Gao et al. BMC Pediatrics(2024) 24:571
https://doi.org/10.1186/s12887-024-05041-1

BMC Pediatrics

RESEARCH

Open AccessCorrelation between anesthetic concentrationand low Apgar scores in neonates born via
Cesarean sections under general anesthesia
Yang Gao1†, Yun Song1†, Jingkun Miao2, Xiaofeng Lei1, Hao Liu2, Lin Gan1, Meng Cai1 and Jin Yu1*
Abstract
Objectives This study aimed to compare plasma concentrations of anesthetic drugs administered during Cesarean
section with low Apgar score in neonates deliveried under general anesthesia and analyze associated risk factors.
Methods Data from 76 neonates undergoing Cesarean section under general anesthesia with blood concentrationsof anesthetic drugs were analyzed. A low Apgar score was defined as ≤ 7. Perioperative maternal and neonatal data
were collected and analyzed. Neonates were divided into a control group (Group CON, n = 65) and a low Apgar scoregroup (Group LAS, n = 11) based on Apgar score.
Results There were no significant differences in the plasma concentrations of anesthetic drugs in maternal artery,umbilical vein or umbilical artery blood between the two groups. Risk factors for neonatal low Apgar scores during
Cesarean section under general anesthesia were premature delivery (aOR 10.2, 95% CI = 1.8–56.9) and preoperative
fetal distress (aOR 9.6, 95% CI = 1.3–69.0). The prediction model was: probability = 1/(e‑Y ), Y= -4.607 + 2.318×(premature delivery) + 2.261× (fetal distress) (yes = 1, no = 0). The Hosmer–Lemeshow test showed χ²= 9.587, P = 0.213,
and the area under the curve (AUC) was 0.850 (0.670 ~ 1.000). With a cutoff value of 0.695, sensitivity and specificity
were 81.8% and 87.7%, respectively.
Conclusions There was no correlation between blood concentration of general anesthetic drugs and Apgar scoreor occurrence of neonatal low Apgar scores. Premature delivery and preoperative fetal distress were identified as
independent risk factors for neonatal low Apgar scores after Cesarean section under general anesthesia.
Keywords General anesthesia, Cesarean section, Neonatal outcome, Apgar score, Anesthetics, Correlation analysis†

Yang Gao and Yun Song contributed equally to this work.

*Correspondence:
Jin Yudodoes@qq.com
1
Department of Anesthesiology, Chongqing Health Center for Womenand Children, Women and Children’s Hospital of Chongqing Medical
University, No. 120, Longshan Road, Yubei District, Chongqing
401147, China
2
Department of Pediatrics, Chongqing Health Center for Womenand Children, Women and Children’s Hospital of Chongqing Medical
University, Chongqing, China© The Author(s) 2024. Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0
International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you
give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified thelicensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images orother third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to thematerial. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation
or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://
creativecommons.org/licenses/by-nc-nd/4.0/.

Gao et al. BMC Pediatrics(2024) 24:571

Introduction
Approximately one million neonates die annually worldwide from intrapartum-related complications, such as
birth asphyxia [1]. Two million neonates suffer fromhypoxic ischemic encephalopathy(HIE), and 1.2 million
experience developmental delays [2]. Various antepartum or intrapartum factors contribute to birth asphyxia,
including primipara mother, placental abruption, intrauterine growth restriction, prolonged second-stage
labor, meconium-stained or bloody amniotic fluid, andabnormal fetal heart rate (FHR) tracings [3]. Multivariate analysis of 1200 neonates identified maternal factors(gestational hypertension, gestational diabetes, placenta
previa, meconium stained amniotic fluid, intrauterine
infection, anemia, educational level and age), fetal factors(twins, gestational age, breech position, umbilical cordaround the neck and fetal distress), and other factors(Cesarean section and prolonged labor) as risk factors forneonatal asphyxia [4].
For Cesarean sections, regional anesthesia is preferred due to its adequate analgesic efficacy and minimal adverse effects on both mother and neonate [5].
General anesthesia may be necessary in cases where
regional anesthesia is ineffective, contraindicated, or for
emergency deliveries [6]. General anesthesia is typicallyreserved for emergency cesarean deliveries or situations
where neuraxial anesthesia is not feasible.
Concerns have been raised about the potential impactof general anesthesia during Cesarean section on neonatal outcomes, including the risk of neonatal low Apgar
scores. However, the relationship between plasma anesthetic drug concentrations during Cesarean sections
under general anesthesia and neonatal Apgar scoresremains unclear. This study aims to compare plasma
anesthetic drug concentrations in neonates with andwithout low Apgar scores and to analyze the potential
risk factors associated with low Apgar scores during
Cesarean sections under general anesthesia.
Methods
Objects and grouping

This study was approved by the Medical Ethics Committee of Chongqing Health Center for Women and Children (reference number: 2021-011),and registered at the
Chinese Clinical Trial Registry (ChiCTR) (www.chictr.
org) with registration ID ChiCTR2100046547. Informed
consent was obtained from all participants. The data of
neonates delivered via Cesarean section under generalanesthesia and maternal perioperative data from April
15, 2021, to April 10, 2022, were reviewed and analyzed.
The general inclusion criteria were neonates delivered via
Cesarean section, the use of the same general anesthesia
scheme, and the measurement and recording of anesthetic drug concentrations. Neonates with congenital

Page 2 of 7

malformations were excluded. The enrolled participants
were divided into a control group (Group CON, n = 65)
and a low Apgar scores group (Group LAS, n = 11) basedon the Apgar score. Neonates with an Apgar score < 8 at
1, 5, or 10 min after birth were classified as having neonatal low Apgar score. A total score of 0–3 points, 4–7
points and 8–10 points indicated severe asphyxia, mild
asphyxia and normal, respectively [7].
The concentrations of anesthetic drugs in the included
subjects were measured using liquid chromatographytandem mass spectrometry. Maternal arterial (MA),umbilical arterial (UA), and umbilical venous (UV) blood
samples were collected after umbilical cord ligation foranalysis of drug concentrations. The samples were centrifuged in sodium citrate-coated anticoagulant tubes at
3000 rpm at 4 °C for 10 min. The plasma was isolated andstored at -80 °C for later analysis. The anesthetic drugs
tested included etomidate, remifentanil and rocuronium
bromide in MA, UV, and UA blood samples.
General anesthesia scheme

General anesthesia for the Cesarean section was administered using a combination of intravenous and inhalation induction. The detailed procedure included inducing
anesthesia with sevoflurane inhalation at 5% and a remifentanil infusion at 5 ng/ml using target-controlled infusion (TCI) mode. Additionally, etomidate (0.25 mg/kg)
and rocuronium bromide (0.6 mg/kg) were administeredas single injections. Sevoflurane was stopped once theeyelash reflex was lost, and tracheal intubation was performed after the muscle relaxants took effect. Anesthesia
was maintained with remifentanil (5 ng/ml) and propofol (3.5 µg/ml) in TCI mode after the neonatal umbilicalcord was disconnected.
Data collection

Maternal and fetal characteristics, blood concentrationsof anesthetic drugs, time from induction to skin incision (I-S), time from induction to delivery (I-D), and timefrom uterine incision to delivery (U-D) were recorded
and analyzed. Apgar scores at 1, 5, and 10 min were collected retrospectively. Maternal indicators included age,body weight, height, body mass index (BMI), gestationalage, gestational hypertension, gestational diabetes, scaruterus (previous Cesarean section), hemoglobin, hematocrit, leukocytes, platelets, plasma prothrombin time(PT), activated partial thrombin time (APTT), D-dimer,
plasma fibrinogen, thrombin time (TT), premature rupture of membranes, placental abruption and polyhydramnios or oligohydramnios. Fetal-related indicators
included fetal sex, twin pregnancy, premature delivery,
abnormal umbilical cord (such as the umbilical cordaround the neck or first exposed umbilical cord), andfetal distress.

Gao et al. BMC Pediatrics(2024) 24:571

Page 3 of 7

Table 1 Preoperative maternal and fetal characteristics

Age, years
Body weight, kg
Height, cm
BMI
Gestation, weeks
Gestational hypertension(Yes/No)
Gestational diabetes (Yes/No)
Scar uterus(previous CS) (Yes/No)
Hemoglobin, g/L
Hematocrit, %Leukocyte, 109/L
Platelet, 109/L
PT, second
APTT, second
FIB, g/L
TT, second
D-Dimer, mg/L FEU
Fetal sex(female/male)
Premature rupture ofmembranes
Twin pregnancy (Yes/No)
Premature delivery (Yes/No)
Placental abruption (Yes/No)
Polyhydramnios or oligohydramnios (Yes/No)
Abnormal umbilical cord
(umbilical cord around neck,umbilical cord exposed first)
Fetal distress (Yes/No)

Table 2 Blood concentrations of anesthetic drugs

Group
CON(n = 65)
31.82 ± 3.8
71.06 ± 9.7
157.80 ± 4.9
28.55 ± 3.8
37.58 ± 1.9
5/60

Group
LAS(n = 11)
30.91 ± 6.4
66.06 ± 12.9
155.18 ± 7.3
27.43 ± 5.5
34.36 ± 3.5
2/9

P
value
0.659
0.243
0.275
0.396
0.012*
0.266

13/52
17/46

4/7
2/9

0.228
0.537

123.06 ± 13.4
35.66 ± 4.3
8.01 ± 2.2
146.26 ± 60.7
10.25 ± 1.1
26.50 ± 2.0
4.49 ± 0.9
17.77 ± 1.8
2.79 ± 1.7
29/34
7/56

118.82 ± 17.9
34.70 ± 3.7
7.85 ± 2.1
166.55 ± 66.3
10.36 ± 0.7
26.90 ± 1.9
4.84 ± 1.4
17.82 ± 1.1
4.11 ± 2.5
6/5
0/11

0.359
0.485
0.820
0.359
0.740
0.547
0.274
0.903
0.032*
0.602
0.585

19/44
16/47
3/60
6/57

5/6
9/2
2/9
2/9

0.317
0.001*
0.102
0.394

13/50

2/9

0.852

4/59

4/7

0.003*

Remifentanil MA, ng/ml
Remifentanil UV, ng/ml
Remifentanil UA, ng/ml
Remifentanil UV / MA
Remifentanil UA / MA
Etomidate MA, ng/ml
Etomidate UV, ng/ml
Etomidate UA, ng/ml
Etomidate UV / MA
Etomidate UA / MA
Rocuronium bromide MA,
ug/ml
Rocuronium bromide UV,
ug/ml
Rocuronium bromide UA,
ug/ml
Rocuronium bromide UV/ MA
Rocuronium bromide UA/ MAGroup CON(n = 65)
3.87 ± 1.3
1.86 ± 0.9
0.94 ± 0.8
0.49 ± 0.2
0.24 ± 0.2
477.17 ± 154.0
322.25 ± 129.0
180.14 ± 66.6
0.70 ± 0.2
0.40 ± 0.1
5.98 ± 2.5Group LAS(n = 11)
4.15 ± 1.5
1.78 ± 0.5
0.77 ± 0.7
0.47 ± 0.1
0.19 ± 0.2
446.16 ± 238.7
276.65 ± 129.3
183.11 ± 118.5
0.70 ± 0.3
0.45 ± 0.2
6.07 ± 2.9

P
value
0.545
0.772
0.499
0.725
0.369
0.662
0.321
0.910
0.985
0.373
0.916

0.80 ± 0.5

0.84 ± 0.4

0.786

0.47 ± 0.3

0.42 ± 0.2

0.627

0.15 ± 0.1

0.18 ± 0.1

0.452

0.09 ± 0.1

0.08 ± 0.1

0.755

identified, and regression equations were constructed asfollows: probability = 1/(e‑Y) and Y = A + B1 × 1 + B2 × 2,
where “A” is a constant, “B” is the regression coefficient ofeach risk factor, “X” is the risk factor, and the probability
represents the risk value of neonatal birth asphyxia undergeneral anesthesia.

Results

BMI: body mass index, TT: thrombin time, PT: plasma prothrombin time, FIB:
plasma fibrinogen, APTT: activated partial thrombin time*Compared with the control group

Statistical analysis

Normally distributed measurement data are presented asmean ± standard deviation, while count data are expressed
as numbers. T-tests were used to compare measurement
data between groups, and the chi-square test was used
for count data comparison. Pearson correlation analysis
was conducted to evaluate the correlation between bloodconcentrations of anesthetic drugs and Apgar scores at
1, 5, and 10 min. A significance level of P < 0.05 was considered statistically significant. Logistic regression analysis was performed to assess the relationship between
potential factors and neonatal low Apgar scores, calculating both crude odds ratio (OR) and adjusted odds ratio(adjusted OR). Binary logistic regression was used toanalyze risk factors, and receiver operating characteristic(ROC) analysis was conducted to evaluate factors influencing prognosis. An area under the curve (AUC) > 0.5
indicated predictive value. Independent risk factors were

Preoperative maternal and fetal characteristics

Neonatal low Apgar scores were observed in 11 out of 76
neonates delivered via Cesarean section under generalanesthesia, resulting in an incidence rate of 14.47%. There
were no significant differences in preoperative maternalor fetal indicators except for gestational age, D-dimer
concentration and fetal distress between the low Apgar
score (LAS) group and the control (CON) group. The
incidence of fetal distress in the CON group was 6.15%(4 out of 65), while in the LAS group, it was significantly
higher at 36.36% (4 out of 11) (P < 0.05) (Table 1).
Blood concentrations of anesthetic drugs

There were no significant differences in the plasma concentrations of anesthetic drugs (remifentanil, etomidate, or rocuronium bromide) between the two groups
in maternal artery blood (MA), umbilical vein (UV), or
umbilical artery (UA) blood (P > 0.05) (Table 2; Figs. 1, 2
and 3).
Correlation analysis

There was no correlation found between the blood concentrations of anesthetic drugs in MA, UV, UA blood andGao et al. BMC Pediatrics(2024) 24:571

Fig. 1 The concentrations of remifentanil in the MA, UV and UA blood samples

Fig. 2 The concentrations of etomidate in MA, UV and UA blood samples

Fig. 3 The concentrations of rocuronium bromide in MA, UV and UA blood samples

Page 4 of 7

Gao et al. BMC Pediatrics(2024) 24:571

Page 5 of 7

Table 3 Correlation coefficients and P-values between bloodconcentrations of anesthetic drugs and apgar scores at 1, 5, and10 minRemifentanil
MA
Remifentanil
UV
Remifentanil
UA
Etomidate MA

Apgar scoreat 1 minr = -0.021, p = 0.863
r = 0.071, p = 0.555
r = 0.176, p = 0.140
r = -0.114, p = 0.339

Etomidate UV

r = 0.177, p = 0.136

Etomidate UA

r = 0.041, p = 0.731

Rocuronium
bromide MA
Rocuronium
bromide UV
Rocuronium
bromide UA

r = 0.036, p = 0.766
r = -0.035, p = 0.768
r = 0.011, p = 0.927

Apgar scoreat 5 minr = -0.033,
p = 0.786
r = 0.011,
p = 0.925
r = 0.106,
p = 0.378
r = 0.081,
p = 0.501
r = 0.196,
p = 0.098
r = 0.114,
p = 0.339
r = 0.151,
p = 0.204
r = -0.064,
p = 0.592
r = -0.046,
p = 0.702

Apgar scoreat 10 minr = -0.013,
p = 0.786
r = 0.014,
p = 0.905
r = 0.120,
p = 0.316
r = 0.073,
p = 0.543
r = 0.164,
p = 0.168
r = 0.045,
p = 0.706
r = 0.128,
p = 0.283
r = -0.078,
p = 0.512
r =-0.088,
p = 0.464

MA: maternal artery blood, UV: umbilical vein blood, UA: umbilical artery blood

Table 4 Procedure duration-related factors between the twogroups
I-S, min
I-D, min
U-D, second

Group CON(n = 65)
2.58 ± 0.6
5.98 ± 2.9
59.69 ± 25.2

Group LAS(n = 11)
2.58 ± 0.6
6.49 ± 2.4
61.00 ± 23.6

P value
0.990
0.513
0.873

I-S represents the time from induction to skin incision; I-D represents the timefrom induction to delivery; and U-D represents the time from uterine incision
to delivery

Fig. 4 The adjusted odds ratios (ORs) for premature delivery, fetal distressand D-dimer levels from multivariate analysis

Apgar scores at 1, 5, and 10 min. The specific correlation
coefficients and P-values are detailed in Table 3.
Procedure duration-related factors

There was no significant difference between the twogroups in term of I-S, I-D, or U-D time (P > 0.05)(Table 4).

Logistic regression analysis

Univariate analysis revealed that premature delivery,
fetal distress and increased D-dimer levels were associated with neonatal low Apgar scores compared to the
CON group (P < 0.05). The logistic regression analysis
results showed that the crude odds ratio (OR) for premature delivery was 13.8 (95% CI, 2.7–70.5; p = 0.002),
for fetal distress it was 8.7 (95% CI, 1.8–42.7; p = 0.041),
and for D-dimer it was 1.4 (95% CI, 1.0–1.9; p = 0.041).
In the multivariate analysis, the adjusted ORs were 10.2
for premature delivery (95% CI = 1.8–56.9; p = 0.008), 9.6
for fetal distress (95% CI = 1.3–69.0; p = 0.025) and 1.4 forD-dimer (95% CI = 1.0–2.0; p = 0.073) (Fig. 4).
Premature delivery and fetal distress were identified as independent risk factors for neonatal low Apgar
scores. The risk prediction model yielded a probabilityof 1/(e‑Y), where Y=-4.607 + 2.318×(premature delivery) + 2.261×(fetal distress). The Hosmer–Lemeshow test
showed χ²= 9.587, P = 0.213, indicating a good model fit.
The risk index for low Apgar scores under general anesthesia was calculated using the model prediction index,
and ROC analysis was conducted with various risk factors. The AUC was 0.850 (0.670 ~ 1.000), with a sensitivity of 81.8% and specificity of 87.7% at a cutoff value of
0.695 (Fig. 5).

Discussion
Birth asphyxia can occur during childbirth, potentiallyleading to conditions such as cerebral palsy and affecting cognitive, behavioral, and motor development later inlife if there is a restriction in oxygen flow to the brain andcompromised cerebral blood circulation [8]. The central
nervous system can sustain irreversible damage fromhypoxic insult due to birth asphyxia, resulting in longterm consequences [9]. Asphyxia during childbirth isoften accompanied by a low Apgar score. Therefore, identifying and preventing risk factors associated with neonatal low Apgar scores can help reduce neonatal asphyxia.
Neuraxial anesthesia is a commonly used and safe
anesthesia technique for Cesarean section deliveries,
recommended by anesthesia guidelines. However, somepatients may have contraindications to neuraxial anesthesia or may refuse it due to fear or anxiety [5]. Consequently, a percentage of Cesarean sections are performed
under general anesthesia.
Traditionally, Cesarean sections under general anesthesia were believed to increase the risk of neonatal low
Apgar score due to the placenta transmission of generalanesthetic drugs. This study aimed to compare anesthetic
drug concentrations in the umbilical artery, umbilicalvein, and maternal arterial tract between neonates withand without low Apgar scores and identify specific risk
factors associated with low Apgar scores in patients
undergoing Cesarean sections under general anesthesia.

Gao et al. BMC Pediatrics(2024) 24:571

Page 6 of 7

Fig. 5 The receiver operating characteristic (ROC) curve of the prediction model

The study found that the incidence of low Apgar scores
was 14.47% in infants delivered via Cesarean section
under general anesthesia (4.08% in full-term deliveries
and 36% in premature deliveries). There was no significant correlation between neonatal low Apgar scores andblood concentration of general anesthetic drugs or the
I-S, I-D or U-D duration. Low Apgar scores were independently associated with premature delivery and preoperative fetal distress.
Advancements in general anesthesia techniques andthe use of short-acting anesthetics have not shown conclusive evidence that general anesthesia during Cesarean sections increases the risk of neonatal birth asphyxia[10]. Studies have reported a better fetal oxygen supply,
higher umbilical cord blood pH and smaller base deficit
in Cesarean sections under general anesthesia comparedto vaginal delivery with epidural anesthesia or Cesarean
sections under subarachnoid block [11]. Randomized
controlled trials have consistently shown similar results,
indicating that neonatal Apgar scores and outcomes are
not affected by the choice of anesthetic technique [12,13].
Among pregnant patients with severe thrombocytopenia, there were no cases of birth asphyxia in the groupthat underwent Cesarean section under general anesthesia. In contrast, two cases of birth asphyxia were reported
in the local anesthesia group [14]. Therefore, the use ofgeneral anesthetic drugs or the choice of general anesthesia modality does not increase the risk of incidence of
low Apgar scores, as indicated by the results of this study.
Anesthetic drug concentration was not found to be a risk
factor for neonatal asphyxia. While prolonged infusion
times (I-S, I-D or U-D) may lead to increased accumulation of anesthetic drugs, they were not identified as risk
factors for neonatal low Apgar scores in this study.

Several studies have assessed the intrapartum factors
and obstetric and fetal conditions associated with birthasphyxia [15–20]. These studies have identified various
risk factors for birth asphyxia, such as preterm birth andfetal distress. However, there is a lack of research specifically investigating the risk factors for neonatal asphyxia
resulting from Cesarean section under general anesthesia. In this study, univariate analysis indicated that premature delivery, preoperative fetal distress, and elevatedD-dimer levels are associated with an increased risk of
neonatal low Apgar scores under general anesthesia.
However, only premature delivery and preoperative fetal
distress remained significant in the multifactor analysis.
Delivery with fetal distress is typically urgent, necessitating emergent anesthesia [21]. General anesthesia isoften preferred for these patients due to its rapid onset
and concerns about hemodynamic complications associated with regional techniques. Preterm birth is a multifactorial condition, with prematurity being a major factor
contributing to birth asphyxia due to alveolar hypoplasia[22, 23]. According to the study findings, the risk of neonatal low Apgar scores is approximately ten times higher
when one or both of the these risk factors are present
during general anesthesia.
This study has two limitations. Firstly, the sample
size was relatively small, although it met the minimum
requirement for multifactor regression analysis. Secondly, the participants included were receiving generalanesthesia and agreed to blood collection for drug concentration measurements, which may have introduced
bias into the analysis.
Conclusions

In conclusion, there was no correlation found between
the blood concentration of general anesthetic drugs andthe occurrence of neonatal low Apgar scores. Premature

Gao et al. BMC Pediatrics(2024) 24:571

delivery and preoperative fetal distress were identified as
independent risk factors for neonatal low Apgar scores
under general anesthesia.
Acknowledgements
We are grateful to Prof. Yongchun Su at Chongqing Youyoubaobei Womenand Children’s Hospital for his manuscript preparation assistance.
Author contributions
JY and XL contributed to the conception and the work design; YG and YS
contributed to the analysis and interpretation of data for the work; YG and MC
drafted the work and revised it critically for important intellectual content;
HL and LG contributed to the drug concentration test. JM supervised the test
procedure. All authors have read and approved the manuscript.

Page 7 of 7

6.
7.
8.
9.
10.

11.

Funding
This study was sponsored by Natural Science Foundation of Chongqingof China (No. cstc2021jcyj-msxmX0763), National Key Clinical Speciality
Construction Project (Obstetrics and Gynecology).

12.

Data availability
The data presented in this study are available on request from thecorresponding author.

13.

Declarations
Ethics approval and consent to participate
This study was approved by the Medical Ethics Committee of Chongqing
Health Center for Women and Children (reference number: 2021-011).
And was performed in accordance with International Conference on
Harmonization - Guidelines for Good Clinical Practice (ICH-GCP) and
Declaration of Helsinki. Informed consents were obtained from all participants.

14.
15.
16.

Consent for publication
Not applicable.

17.

Competing interests
The authors declare no competing interests.

18.
19.

Received: 19 January 2024 / Accepted: 29 August 2024
20.

References
1. Liu L, Oza S, Hogan D, Chu Y, Perin J, Zhu J, et al. Global, regional, andnational causes of under-5 mortality in 2000-15: an updated systematic
analysis with implications for the Sustainable Development Goals. Lancet.
2016;388:3027–35.
2. Lee AC, Kozuki N, Blencowe H, Vos T, Bahalim A, Darmstadt GL, et al. Intrapartum-related neonatal encephalopathy incidence and impairment at regionaland global levels for 2010 with trends from 1990. Pediatr Res. 2013;74(Suppl
1):50–72.
3. Tunc S, Oglak SC, Gedik Ozkose Z, Olmez F. The evaluation of the antepartum
and intrapartum risk factors in predicting the risk of birth asphyxia. J Obstet
Gynecol Res. 2022;48:1370–8.
4. MH J, XH W. Analysis of the occurrence and risk factors for neonatal asphyxia.
Maternal Child Health Care China. 2020;35:2620–2.
5. American College of O. Gynecologists’ Committee on Practice B-O. ACOG
Practice Bulletin 209: Obstetric Analgesia and Anesthesia. Obstet Gynecol.
2019;133:e208–25.

21.
22.
23.

Cai M, Liu H, Peng Y, Miao JK, Lei XF, Yu J. Prolonged Anesthesia induction
to Delivery Time did not influence plasma Remifentanil Concentration inneonates. Drug Des Devel Ther. 2023;17:1395–403.
Association NRGoPBoCM. Expert consensus on the diagnosis of neonatal
asphyxia. Chin J Perinat Med. 2016;19:3–6.
Kurinczuk JJ, White-Koning M, Badawi N. Epidemiology of neonatal
encephalopathy and hypoxic-ischemic encephalopathy. Early Hum Dev.
2010;86:329–38.
Herrera-Marschitz M, Neira-Pena T, Rojas-Mancilla E, Morales P, Bustamante
D, Leyton L, et al. Short- and long-term consequences of perinatal asphyxia:
looking for neuroprotective strategies. Adv Neurobiol. 2015;10:169–98.
Fisher SC, Siag K, Howley MM, Van Zutphen AR, Reefhuis J, Browne ML, et al.
Maternal surgery and anesthesia during pregnancy and risk of birth defects
in the National Birth defects Prevention Study, 1997–2011. Birth Defects Res.
2020;112:162–74.
Szymanowski P, Szepieniec WK, Zarawski M, Gruszecki P, Szweda H, Jozwik
M. The impact of birth anesthesia on the parameters of oxygenation andacid–base balance in umbilical cord blood. J Matern Fetal Neonatal Med.
2020;33:3445–52.
Chen Y, Liu W, Gong X, Cheng Q. Comparison of effects of General Anesthesia
and combined Spinal/Epidural anesthesia for cesarean delivery on umbilicalcord blood gas values: a Double-Blind, randomized, controlled study. Med Sci
Monit. 2019;25:5272–9.
Staikou C, Tsaroucha A, Vakas P, Salakos N, Hasiakos D, Panoulis K, et al. Maternal and umbilical cord oxygen content and acid–base balance in relation
to general, epidural or subarachnoid anesthesia for term elective cesarean
section. Clin Exp Obstet Gynecol. 2013;40:367–71.
Wei J, Liu GL, Liang MY, Wang SM. [Effect of general anesthesia used in cesarean section on maternal-neonatal outcome of pregnancy complicated withsevere Thrombocytopenia]. Zhonghua Fu Chan Ke Za Zhi. 2009;44:665–8.
Igboanugo S, Chen A, Mielke JG. Maternal risk factors for birth asphyxia in
low-resource communities. A systematic review of the literature. J Obstet
Gynecol. 2020;40:1039–55.
Sendeku FW, Azeze GG, Fenta SL. Perinatal asphyxia and its associated factors
in Ethiopia: a systematic review and meta-analysis. BMC Pediatr. 2020;20:135.
Egharevba OI, Kayode-Adedeji BO, Alikah SO. Perinatal asphyxia in a rural
Nigerian hospital: incidence and determinants of early outcome. J Neonatal
Perinat Med. 2018;11:179–83.
Aslam HM, Saleem S, Afzal R, Iqbal U, Saleem SM, Shaikh MW, et al. Risk factors
for birth asphyxia. Ital J Pediatr. 2014;40:94.
Wosenu L, Worku AG, Teshome DF, Gelagay AA. Determinants of birthasphyxia among live birth newborns in University of Gondar referral hospital,
northwest Ethiopia: a case–control study. PLoS ONE. 2018;13:e0203763.
Abdo RA, Halil HM, Kebede BA, Anshebo AA, Gejo NG. Prevalence andcontributing factors of birth asphyxia among the neonates delivered at Nigist
Eleni Mohammed memorial teaching hospital, Southern Ethiopia: a crosssectional study. BMC Pregnancy Childbirth. 2019;19:536.
Hamza J. [Acute fetal distress. The anesthesiologist’s point of view]. Cah
Anesthesiol. 1996;44:309–26.
Frey HA, Klebanoff MA. The epidemiology, etiology, and costs of preterm
birth. Semin Fetal Neonatal Med. 2016;21:68–73.
Ahmed R, Mosa H, Sultan M, Helill SE, Assefa B, Abdu M, et al. Prevalence andrisk factors associated with birth asphyxia among neonates delivered in Ethiopia: a systematic review and meta-analysis. PLoS ONE. 2021;16:e0255488.

Publisher’s note

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