Risk of Transient Tachypnea of the Newborn following Elective Cesarean Section Increases at a Gestational Age of 37 Weeks Compared to That at ≥ 38 Weeks Despite the Exclusion of Pre-Existing Risk Factors for Neonatal Respiratory Disorders (2024)

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Yonago Acta Med
v.67(2); 2024 May
PMC11128081

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Yonago Acta Med. 2024 May; 67(2): 150–156.

Published online 2024 May 11. doi:10.33160/yam.2024.05.009

PMCID: PMC11128081

Yoichi Mino,^* Fumiko Miyahara,^* Mazumi Miura,^* Aya Imamoto,^* Hiromi Fujii,^* Chisaki Moriwaki,^* Kazuki Yoshioka,^* and Noriyuki Namba^*

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ABSTRACT

Background

Elective cesarean sections (ECSs) for early-term pregnancies at 37 weeks of gestational age (GA) aim to reduce the risk of emergency cesarean sections due to the onset of labor or rupture of membranes. However, resultant increases in neonatal respiratory disorders, including transient tachypnea of the newborn (TTN) have been observed. However, few studies have elucidated the associated risk factors. Consequently, we aimed to determine whether differences existed in the clinical outcomes between neonates delivered via ECS at 37 weeks and those delivered at ≥ 38 weeks of GA.

Methods

A retrospective analysis was conducted on 259 neonates born via ECS at Tottori University Hospital, between January 2013 and December 2019, with birthweights ≥ 2500 g and GAs > 37 weeks. The neonates were categorized into two cohorts: births at 37 and at ≥ 38 weeks of GA (37-week and 38-week cohorts). The principal clinical outcomes included the appearance, pulse, grimace, activity, and respiration (Apgar) scores, need for positive-pressure ventilation, incidence of TTN, and length of hospital stay.

Results

No statistically significant differences were observed in the indications for ECS, sex, or birthweight between the two cohorts. The 37-week cohort exhibited a lower 1-min Apgar score than did the 38-week cohort, with no statistically significant differences between the two cohorts, at 5 min. Statistically significant differences were not observed in the need for positive-pressure ventilation during initial resuscitation or length of hospital stay for patients with TTN between the two cohorts. Notably, the 37-week cohort exhibited a significantly higher incidence of TTN than did the 38-week cohort.

Conclusion

ECSs at 37 weeks of GA exhibited an increased risk of TTN than ECSs at ≥ 38 weeks of GA. Strategic neonatal care and adequate preparation can mitigate this risk without affecting the length of hospital stay.

Keywords: Apgar score, cesarean section, gestational age, positive-pressure respiration, transient tachypnea of the newborn

Normal vagin*l delivery is generally the preferred option for birth; however, cesarean section (CS) may be indicated for cases of abnormal labor or fetal concerns. CS can be categorized into emergency (EMCS) and elective CS (ECS), based on the urgency of the indication.

ECS is primarily performed for indications such as a breech presentation, repeated CS, prior uterine surgery, or abnormal placental position. The global prevalence of CS deliveries has been steadily increasing, including in Japan, where the proportion of births by CS has increased from 9.9% in 1987 to 24.8% in 2014, according to statistics from the Ministry of Health, Labour and Welfare.¹ Against this background, the optimal timing of CS has garnered recent attention, particularly concerning neonatal outcomes. Delaying CS until late-stage pregnancy is associated with concerns regarding an increase in the incidence of EMCS due to the onset of labor or rupture of membranes.²^,³ EMCS poses higher risks for both mothers and neonates than ECS.⁴^,⁵^,⁶

In Japan, the number of obstetric facilities has decreased because of a shortage of obstetricians and gynecologists, while an increase in deliveries by general practitioners who do not have an anesthesiologist on-site has been oberved.¹ Therefore, ECS is performed at the 37th week of gestational age (GA) at many facilities to avoid EMCS. However, emerging evidence suggests an elevated risk of transient tachypnea of the newborn (TTN) for neonates delivered via early-term CS.⁷^,⁸^,⁹^,¹⁰^,¹¹^,¹²^,¹³^,¹⁴ The incidence of TTN is higher in CS than that in vagin*l deliveries.¹⁵^,¹⁶ Principally, TTN is theoretically caused by the delayed absorption of alveolar fluid, particularly involving endogenous catecholamines, which occurs more commonly in ECS, without the onset of labor, than in vagin*l deliveries.¹⁷ Moreover, neonatal asphyxia resulting in circulatory failure can elevate central venous pressure, further impeding alveolar fluid absorption and exacerbating the risk of TTN.¹⁸

Multiple factors, including maternal conditions, delivery under general anesthesia, fetal distress, and low birthweight, have been associated with an increase in the incidence of postnatal respiratory disorders, including TTN. Furthermore, many studies have revealed that neonates born at < 39 weeks of GA have an increased risk of developing postnatal respiratory disorders; however, few studies have elucidated the associated risk factors.⁷^,¹⁰^,¹¹^,¹²^,¹³^,¹⁴

Consequently, herein, we conducted a retrospective analytic study to determine whether statistically significant differences existed in the clinical outcomes, particularly the incidence of TTN and need for neonatal intensive care, between neonates delivered via ECS at 37 weeks of GA and those delivered at ≥ 38 weeks of GA. This analysis was performed after controlling for pre-existing risk factors influencing respiratory conditions.

MATERIALS AND METHODS

Ethical considerations

This study was approved by the Ethics Review Committee of Tottori University School of Medicine (Approval Number: 20A111), and was conducted in accordance with the principles of the Declaration of Helsinki. Informed consent was obtained via an opt-out method, where participants were informed about the study and given the opportunity to decline participation. This process was endorsed by the Ethics Review Committee.

Study design, setting, and patient selection

From the 845 infants born via CS at Tottori University Hospital between January 2013 and December 2019, we retrospectively evaluated the medical records of 547 cases of ECS, with birth weights of ≥ 2500 g, born > 37 weeks of GA (Fig. 1).

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Fig. 1.

Schematic diagram of the inclusion of the study group population. Apgar score, appearance, pulse, grimace, activity, and respiration score; CS, cesarean section; GA, gestational age.

Tottori University Hospital is the only comprehensive perinatal medical center in the western part of the Tottori Prefecture, where approximately 150 CS deliveries are performed annually and cases deemed high-risk for either the mother or neonate are managed.

The exclusion criteria were as follows: 1) EMCS because of the onset of labor or rupture of membranes; 2) fetal distress or labor arrest; 3) placental abruption; 4) CS under general anesthesia; 5) multiple pregnancies; 6) maternal conditions, including gestational hypertension, diabetes, thyroid disorders, antipsychotic medication-use, and infections; and 7) fetal or neonatal anomalies, including congenital malformations, chromosomal abnormalities, central respiratory disorders, neonatal asphyxia, and infections. Neonatal asphyxia was defined as an appearance, pulse, grimace, activity, and respiration (Apgar) score of < 7. Following these criteria, a total of 288 cases were excluded, with 118 cases of ECS and 170 cases attributable to the various other exclusion criteria (Fig. 1).

Formation of cohorts

We analyzed the data by dividing the cases into two cohorts: births at 37 weeks of GA (37-week cohort) and births at ≥ 38 weeks of GA (38-week cohort). We retrospectively analyzed the medical records of each cohort, for the following variables: GA (in weeks) and indications for CS.

Moreover, for both the overall and TTN cases, neonatal information was evaluated, which included sex, birthweight, Apgar scores at 1 and 5 min, need for positive-pressure ventilation at birth, presence of post-admission complications, need for positive-pressure ventilation therapy post-admission, incidence of TTN, and length of hospital stay.

The length of hospital stay was defined as discharge occurring on the first postnatal day, i.e., a 1-day stay.

Neonatal care and monitoring

At our institution, neonates delivered via CS are admitted to the neonatal unit for observation of their respiratory and overall conditions. Post-admission, we monitored the saturation of peripheral oxygen (SpO₂), body temperature, heart and respiratory rates, and feeding and elimination status, thus ensuring a healthy overall condition of the neonates.

Neonates delivered via CS were discharged either on the day after birth (1-day stay), or the second day post-birth (2-day stay), if asymptomatic. After being discharged, neonates were able to stay in the same room with their mothers for the remainder of the 7-day period, the mothers’ typical length of hospitalization for ECS. Positive-pressure ventilation at birth was defined as requiring continuous positive airway pressure (CPAP) or use of a mask or bag–valve–mask ventilation. Moreover, positive-pressure ventilation therapy was defined as requiring CPAP therapy or management with a ventilator via intubation.

Post-admission complications included TTN, early vomiting, and hypoglycemia, as diagnosed by neonatologists. TTN was defined as a sustained respiratory rate of 60 breaths per minute, or CO₂ levels exceeding 50 mmHg for > 1 hour without improvement, requiring oxygen supplementation and positive-pressure ventilation therapy.

TTN discharge was defined as meeting all of the following criteria: the ability to wean off respiratory therapy, the absence of frequent episodes of tachypnea, CO₂ levels consistently < 50 mmHg, good oral intake, and stable SpO₂ levels > 95%.

Statistical analyses

Data are presented as numbers (percentages) or medians (ranges). The Mann–Whitney U and Fisher’s exact tests were used for continuous and categorical variables, respectively. Statistical significance was set at P < 0.05. Statistical analyses were performed using EZR version 1.55 (Easy R on R commander), designed for medical statistics, based on R version 4.1.2 (updated on 2021-11-01).¹⁹

RESULTS

Cohorts and complications

Of the 259 patients born via ECS in the study period, 188 and 71 were categorized into the 37-week and 38-week cohorts, respectively (Fig. 1). The indications of ECS shows Table 1. Post-admission complications and postnatal treatments, classified by GA, are presented in Table 2.

Table 1.

Indications of cesarean section

Gestational age	Total	Wk 37	Wk 38~	P value
	(n = 259)	(n = 188)	(n = 71)
Indications of cesarean section -no. (%)
Repeated	173 (66.8%)	122 (64.9%)	51 (71.8%)	0.529
Breech position	25 (9.7%)	21 (11.2%)	4 (5.6%)
Prior uterine surgery	31 (12.0%)	23 (12.2%)	8 (11.3%)
Abnormal placental malposition	23 (8.9%)	18 (9.6%)	5 (7.0%)
Others	7 (2.7%)	4 (2.1%)	3 (4.2%)

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Table 2.

Post-admission complications and postnatal treatments, categorized by the gestational age

Gestational age	Wk 37	Wk 38~
	(n = 188)	(n = 71)
Complications -no. (%)
TTN	49 (26.1%)	10 (14.1%)
Hypoglycemia	5 (2.7%)	2 (2.8%)
Vomiting	3 (1.6%)	3 (4.2%)
No symptoms	131 (69.7%)	56 (78.9%)
Therapy -no. (%)
Oxygen supplementation	14 (7.4%)	3 (4.2%)
CPAP	29 (15.4%)	7 (9.9%)
Mechanical ventilation	6 (3.2%)	0 (0.0%)
Infusion only	7 (3.7%)	1 (1.4%)
No therapy	132 (70.2%)	60 (84.5%)

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CPAP, continuous positive airway pressure; TTN, transient tachypnea of the newborn.

Clinical outcomes

Statistically significant differences were not observed in the indications for ECS, sex (male: 55.3% and 52.1%, respectively; P = 0.676) and birthweight distributions (g) [2798.5 (2504–3507) and 2816 (2535–3627), respectively; P = 0.444], between the 37-week and 38-week cohorts (Table 3). The 37-week cohort had a statistically significantly lower Apgar score at 1 min than did the 38-week cohort [8 (7–9) and 8 (7–9), respectively; P = 0.009] (Fig. 2a). However, the Apgar scores at 5 min showed no significant difference between the two cohorts [9 (7–10) and 9 (8–10), respectively; P = 0.241) (Fig. 2b).

Table 3.

Demographic and clinical characteristics of the patients

Gestational age	Wk 37	Wk 38~	P value
	(n = 188)	(n = 71)
Sex: male -no. (%)	104 (55.3%)	37 (52.1%)	0.676
Birthweight (g) (range)	2798.5 (2504–3507)	2816 (2535–3627)	0.444
Apgar score at 1 min (range)	8 (7–9)	8 (7–9)	0.009
Apgar score at 5 min (range)	9 (7–10)	9 (8–10)	0.241
Positive-pressure ventilation for initial resuscitation -no. (%)	82 (43.6%)	23 (32.4%)	0.119
Incidence rate of TTN-no. (%)	49 (26.1%)	10 (14.1%)	0.046
Respiratory support with positive-pressure ventilation therapy -no. (%)	35 (18.6%)	7 (9.9%)	0.093
Cases without symptoms at admission -no. (%)	169 (89.9%)	66 (93.0%)	0.631
: The cases of TTN developed after admission -no. (%)	32 (18.9%)	5 (7.6%)	0.045
Hospitalization days: all cases (d) (range)	1 (1–14)	1 (1–9)	0.144
: TTN which developed post-admission (d) (range), no.	7 (1–14), n = 49	6 (2–7), n = 10	0.245

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Apgar score, appearance, pulse, grimace, activity, and respiration score; TTN, transient tachypnea of the newborn.

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Fig. 2.

(a) Histogram of Apgar score at 1 min between two cohorts. (b) Histogram of Apgar score at 5 min between two cohorts. Apgar score, appearance, pulse, grimace, activity, and respiration score.

Statistically significant differences were not observed in the need for positive-pressure ventilation during initial resuscitation between the 37-week and 38-week cohorts (43.6% and 32.4%, respectively; P = 0.119). Notably, the 37-week cohort exhibited a significantly higher incidence of TTN than did the 38-week cohort (26.1% and 14.1%, respectively; P = 0.046). Nonetheless, the proportion of patients who received positive-pressure ventilation therapy did not differ statistically significantly between the 37-week and 38-week cohorts (18.6% and 9.9%, respectively; P = 0.093). The post-admission incidence of TTN, despite the absence of initial respiratory symptoms was notably higher in the 37-week cohort than that in the 38-week cohort (18.9% and 7.6%, respectively; P = 0.045). Statistically significant differences were not observed in the length of hospital stay (days), particularly for the cases of TTN, between the 37-week and 38-week cohorts [7 (1–14) and 6 (2–7), respectively; P = 0.245] (Fig. 3).

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Fig. 3.

Boxplot of hospitalization days for TTN cases between two cohorts.

DISCUSSION

This study was conducted in a setting in which all factors that could have potentially caused postnatal respiratory distress had been eliminated. Specifically, cases with an “Apgar score < 7” were excluded because their inclusion could potentially impact the assessment of TTN risk due to disorders in adapting to the extraterrestrial environment immediately after birth and other respiratory disorders. This was done to more accurately evaluate the risk of TTN based on GA. Thus, we were able to more precisely evaluate the impact of GA on the post-CS risk of respiratory disorders in neonates, particularly in the early-term period of 37 weeks of GA, within the defined range of full-term pregnancy. Moreover, the findings of this study highlighted the considerable impact of the timing of ECS on neonatal respiratory outcomes, particularly regarding the increased incidence of TTN in neonates delivered at 37 weeks GA compared to that of those delivered at ≥ 38 weeks of GA.

The primary findings of this study revealed lower Apgar scores at 1 min in the 37-week cohort normalized by 5 min, suggesting an initial respiratory adaptation challenge that resolved shortly, postnatally. Nonetheless, recovery occurred quickly, highlighting the importance of prompt neonatal care.

Using our approach, we aimed to assess the direct impact of GA on the incidence of TTN by excluding cases with known TTN-associated maternal conditions, including diabetes mellitus, as well as other factors, such as EMCS outside regular hours, neonatal asphyxia, and infections.²⁰^,²¹

Furthermore, this study reaffirmed the critical role of GA in neonatal respiratory health, suggesting that the increased incidence of TTN in the 37-week cohort, particularly after excluding pre-existing respiratory distress risk factors was likely due to less mature pulmonary systems and inadequate surfactant production.⁶ On the other hand, at ≥ 38 weeks of GA, these processes are expected to be more fully developed, improving lung function as the neonate begins to breathe. Therefore, subtle changes in lung maturity and surfactant production between 37 and 38 weeks of gestation could significantly impact the risk of respiratory disorders in neonates.

These findings align with those of the existing literature showing that lung maturity, including surfactant production capability, is not fully developed at 37 weeks of GA, contributing to the delayed absorption of alveolar fluid and subsequent TTN. Thus, the observed increase in TTN cases over time in the 37-week cohort, particularly among the initially symptom-free neonates implies that postnatal respiratory interventions, while temporarily effective, do not fully prevent TTN development.

Despite these challenges, no significant differences were observed in the need for positive-pressure ventilation therapy or treatment duration between the 37-week and 38-week cohorts, revealing that outcomes can be optimized with appropriate and timely neonatal care. This highlights the effectiveness of immediate postnatal interventions in managing respiratory complications, particularly with the slight prematurity associated with a delivery at 37 weeks of GA.

Neonates born at ≥ 38 weeks of GA who develop TTN tend to have longer periods of rooming-in with their mothers before discharge compared to those born at 37 weeks of GA and diagnosed with TTN. This suggests that neonates in the 37-week cohort may have limited opportunities for early bonding with their mothers. Therefore, when deciding on the timing of ECS in early-term pregnancies, it is essential to consider not only the increased risk of TTN but also the potential reduction in mother-infant contact time.

Tita et al. have shown that repeated ECS at 37 or 38 weeks of GA is more strongly correlated with adverse neonatal outcomes than 39 completed weeks of GA.⁷ In response, the American College of Obstetricians and Gynecologists has recommended redefining term pregnancies, categorizing 37–38, 39–40, and ≥ 41 weeks of GA, as “Early-term,” “Full-term,” and “Late-term,” respectively.²² However, in Japan, immediate transition to ECS > 39 weeks of GA poses challenges because of numerous factors, including staff constraints at healthcare facilities.

While delaying CS for a more mature GA may reduce respiratory symptoms, the rate of after-hours or EMCS increases.² Inter-facility factors influencing the determination of GA for performing an ECS relate not only to neonatal outcomes, such as the incidence of respiratory disorders, in addition to the crucial entity of the rate of EMCS. In smaller obstetric facilities, delaying the GA for ECS to reduce neonatal complications may increase the burden on staff.³^,²³ Moreover, over 90% of births in the United States of America occur in hospitals, with a trend towards the centralization of childbirth services. In Japan, 47.3% of deliveries occur in clinics,¹ resulting in a substantial number of vagin*l and CS deliveries occurring at healthcare facilities with limited medical staff and resources. These reasons may explain the preference in Japan for selecting a GA of ≤ 38 weeks for ECS, to minimize the factors that result in the conversion of a planned ECS to an EMCS.

Overall, this study found that the incidence of TTN was higher in the 37-week cohort than that in the 38-week cohort; however, no differences were observed in the need for positive-pressure ventilation therapy or length of hospital stay between the 37-week and 38-week cohorts. Providing medical care comparable to that of the 38-week cohort may be possible by preparing and implementing appropriate treatments. Anticipating and promptly responding to the occurrence of potential TTN for an ECS performed in the early-term of pregnancy is essential.

The study had a few limitations that should be mentioned: 1) the retrospective design may have introduced bias; 2) the rarity of an ECS > 39 weeks of GA at our institution, resulting in the small sample size from a single facility; and 3) the location in specialized center for high-risk cases may have introduced bias.

Overall, scheduling an ECS > 38 weeks of GA may be challenging in the Japanese healthcare system; thus, further research is required to assess the utility thereof. Nevertheless, this study revealed a higher incidence of TTN among neonates born at 37 weeks of GA than among those born at ≥ 38 weeks of GA, particularly after accounting for pre-existing risk factors associated with respiratory disorders. Overall, CS is correlated with an increased risk of TTN relative to that of vagin*l delivery; nevertheless, our findings suggest that with proper management of postnatal complications, the duration of hospital stay may not considerably differ between the two modes of delivery. The meticulous assessment of neonatal lung maturity and potential risks is vital in the strategic planning, adequate preparation, and management of early-term CS deliveries in order to mitigate the associated risks.

Acknowledgments

Acknowledgements: We would like to extend our sincerest gratitude to all of the mothers and neonates who participated in this study. We would further like to thank Editage (www.editage.jp) for English language editing.

Footnotes

Contributed by

AUTHOR CONTRIBUTIONS: YM and FM analyzed and interpreted the collected data analysis and wrote the first draft and contributed equally; MM, AI, HF, CM and KY contributed to the collection and analysis of the data and participated in the preparation or critical review of the article for important intellectual content; NN critically reviewed the article and revised the first draft.

The authors declare no conflict of interest.

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