Abstract
Objective
Heterogenous results were reported in the effects of hypoglycemia in pregnancy. This study evaluated pregnancy outcomes in women with hypoglycemia during the antenatal 75-gram oral glucose tolerance test (OGTT).
Methods
OGTT results of the mothers of all live-born delivered in a tertiary obstetrics centre were evaluated between Jan 2021 and June 2022. All patients had OGTT at 26-30th weeks of gestation. Hypoglycemia was defined as any low plasma glucose ≤ 3.5mmol/L on OGTT. Maternal and neonatal outcomes were compared among the four groups; normal results (group 1), hypoglycemia in OGTT (group 2), gestational diabetes mellitus (GDM) (group 3) and pregestational diabetes mellitus (DM) (group 4).
Results
There were 3715 women delivered within the study period and 3164 (85.2%) had normal results. 65 (1.7%) women had hypoglycemia, 464 (12.5%) women had GDM and 22 (0.6%) women had pregestational DM. None of the Group 2 patients were symptomatic. Maternal demographics were comparable. Patients with hypoglycemia during OGTT were not at an increased risk of preterm delivery (1.5% vs. 2.8%, p = 0.86). There was no statistical difference in the incidence of Caesarean Sect. (32.3% vs. 34.4%, p = 0.54), postpartum haemorrhage (10.8% vs. 14.7% p = 0.28). Women with hypoglycemia during OGTT were not at risk of adverse outcome in terms of neonatal intensive care unit admission (16.9% vs. 8.5%, p = 0.28) and Apgar score at 5th minute of life (9.8 vs. 9.8, p = 0.17).
Conclusion
Hypoglycemia in antenatal OGTT is not associated with adverse neonatal or maternal outcomes. It is likely to resolve after delivery.
Keywords: Diabetes mellitus, Oral glucose tolerance test, Postpartum hemorrhage
Background
Gestational diabetes mellitus is a common obstetric complication that affects both the mother and the baby. A 75-g oral glucose tolerance test (OGTT) is the accepted method for diagnosing GDM during pregnancy [1, 2]. The global prevalence of hyperglycemia in pregnancy is estimated at 17%, with variations from 10% in North America to 25% in Southeast Asia [3]. The Hyperglycemia and Adverse Pregnancy Outcomes study published in 2008 [4] prospectively examined 23,316 women using the 75-g oral glucose tolerance test (OGTT). From this study, the diagnostic criteria for GDM were defined as fasting blood glucose ≥ 5.1 mmol/L, 1-hour glucose test ≥ 10 mmol/L, and/or 2-hour glucose test ≥ 8.5 mmol/L.
In addition to the detection of hyperglycemia, some women experienced symptoms of hypoglycemia during the test, including tachycardia, dizziness, nausea, and sweating. The classical Whipple’s triad is established when all three features are fulfilled; these include symptoms of hypoglycemia, low plasma glucose concentration, and symptom resolution after the plasma glucose concentration is increased. Reactive hypoglycemia is defined as symptomatic hypoglycemia after glucose loading, which may represent abnormal glucose metabolism, and is postulated to affect pregnancy outcomes and interfere with fetal growth [5, 6].
Inconsistent results have been reported in studies evaluating the effect of hypoglycemia on OGTT performed during pregnancy. While one study demonstrated no differences in neonatal outcomes [7], another study reported lower birth weights and Apgar scores for neonates in the reactive hypoglycemia group [8]. More recent studies have demonstrated that hypoglycemia in OGTT is not associated with adverse maternal or neonatal outcomes [9]. Although hypoglycemia is consistently defined as a glucose level < 3.5 mmol/L, variations in populations and study designs may account for these inconsistent results. Delibas et al. [7] evaluated pregnant women undergoing a 100 g OGTT, while Yuen et al. [8] and Raviv et al. [9] focused on those with a 75 g OGTT. Additionally, ethnic differences in the prevalence of GDM and hypoglycemia have been noted, with studies indicating that Asian populations may have different insulin responses compared to Caucasians [10, 11] Given this conflicting data, we conducted a retrospective analysis to examine the impact of hypoglycemia during OGTT in our local population.
Methods
This was a retrospective single-center cohort review for women who had 75 g OGTT performed antenatally and delivered from January 2021 to June 2022. at Queen Mary Hospital in Hong Kong. The centre adopted routine universal screening for gestational diabetes by OGTT at 26-30th weeks of gestation. Women with risk factors underwent an additional early OGTT between booking and 18 weeks of gestation. These risk factors included multiple pregnancies, previous babies with a birth weight > 4 kg, family history of diabetes mellitus (DM), maternal obesity, polycystic ovary syndrome, maternal age > 35 years, previous unexplained stillbirth, and previous abnormal babies not related to known chromosomal or genetic abnormalities. Women who underwent OGTT at our center but had no pregnancy outcomes were excluded. Common reasons included pregnancy termination, stillbirth, and delivery in the private sector.
Computerized records and case notes were reviewed, and all OGTT results were retrieved and analysed. Power calculations are not conducted in this retrospective cohort study because the sample size is determined by existing data. Maternal outcomes such as mode of delivery, presence of postpartum hemorrhage, and neonatal outcomes such as APGAR scores, birth weight were reviewed. All patients who were scheduled to have OGTT had the same instructions on fasting. They were advised to fast from midnight of the day of OGTT. The start time for OGTT was 8 a.m. for all groups. Hypoglycemia during OGTT was defined as any low plasma glucose </= 3.5 mmol/L on OGTT [12]. Gestational diabetes (GDM) was defined according to World Health Organization criteria in 2013, i.e. fasting plasma glucose 5.1–6.9 mmol/L and 2-hour plasma glucose 8.5–11.0 mmol/L. The 1-hour plasma glucose level was not checked according to local practice. Women with known DM before pregnancy, incomplete OGTT data, or incomplete delivery outcome data were excluded. Maternal characteristics and neonatal outcomes were compared among the four groups: normal results (group 1), hypoglycemia in OGTT (group 2) and GDM (group 3) and pregestational diabetes mellitus (DM) (group 4).
Women with normal results (group 1) were given reassurance and received routine antenatal care. Women with hypoglycemia in the OGTT (group 2) were contacted and asked if they had completed the 75 g-glucose drink, experienced vomiting after the drink, or developed symptoms of hypoglycemia during the OGTT. Those who did not complete the test or experienced vomiting were asked to repeat the test. Those who developed symptoms of hypoglycemia were also asked if there was resolution of symptoms or signs when hypoglycemia was corrected, which also established Whipple’s triad. If this was confirmed, the patient was admitted for inpatient consultation with an endocrinologist. If Whipple’s triad was not established, we would arrange a postnatal OGTT 6–8 weeks after the estimated date of confinement. If hypoglycemia persisted in the postnatal OGTT, the woman was referred to the endocrinology clinic for further management.
GDM is diagnosed in women with any abnormal serum glucose value at OGTT. Women with GDM (group 3) were referred for counselling by a dietician and diabetic nurses. They were also advised to start self-monitoring of their blood glucose levels and practice dietary control. Pharmacological treatment was offered to those who could not achieve satisfactory blood glucose levels with dietary control. Women with pregestational DM (group 4) would be jointly managed by obstetricians and endocrinologists for screening for diabetic complications, review of glucose monitoring, medication adjustment and insulin titration.
Statistical analysis was performed using SPSS version 25.0 statistical software; p < 0.05 was considered statistically significant. Data were analysed using the Student’s t-test for normally distributed continuous variables and the chi-square test for categorical variables. Comparisons between groups were performed using one-way ANOVA. This study was approved by the Institutional Review Board of The University of Hong Kong/Hospital Authority Hong Kong West Cluster. (No: UW 23–644).
Results
A total of 4458 patients had OGTT tests within the 18-month study period. 3715 women with OGTT results and pregnancy outcome data were identified. Two women with hypoglycemia in the OGTT were symptomatic and both were admitted for endocrinologist consultation. Pregnancy outcome data were not available as both delivered in private hospitals. 743 women were excluded from the analysis because their pregnancy outcome data were not available. Their demographic data were similar to the 3715 women included in our analysis. 123 women had hypoglycemia during OGTT, 65 of them had delivery outcomes available. The prevalence of hypoglycemia during OGTT was 2.75%. The maternal characteristics stratified by OGTT results are presented in Table 1. 3164 (85.2%) patients had normal OGTT results. 65 (1.7%) women had hypoglycemia during the OGTT, 464 (12.5%) were diagnosed with gestational diabetes, and 22 (0.6%) had DM in pregnancy. Maternal demographics, including age and parity were similar between groups.
Table 1.
Maternal demographic stratified by study groups
| OGTT results | Group 1 Normal (n = 3164) |
Group 2 Hypoglycemia (n = 65) |
Group 3 Gestational Diabetes (n = 464) |
Group 4 DM in pregnancy (n = 22) |
P value |
|---|---|---|---|---|---|
|
Maternal age (Years) (Mean, SD) |
33.4 (4.4) | 33.7 (4.6) | 35. (4.0) | 33.8 (6.0) | 0.95 |
|
Chinese (n = 2989) |
2537 (84.9%) | 38 (1.3%) | 401 (13.4%) | 13 (0.4%) | < 0.01 |
|
Caucasian (n = 321) |
281 (87.5%) | 16 (5.0%) | 20 (6.3%) | 4 (1.2%) | < 0.01 |
|
Other ethnicity (n = 405) |
346 (85.5%) | 11 (2.7%) | 43 (10.6%) | 5 (1.2%) | 0.04 |
| Singleton | 2994 (94.6%) | 62 (95.4%) | 439 (94.6%) | 18 (81.8%) | 0.08 |
| Multiple pregnancy | 170 (5.4%) | 3 (4.6%) | 25 (5.4%) | 4 (18.2%) | 0.08 |
| Nulliparity | 1755 (55.5%) | 36 (55.4%) | 210 (45.3%) | 11 (50.0%) | 0.40 |
| Multiparity | 1409 (44.5%) | 29 (44.6%) | 254 (54.7%) | 11 (50.0%) | 0.40 |
More Caucasian mothers ( n = 16, 11.8% of all Caucasian mothers, p < 0.01) were found to have hypoglycemia than mothers of Chinese origin (n = 38, 1.3% of all Chinese mothers) or other ethnicities ( n = 11, 9.38% of all mothers of other ethnicities).
Maternal outcomes are listed in Table 2. The mean gestation at delivery was 38 weeks in groups 1, 3, and 4. Women in group 2 (hypoglycemia) delivered their babies at 39 weeks, but no statistical difference was observed when compared to the other groups (P = 0.29).
Table 2.
Maternal outcome stratified by study groups
| OGTT results | Group 1 Normal (n = 3164) |
Group 2 Hypoglycemia (n = 65) |
Group 3 Gestational Diabetes (n = 464) |
Group 4 DM in pregnancy (n = 22) |
P value |
|---|---|---|---|---|---|
| Induction of labour | 1285 (40.6%) | 30 (46.2%) | 190 (40.9%) | 8 (36.4%) | 0.81 |
| Gestational week at delivery | 38 (2.2) | 39 (1.4) | 38 (1.9) | 38 (0.9) | 0.29 |
| Preterm labour | 90 (2.8%) | 1 (1.5%) | 14 (3.0%) | 1 (4.5%) | 0.86 |
| Caesarean delivery | 1088 (34.4%) | 21 (32.3%) | 185 (39.9%) | 10 (45.5%) | 0.65 |
| Normal vaginal delivery | 1753 (55.4%) | 40 (61.5%) | 248 (53.4%) | 11 (50%) | 0.54 |
| Assisted vaginal delivery | 323 (10.2%) | 4 (6.2%) | 31 (6.7%) | 1 (4.5%) | 0.82 |
| Blood loss at delivery (ml) (mean, SD) | 361(410) | 329 (234) | 377(309) | 461 (395) | 0.50 |
| Postpartum hemorrhage | 466 (14.7%) | 7 (10.8%) | 85 (18.3%) | 6 (27.3%) | 0.28 |
| Postnatal anaemia | 270 (8.5%) | 11 (16.9%) | 50 (10.8%) | 3 (13.6%) | 0.24 |
Hypoglycemia (group 2) at the 2 h after sugar load with range of 1.7–3.5 mmol/L and mean 3.02 +/- 0.46 mmol/L. The majority of women had reactive hypoglycemia at the 2 h after sugar load (n = 60). Five women had hypoglycemia at fasting glucose sampling. These women also had the highest rate of normal vaginal deliveries (61.5%), but the difference was not statistically significant ( p = 0.54). No statistically significant difference in postpartum hemorrhage incidence (P = 0.28) was observed. The incidence of Caesarean section and postnatal anemia was also similar among the four groups.
Table 3 presents neonatal outcomes. Differences in birth weight, low-birth-weight neonates, and those with macrosomia were observed, although the differences were not statistically significant. Nevertheless, hypoglycemia in the OGTT did not appear to show a significant difference with neonatal outcomes. Apgar score at 1st and 5th minute of life also showed no statistical difference (P = 0.64 and 0.17 respectively).
Table 3.
Neonatal outcome stratified by study groups
| OGTT results | Group 1 Normal (n = 3164) |
Group 2 Hypoglycemia (n = 65) |
Group 3 Gestational Diabetes (n = 464) |
Group 4 DM in pregnancy (n = 22) |
P value |
|---|---|---|---|---|---|
| Birth weight (Grams, SD) | 3045.6 (580.3) | 3039.5 (459.0) | 3067.3 (529.9) | 3179.8 (462.3) | 0.76 |
| Birth weight < 2500 g | 425 (13.4%) | 9 (13.8%) | 59 (12.7%) | 2 (9.1%) | 0.86 |
| Birth weight > 4000 g | 96 (3.0%) | 1 (1.5%) | 9 (1.9%) | 0 | 0.91 |
| Neonatal intensive care unit (NICU) admission | 8 (0.25%) | 0 | 4 (0.9%) | 1 (4.5%) | 0.28 |
| Apgar 1-min score (Mean, SD) | 8.6 (1.1) | 8.7 (1.0) | 8.6 (1.2) | 8.9 (0.7) | 0.64 |
| Apgar 5-min score (Mean, SD) | 9.8 (0.7) | 9.8 (0.6) | 9.8 (0.8) | 9.7(0.5) | 0.17 |
All 65 women with hypoglycemia (group 2) in the OGTT were invited to repeat the OGTT after delivery. None of them had established Whipple’s Triad. 21 (43.8%) completed the OGTT postnatally, and all results were normal. The remaining 44 women defaulted our OGTT tests after their deliveries.
Discussion
The pathophysiology of GDM is characterized by decreased insulin sensitivity and increased insulin secretion following sugar load [13–14]. Long-term complications such as type 2 diabetes, metabolic syndrome and cardiovascular disease [15–17] are associated with GDM in women and their offspring. Higher insulin secretion was found in women with GDM [18, 19]; thus, hypoglycemia during the OGTT may indicate an abnormal hyperinsulinemic reaction to sugar load. Our study evaluated the pregnancy outcomes of women with hypoglycemia during the OGTT in a tertiary hospital setting. The main findings of our study were as follows: 1)The prevalence of hypoglycemia during the OGTT in our cohort was 2.75% (123/4458). 2) Ethnic differences in the incidence of hypoglycemia during the OGTT and GDM were observed. There were more Caucasian women with hypoglycemia (5.0%) than Chinese women (1.3%). 3) Pregnancies with hypoglycemia during the OGTT were not associated with adverse maternal or neonatal outcomes.
The correct identification of women with Whipple’s triad is important. The Endocrine Society [20] only recommends evaluation in patients with an established Whipple’s triad to avoid unnecessary investigations. The prevalence of hypoglycemia during the OGTT in our cohort was 2.75%. Previously reported prevalence of reactive hypoglycemia ranges from 6.3 to 17.9% [21–23]. Comparisons between studies are limited by the variable cut-offs for hypoglycemia (between 2.8 and 5.0 mg/dl) following different sugar loads (75–100 g). None of these women had established Whipple’s triad, indicating they did not experience hypoglycemic symptoms. Hypoglycemia was not observed in those who completed postpartum OGTT at 6–8 weeks after delivery. Different prevalence and poor reproducibility of hypoglycemia during OGTT have been reported [21–24] due to heterogeneous definitions of hypoglycemia and the method of OGTT testing. Other biomarkers, such as HbA1C and fructosamine [25], should be considered in the workup for women with hypoglycemia during pregnancy.
The prevalence of GDM differs among ethnicities. Hong Kong has a predominantly Chinese population, but it is also home to various ethnic groups. Our tertiary centre offers universal OGTT screening which meant we included women from different ethnic groups, making our results more generalisable. It is known that Asia has a greater frequency of GDM than European nations [26–28]. Independent of age and BMI, Asians may be genetically predisposed to insulin resistance at a higher rate than Caucasians [29]. We found more Caucasian women with hypoglycemia than Chinese patients or women of other ethnicities (5.0% vs. 1.3% vs. 2.7%, p < 0.01). Although research on ethnic differences in reactive hypoglycemia is limited, some studies suggest that ethnicity can affect hypoglycemia risk in diabetic populations. One study highlighted that Black Caribbean individuals with type 2 diabetes faced a greater risk of experiencing hypoglycemia than their White British counterparts [30]. Future studies should consider these factors to provide a more comprehensive understanding of the condition.
Previous studies did not demonstrate a similar ethnic difference. GDM was more commonly diagnosed in Chinese women than in Caucasian women (13.4% vs. 6.2%, p < 0.01). This is consistent with studies that reported that Asians had higher rates of GDM than white counterparts [10]. Sub-group analysis according to different ethnic groups was performed. No statistically significant difference was found for same maternal and neonatal outcomes. Dietary patterns can significantly influence development of reactive hypoglycemia and GDM risk, and these patterns often vary across ethnicities. Fuller et al. [31] found that unhealthy diets were associated with increased odds of GDM in White European, Mediterranean, and Iranian women, but not consistently in Asian populations. This highlights the need for culturally appropriate dietary assessments and interventions for GDM patients.’
The relationship of low blood glucose levels and whether it alters pregnancy outcomes remains unclear. Studies reported that hypoglycemia during pregnancy is associated with adverse neonatal complications, such as low birth weight [21–23] and a higher incidence of neonatal intensive care unit (NICU) admission [32]. These studies were heterogenous with different cut-offs for hypoglycemia (between 2.5 and 5 mmol/L) following different sugar loads (75–100 g) were used. Postulated reason include maternal undernutrition affecting fetal development by limiting glucose availability to the fetus [24]. Given that our study cohort was situated in a developed city, it is improbable that any of our patients suffered from malnutrition.
More recent studies have suggested that hypoglycemia in the OGTT is not associated with adverse maternal or neonatal outcomes. In the largest sample of 2079 women in which 216 had hypoglycemia during OGTT [9], glucose status did not appear to affect the rates of macrosomia or low birth weight neonates after adjusting for confounders such as maternal age, BMI, and nulliparity. Another group studied the self-monitoring of blood glucose (SMBG) in women with hypoglycemia during the OGTT [8]. They found that women with low glucose levels on OGTT were more likely to have elevated glucose levels on SMBG, but no differences in delivery outcomes. In agreement with these studies, our cohort showed that hypoglycemia during OGTT was not associated with adverse maternal and neonatal outcomes. While maternal age and BMI may act as confounding variables in results interpretation, the definition of hypoglycemia remains consistent, thereby improving the generalizability of our study findings.
To the best of our knowledge, this is the first study in Southeast Asia on pregnant women with hypoglycemia during OGTT, where the prevalence of GDM is the highest. We were able to provide universal OGTT screening for all women at our center. Being a single-center study, we were also able to provide unified antenatal counselling, glucose monitoring, and treatment for the entire patient cohort.
Our study has some limitations, mainly due to its retrospective design. Despite the 18-month study period, the sample size of hypoglycemia in the OGTT was still low in this retrospective cohort. Nevertheless, women with asymptomatic hypoglycemia had pregnancy outcomes comparable to those in the other groups.
Conclusion
Hypoglycemia during OGTT in pregnancy is not associated with adverse neonatal or maternal outcomes in our study; however, the possibility of undetected differences due to limited sample size should be considered. Further long-term prospective studies with standardized glucose monitoring are necessary to determine whether hypoglycemia during OGTT is linked to GDM and its complications.
Author contributions
PWH designed the study. VWYN, MCL, WWKK, CKFW and PWH completed data collection. VWYN, MCL and PWH completed data analysis. VWYN drafted the manuscript. All revised the manuscript and contributed to its final version. All authors read and approved the final manuscript.
Funding
Not applicable.
Data availability
The raw data supporting the conclusions of this article will be made available by the authors on request.
Declarations
Ethics approval and consent to participate
The present study was approved by the Institutional Review Board of The University of Hong Kong/Hospital Authority Hong Kong West Cluster. Informed consent was waived by the same ethics board due to the retrospective nature of the study. No: UW 23–644 Date of approval: 8th January 2024.
Consent for publication
Not Applicable.
Competing interests
The authors declare no competing interests.
Approval date of registry and the registration no. of the study/trial
8th January 2024. (No: HKWC-2023-616).
Conflict of interest
The authors declare no conflict of interests for this article.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Data Availability Statement
The raw data supporting the conclusions of this article will be made available by the authors on request.