0.007
Gestational age at OGTT (weeks)	38.4 ± 1.1	38.3 ± 1	0.7
Caesarean delivery	13.3 (34)	31.3 (5)	0.06
Male neonate	51.6 (141)	68.8 (11)	0.3

BMI: body mass index; GCT: glucose challenge test; OGTT: oral glucose tolerance test.

Data presented as median (minimum–maximum), mean ± standard deviation or percentage (number).

The main indications for term OGTT were suspected macrosomia and/or polyhydramnios (Table 2). The indications were similar in both groups and no correlation was found between the indication for the test and the test results. Pre-pregnancy BMI was significantly lower for the P-OGTT group compared to the N-OGTT group (22.0 ± 3.5 kg/m² vs 24.4 ± 4.3 kg/m²; p = 0.04) while the difference in the BMI at delivery was not significant (29.8 ± 4.6 vs 27.6 ± 3.3; p = 0.08).

Table 2.

Incidence of the different indications for term OGTT.

	Normal OGTT (n = 256)^a	Pathological OGTT (n = 16)^a
Suspected macrosomia	55.0 (141)	37.5 (6)
Polyhydramnios	23.0 (59)	31.3 (5)
Suspected macrosomia + polyhydramnios	10.1 (26)	18.8 (3)
Suspected macrosomia + history of GDM	0.8 (2)	0
130<GCT<139 mg/dl (7.2–7.7 mmol/l)	1.2 (3)	6.3 (1)
Unknown	9.7 (25)	6.3 (1)

GCT: glucose challenge test; GDM: gestational diabetes mellitus.

Data presented as percentage (number).

The gestational age at delivery was higher in the N-OGTT group as compared to the P-OGTT group (40.2 ± 0.9 vs 39.5 ± 1, respectively; p = 0.01).

The mean GCT in the N-OGTT group was significantly lower than that of the P-OGTT group (105 ± 17 mg/dl (5.8 ± 0.9 mmol/l) vs 117 ± 13 mg/dl (6.5 ± 0.7 mmol/l), respectively; p = 0.007) (Figure 1).

Figure 1.

The distribution of glucose challenge test (GCT) results in women with normal and pathological term oral glucose tolerance test (OGTT).

Although a clear trend toward a higher CD rate in the P-OGTT group was noticed, this difference did not reach statistical significance (31.3% vs 13.3%, p = 0.06). Only two women in the P-OGTT group delivered by an emergency CD, one due to a non-reassuring fetal heart rate pattern and the other due to a failed induction of labor.

The mean neonatal birth weight was not significantly different between the N-OGTT and the P-OGTT groups (3695 ± 412 and 3540 ± 370 g, respectively; p = 0.14) (Table 3). Only one woman in the P-OGTT group delivered a macrosomic infant, and the rate of macrosomia was not significantly different between the groups (N-OGTT: 24.6% vs P-OGTT: 6.3%, p = 0.13). Four cases of SD were reported (1.5%), all in the N-OGTT group.

Table 3.

Short-term maternal and neonatal outcomes in women with normal and pathological term oral glucose tolerance test (OGTT).

	Normal OGTT (n = 256)^a	Pathological OGTT (n = 16)^a	p-value
Post-partum hemorrhage	2.2 (6)	– (0)	1
Neonatal birth weight (g)	3695 ± 412	3540 ± 370	0.14
APGAR<7 at 5 min	0.8 (2)	– (0)	1
Macrosomia	24.6 (63)	6.3 (1)	0.13
Shoulder dystocia	1.6 (4)	– (0)	1
Neonatal hypoglycemia		0	1

OGTT: Oral glucose tolerance test.

Data presented as mean ± standard deviation or percentage (number).

Four neonates had severe hypoglycemia, all born to mothers in the N-OGTT group, and only one was LGA (4438 g at 37 weeks of gestation).

Regarding other short-term maternal and neonatal complications, there were no significant differences between the two groups in the rate of PPH and low APGAR score at 5 min. No cases of high-degree perineal tears occurred in our cohort.

In addition, we analyzed the data with the more stringent criteria for the diagnosis of GDM while also considering women with a single abnormal value in the OGTT to be in the P-OGTT group, yet, the results remained consistent, apart from the difference in CD rate which now reached statistical significance (Table 4).

Table 4.

Maternal and neonatal outcomes including single abnormal value in the P-OGTT group.

	Normal OGTT (n = 233)^a	Pathological OGTT (n = 39)^a	p-value
Caesarean delivery	12.4 (29)	25.6 (10)	0.04
Macrosomia	24.0 (56)	20.5 (8)	0.8
Neonatal hypoglycemia	1.7 (4)	5.1 (2)	0.2

OGTT: Oral glucose tolerance test.

Data presented as mean ± standard deviation or percentage (number).

Discussion

In our cohort of 272 women with a documented OGTT at term and a normal GCT, only 16 (5%) had a pathological OGTT. The primary goal of performing OGTT at term is to reduce further maternal and fetal complications related to abnormal glucose metabolism. In this relatively large cohort, we were unable to detect any increase in perinatal complications with this late diagnosis of GDM.

The prevention of maternal and neonatal complications during labor is a primary goal of modern obstetrics. Macrosomia is one of the major causes of birth-related injuries for both the mother and neonate. Protracted labor, increased risk of CD, PPH, SD, and brachial nerve injuries are some of the risks associated with macrosomia. As for today, there are few tools to prevent macrosomia and its consequences, mainly SD.^5,15 Once macrosomia is suspected, a CD is considered. The estimated fetal weight at which a CD should be performed to reduce injuries related to macrosomia is controversial and differs between national societies guidelines.^5,6,16,17 As diabetes during pregnancy is, to some extent, a modifiable risk factor for macrosomia as well as an independent risk factor for pregnancy and labor-related complications, ruling-out diabetes is of substantial importance. Even more so, due to the evidence that the presence of diabetes, at any given fetal weight, increases the risk for SD. Hence, it is commonly acceptable to use a lower threshold for a CD in women with diabetes. The ACOG^4,5 recommends CD when EFW exceeds 4500 g in women with diabetes compared to 5000 g in the absence of diabetes, whereas at our institute, we use a lower threshold of 4000 g, and in specific cases of multiparous women up to 4250 g (and 4500 g without diabetes).

As pregnancy advances to term, there is a decrease in insulin sensitivity, and more parturients may test positive for gestational diabetes.^18–20 Thus, it may be reasonable to evaluate for the presence of diabetes in suspected cases, for example, polyhydramnios or a suspected LGA fetus; however, it is not clear which test should be used at this time point and whether a late diagnosis of gestational diabetes will improve pregnancy outcomes. An optional tool for this purpose is the 100 g OGTT. While this test has high sensitivity and specificity when performed at the appropriate timing in pregnancy (i.e. during the late second trimester), its use at term gestation is questionable, and to a greater extent, when performed in cases with a negative diabetes screening at an earlier stage of pregnancy. Geifman-Holtzman et al.¹⁰ used OGTT to define impaired glucose metabolism at term in 170 women with suspected macrosomia and a normal GCT in the second trimester. They found 10 women with a pathological OGTT, half of which had a GCT below 120 mg/dl (6.7 mmol/l). The authors suggested that in specific cases of suspected macrosomia, regardless of a previous GCT value, using OGTT might be justified. Notwithstanding, and in line with our results, using OGTT did not alter the detection rate of macrosomia in their study.

Other than decreasing insulin sensitivity, another possible explanation to a “newly” suspected impaired glucose metabolism at term may be a false-negative result in the GCT performed earlier in pregnancy. In order to characterize predictors for a false negative GCT, Goldberg et al.¹⁸ performed an OGTT on 1129 women regardless of their GCT value. Out of 202 women with a negative GCT (<140 mg/dl (<7.8 mmol/l)), they found eight false-negative cases. The only significant difference between the true- and false-negative cases was a higher mean GCT value (106 mg/dl (5.9 mmol/l) vs 118 mg/dl (6.6 mmol/l), respectively), but the authors noted a “considerable overlap” that prevented them from establishing a clear glucose cut-off value to rule out GDM. In our study, we found a similar difference in the GCT values between those with normal or pathological term OGTT (105 mg/dl (5.8 mmol/l) vs 117 mg/dl (6.5 mmol/l), respectively), and a similar overlap between the groups, preventing us as well from establishing a cut-off to predict a pathological OGTT.

Other than glucose status, several other maternal characteristics may affect fetal weight, for example, pre-pregnancy weight, weight gain during pregnancy, and genetics,^19–24 and different characteristics may alter fetal growth at different stages of pregnancy. Schaefer-Graf et al.¹⁹ showed that at the end of the second trimester, through the beginning of the third trimester, maternal genetic and historic parameters have a more substantial influence on fetal weight compared to maternal glycemia that plays a significant role in the late third trimester. The influence of maternal glucose status at late pregnancy on fetal weight was also shown by Ott et al.,²³ who found that in mothers with diabetes, there is a correlation between third trimester and near-delivery maternal glucose status and higher birth weight and macrosomia rates. In contrast, and consistent with the findings of Geifman-Holtzman et al.,¹⁰ we found similar mean neonatal birth weight and macrosomia rates among women with a normal or a pathological OGTT. Hence, using OGTT at term to diagnose impaired glucose metabolism was of no value in discriminating macrosomic from normal weight fetuses.

Ricart et al.²¹ showed that maternal obesity, represented as pre-pregnancy BMI, was an independent and stronger predictor of perinatal outcome compared to abnormal maternal glucose intolerance. Poprzeczny et al.²⁵ also found an association between maternal and fetal weight, which was not mediated by gestational diabetes. Contrary to that, Ott et al.²³ showed that after adjusting for maternal glucose status, maternal anthropometric parameters were not independent risk factors for higher neonatal birth weight. In our study, pre-pregnancy BMI was lower for the P-OGTT group yet, we found no differences in perinatal or maternal outcomes between the groups.

Interestingly, in our study, all four cases of SD occurred in the N-OGTT group. In two cases, there was a macrosomic infant (4092 and 4160 g) and the other two were normal weight babies (3297 and 3842). All cases were described as “Mild,” and no short-term maternal or neonatal complications were reported (e.g. PPH, high-degree perineal tears, low APGAR score, or brachial plexus injury).

One of the more significant neonatal consequences of both diabetes and macrosomia is neonatal hypoglycemia.^3,4,13 In our cohort, there were four cases of neonatal hypoglycemia, and all were born to mothers in the N-OGTT group. Domanski et al.²⁶ showed that infants of mothers with diabetes have an odds ratio of 11.7 to have hypoglycemia compared to infants of mothers without diabetes. In another study by Esakoff et al.,³ hypoglycemia was twice as likely in macrosomic babies compared to normal weight babies and four times higher with the combination of macrosomia and gestational diabetes. According to our results, term OGTT could not predict nor differentiate neonates that developed hypoglycemia from those who did not.

The only difference (although not reaching statistical significance) found in our study between the normal and pathological OGTT groups was a higher CD rate in the pathological group (31.3% vs 13.3%, p = 0.06). This finding is not surprising as we recommend a CD in cases of combined diabetes and suspected macrosomia. Of note, only two out of the 16 women with a pathological OGTT at term had an emergency CD, one due to a non-reassuring fetal heart rate pattern and the second due to a failed induction.

Few other studies have tried to evaluate the use of OGTT in the third trimester of pregnancy and found that a pathological test was not related to adverse outcomes,^8–11 yet, two of these studies included women at an earlier gestational age (30–36 weeks),^8,9 and only two, as in our study, included women at term. Diagnosing glucose intolerance at term, with proximity to decision-making on labor and delivery management, does not allow time to modify the possible risks. Hence, it is essential to find a test that would accurately identify glucose intolerance and may help prevent its potential consequences. Our study, consistent with the recently published results of Mohr Sasson et al.,¹¹ demonstrates the limited value of an OGTT performed at term in the clinical management of women suspected to have a missed diagnosis of GDM. Not only could it not identify women at increased risk for obstetric complications, an abnormal result increased the risk of a CD. Other strategies to identify women at term with a suspected missed/late diagnosis of GDM should be explored. If time allows self-monitoring of blood glucose (SMBG) with similar cut-offs to those used to decide on treatment initiation in GDM cases, might provide an additional representation of the glucose status.^27,28 SMBG has been also suggested as an alternative to OGTT to identify hyperglycemia in pregnancy during the COVID pandemic.²⁹ Other options to consider include continuous glucose monitoring devices or a flash glucose monitoring system which were shown to have accurate and reliable glucose measurements also in pregnant women.^30–32

The main strengths of our study arise from its large cohort originating from a single health insurance provider and a single tertiary hospital, minimizing biases related to different protocols and clinical management practices in this controversial issue. However, our study is not without limitations and those limitations stem from its retrospective design. Management of women was at the discretion of the attending physicians, and we cannot argue on the justification of the OGTT performed and the decisions made based on its result. The retrospective nature of the study does not allow inferring a causal relationship between the pathologic OGTT results and the higher CD rates. Although we found no significant differences in our comparisons, this, in part, could be due to a type 2 error given the relatively low-rate of some obstetric complications in our study. Furthermore, the study included only short-term maternal and neonatal complication, thus we cannot infer regarding the long-term effect of a pathological OGTT.

In conclusion, our study demonstrates that a pathological 100 g OGTT at term pregnancy was unable to identify women at risk for obstetric complications related to impaired glucose metabolism. Moreover, the results of this test may contribute to decisions about CD that is not necessarily justified. Other methods, such as daily glucose monitoring, might be of value and should be considered when possible. Of note, the rates found for some of the complications (macrosomia, SD) were higher than expected in the general pregnant population, suggesting that the suspicion of the attending physician might have been justified, and those women have an inherent risk that should be taken into considerations while advising labor management regardless of the OGTT result. More studies are needed to establish a better diagnostic tool for impaired glucose metabolism at term and to assess its implication on mothers and newborns.

Footnotes

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Ethical approval

The local Institutional Review Board approved the study protocol and the use of demographical and clinical data for research purposes.

Guarantor

EV is the guarantor of the present work.

Contributorship

OB and EV researched literature and conceived the study. OB was involved in gaining ethical approval. All authors were involved in protocol development. EV, TW, and OB were involved in data analysis. OB wrote the first draft of the manuscript. All authors reviewed and edited the manuscript and approved the final version of the manuscript

ORCID iD

Oren Barak

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