Respiratory outcomes of neonates born after previable premature rupture of membranes and treated with gentle ventilation

doi:10.21203/rs.3.rs-3759277/v1

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Respiratory outcomes of neonates born after previable premature rupture of membranes and treated with gentle ventilation

https://doi.org/10.21203/rs.3.rs-3759277/v1

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published 31 May, 2024

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Objective: We aim to describe neonatal respiratory outcomes following previable preterm premature rupture of membranes(PPROM) when gentle ventilation is utilized. We also report maternal morbidity and mortality.

Study Design: This is a retrospective single center cohort study of infants delivered between 2016 and 2020 that included infants born at ≥23 weeks without major congenital anomaly after a pregnancy complicated with PPROM before 23-week gestation. Statistical analysis utilized unpaired Student’s t test or Mann-Whitney U test when appropriate.

Results: 35 infants from 33 pregnancies were included. 91.4% of infants survived until discharge and 12.1% developed Bronchopulmonary Dysplasia(BPD). Those who developed BPD had significantly lower amniotic fluid levels prior to delivery(p<0.05). There was no significant maternal morbidity or mortality in this cohort.

Conclusion: This cohort had high survival and low rates of respiratory morbidities. This suggests the use of gentle ventilation might be the optimal strategy for patients born after previable PPROM.

Health sciences/Diseases/Respiratory tract diseases

Health sciences/Health care/Paediatrics

Approximately one third of preterm births are complicated by preterm premature rupture of membranes (PPROM), defined as chorioamniotic membrane rupture before 37 weeks gestation.[1] Previable PPROM, or PPROM occurring before 23 weeks gestational age (GA), results in a wide range of neonatal morbidities and increased risk of mortality in addition to potential maternal complications.

PPROM is almost always associated with prematurity, the degree of which is widely understood to be the greatest predictor of neonatal outcomes.[2] However, GA at membrane rupture is also an independent risk factor for poor outcomes, and when controlling for GA at birth, infants born after previable PPROM have more severe morbidities and higher mortality.[3] Respiratory outcomes are particularly severe given the association of PPROM with oligo- and anhydramnios, consequently with some degree of pulmonary hypoplasia. Thus, infants born prematurely after previable PPROM are at high risk of developing severe respiratory distress syndrome (RDS) requiring long term mechanical ventilation and subsequently bronchopulmonary dysplasia (BPD).[2] These complications are the sources of both short- and long-term morbidity in infants.[2]

The level IV Neonatal Intensive Care Unit (NICU) at Columbia University Irving Medical Center (CUIMC) offers a unique approach of “gentle ventilation” utilizing bubble CPAP (bCPAP) for premature infants with respiratory failure. This approach has been associated with decreased use of mechanical ventilation, less chronic lung disease, and excellent respiratory outcomes which are reflected in our institution’s BPD rate of 9% between 2016 and 2018.[4-7] Outcomes for premature infants born after previable PPROM and managed with “gentle ventilation” have not yet been described, and an elucidation of these outcomes may contribute to a fuller understanding of best management for these infants.

This study aims to assess short- and long-term respiratory outcomes of premature neonates delivered at >23 weeks GA exposed to previable PPROM and treated with “gentle ventilation”. The secondary aims are to describe neonatal survival and maternal mortality and PPROM-related morbidities.

Background:

CUIMC Pregnancy management with previable PPROM

Patients who experience PPROM at a previable gestation and opt for expectant management, are admitted at 23 weeks and receive latency antibiotics and corticosteroids for fetal lung maturity. Magnesium for fetal neuroprotection is administered for those at risk of imminent preterm delivery at less than 32 weeks of gestation. Prior to 23 weeks, patients undergo weekly sonogram and clinical assessment. At-home temperature checks and self-monitoring for symptoms and signs of infection, abruption, and labor are recommended, with antibiotics deferred until inpatient admission.

'Gentle ventilation’ approach

Our institution provides bCPAP as a first step treatment for spontaneously breathing premature infants with respiratory distress syndrome (RDS). We utilize the Fisher Paykell CPAP system (East Tamaki, New Zeland) with the use of Hudson nasal prongs (Northfield, Illinois USA).[8] bCPAP pressure is achieved by varying the resistance to flow in the expired tubing by using water seal. Unlike other CPAP delivery systems, bCPAP creates pressure oscillation from the bubbles created due to the water seal, which is transmitted back to the nares to deliver a variable rather than constant pressure.[5] Intubation, mechanical ventilation and surfactant administration are offered only when bCPAP failure occurs. bCPAP failure is defined as inadequate oxygenation with a fraction of inspired oxygen equal or greater than 0.6, or respiratory acidosis with an arterial pH less than 7.20 or hypercapnia with PaCO2 greater than 65, or frequent episodes of apnea requiring frequent stimulation or bag mask ventilation.[5] Our comfort in managing critically ill patients with bCPAP is reflected in the overall low rate of intubation. As previously reported, greater than 70% of infants weighing between 1001 and 1500 grams with respiratory distress syndrome were successfully managed with bCPAP alone. Furthermore only 27% of infants less than 1500 grams required exogenous surfactant administration as compared to 61% within the Vermont Oxford Network (VON).[9, 10]

Study Sample

We conducted a retrospective single center cohort study of infants delivered at CUIMC between January 2016 and December 2020 to mothers whose pregnancies were complicated by PPROM prior to 23 weeks’ gestation. This study was approved by the Institutional Review Board at CUIMC (IRB-AAAS0452). Due to the retrospective study design parental consent was not required. Infants who were delivered prior to 23 weeks gestation were excluded, as during the study period resuscitation was not offered to infants born lower than this GA. Infants with severe congenital anomalies were excluded, as were infants whose parents opted for a comfort care approach rather than ICU intervention.

For each infant identified antenatal and clinical characteristics were collected. Maternal clinical characteristics and outcomes were also collected. In addition, for those infants who remained within our network, long term follow-up data on respiratory outcomes were captured in the chart review.

Definitions:

Oligohydramnios is defined as the amniotic fluid index (AFI), calculated as the sum of the deepest pockets of amniotic fluid in the four quadrants of the uterus, being less than 5 cm. Anhydramnios is defined as an amniotic fluid index of 0 cm.

For the purpose of this study the VON definition of BPD is utilized to describe the BPD rate within this cohort. The VON defines BPD as any supplemental oxygen requirement at 36 week post menstrual age or if an infant is transferred to another institution on supplemental oxygen prior to 36 weeks post menstrual age.

Statistical analysis:

Data are expressed as absolute numbers and mean or medians where appropriate based on normality of the data as determined by the Shapiro Wilk-test. Statistical analysis was carried out using unpaired Student’s t test or Mann Whitney U test when appropriate. This analysis was utilized for comparison of those with and without the combined outcome of BPD/death as well as the comparison of those who required and did not require intubation. Statistical analysis using the Chi-Squared test was utilized to determine if there was an association between the cause of PPROM (spontaneous vs. procedural) and the combined outcome of BPD/death.

A correlation analysis of length of stay with GA at rupture of membranes (ROM), GA at delivery and lowest AFI level during the pregnancy was performed. The correlation coefficient is expressed as Pearsons’s coefficient or Spearman’s coefficient where appropriate based on the normality of the data as determined by the Shapiro Wilk- test. For all statistical tests, statistical significance was accepted at a p-value less than 0.05. Study data was analyzed using JASP software (v 0.18).[11]

Thirty-five premature neonates, delivered at or after 23 weeks GA were identified. Patient characteristics are shown in Table 1. We included 26 singletons and nine neonates from seven multiple gestation pregnancies with verified previable PPROM, defined as PPROM < 23 weeks gestation. Of the seven multiple gestations, one was a tri-chorionic tri-amniotic triplet pregnancy which resulted in PPROM of Triplet A. Six monochorionic diamniotic twins experienced PPROM of either both or only one Twin. Only those multiples directly exposed to PPROM were included. All infants included in this study demonstrated either oligohydramnios or anhydramnios at least one time point during the pregnancy. Those who opted to pursue comfort care were excluded from analysis.

Table 1
1a. Maternal Characteristics
Pregnancies	33
Maternal age (years) **	33.0 (5.5)
Multiple Gestations^	7 (21.2%)
Any Prenatal steroids^	31 (93.9%)
Complete Course of Prenatal Steroids^	29 (87.9%)
Antibiotics ^	30 (90.1%)
Maternal mortality	0
Sepsis	0
Chorioamnionitis^	5 (15.2%)
Cord prolapse^	1 (3.0%)
Abruption^	6 (18.2%)
Cesarian section^	24 (72.7%)
Classical C-section^	8(18.2%)
1b. Fetal Characteristics
Fetuses affected by PPROM	35
GA at rupture of membrane (weeks)**	21.0 (4.5)
Latency (days)*	62.6 (30.3)
Oligohydramnios^	23 (65.7%)
Anhydramnios^	12 (34.3%)
Lowest AFI (cm)**	1.4 (2.75)
Male neonate^	23 (65.7%)
GA at birth (weeks)**	29.0 (5.0)
Birthweight (grams)**	1150 (800)
* (mean +/- standard deviation)
**(median +/- IQR)
^ absolute number (percentage)

Respiratory outcomes during the initial admission are shown in Table 2. 22 patients (63%) in this cohort did not require mechanical ventilation and were managed utilizing bCPAP as the only mode of respiratory therapy. In terms of postnatal management, three patients (9.1%) required postnatal steroids to assist with extubation and two patients (5.7%) needed treatment for pulmonary hypertension. When looking at the combined outcome of death or BPD, those affected by this outcome had a significantly lower AFI than those without, (0cm vs 2cm, p < 0.05, Table 3). When considering prenatal interventions, prenatal steroids were not given or were incomplete in all pregnancies that resulted in death before discharge (n = 3). The two infants who died in the delivery room were not exposed to any prenatal steroids. One infant who died during the NICU stay and was diagnosed with severe BPD had not received a complete course of prenatal steroids. GA at time of rupture was not significantly different between those who had survival without BPD and those who either died or developed BPD (19.7 weeks vs 19.5 weeks, p > 0.05, Table 3). There was no association of BPD/Death and cause of PPROM (procedure related vs. spontaneous). 90.9% of the patients in this cohort were discharged home on room air and no patient in the cohort required a tracheostomy. As seen in Fig. 1, length of stay was most strongly associated with GA at time of delivery. There was no association with GA at time of rupture and a weak association with AFI level.

Table 2

Neonatal Outcomes
2a. Delivery Room Outcomes	n = 35
Survival of initial resuscitation^	33 (94.3%)
CPAP at birth^	29 (82.9%)
Intubated first day of life^	11 (31.4%)
Chest compressions first day of life^	4 (11.4%)
Inotropic drips first day of life^	4 (11.4%)
Surfactant^	12 (34.3%)
2b. NICU Outcomes	n = 33
Duration of any respiratory support (days)**	29 (65.0)
Duration intubation/MV for respiratory failure (days) (n = 13) **	8 (17.0)
CPAP only during admission^	22 (66.7%)
Required high frequency oscillatory ventilation^	4 (12.1%)
Pneumothorax^	4 (12.1%)
Treated with DART protocol^	3 (9.1%)
At post-menstrual age 36 weeks on any respiratory support^	10 (30.3%)
At post-menstrual age 36 weeks with O2 requirement^	4 (12.1%)
Pulmonary Hypertension requiring treatment^	2 (5.7%)
Death before discharge^	1 (3.0%)
Discharged home^	32 (97.0%)
Discharge home in room air^	30 (90.9%)
Total Deaths in DR and NICU^ (n = 35)	3 (8.6%)
* (mean +/- standard deviation)
**(median +/- IQR)
^ absolute number (percentage)

Table 3

Neonatal Respiratory Outcomes
	Intubation not required (n = 22)	Intubation and MV Required (n = 13)
GA at ROM (weeks)*	19.33 (2.60)	20.36(1.36)
Lowest AFI (cm) *, ^	2.18 (1.70)	0.65 (0.83)
GA at birth (weeks)*	29.38 (3.62)	27.09 (2.51)
	Survival without BPD ( n = 29)	Death or BPD (n = 6)
GA at ROM (weeks)*	19.69 (2.38)	19.50 (2.17)
Lowest AFI (cm)**,^	2 (2.80)	0 (0.68)
GA at birth (weeks)*,^	29.24 (3.33)	25.83 (2.64)
* (mean +/- standard deviation)
**(median +/- IQR)
^p < 0.05

Long term follow-up data was available for 20 of the 32 patients who survived to hospital discharge. These patients were seen at our institution up until an average age of three and a half years with follow-up ranging from one to seven years of age. Of these 20 patients, one patient who is three years old has significant respiratory morbidity and requires CPAP overnight for lung disease.

Maternal morbidity was low within our cohort. There was no maternal mortality or clinical sepsis within our cohort (Table 1a).

To our knowledge, this study is the first to examine respiratory outcomes in neonates exposed to previable PPROM and treated with “gentle ventilation”.

The study suggests that the use of “gentle ventilation” is associated with better short- and long-term respiratory outcomes and improved survival to discharge than expected in this particularly vulnerable population. In our cohort, there was no severe maternal morbidity or mortality associated with expectant management of previable PPROM.

Previable PPROM has historically been associated with very poor respiratory outcomes, including BPD, pulmonary hypertension, and need for prolonged mechanical ventilation, as well as with high mortality and all-cause morbidity. Previous studies have found variable, but overall high incidence of BPD in neonates born after previable PPROM. Wagner (2016) reported an incidence of BPD of 32% in a population of 40 neonates born at 25–27 weeks GA who were admitted for intensive care to the NICU.[12] Sim (2020) reported an even higher incidence of BPD of 84.4% for neonates born at any GA and admitted to the NICU.[13] Paulsen (2023) reported a 22.2% incidence of BPD among neonates admitted to the NICU, while Manuck (2014) reported 49.5% incidence of BPD.[3, 14] In comparison, our center’s incidence of BPD was markedly lower, with 12.1% of 33 neonates admitted to the NICU meeting VON criteria for BPD. That said, the aforementioned studies did not include what definition of BPD they utilized, making direct comparisons difficult, as reported by Kim (2020).[4]

In our cohort, no infants required a tracheostomy, and only two infants were discharged home with oxygen delivered via Nasal Cannula. In addition, our finding of a 5.7% incidence of pulmonary hypertension is lower than reports of pulmonary hypertension in similar groups. In Bhat’s 2011 study of extremely low birthweight infants, 17.9% of their cohort had pulmonary hypertension.[15] Yum (2018) recently investigated the impact of histologic chorioamnionitis on pulmonary hypertension, the overall incidence of pulmonary hypertension in those with and without evidence of histologic chorioamnionitis was reported to be 14.9%. This cohort was similar to our study in terms of GA at birth and birthweight, with the exception that only 20.7% of these reported pregnancies were complicated by PPROM.[16] Though long term follow up is limited to only 20 patients in this cohort, only one patient had any significant respiratory illness reported.

The low incidence of BPD in our population is likely linked to very limited use of mechanical ventilation. Prior studies have found that mechanical ventilation was required for many or most neonates born after previable PPROM, including 80% of neonates in Wagner’s 2016 study who were intubated for a median duration of five days.[12] At our center, however, only 37.5% of neonates were mechanically ventilated for median duration eight days. Our center’s focus on “gentle ventilation” with the use of bCPAP, likely accounts for the lower rates of mechanical ventilation that may in turn be related to lower incidence of BPD, due to less exposure to volutrauma and barotrauma. Kim (2021) recently reported the rate of BPD for all infants born at or before 32 weeks at our center to be as low as 9%.[4]

When we evaluated prenatal characteristics, we found both a need for mechanical ventilation and LOS to be associated with the degree of oligohydramnios based on AFI level. In addition, the combined outcome of BPD or death was also associated with the level of oligohydramnios. This is in keeping with previously published studies, with rates of BPD after oligohydramnios in previable PPROM as high as 68.1%.[17] Oligohydramnios is known to be a predictor of poor respiratory outcomes independently of PPROM, and its association with morbidity in PPROM is thus unsurprising. Of note, within our cohort all pregnancies were complicated by either oligohydramnios or anhydraminos, suggesting that the infants in this cohort were likely at increased risk of poor respiratory outcome compared to infants in other studies who did not experience oligohydramnios in the setting of previable PPROM.

Prematurity is also known to be a predictor of poor respiratory outcomes. We found that GA at birth to be associated with need for mechanical ventilation, the combined outcome of BPD or death, and longer LOS. These findings are consistent with previous reports, including Esteves (2016), Can (2022) and Imterat (2019), which reported an earlier GA at delivery to be a predictor of poor neonatal composite outcomes including respiratory morbidities in previable PPROM.[18–20]

Notably, however, in our population GA at ROM was not associated with poor outcomes including need for mechanical ventilation and BPD/death, nor was earlier GA at ROM associated with LOS (Fig. 1). This finding was in contrast to prior studies, including Weiner (2019), Pendse (2021), LeMoine (2020), and Kibel (2016), in which GA at ROM was a predictor of poor respiratory outcomes.[21–24] Our results indicate that neonatal outcomes may be impacted by prematurity and degree of oligohydramnios to a greater degree than by GA at ROM, which would suggest that previable PPROM itself is a less important risk factor for unfavorable outcomes than these commonly associated comorbidities.

Verspyck (2014) found previable PPROM to be an independent risk factor for composite adverse respiratory outcomes, including BPD and PH, with incidence of 62.8% among 35 infants born after 24 weeks GA following PPROM between 14 and 24 weeks GA, as compared to 22.8% among 70 infants without PPROM.[25] Our center’s comparatively lower rates of respiratory morbidities after previable PPROM are in line with the center’s overall positive respiratory outcomes, which is likely associated with prioritization of “gentle ventilation”.

Reported overall morbidity and mortality rates in PPROM have varied widely. Many articles report low rates of survival and in those who do survive high rates of morbidity. Kibel (2016) reported overall survival rates of 49% in a cohort of 104 neonates born after PPROM between 20 and 23 weeks GA, although the survival rate among neonates admitted to the NICU was 77%.[24] Esteves (2009) reported a similar survival rate of 46% among all neonates born after previable PPROM, with a significantly higher survival rate of 88% when they excluded those born before viability and treated with comfort care.[18] LeMoine (2020) reported survival rate of only 28% for those neonates born after previable PPROM.[23] Other studies, however, have reported much better survival rates. Wagner (2016) reported a 95% survival rate when all but 2 of 40 neonates born after previable PPROM survived to discharge.[12] Our data most closely resembles this latter category, with survival to discharge of 91.4% of infants, and death of only one neonate after admission to the NICU. These results are likely linked to our previously-discussed positive respiratory outcomes but may also reflect our calculation of mortality, which excludes neonates treated with comfort care. Our results demonstrate the impact of antenatal steroid administration on respiratory outcomes. The three deaths in our study were secondary to respiratory failure, affecting two infants who died on the first day of life despite full resuscitation and a third who died at three months of life secondary to intractable BPD. Interestingly, prenatally, these infants did not receive a complete two-day course of betamethasone prior to delivery. This finding adds to the significant existing body of literature supporting antenatal steroids in prematurity and supports the argument for antenatal steroids in previable PPROM specifically.

Prior studies have reported a range of maternal morbidities associated with previable PPROM. Dotters-Katz (2017) reported 14% composite maternal morbidity in patients who elected for expectant management after previable PPROM, of which the most common causes of morbidity were postpartum hemorrhage and endometritis.[26] The authors also found 1.2% incidence of sepsis, but no maternal deaths. Within our study there were no instances of maternal sepsis or mortality. While there were no incidences of severe maternal morbidity or mortality, 18.2% of the women in this cohort required a classical c-section which can impact management of future pregnancies.

One of the limitations of this study is that it is a cohort from a single center, and thus the results are not generalizable to other institutions who do not practice respiratory management with an approach of “gentle ventilation”. That said, these results reflect the positive outcomes one can achieve when such approach is followed by all practitioners in the NICU, from attending physicians to bedside nurse. Another limitation is the relatively small sample size.

One of the strengths of the study is that all patients within this cohort were exposed to either anhydramnios or oligohydramnios during fetal life. This sets it apart from other studies such as Simons (2020) that have a larger sample size, but only slightly more than half of those included in that cohort were exposed to oligohydramnios during fetal life.[27]

Our findings of overall favorable outcomes for neonates exposed to previable PPROM, include high survival and low rates of respiratory morbidities. In addition, our respiratory outcomes may be attributable to our center’s use of “gentle ventilation” and bubble CPAP, indicating the possible benefit of these practices. These results suggest that counselling for pregnancies affected by previable PPROM may be able to offer reasonably optimistic outlooks where “gentle ventilation” is utilized.

The authors have no conflict of interests to report.

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There is NO conflict of interest to disclose.

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You are reading this latest preprint version

Respiratory outcomes of neonates born after previable premature rupture of membranes and treated with gentle ventilation

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Journal Publication

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Abstract

Figures

Introduction

Patients and methods

Background:

CUIMC Pregnancy management with previable PPROM

Study Sample

Definitions:

Statistical analysis:

Results

Discussion

Declarations

References

Additional Declarations

Status:

Journal Publication

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