# Assessment of colour-code protocol and neonatal outcomes for emergency caesarean sections

Marie-Alice Yanni, Oriane Vetier, Linda Lassel, Helene Isly, Isabelle Enderle,

Maela Le Lou

► To cite this version:

Marie-Alice Yanni, Oriane Vetier, Linda Lassel, Helene Isly, Isabelle Enderle, et al. Assessment of colour-code protocol and neonatal outcomes for emergency caesarean sections. Journal of Gynecology Obstetrics and Human Reproduction, 2025, 54 (5), pp.102932. 10.1016/j.jogoh.2025.102932. hal-04982013

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Original Article

# Assessment of colour-code protocol and neonatal outcomes for emergency caesarean sections

Marie-Alice Yanni<sup>a, *</sup>, Oriane Vetier<sup>b</sup>, Linda Lassel<sup>a</sup>, Hélène Isly<sup>a</sup>, Isabelle Enderlé<sup>a</sup>, Maela Le Lou<sup>a, c</sup>

<figure><img src="image_3.png" /></figure>

ARTICLE INFO

Keywords:

Emergency caesareans

Colour-code protocol

Decision-delivery interval

Neonatal outcomes

Maternal complications

A B S T R A C T

**Context:** The use of colour codes for emergency caesareans has significantly improved team communication and protocol compliance over time. However, the impact on neonatal prognosis remains to be demonstrated.

**Objectives:** Our main objective was to evaluate changes in neonatal morbidity and mortality over time for orange-code (decision-delivery interval ≤ 30 mins) and red-code caesareans (decision-delivery interval ≤ 15 mins), since the introduction of the colour-code protocol. The secondary objectives were to describe maternal complications and types of anaesthesia.

**Methods:** This retrospective single-centre observational study was carried out in the maternity ward of the Rennes University Hospital and included all patients for whom an emergency caesarean was performed with an orange or red code between 1st January 2015 and 31st December 2021. A composite endpoint of neonatal morbidity and mortality was defined as the primary outcome. A sample of 1301 patients and 1346 newborns was analysed.

**Results:** Compliance with the colour-code protocol increased significantly during the study period to reach in 2021 97.8 % usage of appropriate colour codes according to the indication (p < 0.0001) and 92.1 % concordance between the colour code and the decision-delivery interval (p < 0.0001). In contrast, changes in neonatal outcomes were minimal and not statistically significant (p = 0.5873). However, the risk of maternal complications did not increase and there was no difference in the rate of general anaesthesia (p = 0.2002).

**Conclusion:** The colour-code protocol did not show significant changes in neonatal outcomes but remains a relevant reference tool to coordinate the labour ward teams.

Introduction

Originally exceptional, caesarean has become one of the most performed surgical procedures worldwide and has saved many lives. In France, the last National Perinatal Survey of 2021 showed that 21.4 % of all deliveries were by caesarean section [1].

In the setting of emergency caesareans, it is important to establish clear indications and decision-delivery intervals. Indeed, the capacity for rapid analysis is crucial in obstetrics and every minute counts. In cases of a subacute hypoxia, the neonatal cord pH drops by 0.01 every 2–3 mins, and by 0.01 every minute in cases of an acute hypoxia [2]. Reducing the decision-delivery interval has been shown to reduce neonatal morbidity [3].

To date, however, there is no international consensus on the ideal

decision-delivery interval [4]. A multicentre study in 2017 involving 26 maternity wards in France showed persistent disparities [5]. In 2000, Dupuis *et al*. developed a classification and colour code for non-elective caesareans using three categories according to the degree of emergency: [6,7]

- Green code for non-urgent non-elective caesareans with a decision-delivery interval ≤ 1 hour,

- Orange code for non-extreme emergencies with a recommended decision-delivery interval ≤ 30 mins,

- Red code for caesareans in extreme emergency with an immediate threat to the maternal or foetal vital prognosis and a decision-delivery interval ≤ 15 mins.

<footnote><sup>a</sup> Department of Obstetrics, Gynecology and Human Reproduction, University Hospital of Rennes, France</footnote>

<footnote><sup>b</sup> Department of Obstetrics and Gynecology, Hospital of Saint Brieuc, Brittany, France</footnote>

<footnote><sup>c</sup> University of Rennes, INSERM, LTSI - UMR 1099, Rennes F-35000, France</footnote>

<footnote>* Corresponding author.</footnote>

<footnote>E-mail address: marie-alice.yanni@chu-rennes.fr (M.-A. Yanni).</footnote>
This colour-code protocol was introduced in the maternity ward of the Rennes University Hospital (France) in 2014 for emergency caesareans before or during labour. In 2020, a local retrospective study conducted by Vetier *et al.* showed a significant improvement in compliance with the colour-code protocol over time [8]. They reported an increase in the use of the appropriate colour code, compliance with the decision-delivery interval, more detailed data reporting in the obstetric files, and better coordination between the healthcare teams. However, the effect on neonatal morbidity remained inconclusive.

The main objective of the current study was to assess neonatal morbidity and mortality over time after an emergency caesarean since the introduction of the colour-code protocol. The secondary objectives were to assess maternal complications and anaesthetic procedures, particularly the use of general anaesthesia.

## Methods

### Study design

This retrospective single-centre observational study was conducted over a 7-year period between 2015 and 2021 in the maternity ward of Rennes University Hospital (France). The ward is a tertiary maternal-foetal centre performing 3700 deliveries per year, 18.8 % of which are by caesarean section. Emergency caesareans represent 13 % of all deliveries.

### Population

All patients who underwent an emergency caesarean with an orange or red code between 1st January 2015 and 31st December 2021 were included. The inclusion criteria were singleton or multiple pregnancies, at least 24 weeks of gestation, and absence of documented disapproval to participate in research. Indeed, all the patients have been informed of their right of opposition. Patients were excluded if they had an elective or a green-code caesarean.

### Protocol

The labour ward of the Rennes University Hospital has 14 delivery rooms and three adjoining operating theatres for caesareans. The attending medical team is composed of four midwives and four childcare assistants around the clock with an additional midwife specifically designated for caesareans between 8:00 a.m. and 4:00 p.m. One obstetrician, two obstetric interns, one anaesthetist, one intern anaesthetist, one neonatologist pediatrician and one pediatric intern are also present on site.

The use of the colour-code protocol based on Dupuis *et al.*'s model was established in our centre in 2014. Each colour corresponds to a series of indications, a recommended decision-delivery interval, and specifies the roles of the different caregivers. The green code corresponds to a decision-delivery interval ≤ 1 hour for arrest of cervical dilation, labour induction failure, or foetal dystocic presentations with no foetal hypoxia. The orange code corresponds to a decision-delivery interval ≤ 30 mins and is attributed to non-extreme emergencies including foetal heart rate abnormalities on cardiotocography (CTG), failed instrumental delivery, or eclampsia. Finally, the red code corresponds to a decision-delivery interval ≤ 15 mins and is attributed to situations of immediate threat to the mother's life or acute foetal hypoxia. It is assigned in the event of foetal bradycardia, failed instrumental delivery with foetal heart rate abnormalities on CTG, cord prolapse, suspicion of placental abruption or uterine rupture, severe maternal haemorrhage, or maternal heart failure. In cases not included in this protocol, the obstetrician is free to assign a colour code according to their analysis of the situation and to deliver the baby within the corresponding interval.

### Nature of the collected data

Data were collected using DxCare® software by searching for the keywords "Delivery by caesarean during labour by laparotomy" and "Delivery by emergency caesarean except labour by laparotomy". The medical information department of the hospital provided the exhaustive list of concerned files. If information was lacking in the computerized files, paper files were also consulted, including partograms or CTG recordings.

The data extracted concerned maternal age, body mass index, gravidity, parity, history of scarred uterus, and singleton or multiple pregnancy. The occurrence of foetal death was also noted. Data concerning the caesarean section included the gestational age at which it was performed, whether it was before or during labour, and possible labour induction. Peroperative data comprised the incision time, operative technique and duration, surgical difficulties, and total blood loss. In terms of anaesthesia, epidural analgesia prior to caesarean was recorded as well as the type of anaesthesia during the operation. The indication for the caesarean and the colour code were reported for each patient to ensure their concordance. As part of the analysis of compliance with the colour-code protocol and the changes in neonatal outcomes, the decision-delivery interval was calculated using the time of the decision to perform a caesarean and the time of birth. Compliance of this interval with the colour code was checked.

### Primary and secondary outcomes

The primary outcome was the composite endpoint of neonatal morbidity and mortality. Even if there is no consensus about this, we chose to apply the pediatric definition of peripartum asphyxia and included an APGAR score at 5 mins < 7, and/or an arterial pH < 7.00 at birth, and/or an arterial lactate level > 7.00mmol/L, and/or admission of the new-born to the neonatal intensive care unit, and/or therapeutic hypothermia, and/or neonatal death.

The secondary endpoints were related to maternal outcomes, including operative duration, length of hospitalization after delivery, possible adverse events such as postpartum haemorrhage (bleeding > 500 mL), infection, or pelvic-organ wound with potential surgical reintervention. Finally, anaesthesia modalities and the rate of general anaesthesia were studied.

We also planned subgroup analysis according to the gestational age and to the colour code. These groups were defined a priori.

### Statistical analysis

Quantitative variables are described using the effective N, mean and standard deviation, minimum, first quartile (Q1), median, third quartile (Q3), and maximum. A parametric ANOVA model was used for normal distribution. Otherwise, a nonparametric Kruskal-Wallis test was performed. The variable "year" was treated as a categorical variable. For qualitative variables, the effective N and the percentage are presented for each modality. The groups were compared using a parametric Chi² test or a nonparametric Fisher test. The non-independence of the data compared was taken into account in particular for twins. A mixed generalized linear model was applied for binary data, and a linear mixed model was used for quantitative data. Data were transformed into ranks if the variable did not follow a normal distribution. We made comparisons of the years between them. These analyses were carried out using the software SAS®, version 9.4.

### Ethics approval

The study was carried out after approval from the local ethics committee of the Rennes University Hospital, obtained on 23rd September 2020 (Reference: 20.119).
# Results

## Obstetrics activity at the Rennes University Hospital and patient selection

According to the colour-code protocol, the green code was applied for caesareans with no real acute risk of maternal or foetal distress, and for which a strict interval between the decision to perform a caesarean and birth would not seem to influence neonatal prognosis. After exclusion of this category, 1301 patients were included, for whom an orange- or red-code caesarean was performed between 1st January 2015 and 31st December 2021. (Fig. 1)

## Characteristics of the study population

Descriptive maternal, pregnancy and childbirth data are presented in Table 1. The patients were 30.7 ± 5.7 years old. 665 (51.1 %) patients were primiparous, and 23.8 % presented with a scarred uterus. There were mostly singleton pregnancies (96.2 %). Foetal death occurred in four (0.3 %) cases. 82.6 % of caesareans were performed during labour, and 37.3 % were performed after labour induction. The mean gestational age at delivery was 38.3 weeks of pregnancy (24.4; 37.1; 39.7; 41.0; 43.1), and 23.4 % of the caesareans were performed before 37 weeks of gestation. These data were similar overall from one year to another, although there were significant differences for primiparity ($p = 0.0351$), singleton pregnancies ($p = 0.0443$), and labour induction ($p = 0.0195$).

Using a Chi² test, 853 (65.6 %) patients had an orange-code caesarean and 358 (27.5 %) had a red-code caesarean. The remaining 90 (6.9 %) situations corresponded to an absence of mention of colour code or to caesareans classified as green code despite an indication corresponding to an orange code. The colour code was absent for 86 (6.6 %) patients, including 67 patients (44.1 %) in 2015 and none in 2020 or 2021.

The main indication for orange-code caesareans was foetal heart rate abnormalities. Foetal bradycardia was the main indication for red-code caesareans. Compliance with the colour code according to the indication significantly improved over the years, reaching 97.8 % in 2021 ($p < 0.0001$). The agreement between the decision-delivery interval and colour code also gradually increased to reach 92.1 % in 2021 ($p < 0.0001$).

## Results on the primary outcome

At birth, the arterial pH was $7.18 \pm 0.14$, and the arterial lactate level was $6.1 \pm 3.3$. Arterial pH < 7 was found in $8.7\%$ of the cases with a slight but non-significant change over time ($12.3\%$ in 2015 against $9.6\%$ in 2021, $p = 0.5432$). $31.3\%$ of the new-borns had an arterial lactate level > 7.00 mmol/L, which also slightly, but not significantly, changed

<figure><img src="image_4.png" /><figcaption>Fig. 1. Patient flowchart.</figcaption></figure>
<table><caption>**Table 1**
Maternal and pregnancy characteristics in the overall population and for each year.</caption><thead><tr><th rowspan="2"></th><th colspan="2">Maternal population<br>(n = 1301)</th><th colspan="2">2015 (n = 152)</th><th colspan="2">2016 (n = 173)</th><th colspan="2">2017 (n = 226)</th><th colspan="2">2018 (n = 196)</th><th colspan="2">2019 (n = 207)</th><th colspan="2">2020 (n = 161)</th><th colspan="2">2021 (n = 186)</th><th rowspan="2">p</th></tr><tr><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th></tr></thead><tbody><tr><td>Maternal age</td><td>30.7 ± 5.7</td><td></td><td>31.2 ± 5.7</td><td></td><td>30.6 ± 5.6</td><td></td><td>30.0 ± 5.7</td><td></td><td>30.8 ± 5.6</td><td></td><td>30.8 ± 5.3</td><td></td><td>31.6 ± 5.9</td><td></td><td>30.5 ± 5.8</td><td></td><td>p = 0.1620 (A)</td></tr><tr><td>BMI before pregnancy</td><td>25.5 ± 5.7</td><td></td><td>25.2 ± 5.4</td><td></td><td>25.3 ± 6.1</td><td></td><td>24.7 ± 4.9</td><td></td><td>25.7 ± 5.9</td><td></td><td>25.8 ± 5.9</td><td></td><td>25.9 ± 6.0</td><td></td><td>26.0 ± 5.9</td><td></td><td>p = 0.1727 (A)</td></tr><tr><td>Primiparity</td><td>665 (51.1 %)</td><td></td><td>69 (45.4 %)</td><td></td><td>94 (54.3 %)</td><td></td><td>133 (58.8 %)</td><td></td><td>96 (49.0 %)</td><td></td><td>91 (44.0 %)</td><td></td><td>88 (54.7 %)</td><td></td><td>94 (50.5 %)</td><td></td><td>p = 0.0351 (K)</td></tr><tr><td>Multiparity</td><td>636 (48.9 %)</td><td></td><td>83 (54.6 %)</td><td></td><td>79 (45.7 %)</td><td></td><td>93 (41.2 %)</td><td></td><td>100 (51.0 %)</td><td></td><td>116 (56.0 %)</td><td></td><td>73 (45.3 %)</td><td></td><td>92 (49.5 %)</td><td></td><td></td></tr><tr><td>Singleton</td><td>1252 (96.2 %)</td><td></td><td>150 (98.7 %)</td><td></td><td>167 (96.5 %)</td><td></td><td>221 (97.8 %)</td><td></td><td>190 (96.9 %)</td><td></td><td>198 (95.7 %)</td><td></td><td>148 (91.9 %)</td><td></td><td>178 (95.7 %)</td><td></td><td>p = 0.0443 (K)</td></tr><tr><td>Twin pregnancy</td><td>49 (3.8 %)</td><td></td><td>2 (1.3 %)</td><td></td><td>6 (3.5 %)</td><td></td><td>5 (2.2 %)</td><td></td><td>6 (3.1 %)</td><td></td><td>9 (4.3 %)</td><td></td><td>13 (8.1 %)</td><td></td><td>8 (4.3 %)</td><td></td><td></td></tr><tr><td>Fetal death</td><td>4 (0.3 %)</td><td></td><td>1 (0.7 %)</td><td></td><td>1 (0.6 %)</td><td></td><td>0 (0.0 %)</td><td></td><td>0 (0.0 %)</td><td></td><td>0 (0.0 %)</td><td></td><td>1 (0.6 %)</td><td></td><td>1 (0.5 %)</td><td></td><td>p = 0.5503 (F)</td></tr><tr><td>Uni-scared uterus</td><td>288 (22.1 %)</td><td></td><td>36 (23.7 %)</td><td></td><td>34 (19.7 %)</td><td></td><td>36 (15.9 %)</td><td></td><td>48 (24.5 %)</td><td></td><td>56 (27.1 %)</td><td></td><td>39 (24.2 %)</td><td></td><td>39 (21.0 %)</td><td></td><td>p = 0.1259 (K)</td></tr><tr><td>Multi-scared uterus</td><td>22 (1.7 %)</td><td></td><td>5 (3.3 %)</td><td></td><td>3 (1.7 %)</td><td></td><td>2 (0.9 %)</td><td></td><td>2 (1.0 %)</td><td></td><td>4 (1.9 %)</td><td></td><td>2 (1.2 %)</td><td></td><td>4 (2.2 %)</td><td></td><td>p = 0.6676 (F)</td></tr><tr><td>Caesarean during labour</td><td>1074 (82.6 %)</td><td></td><td>123 (80.9 %)</td><td></td><td>146 (84.4 %)</td><td></td><td>174 (77.0 %)</td><td></td><td>165 (84.2 %)</td><td></td><td>174 (84.1 %)</td><td></td><td>139 (86.3 %)</td><td></td><td>153 (82.3 %)</td><td></td><td>p = 0.2301 (K)</td></tr><tr><td>Labour induction</td><td>485 (37.3 %)</td><td></td><td>43 (28.3 %)</td><td></td><td>75 (43.4 %)</td><td></td><td>99 (43.8 %)</td><td></td><td>72 (36.7 %)</td><td></td><td>81 (39.1 %)</td><td></td><td>55 (34.2 %)</td><td></td><td>60 (32.3 %)</td><td></td><td>p = 0.0195 (K)</td></tr><tr><td>Gestational age</td><td>38.3 ± 3.9</td><td></td><td>38.4 ± 3.6</td><td></td><td>38.3 ± 3.8</td><td></td><td>38.1 ± 4.1</td><td></td><td>38.0 ± 3.9</td><td></td><td>38.5 ± 3.6</td><td></td><td>38.5 ± 3.9</td><td></td><td>38.1 ± 4.1</td><td></td><td>p = 0.7521 (KW)</td></tr><tr><td>Gestational age &lt;37WG</td><td>304 (23.4 %)</td><td></td><td>35 (23.0 %)</td><td></td><td>44 (25.4 %)</td><td></td><td>56 (24.8 %)</td><td></td><td>46 (23.5 %)</td><td></td><td>45 (21.7 %)</td><td></td><td>32 (19.9 %)</td><td></td><td>46 (24.7 %)</td><td></td><td>p = 0.8932 (K)</td></tr></tbody></table>

BMI: body mass index (weight in kilograms/size² in meters). Results are expressed as mean ± standard deviation and number n (percentage %). K= Chi² test, F= Fisher test, KW= Kruskal-Wallis test, A= ANOVA.

<table><caption>**Table 2**
New-borns data, in overall population and by year.</caption><thead><tr><th rowspan="2"></th><th colspan="2">Newborns<br>population (n = 1346)</th><th colspan="2">2015 (n = 153)</th><th colspan="2">2016 (n = 178)</th><th colspan="2">2017 (n = 231)</th><th colspan="2">2018 (n = 202)</th><th colspan="2">2019 (n = 216)</th><th colspan="2">2020 (n = 173)</th><th colspan="2">2021 (n = 193)</th></tr><tr><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th></tr></thead><tbody><tr><td>Arterial pH &lt; 7</td><td>111 (8.7 %)</td><td></td><td>17 (12.3 %)</td><td></td><td>17 (10.6 %)</td><td></td><td>14 (6.3 %)</td><td></td><td>15 (7.8 %)</td><td></td><td>18 (8.6 %)</td><td></td><td>12 (7.1 %)</td><td></td><td>18 (9.6 %)</td><td></td><td></td></tr><tr><td>Arterial lactate level &gt; 7mmol/L</td><td>415 (31.3 %)</td><td></td><td>52 (34.4 %)</td><td></td><td>46 (26.6 %)</td><td></td><td>64 (27.8 %)</td><td></td><td>70 (35.5 %)</td><td></td><td>75 (35.2 %)</td><td></td><td>50 (29.2 %)</td><td></td><td>58 (30.2 %)</td><td></td><td></td></tr><tr><td>APGAR score at 5 mins &lt; 7</td><td>200 (14.9 %)</td><td></td><td>20 (13.1 %)</td><td></td><td>20 (11.2 %)</td><td></td><td>35 (15.2 %)</td><td></td><td>28 (13.9 %)</td><td></td><td>37 (17.1 %)</td><td></td><td>23 (13.5 %)</td><td></td><td>37 (19.4 %)</td><td></td><td></td></tr><tr><td>Hospitalization in intensive care unit or neonatology</td><td>467 (34.7 %)</td><td></td><td>52 (34.0 %)</td><td></td><td>65 (36.5 %)</td><td></td><td>85 (36.8 %)</td><td></td><td>67 (33.2 %)</td><td></td><td>73 (33.8 %)</td><td></td><td>53 (30.6 %)</td><td></td><td>72 (37.3 %)</td><td></td><td></td></tr><tr><td>Therapeutic hypothermia</td><td>35 (2.6 %)</td><td></td><td>3 (2.0 %)</td><td></td><td>4 (2.2 %)</td><td></td><td>7 (3.0 %)</td><td></td><td>4 (2.0 %)</td><td></td><td>5 (2.3 %)</td><td></td><td>6 (3.5 %)</td><td></td><td>6 (3.1 %)</td><td></td><td></td></tr><tr><td>Neonatal death</td><td>32 (2.4 %)</td><td></td><td>5 (3.3 %)</td><td></td><td>3 (1.7 %)</td><td></td><td>4 (1.7 %)</td><td></td><td>6 (3.0 %)</td><td></td><td>6 (2.8 %)</td><td></td><td>3 (1.7 %)</td><td></td><td>5 (2.6 %)</td><td></td><td></td></tr><tr><td></td><td>1318 (28)</td><td></td><td>147 (6)</td><td></td><td>171 (7)</td><td></td><td>227 (4)</td><td></td><td>201 (1)</td><td></td><td>212 (4)</td><td></td><td>170 (3)</td><td></td><td>190 (3)</td><td></td><td></td></tr><tr><td>Primary outcome</td><td>718 (54.5 %)</td><td></td><td>83 (56.5 %)</td><td></td><td>89 (52.0 %)</td><td></td><td>121 (53.3 %)</td><td></td><td>110 (54.7 %)</td><td></td><td>128 (60.4 %)</td><td></td><td>88 (51.8 %)</td><td></td><td>99 (52.1 %)</td><td></td><td></td></tr></tbody></table>

Qualitative parameters: Number n (percentage %). Quantitative parameters: Mean ± standard deviation (min; Q1; median; Q3; max). Primary outcome: APGAR score at 5 mins &lt;7, arterial pH &lt;7, hospitalization in neonatology, therapeutic hypothermia, and neonatal death. Mixed generalized linear model: *p* = 0.5873.
<figure><img src="image_5.png" /><figcaption>Fig. 2. Changes in the primary endpoint over time in overall population, for orange or red codes.</figcaption></figure>

over the study period (34.4 % in 2015 and 30.2 % in 2021, *p* = 0.5285). The APGAR score at 5 mins was < 7 in 14.9 % of the cases: 13.1 % in 2015 compared with 19.4 % in 2021. 34.7 % of the new-borns were hospitalized in the intensive care or neonatology unit (34 % in 2015 and 37.3 % in 2021), for an average duration of 34.4 days (1.0; 9.0; 22.0; 50.0; 400.0). The rate of therapeutic hypothermia for neuroprotection was stable at 2.6 %. Neonatal death occurred for 32 (2.4 %) infants in the overall population with annual numbers ranging from three (1.7 %) to six (3 %). Overall, the primary outcome was present for 718 (54.5 %) of the 1318 new-borns in the general population (56.5 % in 2015 and 52.1 % in 2021, *p* = 0.5873) (Table 2).

We then carried out a subgroup analysis according to gestational age. For full-term births (i.e., after 37 weeks of gestation), 10.8 % of the new-borns had an APGAR score at 5 mins < 7, 7.8 % had an arterial pH < 7, and 30.8 % an arterial lactate level > 7.00mmol/L. In 2015, 11.5 % had a pH < 7 compared with 5 % in 2021. 16.4 % of the full-term new-borns were hospitalized, and 2.4 % were placed in therapeutic hypothermia. The primary outcome was present for 43.2 % of these new-borns in 2015, versus 36 % in 2021 (*p* = 0.2571).

We also carried out a subgroup analysis according to the colour code (Fig. 2). Among orange-code caesareans, 50.5 % of 872 new-borns presented the primary endpoint with a pH threshold defined at 7 (52.4 % in 2015 and 46.2 % in 2021, *p* = 0.5886). As there is no consensus in the literature about the pH at which the neonatal prognosis is impacted, we reassessed the composite primary endpoint after modifying the pH threshold. When using a less severe threshold, our results indicated clinically interesting differences, although they were still not statistically significant. When the threshold pH value was set at < 7.15, 54.4 % of new-borns presented the primary endpoint (61.9 % in 2015 and 47.7 % in 2021, *p* = 0.3154). A clinical difference was suggested in the neonatal condition since the protocol was included, especially for orange-code and full-term caesareans (*p* = 0.2109). Among red-code caesareans, 63.8 % of 384 new-borns presented the primary outcome with a pH threshold of 7 (67.6 % in 2015 and 64.4 % in 2021, *p* = 0.9634). At a pH threshold of 7.15, 70.7 % of these new-borns presented the primary endpoint (78.4 % in 2015 and 69.5 % in 2021, *p* = 0.7815).

## Results on the secondary outcomes

### Maternal complications

Maternal data concerning surgery, postoperative course, and

complications are presented in Table 3. Overall, 8.9 % of the mothers had postpartum haemorrhage with a rate of 6.5 % in 2021 (*p* < 0.0001). The overall rate of severe bleeding (≥ 1000 mL) was 5.5 %, but there was no significant difference between the years (*p* = 0.1310).

No difference emerged in the analysis according to the colour code. However, the rate of postpartum haemorrhage seemed slightly higher for the red-code caesareans, with a rate of 10.3 % versus 7.9 % for the orange-code caesareans (*p* = 0.1598). (Fig. 3)

### Anaesthesia

Epidural analgesia was used for 67.3 % of the patients before their caesarean. Overall, 56.6 % of the caesareans were performed with epidural anaesthesia, 15.6 % with spinal anaesthesia, and 27.7 % under general anaesthesia. The rate of general anaesthesia did not vary over time: 25 % in 2015, 31.8 % in 2016, 28 % in 2020 and 34.4 % in 2021 (*p* = 0.2002, chi² test) (Table 3).

Epidural anaesthesia was the main type of anaesthesia for orange-code caesareans (64.2 %), while general anaesthesia was more frequent for the red codes (58.1 % versus 16.4 % for the orange-code, *p* < 0.0001).

## Discussion

### Main neonatal results

Compliance with the colour-code protocol increased significantly over time, reaching 97.8 % usage of the appropriate colour code for the indication in 2021 (*p* < 0.0001) and 92.1 % concordance between the colour code and the decision-delivery interval (*p* < 0.0001). These results are in agreement with those of Le Mitouard et al. [5] and of the previous study conducted in our centre in 2020 [8].

We did not find any statistically significant change in the neonatal morbidity and mortality over time (*p* = 0.5873). The primary endpoint was present for 43.2 % of the children born after 37 weeks of gestation in 2015 compared with 36 % in 2021 (*p* = 0.2571). In this group, considering pH only, 11.5 % had a pH < 7 in 2015 versus 5 % in 2021 (*p* = 0.2309). These results suggest a small clinical difference since the protocol was introduced, especially in the orange-code and full-term caesarean group (*p* = 0.2109).

Red-code caesareans represented 7.88 % of all the caesareans in our study and 1.49 % of all deliveries. These figures are consistent with those from Dubois et al. who reported a rate of 1.9 % of all deliveries in
<table><caption>**Table 3**
Analysis of maternal secondary endpoints.</caption><thead><tr><th></th><th>Maternal population<br>(n = 1301)</th><th>2015 (n = 152)</th><th>2016 (n = 173)</th><th>2017 (n = 226)</th><th>2018 (n = 196)</th><th>2019 (n = 207)</th><th>2020 (n = 161)</th><th>2021 (n = 186)</th><th>p</th></tr></thead><tbody><tr><td>Total loss (blood + amniotic fluid) (milliliters)</td><td>406 ± 343</td><td>414 ± 307</td><td>436 ± 321</td><td>407 ± 264</td><td>364 ± 291</td><td>427 ± 525</td><td>374 ± 317</td><td>422 ± 287</td><td>0.0168 (KW)</td></tr><tr><td>Haemorrhage</td><td>116 (8.9 %)</td><td>16 (10.5 %)</td><td>37 (21.4 %)</td><td>34 (15.0 %)</td><td>8 (4.1 %)</td><td>4 (1.9 %)</td><td>5 (3.1 %)</td><td>12 (6.5 %)</td><td>&lt; 0.0001 (K)</td></tr><tr><td>Severe haemorrhage</td><td>71 (5.5 %)</td><td>6 (3.9 %)</td><td>16 (9.2 %)</td><td>12 (5.3 %)</td><td>5 (2.6 %)</td><td>14 (6.8 %)</td><td>7 (4.3 %)</td><td>11 (5.9 %)</td><td>0.1310 (K)</td></tr><tr><td>Operative duration (minutes)</td><td>40 ± 16</td><td>43 ± 15</td><td>41 ± 14</td><td>40 ± 14</td><td>38 ± 13</td><td>39 ± 21</td><td>42 ± 17</td><td>42 ± 15</td><td>0.0002 (KW)</td></tr><tr><td>Length of maternal hospitalization (nights)</td><td>6.6 ± 2.5</td><td>6.5 ± 2.5</td><td>6.4 ± 2.5</td><td>6.7 ± 2.5</td><td>6.6 ± 2.6</td><td>7.1 ± 2.8</td><td>6.4 ± 1.9</td><td>6.1 ± 2.5</td><td>&lt; 0.0001 (KW)</td></tr><tr><td>Venous thromboembolic disease</td><td>1 (0.1 %)</td><td>0 (0.0 %)</td><td>0 (0.0 %)</td><td>0 (0.0 %)</td><td>0 (0.0 %)</td><td>1 (0.5 %)</td><td>0 (0.0 %)</td><td>0 (0.0 %)</td><td>0.8263 (F)</td></tr><tr><td>Infection</td><td>16 (1.2 %)</td><td>3 (2.0 %)</td><td>5 (2.9 %)</td><td>2 (0.9 %)</td><td>5 (2.6 %)</td><td>0 (0.0 %)</td><td>0 (0.0 %)</td><td>1 (0.5 %)</td><td>0.0242 (F)</td></tr><tr><td>Bladder wound</td><td>9 (0.7 %)</td><td>2 (1.3 %)</td><td>0 (0.0 %)</td><td>1 (0.4 %)</td><td>1 (0.5 %)</td><td>2 (1.0 %)</td><td>2 (1.2 %)</td><td>1 (0.5 %)</td><td>0.7618 (F)</td></tr><tr><td>Preeclampsia, HELLP syndrome</td><td>32 (2.5 %)</td><td>4 (2.6 %)</td><td>3 (1.7 %)</td><td>6 (2.7 %)</td><td>4 (2.0 %)</td><td>6 (2.9 %)</td><td>3 (1.9 %)</td><td>6 (3.2 %)</td><td>0.9700 (F)</td></tr><tr><td>Surgical reintervention</td><td>18 (1.4 %)</td><td>1 (0.7 %)</td><td>2 (1.2 %)</td><td>3 (1.3 %)</td><td>3 (1.5 %)</td><td>4 (2.5 %)</td><td>114 (70.8 %)</td><td>2 (1.1 %)</td><td>0.9246 (F)</td></tr><tr><td>Epidural analgesia before caesarean</td><td>874 (67.3 %)</td><td>97 (63.8 %)</td><td>113 (65.7 %)</td><td>142 (63.1 %)</td><td>147 (75.0 %)</td><td>144 (69.6 %)</td><td>114 (70.8 %)</td><td>117 (62.9 %)</td><td>0.0845 (K)</td></tr><tr><td>Anaesthesia for caesarean</td><td>737 (56.6 %)</td><td>81 (53.3 %)</td><td>89 (51.4 %)</td><td>127 (56.2 %)</td><td>125 (63.8 %)</td><td>124 (59.9 %)</td><td>95 (59.0 %)</td><td>96 (51.6 %)</td><td></td></tr><tr><td>Epidural anaesthesia</td><td>203 (15.6 %)</td><td>33 (21.7 %)</td><td>29 (16.8 %)</td><td>38 (16.8 %)</td><td>24 (12.2 %)</td><td>32 (15.5 %)</td><td>21 (13.0 %)</td><td>26 (14.0 %)</td><td></td></tr><tr><td>Spinal anaesthesia</td><td>361 (27.7 %)</td><td>38 (25.0 %)</td><td>55 (31.8 %)</td><td>61 (27.0 %)</td><td>47 (24.0 %)</td><td>51 (24.6 %)</td><td>45 (28.0 %)</td><td>64 (34.4 %)</td><td></td></tr><tr><td>General anaesthesia</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td>0.2002 (K)</td></tr></tbody></table>

Total loss = blood and amniotic fluid in milliliters. Length of hospitalization in number of nights.

K= Chi² test, F= Fisher test, KW= Kruskal-Wallis test.

Grenoble in 2021 [9]. According to Lagrew et al., these extreme emergency situations concern 1 to 2 % of deliveries overall [10]. With a pH threshold set at 7, primary endpoint was present for 63.8 % of the new-borns in this group (67.6 % in 2015 and 64.4 % in 2021, *p* = 0.9634).

## Maternal secondary results

The risk of maternal complications remained stable. We found a reduction in postpartum haemorrhage with a rate of 6.5 % in 2021 (*p* < 0.0001), and the overall rate of severe haemorrhage was 5.5 % (*p* = 0.1310). This can be explained by the reduction in the use of oxytocin during labour and the new protocol for the preventive administration of oxytocin at birth. There was no difference according to the colour code. Indeed, as demonstrated by Weiner et al. and Le Mitouard et al., the introduction of such a protocol reducing the decision-delivery interval is not associated with more maternal complications [11,5]. However, we did observe a slightly higher rate of postpartum haemorrhage in red-code caesareans (10.3 %) compared with orange-code caesareans (7.9 %) (*p* = 0.1598). These figures are consistent with the incidence of postpartum haemorrhage in France which occurs in between 5 and 10 % of deliveries [12,13]. This finding suggests that a red code should not be attributed inappropriately as they could increase the risk of postpartum haemorrhage.

In our study, 27.7 % of the caesareans were performed using general anaesthesia: 16.4 % for orange-code caesareans, most often because of insufficient primary epidural or spinal anaesthesia, and 58.1 % for red-code caesareans (*p* < 0.0001). This point also reflects the importance of correct allocation of the red code. As recommended by the French Society of Anaesthesia-Resuscitation, in the event of a caesarean in extreme emergency, most red-code caesareans are performed under general anaesthesia, which would theoretically increase maternal risks [14].

Overall then, it would appear essential to carefully assess the indications for an emergency caesarean and not to attribute a red-code excessively. On this subject, Bloc et al. found that only a third of red-code caesareans were actually indicated [15].

## Strengths and limitations of the study

Our study of 1301 patients and 1346 newborns – one of the largest series assessing the colour-code protocol – ensures representative results.

However, some limitations deserve to be mentioned. The retrospective design has inherent biases, particularly concerning missing data. In addition, this was a single-centre study, in a tertiary care centre with all practitioners on duty and none on call, which suggests limitation in the external validation of the results in other types of maternity units.

As there is no trend test, the notion of decrease over time is not tested. Indeed, we have only tested the notion of difference over time. For some outcomes, there is a visible increase, for example in 2019 and the primary outcome, therefore the evolution over time is not linear.

Furthermore, we did not take into account changes in routine practice that occurred over the 7-year study period such as the use of oxytocin, national labour recommendations, simulation training..., which could impact maternal and foetal outcomes.

Another shortcoming is that we did not explore the parents' feelings or satisfaction rates, the mothers' psychological state, or the mother-child bond [16,17]. The indication for an emergency caesarean and the presence of a colour code can contribute to patient anxiety, particularly if a red code is mentioned [18,19]. Thus, trying to understand how the patient adapts their behaviour is an important issue for better maternal, foetal, and neonatal care.
<figure><img src="image_6.png" /><figcaption>**Fig. 3.** Maternal complications according to the colour code (orange or red).</figcaption></figure>

## Implications and perspectives

Despite the neonatal data suggesting a clinically relevant change, our results did not reach significance. Other publications support these findings and have not reported any significant improvement in neonatal status associated with a reduction in the decision-delivery interval [20, 21]. But these observations do not mean that reducing the decision-delivery interval has no effect on neonatal outcomes [22]. Red-code caesareans correspond to the situations most at risk of acidosis and severe hypoxia. The pathology leading to emergency caesarean seems to bear more weight in neonatal prognosis than compliance with the protocol and a short decision-delivery interval [23]. In this setting it may be difficult, or indeed impossible, to avoid an unfavourable outcome despite a rapidly induced birth.

Some French teams have chosen not to use this global colour-code protocol, with the exception of a specific red-code procedure in the event of an extreme emergency, allowing alerts and better communication between the healthcare teams. However, we can maintain that non-elective caesarean sections are at higher risk in terms of maternal and foetal morbidity than elective caesareans, justifying the protocol. Grabarz et al. found more complications in case of caesareans performed during labour, depending on the degree of emergency, which mainly concerned haemorrhage and infection [24].

Finally, a successful outcome for a non-elective caesarean depends on the expertise of the team, and the indications must always be applied with caution. To this end, a study using a Delphi expert consensus method conducted in Grenoble (France) in 2021 developed a tool to help teams assess whether a red-code caesarean is really relevant [10].

## Conclusion

The use of the colour-code protocol in our centre was associated with a reduction in the decision-delivery interval over time. Our observations also demonstrate a slight but not significant change in neonatal morbidity and mortality, without increasing maternal complications. Even if the impact of this colour-code protocol on neonatal morbidity is not statistically proven, it remains clinically relevant as each avoided perinatal death or brain injury represents a victory in itself. Each baby counts.

## Funding

None.

## Ethics approval

The local ethics committee of Rennes University Hospital approved the study (Reference 20.119).

## Declaration of competing interest

The authors report no conflict of interest.

## References

[1] Enquête Nationale Périnatale, rapport 2021, les naissances, le suivi à deux mois et les établissements, situation et évolution depuis 2016. October 2022.

[2] Ghi T, Chandraharan E, Fieni S, Dall'Asta A, Galli L, Ferretti A, Ricciardi P, Locatelli A, Lambicchi L, Bellussi F, Pilu G, Frusca T. Correlation between umbilical vein-to-artery delta pH and type of intrapartum hypoxia in a cohort of academic neonates: a retrospective analysis of CTG findings. Eur J Obst Gynecol Reprod Biol 2018;231:25-9.

[3] Kayani SI, Walkinshaw SA, Preston C. Pregnancy outcome in severe placental abruption. British J Obstet Gynecol 2003;110:679-83.

[4] Grobman WA, Bailit J, Sandoval G, Reddy UM, Wapner RJ, Varner MW, et al. The association of decision-to-incision time for cesarean delivery with maternal and neonatal outcomes. Am J Perinatol 2018;35(3):247-53.

[5] Le Mitouard M, Gaucher L, Huissoud C, Gaucherand P, Rudigoz RC, Dupont C, Cortet M. Decision-delivery intervals: impact of a color code protocol for emergency caesareans. Eur J Obst Gynecol Reprod Biol 2020;246:29-34.

[6] Dupuis O, Sayegh I, Decullier E, Dupont C, Clément H-J, Berland M, et al. Red, orange and green caesarean sections: a new communication tool for on-call obstetricians. Eur J Obstet, Gynecol Reprod Biol 2008;140(2):206-11.

[7] Lucas DN, Yentis SM, Kinsella SM, Holdcroft A, May AE, et al. Urgency of caesarean section: a new classification. J R Soc Med 2000;93(7). 346-50.

[8] Vetier O, Yanni MA, Lassel L, Isly H, Beuchée A, Nyangoh-Timoh K, Lavoué V, Beranger R, Le Louis M. Assessment of compliance with color code protocol for non-elective cesarean section and its impact on time to delivery interval and neonatal outcomes. J Gynecol Obst Human Reprod 2023;52:102510.

[9] Dubois C, Preaubert L, Forey PL, Equy V, Riethmuller D. Césariennes en code rouge : établissement d'une grille de pertinence permettant l'analyse d'une année de pratique en CHU. Gynécologie Obstétrique Fertilité et Sénologie 2022;50(Issue 2): 436.

[10] Lagrew DC, Bush MC, McKeown AM, Lagrew NG. Emergent (crash) cesarean delivery: indications and outcomes. Am J Obstet Gynecol 2006;51(6):16381643. 194.

[11] Weiner E, Bar J, Fainstein N, Ben-Haroush A, Sadan O, Golan A, et al. The effect of a program to shorten the decision-to-delivery interval for emergent cesarean section on maternal and neonatal outcome. Am J Obstet Gynecol 2014;210.

[12] Deneux-Tharaux C, Bonnet MP, Tort J. Epidémiologie de l'hémorragie du post-partum. J de Gynécologie Obstétrique et Biologie de la Reprod 2014;43(Issue 10): 936-50.

[13] Say L, Chou D, Gemmill A, et al. Global causes of maternal death: a WHO systematic analysis. Lancet Global Health 2014;2(6):e323-33.

[14] Guglielminotti J, Landau R, Li G. Adverse events and factors associated with potentially avoidable use of general anesthesia in cesarean deliveries. Anesthesiology 2019;130(6):912922.

[15] Bloc F, Dupuis O, Massardier J, Gaucherand P, Doret M. Are we overusing of crash c-section procedure? J Gynecol Obstet Biol Reprod (Paris) 2010;39(2). 133-8.
[16] Bodin E, Peretti V, Rouillay J, Tran PL, Boukerrou M. Posttraumatic stress disorder and emergency cesarean delivery: incidence and risk factors. Gynecol Obstet Fertility Senol 2022;50(Issue 3):240-60.

[17] Froeliger A, Deneux-Tharaux C, Loussert L, Madar H, Sentilhes L. Tranexamic acid for preventing postpartum hemorrhage after Cesarean Delivery (TRAAP2) trial study group. Posttraumatic stress disorder 2 months after cesarean delivery: a multicenter prospective study. Am J Obstet Gynecol 2024. S0002-9378(24)00440-X.

[18] Ryding EL. Experience of emergency cesarean section: a phenological study of 53 women. Birth 1998;25(4):246-51.

[19] Andersen LB, Melvaer LB, Videbech P, Lamont RF, Joergensen JS. Risk factors for developing post-traumatic stress disorder following childbirth: a systematic review. Acta Obstet Gynecol Scand 2012;91(11):12611272.

[20] Tolcher MC, Johnson RL, El-Nashar SA, West CP. Decision-to-incision time and neonatal outcomes: a systematic review and meta-analysis. Obstet Gynecol 2014; 123:536-48.

[21] Leung TY, Lao TT. Timing of caesarean section according to urgency. Best Practice Res Clin Obstet Gynecol 2013;27:251-67.

[22] Grobman WA, Bailit J, Sandoval G, Reddy UM, Wapner RJ, Varner MW, et al. The association of decision-to-incision time for cesarean delivery with maternal and neonatal outcomes. Am J Perinatol 2018;35(3):247-253.

[23] Pierre F, Rudigoz RC. Emergency caesarean delivery: is there an ideal decision-to-delivery interval? J Gynecol Obstet Reprod Biol 2008;37:41-7.

[24] Grabarz A, Ghesquière L, Debarge V, Ramdane N, Delporte V, Bodart S, et al. Cesarean section complications according to degree of emergency during labor. Eur J Obstet Gynecol Reprod Biol 2021;256:320-5.