Delayed umbilical cord clamping (DCC) allows the delivery of residual placental blood to a neonate. It is performed by clamping the umbilical cord more than 30 s after birth. Although performing DCC for more than 30 s is recommended, the exact definition regarding the duration remains unavailable [1]. According to a recent review article, DCC is beneficial to both preterm and full-term neonates [2]. Compared with early-cord-clamping, DCC reduces the need for anemia-induced blood transfusions and the incidence of intraventricular hemorrhage in preterm neonates [3]. In-hospital mortality is also decreased in preterm neonates with DCC experience [3, 4, 5]. Furthermore, DCC is associated with hematocrit increase and an improvement in iron stores in the first several months of life in full-term neonates [3]. The World Health Organization and international governing bodies for health care subsequently endorsed DCC [2]. However, in certain clinical situations, such as a nonvigorous neonate or a neonate requiring resuscitation, DCC is recommended to be avoided [6]. Similarly, early-cord-clamping is specifically advised in clinical situations such as maternal hemodynamic instability, maternal hemorrhage, abnormal placentation (placenta previa and abruption), and when the placental circulation is not assured, such as in cord avulsion or fetal growth restriction with abnormal Doppler sonography findings [6].

Clinically, when a neonate is nonvigorous immediately after birth (especially during a cesarean delivery), determining whether to proceed with DCC is difficult. In vaginal delivery, fetal status can be assessed by fetal heart rate monitoring (when available) until immediately before birth, but during a cesarean delivery, such an evaluation cannot be made until after birth. The Apgar score (omitting the heart rate) can be applied to assess neonatal condition on the cesarean operating table. Moreover, the initiation of crying, which represents well-established spontaneous respiration (SR) and a good transition from fetal to newborn life, is an another easy way to evaluate neonatal condition. If the initiation of crying is late during DCC, the neonate’s condition might be unfavorable even when the placental circulation with its gas exchange is maintained.

This study aimed to investigate any difference in cord arterial blood gas (cABG) parameters, as well as neonatal outcomes, according to the start of SR during DCC in cesarean section.

This study aimed to detect any difference in cABG parameters depending on SR onset during DCC in cesarean section. Regardless of the SR start time and GA at birth, all of the cABG parameters were within the normal range. In full-term neonates, PaCO${}_2$ was significantly lower in those who cried earlier than in those who cried later; however, the pH was not significantly associated with the onset of SR. In preterm neonates, the cABG parameters were almost equivalent for any onset of SR. Thus, even if a preterm neonate cries late, the cABG parameters yield no effects that may potentially affect neonatal prognosis.

Studies on the relationship between SR and DCC and their associations with perinatal outcomes are limited, especially for cesarean delivery. Ersdal et al. [7] observed that the mortality rate in neonates tends to be higher if the cord is clamped before or immediately after the SR onset. In particular, 60% of their neonatal group with a poor outcome had a time interval between the first breath and cord clamping of less than 30 s. In our study, approximately 95% of our neonates started crying within 30 s of birth (occurring before DCC), and no fetal deaths occurred. In full-term neonates, only two were admitted to the NICU, including one for the postnatal work-up of a prenatal arachnoid cyst and the other for intermittent oxygen desaturation during feeding. Recently, several studies have been conducted on maintaining DCC while providing assisted ventilation as necessary during cesarean section for early preterm neonates. According to these studies, maintaining DCC while providing assisted ventilation to preterm neonates with inadequate breathing is feasible [8, 9]. It confirmed umbilical vein pH values, but even with assisted ventilation, the values remained to have no significant difference. This finding is similar to our study, where even in preterm neonates who cried late, the pH values still did not significantly differ in the cABG analysis, although our study measured pH in the umbilical artery [8].

Studies on DCC and cABG have been conducted, but most of them included vaginal deliveries and different protocols. Longitudinal studies have measured changes in cABG parameters over time when DCC was performed. Conversely, some studies have compared cABG parameters between the DCC and early-cord-clamping groups. In a previous longitudinal study, pH decreased and PaO${}_2$ increased over time when DCC was performed in vaginal deliveries [10, 11]. Recently, Giovannini et al. [12] included cesarean deliveries and compared cABG parameters that were measured immediately after birth and 3 min later when DCC was performed in the cesarean and vaginal delivery groups. The cesarean deliveries had significantly increased pH and arterial lactate levels compared with vaginal deliveries, and the acid–base status tended to result in mixed acidosis. In our full-term cesarean deliveries, neonates with late SR onset tended to have lower pH and higher lactate, HCO${}_3$${}^{-}$, and PaCO${}_2$ levels, although most of the differences were not statistically significant. One possible explanation is that a faster SR corresponds to a higher likelihood of compensation for mixed acidosis. However, our preterm cesarean deliveries also did not show such tendency. The prematurity of the neonate’s gas exchange mechanism may have affected such results.

Most of the studies comparing cABG parameters between the DCC and early-cord-clamping groups have reported increased PaO${}_2$ levels in the DCC group [13, 14]. One previous study that included both cesarean and preterm deliveries reported that only PaO${}_2$ was higher in the DCC group than in the early-cord-clamping group [13]. The authors of this study hypothesized that adjustment to cABG clinical reference intervals is not necessary for deliveries using DCC. Other studies have interpreted PaO${}_2$ increment in DCC deliveries as a respiration effect of neonates [14]. Although the protocols and comparisons used in these previous studies were different from those in our study, our full-term neonates who started breathing earlier also tended to have increased PaO${}_2$ levels. However, our preterm neonates who started breathing earlier did not demonstrate the same increased PaO${}_2$ or decreased PaCO${}_2$, possibly because of the prematurity of the neonate’s gas exchange mechanism [15].

Our study’s major advantage was the clinical assistance in performing DCC during cesarean deliveries. Cesarean delivery contributes to maternal hypotension because of spinal anesthesia and being in a supine position. Maternal hypotension may lead to placental hypoperfusion, transient fetal hypoxia, and subsequent metabolic acidosis [16, 17]. Thus, determining whether DCC should be maintained for nonvigorous neonates, especially those who are not crying, is difficult. During cesarean section, SR, as represented by crying, is an easy way to assess neonatal condition. Nevertheless, cABG analysis is recommended to evaluate birth asphyxia and adverse perinatal events [1]. Currently, evidence on DCC efficacy in resuscitation scenarios reportedly remains limited. One small randomized study reported on safety outcomes for DCC in such scenarios. The preterm neonates who were included in the study had a median 1 min Apgar score of 2, which indicates weakness; however, those who underwent DCC demonstrated increased hematocrit level at 72 h and a decreased requirement for transfusions in the first 28 days of life [18]. Nonvigorous neonates are more likely to benefit from placental transfusion obtained through DCC because of the continued gas exchange occurring via the intact placental circulation [6]. In addition, the feasibility of applying resuscitation to prolong DCC for unstable neonates has been previously demonstrated [19, 20]. More recently, the concept of physiology-based cord clamping (PBCC), which involves cord clamping when the neonate achieves stable SR with an adequate heart rate, was introduced and demonstrated to be beneficial [21]. Resuscitation can also be used to assist in achieving PBCC. However, the benefits of DCC and PBCC are not yet fully clear; thus, their application in nonvigorous neonates remains uncertain.

This study has several limitations that warrant discussion. First, the low number of neonates with late SR onset makes comparisons with early SR onset less reliable. Second, most of the preterm neonates were late preterm rather than early preterm; hence, this study may not adequately reflect information on early preterm neonates because late preterm neonates could be more similar to full-term neonates in some aspects. This similarity can be observed in our results. Third, this study equated SR with crying during the analysis. Some infants may begin SR without crying, whereas others may start crying without initiating SR. Differentiating these two actions during cesarean section is very challenging. Considering these limitations, to generalize the findings of this study, we need to evaluate as well the neonate’s tone alongside crying when assessing the need for resuscitation. Additionally, conducting studies involving a higher number of neonates, particularly preterm ones, could provide more meaningful results using multivariate analysis and other statistical methods.

In all preterm and full-term neonates, all cABG parameters were within the normal range regardless of the SR start time. However, given the small number of cases and limitations of this study, we cautiously suggest that maintaining DCC in cesarean deliveries may be considered, even when the start of crying is delayed, while further research is needed to establish a more definitive recommendation.

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

JHK designed the research study, wrote the manuscript. HEK and SC analyzed the data. JWA conceived the the study and gave final approval of the version to be published. All authors contributed to editorial changes in the manuscript. All authors read and approved the final manuscript. All authors have participated sufficiently in the work and agreed to be accountable for all aspects of the work.

All subjects gave their informed consent for inclusion before they participated in the study. The study was conducted in accordance with the Declaration of Helsinki, and the protocol was approved by the Ethics Committee of Ulsan University hospital Institutional Review Board (approval number: 2021-10-031-002).

Thanks to all the peer reviewers for their opinions and suggestion.

This research received no external funding.

The authors declare no conflict of interest.