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. 2023 Oct 21;15(2):187–193. doi: 10.1007/s13340-023-00666-6

Risk factors of late-onset gestational diabetes diagnosed during 24–28 weeks of gestation after normal early screening: a case–control study

Dittakarn Boriboonhirunsarn 1,, Kwanjutha Jetsadakraisorn 1
PMCID: PMC10959907  PMID: 38524937

Abstract

Objective

To determine the risk factors associated with late-onset GDM (diagnosed between 24 and 28 weeks of gestation) after normal early screening.

Methods

A case–control study was conducted in 600 singleton pregnant women who started antenatal care before 20 weeks with normal early GDM screening. Repeat screening was performed at 24–28 weeks. Cases were 120 women with late-onset GDM and 480 controls were those without GDM. Risk factors for late-onset GDM were evaluated and pregnancy outcomes were compared.

Results

Cases were significantly older, and more likely to be overweight or obese. 50-g GCT of ≥ 160 mg/dL and abnormal 1 value of 100-g OGTT significantly increased the risk of late-onset GDM (p = 0.004 and < 0.001 respectively). Independent risk factors were abnormal 1 value of 100-g OGTT from first screening (adjusted OR 5.49, 95% CI 2.70–11.17, p < 0.001), age ≥ 30 years (adjusted OR 2.71, 95% CI 1.66–4.43, p < 0.001), DM in family (adjusted OR 1.76, 95% CI 1.07–2.88, p = 0.025), and BMI ≥ 25 kg/m2 (adjusted OR 1.86, 95% CI 1.17–2.97, p = 0.009). Late-onset GDM significantly increased the risk of preeclampsia, cesarean delivery, LGA, and macrosomia.

Conclusion

Independent factors associated with late-onset GDM included abnormal 1 value of 100-g OGTT from first screening, age ≥ 30 years, DM in family, and being overweight or obese.

Keywords: Gestational diabetes, Late-onset, Risk factors, Pregnancy outcomes

Introduction

Gestational diabetes mellitus (GDM) is a common condition in which glucose intolerance occurs during pregnancy [13]. GDM is associated with an increase in various maternal morbidities such as cesarean deliveries, shoulder dystocia, preeclampsia, and the subsequent development of type 2 DM. Perinatal and neonatal morbidities such as large for gestational age (LGA), macrosomia, hypoglycemia, polycythemia, and hyperbilirubinemia are also increased. Long-term sequelae in offspring with in utero exposure to maternal hyperglycemia may include higher risks for obesity and diabetes later in life [13].

GDM has been reported to be on the rise globally [3]. A similar trend has also been observed in Thailand. In a large university hospital in Thailand, reported GDM prevalence was 10.2% in 2004 [4], 14.1% in 2015 [5], and 13.8% from the most recent data in 2018 [6, 7]. Although the majority of GDM could be diagnosed early in pregnancy (early-onset GDM), there were still a considerable number of GDM cases that were diagnosed during 24–28 weeks of gestation (late-onset GDM) [4, 7]. The reported incidence of late-onset GDM varied between studies from 5 to 15% of those with normal initial tests [4, 7, 8]. These previous reports on late-onset GDM were based on risk-based screening approach, but an early universal GDM screening protocol is currently adopted according to institutional policy and guideline and late-onset GDM has been observed in approximately 6% after normal early screening [9].

Increase in adverse pregnancy outcomes among early-onset GDM has been described in many previous studies, including LGA, macrosomia, cesarean delivery, and preeclampsia. However, such adverse outcomes were also increased among late-onset GDM compared to those without GDM [7, 1015].

Several factors have been reported to increase the risk of late-onset GDM, including family history of DM, previous GDM, high pre-pregnancy BMI, advanced maternal age, and gestational weight gain [4, 7, 8, 10, 16]. In addition, abnormalities of initial test results have also been reported to be associate dwith the risk of late-onset GDM, including abnormal 50-g glucose challenge test (GCT) or one abnormal value of 100-g oral glucose tolerance test (OGTT) of early screening [8, 16]. A previous study showed that the 1-h value of 100-g OGTT was the best predictor of late-onset GDM [17]. However, the results varied between studies.

The primary aim of this study was to determine the risk factors associated with late-onset GDM in a large university hospital in Thailand. In addition, pregnancy outcomes were compared between those with and without late-onset GDM. The results of this study could help in the better identification of women at higher risk of developing GDM after normal initial test results and could lead to possible preventive measures to minimize the risk of GDM and related complications.

Materials and methods

After approval from Siriraj Institutional Review Board (SIRB, COA no. Si 131/2022; approval date February 25, 2022), a case–control study was conducted at the Department of Obstetrics and Gynecology, Faculty of Medicine Siriraj Hospital. Siriraj Hospital is the largest university-based tertiary care hospital in Thailand with approximately 7000 deliveries each year. Informed consent was not obtained since the data was collected retrospectively from medical records.

According to the current institutional guideline [9], GDM screening is offered to all pregnant women as early universal screening, using a 2-step approach. A 50-g glucose challenge test (GCT) is used as a screening test with a 140 mg/dL cutoff and a 100-g oral glucose tolerance test (OGTT) is used as a diagnostic test using Carpenter and Coustan criteria. The tests are offered at first antenatal care visit and repeated during 24–28 weeks of gestation if the first test results are normal. Pregnant women who were diagnosed with GDM were offered nutritional and behavioral counseling. A fasting plasma glucose and/or 2-h postprandial plasma glucose were used for follow up and evaluation of glycemic control. According to institutional guideline, HbA1c was not evaluated in the screening, diagnosis, and management of GDM. Insulin therapy was initiated as necessary. Labor and delivery care were provided according to institutional guideline by on-duty residents under staff supervision.

Inclusion criteria were singleton pregnant women who started antenatal care before 20 weeks of gestation with normal results from their first GDM screening, according to institutional guideline. Pregnant women who received GDM screening by different approaches, had pre-pregnancy DM, and those with fetal anomalies or fetal death were excluded. With an estimated rate of abnormal initial 50-g GCT results of 40% among women without GDM and 55% among those with late-onset GDM, at least 107 cases and 428 controls (1:4 ratio) were required to achieve 80% power.

Retrospective data collection was made from women attending antenatal care clinic during 2020–2021, after the implementation of early universal GDM screening. Cases were 120 women diagnosed with GDM during 24–28 weeks after normal initial screening (late-onset GDM) and controls were 480 women without GDM from both screenings. For each case, 4 controls were randomly selected from women without GDM who attended antenatal care clinic during the same period as cases.

Medical records of included women were reviewed and data were extracted. Data collection included baseline and obstetric characteristics, antenatal care data, GDM risk factors, results of GDM screening, GDM treatment, and pregnancy outcomes. Pre-pregnancy body mass index (BMI) and appropriateness of gestational weight gain were assessed according to the Institute of Medicine recommendation [18].

Descriptive statistics, including mean, standard deviation, number, and percentage were used to describe various characteristics as appropriate. Student t-test and Chi-square test or Fisher’s Exact test were used to compare various characteristics between cases and controls. Logistic regression analysis was used to determine independent associated factors for GDM diagnosed during 24–28 weeks after normal first screening results, adjusted for potential confounders. Adjusted odds rations (OR) and 95% confidence intervals (CI) were estimated. A p-value of < 0.05 was considered statistically significant. All analyses were performed using IBM SPSS Statistics for Windows®, Version 21.0. Armonk, NY: IBM Corp.

Results

A total of 600 pregnant women were included. Cases were 120 pregnant women with GDM diagnosed during 24–28 weeks of gestation after normal first screening. The other 480 pregnant women without GDM after 2 screenings were served as control group. Baseline characteristics between the 2 groups are shown in Table 1. Compared with control group, cases were significantly older (33.6 vs. 30.4 years, p < 0.001) and had higher BMI (24.4 vs. 22.4 kg/m2, p < 0.001). They were also significantly more likely to be overweight or obese (35.8% vs. 20.6%, OR = 1.8, p = 0.006) and less likely to be underweight (5.8% vs. 17.5%, OR = 0.3, p = 0.009). Regarding GDM risks, cases were significantly more likely to have age ≥ 30 years (78.3% vs. 52.7%, OR = 3.2, p < 0.001), family history of DM (29.2% vs. 16.9%, OR = 2.0, p = 0.002), and BMI ≥ 25 kg/m2 (35.8% vs. 20.6%, OR = 2.1, p = 0.001).

Table 1.

Baseline characteristics between the 2 groups

Characteristics Controls N = 480 Cases N = 120 OR (95% CI) p-value
Mean age ± SD (years) 30.4 ± 5.9 33.6 ± 5.4 NA  < 0.001
Mean BMI ± SD (kg/m2) 22.4 ± 4.4 24.4 ± 4.6 NA  < 0.001
N (%) N (%)
Nulliparous 228 (47.5) 59 (49.2) 1.1 (0.7–1.6) 0.744
BMI category  < 0.001
 Normal (18.5–24.9 kg/m2) 297 (61.9) 70 (58.3) 1.0
 Underweight (< 18.5 kg/m2) 84 (17.5) 7 (5.8) 0.3 (0.2–0.8) 0.009
 Overweight or obese (25–29.9 or ≥ 30 kg/m2) 99 (20.6) 43 (35.8) 1.8 (1.2–2.9) 0.006
GDM risks
 Age ≥ 30 years 253 (52.7) 94 (78.3) 3.2 (2.0- 5.2)  < 0.001
 DM in family 81 (16.9) 35 (29.2) 2.0 (1.3–3.2) 0.002
 BMI ≥ 25 kg/m2 99 (20.6) 43 (35.8) 2.1 (1.4–3.3) 0.001
 Previous GDM 1 (0.2) 1 (0.8) 4.0 (0.3–64.8) 0.360a
 Previous macrosomia 0 (0) 1 (0.8) NA 0.200a

SD = standard deviation, BMI = body mass index, GDM = gestational diabetes, DM = diabetes mellitus, NA = not available

aFisher exact test

Table 2 shows the results of GDM tests between the 2 groups. Mean GA at first screening was comparable. Mean 50-g GCT value and all of 100-g OGTT values were significantly higher in cases than controls (p < 0.05). Those with 50-g GCT of ≥ 160 mg/dL (OR 1.9, p = 0.004) and abnormal 1 value of 100-g OGTT significantly increased the risk of GDM during 24–28 weeks of gestation (OR = 6.7, p < 0.001). For second screening, mean 50-g GCT value and all of 100-g OGTT values were also significantly higher in cases than controls (p < 0.001). Total and weekly weight gain from first to second screening were comparable between the 2 groups. Further analysis also showed that those with abnormal 1 value of 100-g OGTT were more likely to be overweight or obese and had high GCT values at both initial and repeat screening than the others. On the other hand, cases and controls with abnormal 1 value of 100-g OGTT were comparable with regard to many characteristics, including age (35.2 ± 4.8 vs. 33.2 ± 6.7 years, p = 0.093), BMI (25.7 ± 5.6 vs. 24.0 ± 5.7 kg/m2, p = 0.325), rates of overweight and obesity (42.3% vs. 31.6%, p = 0.463), and GCT results (168.4 ± 6.2 vs. 174.4 ± 13.7 mg/dL, p = 0.199). 

Table 2.

Results of GDM tests between the two groups

GDM test results Controls N = 480 Cases N = 120 OR (95% CI) p value
First screening
Mean GA at screening ± SD (weeks) 9.5 ± 3.61 9.4 ± 3.45 NA 0.905
Mean 50-g GCT value ± SD (mg/dL) 138.4 ± 30.7 150.4 ± 28.1 NA  < 0.001
Mean 100-g OGTT value ± SD (mg/dL)
 Fasting 77.2 ± 7.2 79.3 ± 6.2 NA 0.027
 1-h 134.7 ± 28.4 160.4 ± 26.3 NA  < 0.001
 2-h 111.5 ± 21.8 136.4 ± 23.7 NA  < 0.001
 3-h 96.6 ± 18.8 108.2 ± 21.5 NA  < 0.001
50-g GCT level 0.015
  < 140 mg/dL 245 (51%) 46 (38.3%) 1.0
 140–159 mg/dL 94 (19.6%) 23 (19.2%) 1.3 (0.8–2.3) 0.348
 ≥ 160 mg/dL 141 (29.4%) 51 (42.5%) 1.9 (1.3–3.0) 0.004
Abnormal 1 value of 100-g OGTT 19 (4.0%) 26 (21.7%) 6.7 (3.6–12.6)  < 0.001
Second screening
Mean GA at screening ± SD (weeks) 25.8 ± 1.6 26.4 ± 1.7 NA  < 0.001
Mean 50-g GCT value ± SD (mg/dL) 122.9 ± 25.7 172.5 ± 21.5 NA  < 0.001
Mean 100-g OGTT value ± SD (mg/dL)
 Fasting 75.9 ± 6.9 81.5 ± 10.7 NA  < 0.001
 1-h 156.3 ± 21.5 191.8 ± 19.3 NA  < 0.001
 2-h 124.6 ± 18.9 173.4 ± 22.3 NA  < 0.001
 3-h 108.1 ± 20.3 135.9 ± 26.7 NA  < 0.001
Mean weight gain from first screening ± SD (kg) 6.8 ± 3.4 6.7 ± 4.0 NA 0.286
Weekly weight gain from first screening ± SD (kg) 0.4 ± 0.2 0.4 ± 0.2 NA 0.720

GDM = gestational diabetes, SD = standard deviation, GA = gestational age, GCT = glucose challenge test, OGTT = oral glucose tolerance test, NA = not available

Pregnancy and neonatal outcomes between groups were compared and the results are shown in Table 3. Only 4.2% of late-onset GDM women needed insulin therapy. Mean gestational weight gain and GA at delivery were significantly lower among cases than those of controls (13.0 vs. 14.3 kg, p = 0.017 and 38.0 vs. 38.3 weeks, p = 0.043, respectively). However, there is no clinical significance in terms of GA at delivery and rate of preterm birth and excessive weight gain were comparable. Cases were significantly more likely to have primary cesarean section than controls (36.7% vs. 23.3%, p = 0.003). Significant higher rate of preeclampsia was also observed among cases (10.8% vs 5%, p = 0.018).

Table 3.

Comparison of pregnancy outcomes between the two groups

Outcomes Controls N = 480 Cases N = 120 p value
Maternal outcomes
Insulin requirement 5 (4.2%)
Mean GWG ± SD (kg) 14.3 ± 5.2 13.0 ± 4.8 0.017
GWG category
 Normal 184 (38.3%) 41 (34.2%) 0.218
 Inadequate 104 (21.7%) 35 (29.2%)
 Excessive 192 (40.0%) 44 (36.7%)
Mean GA at delivery ± SD (weeks) 38.3 ± 1.3 38.0 ± 1.7 0.043
Preterm birth 38 (7.9%) 14 (11.7%) 0.192
Route of delivery
 Vaginal delivery 282 (58.8%) 51 (42.5%) 0.003
 Primary C/S 112 (23.3%) 44 (36.7%)
 Repeat C/S 86 (17.9%) 25 (20.8%)
Preeclampsia 24 (5.0%) 13 (10.8%) 0.018
Neonatal outcomes
Mean birth weight ± SD (g) 3058.5 ± 424.7 3194.9 ± 514.8 0.003
Birth weight for GA
 AGA 385 (80.2%) 87 (72.5%) 0.003
 SGA 31 (6.5%) 3 (2.5%)
 LGA 64 (13.3%) 30 (25.0%)
Macrosomia 7 (1.5%) 6 (5%) 0.029
Apgar < 7 at 1 min 14 (2.9%) 4 (3.3%) 0.768
Apgar < 7 at 5 min 0 (0%) 1 (0.8%) 0.200
Neonatal hypoglycemia 1 (0.2%) 4 (3.3%) 0.006
Phototherapy 27 (5.6%) 19 (15.8%)  < 0.001
NICU admission 8 (1.7%) 4 (3.3%) 0.270

SD = standard deviation, GWG = gestational weight gain, GA = gestational age, C/S = cesarean section, AGA = appropriate for gestational age, SGA = small for gestational age, LGA = large for gestational age

For neonatal outcomes, mean birth weight of infants born from GDM mothers were significantly higher than those of controls (3194.9 vs 3058.5 g, p = 0.003). However, rates of LGA and macrosomia were significantly higher among cases (25% vs. 13.3%, p = 0.003, and 5% vs. 1.5%, p = 0.029, respectively). Neonatal hypoglycemia and the need of phototherapy were also significantly higher among cases (3.3% vs 0.2%, p = 0.006, and 15.8% 5.6%, p < 0.001 respectively). Rates of birth asphyxia and NICU admission were comparable.

Logistic regression analysis was performed to determine independent associated factors for GDM diagnosed during 24–28 weeks after normal first screening and the results are shown in Table 4. Significant independent factors were abnormal 1 value of 100-g OGTT from first screening (adjusted OR 5.49, 95% CI 2.70–11.17, p < 0.001), age ≥ 30 years (adjusted OR 2.71, 95% CI 1.66–4.43, p < 0.001), family history of DM (adjusted OR 1.76, 95% CI 1.07–2.88, p = 0.025), and BMI ≥ 25 kg/m2 (adjusted OR 1.86, 95% CI 1.17–2.97, p = 0.009).

Table 4.

Logistic regression analysis to determine independent associated factors for late-onset GDM

Risk factors Adjusted OR 95% CI p value
GCT results at first screening
  < 140 mg/dL 1.0
 140–159 mg/dL 0.90 0.50–1.62 0.721
  ≥ 160 mg/dL 1.05 0.63–1.76 0.861
Abnormal 1 value of 100 g OGTT from first screening 5.49 2.70–11.17  < 0.001
Age ≥ 30 years 2.71 1.66–4.43  < 0.001
DM in family 1.76 1.07–2.88 0.025
BMI ≥ 25 kg/m2 1.86 1.17–2.97 0.009

GDM = gestational diabetes, GCT = glucose challenge test, OGTT = oral glucose tolerance test, DM = diabetes mellitus, BMI = body mass index

Discussion

Pregnancy induces complex interactions of hormones and metabolic mediators that create insulin resistance and modify maternal carbohydrate, lipid, and amino acid metabolism to ensure adequate nutrient supply to the fetus. Insulin resistance continues to increase as pregnancy advances and is well established by the 24th week of gestation [3]. A 50–60% decrease in insulin sensitivity is seen with advancing gestation both in women with normal glucose tolerance and in women with GDM [19, 20]. Therefore, screening for GDM is usually recommended to perform at 24–28 weeks of gestation. However, it is recommended that GDM should also be screened early in pregnancy among high-risk women and settings with high GDM prevalence [13].

The need for repeat GDM screening after normal results early in pregnancy was emphasized by the results of many previous studies. An increasing trend of late-onset GDM has been observed from previous studies in our institution, where the incidence was 4.9% in 2004, [4] 7% in 2008, [21] and 15% in 2016, [8] and a recent study in another institute reported a prevalence of 17.8% [22]. These were based on a risk-based screening approach. According to the current early universal screening, the prevalence of late-onset GDM was 6% (7.5% among high-risk women and 3.1% among low-risk women) [9]. Understanding associated risk factors for late-onset GDM could help raise awareness on repeat GDM screening during 24–28 weeks of gestation as well as minimize related adverse pregnancy outcomes in this specific high-risk group.

The results of this study showed that independent risk for developing late-onset GDM included abnormal 1 value of OGTT from first screening, age ≥ 30 years, family history of DM, and BMI ≥ 25 kg/m2. Many studies have reported that the risk of late-onset GDM increases with degree of abnormalities in initial screening, especially abnormal 1 value of OGTT [8, 16, 21, 22]. A recent Thai study reported an incidence of late-onset GDM of 18.8%, 8.3%, and 41.4% in women with normal 50-g GCT, abnormal 50-g GCT, and abnormal 1 value of OGTT from initial test, respectively [22]. Similar results were observed in this study as well, and multivariate analysis showed that abnormal 1 value of OGTT was the strongest independent factor for late-onset GDM with adjusted OR of 5.49. Further analysis showed that these women were at higher risk for GDM as they were more likely to be overweight or obese and had higher screening GCT values. Pregnant women with 1 abnormal value of OGTT early in pregnancy might have some degree of carbohydrate intolerance and insulin resistance, but not high enough to develop GDM. As pregnancy progresses and insulin resistance increases, they are eventually diagnosed with GDM through repeat screening.

Maternal factors associated with late-onset GDM have also been reported, including maternal age of ≥ 30 or 35 years, family history of DM, BMI of ≥ 25 or 30 kg/m2, and previous GDM [4, 7, 10, 15]. This was similar to what was observed in this study that maternal age ≥ 30 years, family history of DM, and BMI ≥ 25 kg/m2 independently increased the risk of late-onset GDM. It is possible that these maternal factors are also related to preexisting insulin resistance, making them more susceptible to developing GDM [3].

Similar risk factors are also consistently reported in the literature, but they are used for GDM routinely screened by different strategies but not early universal screening. The results of this study are among a few, if any, that use the early universal GDM screening scheme. In addition, the risk factors are to be specifically applied to those with normal initial screening, which could make both the women and caring physicians aware of the risk of GDM later in pregnancy and could also lead to risk reduction strategies for these women. It can also be implied and confirmed that these risk factors have a strong correlation with the development of GDM at any stage of pregnancy.

Weight gain during pregnancy has been reported to be associated with GDM [2325]. A meta-analysis showed that excessive gestational weight gain prior to GDM screening has been associated with GDM, regardless of BMI status [24]. In terms of late-onset GDM, a previous study reported that women with late-onset GDM had significantly greater second trimester weight gain [8] and another study reported that second trimester weight gain of > 7 kg was a significant associated factor [16]. However, although gestational weight gain was significantly lower in women with late-GDM but weekly weight gain and rates of excessive weight gain were comparable between the 2 groups in this study.

In terms of pregnancy outcomes, early-onset GDM has been commonly reported to result in worse pregnancy outcomes than late-onset GDM, including LGA, macrosomia, and preeclampsia [7, 1015]. Since women diagnosed with early-onset GDM were not included in this study, the differences in pregnancy outcomes between the 2 groups should be further evaluated in the future. Nonetheless, GDM-related complications have been reported to increase in women with late-onset GDM compared to those without GDM [7, 8, 15]. Similar results were also observed that late-onset GDM increased the risk of preeclampsia, cesarean delivery, LGA, and macrosomia compared to those without GDM. On the other hand, a recent study in Thailand reported similar outcomes between normal pregnant women and late-onset GDM regarding birth weight and macrosomia [22]. Awareness should be raised regarding this issue in the management of late-onset GDM. Whether early management of women at higher risk for late-onset GDM would result in better pregnancy outcomes is not well established, and its benefits need further evaluation in the future.

Different results between studies might be due to differences in population, baseline GDM risks, screening protocols and strategies. The results showed that only less than 1% had previous GDM, and insulin requirement was only 4.2% in late-GDM cases. These rates were relatively lower than those previously reported in other populations [1, 2]. However, the results were in line with previous publications from the same institute [9, 26]. It is also possible that women with higher risk were already diagnosed with GDM early in pregnancy that were not included in the current study. This might be a characteristic of our population that limited the generalization of the results. There are also variations in the management scheme that might preclude valid comparisons of pregnancy outcomes. As GDM screening strategies are still controversial and vary between settings, further larger study with a uniform GDM screening protocol should be considered to explore various related issues, specific for each setting.

Potential strengths of this study include that this is the first study on the risk of late-onset GDM from early universal GDM screening in Thailand. All included women received uniform GDM screening and diagnosis according to institutional guideline that there should not be misclassification between cases and controls. All tests were performed in a qualified laboratory, so the results are valid and reliable. However, there might be some limitations. Due to the retrospective nature of the study, some information might be less accurate or not available. There are also some unmeasurable issues that might affect and confound the results, such as compliance with nutritional counseling and management, lifestyle modifications, etc. However, this should not significantly affect the results.

In conclusion, significant independent factors for the development of late-onset GDM from early universal GDM screening were abnormal 1 value of 100 g OGTT from the first screening, age ≥ 30 years, family history of DM, and BMI ≥ 25 kg/m2. Late-onset GDM also increased the risk of adverse pregnancy outcomes compared to those without GDM. Awareness should be raised among caring physicians about these at-risk pregnant women, although they had normal initial test results. Strategies to minimize the risk of late-onset GDM should be further explored, which might include nutritional and medical management, lifestyle modifications, and weight gain control, as well as effects on maternal and neonatal outcomes.

Author contributions

All authors contributed to the study conception and design. All authors contributed to the study conception and design. KJ was responsible for data collection under supervision of DB. DB analyzed the data and both DB and KJ interpreted the results together. KJ drafted the manuscript and DB critically revised the manuscript. All the authors approved and agreed with this final version of the manuscript.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Declarations

Conflict of interest

None.

Ethical approval

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and/or with the Helsinki Declaration of 1964 and later versions. Informed consent or substitute for it was obtained from all patients for being included in the study.

Research involving human participants and/or animals

The study was approved by Siriraj Institutional Review Board (COA no. Si 131/2022; approval date February, 25 2022).

Informed consent

Informed consent was not obtained from the participants due to retrospective nature of data collection.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.


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