Abstract
Background
Antenatal identification of “at risk” fetuses is crucial for timely intervention to aid in achieving better perinatal outcomes. One such means is the use of Doppler for fetal hemodynamic monitoring. Using the same our study aimed to compare the utility of two Doppler parameters, Cerebroplacental ratio (CPR) and Umbilicocerebral ratio (UCR), in predicting adverse neonatal outcomes.
Methods
A total of 280 antenatal women participated in a prospective observational study following 28 weeks of gestation, and CPR and UCR (inverse of CPR) were determined by serial Doppler ultrasound. This was converted to gestational age-specific percentiles and Z-scores using Fetal Medicine Foundation (FMF) as a reference for CPR and study by Acharya et al. for UCR.
Results
Out of the 277 participants analyzed, abnormal Doppler parameters were present in 27 (9.7%) women. The abnormal Doppler group had a considerably greater occurrence of adverse outcomes, including Apgar score < 7 at 1 min, small for dates, neonatal hypoglycemia, requirement of ventilatory support, prolonged hospitalization, NICU (Neonatal intensive care unit) admission, and a composite of adverse outcomes. ROC (Receiver operating characteristic) curves exhibited an AUC (Area Under the Curve) of 0.76 for both CPR and UCR and a slightly higher AUC of 0.83 and 0.85 for their centiles and Z-scores, respectively.
Conclusion
Both CPR and UCR Doppler parameters are no different from each other in predicting adverse neonatal outcomes. The same holds true even on conversion to gestational age-specific centiles and Z-scores.
Keywords: Doppler ultrasonography, Cerebroplacental ratio, Umbilicocerebral ratio, Adverse neonatal outcomes
Introduction
Globally, in the year 2015, 2.6 million women encountered the death of their infants in the last trimester of pregnancy or during labor most of which were concentrated in middle- and low-income countries with a big chunk occurring as result of fetal growth restriction (FGR) [1]. Most of these could have been prevented with optimal care. Hence, an early diagnosis with close antenatal surveillance would aid in tailoring a better management thus improving the perinatal outcomes.
The use of Doppler ultrasonography as a repetitive and non-invasive tool to study the circulation in the fetus, placenta, and uterus in high-risk pregnancies has shown benefits. The CPR is a Doppler index that combines the effects of increased resistance in placental flow and changes in cerebral blood flow, which are shown as increased diastolic flow due to cerebrovascular dilatation brought on by hypoxia. It has become a significant predictor of adverse pregnancy outcomes. It has implications in the determination of fetal well-being not only in those detected as SGA (“Small for Gestational Age”) but also in AGA (“Appropriate for Gestational Age”) fetuses [2]. Recently, another Doppler parameter UCR from the secondary analysis of the TRUFFLE (“Trial of Randomized Umbilical and Fetal Flow in Europe”) was studied. In fetuses identified by early-onset growth limitation, UCR, which was computed by reversing the CPR, was proposed to be a superior predictor of survival of an infant without any neurological damage at age of two years [3].
Hence, the current study was undertaken to compare the Doppler ultrasonography parameters UCR and CPR in the prediction of unfavorable neonatal outcomes in all antenatal women presenting after 28 weeks of gestation using gestational age-specific values published by Fetal Medicine Foundation [4] and Acharya et al. [5] for CPR and UCR, respectively.
Materials and Methods
From August 2020 to May 2022, the Department of obstetrics and gynecology, and neonatology at AIIMS (All India Institute of Medical Sciences), Bhubaneswar carried out this prospective observational study. The Institute Ethics Committee’s (IEC/AIIMS BBSR/PG Thesis/2020–21/17) approval was obtained before the study. Prior to their enrollment, all individuals provided written informed consent.
All antenatal women aged 18–45 years with singleton pregnancy presenting beyond 28 weeks of gestation were included, excluding those diagnosed with any gross fetal congenital anomaly not compatible with life or known fetal chromosomal abnormality.
At the time of recruitment, a detailed history including the patient’s parity status, age, gestational age at presentation, obstetric score, and maternal patient profile was recorded. General physical examination with measurement of weight, height, BP (Blood Pressure) BMI (Body Mass Index), and obstetric examination was performed. Obstetric score assignment was done according to the history that was given by the patient. Gestational age was determined by recalling the LMP (Last Menstrual Period) date, and the results were validated with the first ultrasound, ideally performed during the first trimester of pregnancy. The diagnosis was made with clinical examination, history, baseline as well as biochemical parameters. Other relevant investigations as clinically indicated were also done.
The recruited women were subjected to Doppler ultrasonography with Mindray Ultrasound equipment (Strenzen, China, Mindray Bio-medical Electronics Co. Ltd), model no. 365 A and UMT-150 in the OPD and Labour ward of the Obstetrics and Gynaecology department. Doppler indices namely MCA PI (“Middle cerebral artery pulsatility index”) and UA PI (“Umbilical artery pulsatility index”) were obtained and UCR and CPR were computed. The cut-off centile for CPR and UCR were kept at 5 centile and 95 centile, respectively. Following this, the participants were followed up as per the protocol of the institute based on the ISUOG (“International Society of Ultrasound in Obstetrics and Gynaecology”) guidelines [6]. The last values of CPR and UCR obtained 1 week before delivery were used for analysis as per the gestational age and the two parameters were then compared and their role in the prediction of adverse neonatal outcomes was examined.
Neonatal outcomes which were studied involved size-for-date (as per the INTERGROWTH-21 chart), poor Apgar at one minute and five minutes of life, hypoglycemia (blood glucose value < 45 mg% and < 50 mg% in the infants of Diabetic mothers) as per neonatal-perinatal database (NNPD) working definitions [7], polycythemia (capillary hematocrit of more than 70 percent or venous hematocrit more than 65 percent after twenty four hrs of age), Neonatal asphyxia (Apgar < 7 at 1 min), neonatal sepsis (sepsis screen positive), neonatal acidosis (umbilical artery pH less than 7.0), requirement of ventilatory support, neonatal intensive care unit ( NICU) admission, prolonged hospital stay for neonatal indications (more than 7 days), neonatal death (during hospital stay).
Taking the AUC for CPR in predicting adverse neonatal outcomes as 0.7 (from previous studies) [8] and considering the AUC for UCR to be 0.8 and assuming the prevalance of adverse neonatal outcomes in patients with abnormal ultrasonographic findings as 20%, ratio of those with abnormal ultrasonographic features to those with normal ultrasonographic features to be 1:4 (taken from patients visiting gyanecology OPD and Labour Room where around 25% patients have abnormal ultrasound findings) with the confidence level of 95% and power of the study as 80%,the sample size calculated was 255 using the medcalc software. Assuming 10% lost to follow up, the corrected size of sample was 280.
Following data collection, IBM-SPSS (“Statistical Package for the Social Sciences”) version 23 was utilized for statistical analysis and Microsoft Excel 2019 was used for data entry. In descriptive statistics, percentages and frequency were employed for categorical data, and mean (± S.D.) was utilized for continuous variables. To compare groups of data having a continuous distribution, the independent sample ‘t’ test was employed. In case the data were not normally distributed, the Wilcoxon test had been employed. The chi-squared test had been utilized for group comparisons of categorical data. To maintain statistical significance, p-value of less than 0.05 was used. ROC curves were constructed, and utilizing the gestational age-specific Z-scores and centiles, prediction analysis of multiple outcomes was carried out from each of the CPR and UCR values.
Results
Three of the 280 patients who were included in the study were lost to follow-up following their initial ultrasonographic evaluation, with all of them having normal Doppler parameters, in accordance with the estimated sample size. Hereafter, statistical analysis was conducted among the remaining 277 participants, out of which 250 (90.3%) had normal Doppler ultrasonography, and 27 (9.7%) had either of the two Doppler values (CPR or UCR) abnormal (Fig. 1).
Fig. 1.
STROBE diagram
The mean age at presentation was 28.26 ± 4.47 years, and the average gestational age at the time of Doppler was 37.39 ± 2.03 weeks. The maternal baseline characteristics distribution between normal and abnormal Doppler parameters were similar except for gestational age at the time of Doppler (p < 0.001). The same has been summarized in Table 1. Similarly, among the maternal risk factors that came out to be statistically significant were hypertensive disorders of pregnancy (HDP), bad obstetric history (BOH), and the risk factors categorized as “others” which included cases of abruption and infections (p 0.02). The Doppler parameters that were studied have been summarized in Table 2.
Table 1.
Maternal baseline characteristics distribution between normal and abnormal Doppler parameters
| Parameters | Doppler inference | p value | ||
|---|---|---|---|---|
| Overall | Normal (n = 250) | Abnormal (n = 27) | ||
| Age (Years) | 28.26 ± 4.47 | 28.16 ± 4.33 | 29.19 ± 5.60 | 0.4692 |
| Booking status | 0.2203 | |||
| Unbooked | 123 (44.4%) | 108 (43.2%) | 15 (55.6%) | |
| Booked | 154 (55.6%) | 142 (56.8%) | 12 (44.4%) | |
| Gravida | 0.3973 | |||
| Primigravida | 153 (55.8%) | 142 (56.7%) | 13 (48.1%) | |
| Multigravida | 121 (44.2%) | 108 (43.3%) | 14 (51.9%) | |
| Parity | 0.1823 | |||
| Nullipara | 189 (68.2%) | 174 (69.6%) | 15 (55.6%) | |
| Primipara | 68 (24.5%) | 60 (24.0%) | 8 (29.6%) | |
| Multipara | 20 (7.2%) | 16 (6.4%) | 4 (14.8%) | |
| BMI | 0.1201 | |||
| < 18.5 kg/m2 | 5 (1.8%) | 3 (1.2%) | 2 (7.4%) | |
| 18.5–22.9 kg/m2 | 182 (65.7%) | 165 (66.0%) | 17 (63.0%) | |
| 23–24.9 kg/m2 | 84 (30.3%) | 77 (30.8%) | 7 (25.9%) | |
| ≥ 25 kg/m2 | 6 (2.2%) | 5 (2.0%) | 1 (3.7%) | |
| GA at Doppler (Weeks)*** | 37.39 ± 2.03 | 37.65 ± 1.69 | 34.94 ± 3.10 | < 0.0012 |
| Maternal profile: anaemia | 19 (6.9%) | 18 (7.2%) | 1 (3.7%) | 0.7051 |
| Hematological D/O | 8 (2.8%) | 7 (2.8%) | 1 (3.7%) | 0.5651 |
| RH negative pregnancy | 7 (2.5%) | 6 (2.4%) | 1 (3.7%) | 0.5161 |
| HDP*** | 38 (13.7%) | 25 (10.0%) | 13 (48.1%) | < 0.0011 |
| Thyroid disorder | 43 (15.5%) | 38 (15.2%) | 5 (18.5%) | 0.5851 |
| Diabetes | 44 (15.8%) | 42 (16.8%) | 2 (7.4%) | 0.2741 |
| Liver disorders | 17 (6.1%) | 16 (6.4%) | 1 (3.7%) | 1.0001 |
| Cardiac disorder | 4 (1.4%) | 4 (1.6%) | 0 (0.0%) | 1.0001 |
| BOH*** | 12 (4.3%) | 5 (2.0%) | 7 (25.9%) | < 0.0011 |
| Others*** | 7 (2.5%) | 4 (1.6%) | 3 (11.1%) | 0.0221 |
Data expressed as frequency (percentage) with exception of age, BMI and gestational age, which is expressed as mean (± 2S.D.)
Bad obstetric history (BOH) defined as previous unexplained intra-uterine death/still-birth/early neonatal death or previous two spontaneous abortions
BMI—body mass index, S.D. —standard deviation, HDP—hypertensive disorders of pregnancy
***Significant at p value < 0.05
Test of significance: 1: Fisher’s exact test, 2: Wilcoxon–Mann–Whitney U test, 3: Chi-squared test
Table 2.
Summary of Doppler ultrasonographic parameters
| Doppler details | Mean ± SD || frequency (%) |
|---|---|
| MCA PI | 1.46 ± 0.19 |
| UA PI | 0.90 ± 0.19 |
| CPR | 1.66 ± 0.25 |
| CPR inference | |
| Abnormal(< 5 centile) | 21 (7.6%) |
| Normal | 256 (92.4%) |
| CPR centile | 33.86 ± 18.15 |
| CPR Z-score | − 0.58 ± 0.84 |
| UCR | 0.62 ± 0.13 |
| UCR Inference | |
| Abnormal(> 95 centile) | 25 (9.0%) |
| Normal | 252 (91.0%) |
| UCR centile | 77.19 ± 13.68 |
| UCR Z-score | 0.90 ± 0.69 |
| Doppler inference | |
| Normal | 250 (90.3%) |
| Abnormal | 27 (9.7%) |
The correlation between abnormal Doppler ultrasonography and adverse neonatal outcomes revealed that the incidence of poor APGAR score, SFD, requirement for ventilatory support, neonatal hypoglycemia, and NICU admission including composite of adverse neonatal outcomes were significantly higher in the abnormal Doppler ultrasonography group. Three newborns died, and the Dopplers of all three of them were abnormal. Table 3 provides a summary of the same.
Table 3.
Association of adverse neonatal outcomes with Doppler ultrasonography findings
| Parameters | Doppler inference | p value | |
|---|---|---|---|
| Normal (n = 250) | Abnormal (n = 27) | ||
| APGAR (1 Min)*** | 8.93 ± 0.82 | 7.96 ± 1.74 | < 0.0012 |
| APGAR Category (1 Min)*** | < 0.0011 | ||
| < 7 | 5 (2.0%) | 6 (22.2%) | |
| ≥ 7 | 245 (98.0%) | 21 (77.8%) | |
| APGAR (5 Min) | 9.23 ± 0.87 | 8.93 ± 1.24 | 0.2792 |
| APGAR Category (5 Min) | 0.1341 | ||
| < 7 | 5 (2.0%) | 2 (7.7%) | |
| ≥ 7 | 245 (98.0%) | 25(92.3%) | |
| Size-for-Date*** | < 0.0011 | ||
| AFD | 226 (90.4%) | 9 (33.3%) | |
| LFD | 1 (0.4%) | 0 (0.0%) | |
| SFD | 23 (9.2%) | 18 (66.7%) | |
| Neonatal outcome: hypoglycemia*** | 6 (2.4%) | 13 (48.1%) | < 0.0011 |
| Polycythemia*** | 2 (0.8%) | 5 (18.5%) | < 0.0011 |
| Neonatal asphyxia*** | 2 (0.8%) | 5 (18.5%) | < 0.0011 |
| Acidosis | 2 (0.8%) | 1 (3.7%) | 0.2661 |
| Neonatal sepsis*** | 0 (0.0%) | 4 (14.8%) | < 0.0011 |
| Requirement Of ventilatory support*** | 5 (2.0%) | 9 (33.3%) | < 0.0011 |
| NICU admission*** | 11 (4.4%) | 18 (66.7%) | < 0.0011 |
| Prolonged hospital stay*** | 16 (6.4%) | 17 (63.0%) | < 0.0011 |
| Duration of hospital stay (Days)*** | 4.90 ± 3.10 | 11.70 ± 7.94 | < 0.0012 |
| Neonatal death*** | 0 (0.0%) | 3 (11.1%) | < 0.0011 |
| Composite neonatal outcome*** | < 0.0013 | ||
| Good | 219 (87.6%) | 5 (18.5%) | |
| Poor | 31 (12.4%) | 22 (81.5%) | |
AFD—appropriate for date, SFD—small for date, LFD—large for date, NICU—neonatal intensive care unit
***Significant at p value < 0.05
Tests of significance used, 1: Fisher’s exact test, 2: Wilcoxon–Mann–Whitney U test, 3: Chi-squared test
The study of Doppler parameters in predicting neonatal outcomes using ROC curves has been shown in Fig. 2. The cut-off obtained for CPR centile and Z-score was 22% and − 0.78, respectively, while that of UCR was 84% and 1 for centile and Z-score, respectively. Both UCR centile and Z-scores showed higher sensitivity (79.2%) compared to CPR. However, the diagnostic accuracies of both parameters were comparable.
Fig. 2.
The ROC curve in predicting adverse neonatal outcome for a CPR centile b CPR Z-score c UCR centile d UCR Z-score
The specificity, sensitivity, and predictive values along with the diagnostic accuracy of every Doppler parameter have been summarized in Table 4. The maximum sensitivity was found to be of UCR centile and Z-score (79.2%), followed by CPR centile and Z score (69.8%) while the highest diagnostic accuracy was found to be that of UCR inference (87%).
Table 4.
Test characteristics of each Doppler parameter
| Variable | Sensitivity (95% CI) | Specificity (95% CI) | Positive predictive value (95% CI) | Negative predictive value (95% CI) | Diagnostic Accuracy (95% CI) |
|---|---|---|---|---|---|
| CPR* | 54.7% (40–68) | 90.2% (86–94) | 56.9% (42–71) | 89.4% (85–93) | 83.4% (78–88) |
| CPR inference | 34.0% (22–48) | 98.7% (96–100) | 85.7% (64–97) | 86.3% (82–90) | 86.3% (82–90) |
| CPR centile* | 69.8% (56–82) | 82.1% (76–87) | 48.1% (37–60) | 92.0% (87–95) | 79.8% (75–84) |
| CPR Z-score* | 69.8% (56–82) | 83.5% (78–88) | 50.0% (38–62) | 92.1% (88–95) | 80.9% (76–85) |
| UCR* | 54.7% (40–68) | 90.2% (86–94) | 56.9% (42–71) | 89.4% (85–93) | 83.4% (78–88) |
| UCR inference | 39.6% (26–54) | 98.2% (95–100) | 84.0% (64–95) | 87.3% (83–91) | 87.0% (82–91) |
| UCR centile* | 79.2% (66–89) | 79.5% (74–85) | 47.7% (37–59) | 94.2% (90–97) | 79.4% (74–84) |
| UCR Z-score* | 79.2% (66–89) | 79.9% (74–85) | 48.3% (37–59) | 94.2% (90–97) | 79.8% (75–84) |
CPR—Cerebroplacental ratio, UCR—Umbilicocerebral ratio
*Cut-off obtained by ROC
Discussion
Our study was primarily aimed at comparing the two Doppler parameters CPR and UCR using their gestational age-specific values in unselected third-trimester antenatal women in the prediction of adverse neonatal outcomes. The distribution of baseline characteristics between the groups was alike with exceptions of gestational age at Doppler along with maternal profile which included HDP, BOH, and ‘others’. The gestational age at Doppler of the group with normal Doppler was significantly later than abnormal group. Both HDP and BOH are known risk factors of pregnancy resulting in uteroplacental insufficiency reflected in Doppler abnormalities (54), [9]. However, the ‘others’ category which included cases of urinary tract and other maternal infections showed a statistically significant difference as overall less number of cases were included in this group.
When comparing the two Doppler metrics to predict adverse neonatal outcomes, there was no discernible difference between them with AUC being same for both CPR and UCR (0.76). These findings align with a few recent studies assessing the same [10–12]. Furthermore, our study’s AUC value is comparable to that of a retrospective study conducted on women who had already been diagnosed with FGR and SGA by Coenen et al., where the AUC values for CPR and UCR were 0.708 [13].
Until recently, CPR was used as the standard marker for the prediction of neonatal outcomes with the relevance of UCR being relatively less studied. In our study, we additionally calculated the centiles and Z-scores of the two parameters to have their comparative assessment in the prediction of neonatal outcomes. When centiles were compared, both CPR and UCR had AUC of 0.833 and 0.855, respectively, which was better than when their absolute values were compared. However, a recent retrospective case–control study by Villalain et al. showed CPR and UCR centiles having AUCs of 0.56 [14]. This could possibly be due to the difference in the range of gestational age at inclusion where we had taken all third trimester pregnancies while in their study gestational ages between 36 and 40 weeks were included and with a much larger sample size of 646 pregnancies.
Similarly, when compared in terms of Z-score, consistent with other studies there was no variance in the AUC obtained for UCR and CPR. Taking the study by Leavitt et al. in 2021 into consideration [15], the AUC of the Z scores for CPR and UCR were 0.70 and 0.68 correspondingly which was in contrast to our study where the AUC were 0.83 and 0.85, respectively. Nevertheless, the PPV (positive predictive values) of both parameters were comparable. As far as UCR Z-scores are concerned, which had the highest sensitivity, a cut-off of 1 was obtained. This was in agreement with a prospective study by Stampalija et al. [16] where UCR Z-scores for analysis were taken as > / = 1 and > / = 1.5 irrespective of the gestational age.
UCR inference (> 95 centiles) and CPR inference (< 5 centiles) had the highest diagnostic accuracy for the prediction of unfavorable neonatal outcomes among all the Doppler parameters studied with values being 87 and 86.3%, respectively. This was in contrast with other studies which reported poor diagnostic accuracies for CPR and UCR like that of K Leavitt et al. 2021 [15], where detection rates were 40% using a fixed false positive rate of 10% which in our study was up to 17%. A slightly higher detection rate of 60% for low neonatal pH was obtained in a study by Familiari et al. [17]; however, the study population was that of term pregnancies complicated by gestational diabetes, and values were expressed in MoM. The inclusion of participants who already had absent flows in UA at the time of presentation or follow-up could be a reason for the higher accuracy obtained in our study compared to others. In terms of sensitivity, the CPR absolute gestational age-specific value had a sensitivity of 54.7% which was similar to those obtained in a systemic review and meta-analysis by Conde-Agudelo et al. (2018) [8] where CPR had a pooled sensitivity of 57% for prediction of any composite of adverse outcomes.
Association of each adverse neonatal outcome with Doppler parameters when studied showed a significant difference between the groups with normal and abnormal Doppler be it CPR or UCR except for one that was acidosis. This probably could be due to the small number of cases with acidosis. This association was consistent with the previous studies evaluating outcomes such as SGA, admission to NICU, poor APGAR scores at birth, preterm delivery as well as a composite of these adverse outcomes by Stumpfe FM et al. [11], Leavitt et al. [15], and M.L. Winchester et al. [18].
Additionally, when maternal patient profile was studied in patients with abnormal Dopplers, hypertensive disorders of pregnancy as well as a BOH which in most cases was a previous pregnancy complicated with gestational hypertension and pre-eclampsia leading to intra-uterine demise or still birth was found to be associated significantly.
HDP be it gestational hypertension or chronic hypertension or pre-eclampsia affecting around 5–10% of all pregnancies worldwide is a known risk factor resulting in uteroplacental insufficiency reflected in Doppler abnormalities leading to intrauterine growth retardation, necessitating preterm delivery in many cases and associated neonatal morbidity and mortality [19]. This was consistent with many longitudinal studies establishing the role of Doppler in monitoring pregnancies complicated by hypertension or a previous history of bad obstetric outcomes [9, 20].
Strengths of the Study
Prospective design and consecutive recruitment of the participants are the key strengths of the study where a Doppler ultrasound was done for all antenatal women (both higher and lower-risk women) in the 3rd trimester. In this way, the missing data were also minimized. Additionally, the gestational age-specific values of the Doppler parameters CPR and UCR were used for studying the outcomes, and values obtained 1 week before the delivery were taken into analysis both of which add to the validity of the study. Besides comparing the absolute values of CPR and UCR, the converted centiles and Z-scores were also compared.
Limitations
As a single-center study with a small sample size, the findings might not apply to other contexts. Also, we have not performed a multivariate analysis of maternal risk factors such as hypertension, diabetes, etc. for every adverse neonatal outcome to lower the impact of confounding factors.
Conclusion
This prospective study was carried out on 280 women undergoing routine third-trimester Doppler ultrasound within a week of delivery with a primary aim to compare the performance of UCR and CPR in predicting adverse neonatal outcomes. We found that while both UCR and CPR were significantly linked with neonatal outcomes, there was no variance between the two in the prediction of these outcomes (AUC is 0.76 for both). The same holds true when the absolute values were converted into gestational age-specific centiles and Z-scores. However, use of centiles and Z-scores increased the sensitivity (AUC being 0.83 and 0.85, respectively, for both CPR and UCR centiles as well as Z-scores). We also found that most women with abnormal Doppler study had pregnancies complicated by hypertension and BOH.
Author Contributions
All authors contributed to study design and concept. BB wrote the first draft of the manuscript and all authors reviewed the previous versions of the manuscript. All authors helped in data collection and preparation of the final manuscript to be submitted. The manuscript has been read and approved by all the authors, the requirements for authorship have been met, and each author believes that the manuscript represents honest work.
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
Declarations
Conflict of Interest
The authors have no relevant financial or non-financial interests to disclose.
Ethical Approval
This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Institute Ethics Committee of All India Institute of Medical Sciences, Bhubaneswar reference number (IEC/AIIMS BBSR/PG Thesis/2020- 21/17).
Consent to Participate
Informed consent was obtained from all individual participants included in the study.
Consent to Publish
The authors affirm that human research participants provided informed consent for publication of the study.
Footnotes
Bhavya Bhardwaj is a Junior Resident, Sweta Singh is a Professor and HOD, Jasmina Begum is an Associate Professor, Tapas K. Som is an Additional Professor, and Sudipta Mohakud is an Additional Professor.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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