Early Human Development 91 (2015) 71–75

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Effects of Sustained Lung Inflation, a lung recruitment maneuver in primary acute respiratory distress syndrome, in respiratory and cerebral outcomes in preterm infants Chiara Grasso, Pietro Sciacca, Valentina Giacchi, Caterina Carpinato, Carmine Mattia, Grazia Maria Palano, Pasqua Betta ⁎ Department of Pediatrics, Neonatology, NICU, University of Catania, “Policlinico of Catania”, Italy

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Article history: Received 27 August 2014 Received in revised form 22 November 2014 Accepted 2 December 2014 Available online xxxx Keywords: Sustained Neonatal resuscitation Surfactant Pulmonary recruitment maneuvers Iatrogenic risks

a b s t r a c t Background: Sustained Lung Inflation (SLI) is a maneuver of lung recruitment in preterm newborns at birth that can facilitate the achieving of larger inflation volumes, leading to the clearance of lung fluid and formation of functional residual capacity (FRC). Aim: To investigate if Sustained Lung Inflation (SLI) reduces the need of invasive procedures and iatrogenic risks. Study design: 78 newborns (gestational age ≤ 34 weeks, weighing ≤ 2000 g) who didn't breathe adequately at birth and needed to receive SLI in addition to other resuscitation maneuvers (2010 guidelines). Subjects: 78 preterm infants born one after the other in our department of Neonatology of Catania University from 2010 to 2012. Outcome measures: The need of intubation and surfactant, the ventilation required, radiological signs, the incidence of intraventricular hemorrhage (IVH), periventricular leukomalacia, retinopathy in prematurity from III to IV plus grades, bronchopulmonary dysplasia, patent ductus arteriosus, pneumothorax and necrotizing enterocolitis. Results: In the SLI group infants needed less intubation in the delivery room (6% vs 21%; p b 0.01), less invasive mechanical ventilation (14% vs 55%; p ≤ 0.001) and shorter duration of ventilation (9.1 days vs 13.8 days; p ≤ 0.001). There wasn't any difference for nasal continuous positive airway pressure (82% vs 77%; p = 0.43); but there was less surfactant administration (54% vs 85%; p ≤ 0.001) and more infants received INSURE (40% vs 29%; p = 0.17). We didn't found any differences in the outcomes, except for more mild intraventricular hemorrhage in the SLI group (23% vs 14%; p = 0.15; OR = 1.83). Conclusion: SLI is easier to perform even with a single operator, it reduces the necessity of more complicated maneuvers and surfactant without statistically evident adverse effects. © 2014 Published by Elsevier Ireland Ltd.

1. Introduction Sustained Lung Inflation (SLI) is a maneuver of lung recruitment characterized by the application of a peak pressure of 25–30 cm H2O

Abbreviations:AHA,American HeartAssociation;BPD,bronchopulmonarydysplasia; CI, confidence interval; FiO2, fraction of inspired oxygen; FRC, functional residual capacity; INSURE, INtubation, a dose of SURfactant and Extubation; IUGR, intrauterine growth restriction; IVH, intraventricular hemorrhage; MAP, mean airway pressure; n-CPAP, nasal continuous positive airway pressure; NICU, neonatal intensive care unit; OR, odds ratio; pCO2, pressure of carbon dioxide; PDA, patent ductus arteriosus; PMA, postmenstrual age; PEEP, positive end-expiratory pressure; PROM, premature rupture of membrane; RDS, respiratory distress syndrome; SaO2, arterial oxygenation saturation; SD, standard deviation; SLI, Sustained Lung Inflation. ⁎ Corresponding author at: Department of Pediatrics, Neonatology, NICU, University of Catania, “Policlinico of Catania”, Via Santa Sofia 78, 95123 Catania, Italy. Tel.: + 39 0953781197; fax: +39 0953781123. E-mail address: [email protected] (P. Betta).

http://dx.doi.org/10.1016/j.earlhumdev.2014.12.002 0378-3782/© 2014 Published by Elsevier Ireland Ltd.

for 10–20 s in preterm newborns at birth. Vyas et al. [1] in 1981, studied the effects of SLI applied for a time of 5 s in preterm newborn resuscitation and proved that this method increased the tidal volume, facilitating the achieving of larger inflation volumes, leading to the clearance of lung fluid and formation of functional residual capacity (FRC) [1]. Lista et al. increased at 10–20 s the time of application of SLI and they asserted that the application of SLI at birth in preterm infants with respiratory distress might decrease the need for mechanical ventilation without inducing evident adverse effects [2]. Harling et al. conversely showed no improvement in the outcome after sustained inflations of 5 s and suggested that immature lungs may be unable to respond to this inflation maneuver [3]. te Pas and Walther showed an increase of complications in the infants treated with SLI, such as severe intraventricular hemorrhage, although they did not reach a statistical significance [4]. In this retrospective cohort study, we analyze the outcome and the onset of complications in infants receiving (SLI group) and infants not receiving it (conventional group).

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2. Patients and methods We conducted an observational analytical cross-sectional case– control study on 78 infants born one after the other in our department of Neonatology of Catania University from 2010 to 2012. The study was conducted in accordance with the Helsinki Declaration, and the study protocol was approved by the (local) Ethics Committee of the Medical University of Catania. Inclusion criteria comprised gestational age ≤ 34 weeks, weight ≤2000 grams (g), absence or inadequate breathing at birth and performance of SLI [5] in addition to the other resuscitation maneuvers according to the guidelines of 2010 [6] (SLI group). Exclusion criteria comprised major congenital anomalies. We have analyzed the need of intubation and surfactant administration, the type and duration of ventilation required, radiological signs of severe respiratory distress, the timing of hospitalization and the growth of the infants. We have also studied the outcome focusing on the incidence of intraventricular hemorrhage (IVH), periventricular leukomalacia, retinopathy in prematurity from III to IV plus grades, bronchopulmonary dysplasia, patent ductus arteriosus, pneumothorax and necrotizing enterocolitis. According to NIH Consensus Development Conference we defined intraventricular hemorrhage (IVH) as a spectrum of hemorrhagic brain injury most typically occurring in the first week of life in very premature infant and periventricular leukomalacia as focal cystic damage of white matter tracts (made of nerve axons that connect different brain regions covered by the insulating substance, myelin) [7]. According to the National Institutes of Child Health and Human Development Neonatal Research Network we distinguished bronchopulmonary dysplasia (BPD) in mild BPD defined as a need for supplemental oxygen (O2) for ≥28 days but not at 36 weeks' postmenstrual age (PMA) or discharge, moderate BPD as O2 for ≥28 days plus treatment with b 30% O2 at 36 weeks' PMA, and severe BPD as O2 for ≥28 days plus ≥30% O2 and/or positive pressure at 36 weeks' PMA [8]. We compared the data of patients with those of a control group of 78 infants with the same gestational age and weight, born one after the other in our department of Neonatology of Catania University from 2008 to 2010, requiring resuscitation maneuvers at birth (conventional group) according to the guidelines of 2010 [9]. 2.1. Statistical analysis Statistical data were derived using Student's t test for parametric and the Mann–Whitney U test for non-parametric continuous variables and χ2 test for categorical variables. p values were considered statistically significant if p b 0.05. For the categorical variables we analyzed the odds ratio (OR) with the 95% confidence interval.

observation period, were transferred to the NICU. Newborns who did not need intubation were transferred with nasal CPAP and their oxygen saturation was monitored [6]. 2.3. Maneuvers at the NICU Soon as the infant arrived in NICU pulse oximetry values, objective data and chest radiographs were collected. Infants were intubated and mechanically ventilated if they had oxygen saturation values ≤ 88% while receiving FiO2 ≥ 40%, or pCO2 N 60 mm Hg with a pH b 7.20, or if they had more than 4 apneic episodes in 1 h. Therapy with caffeine was started as soon as possible in infants younger than 30 weeks and in older infants who had apnea. All intubated newborns received, immediately, a dose of surfactant (Curosurf, Chiesi, Italy) while for newborns who required ventilatory assistance with MAP N 7 cm H2O and FiO2 N 40% a second dose of surfactant was performed at a distance of at least 6 h after the first dose [10]. No intubated preterm infants who showed clinical features of respiratory distress syndrome (RDS) such us sternal, intercostal or subcostal retraction, grunting, tachypnea and the need of oxygen supplementation, received INtubation, a dose of SURfactant and shortly after Extubation (INSURE) [10–12]. We proceeded to the extubation as soon as FiO2 needed was lowered b30% and the mean airway pressure b7 cm H2O. We continued with nasal continuous positive airway pressure (n-CPAP) ventilation until infants had no sign of distress and were stable with pCO2 b 60 mm Hg and SaO2 N 92% without supplementary O2. All infants received a cerebral ultrasound study and a retinal examination from the 21st day of life and subsequent checks if necessary. The management at the NICU was the same in both the SLI and conventional groups. 3. Results The SLI group presented a mean gestational age of 30.4 weeks (range 23 to 33.5 weeks) and a mean weight of 1.335 g ± 376 (range 335 to 1975 g). The control group did not present a significant difference in both gestational age (mean 30.5 weeks; range 22 to 34 weeks) and weight (mean 1371 g ± 411; 400 to 2000 g). The demographic characteristics of both groups are shown in Table 1. Six newborns in the SLI group (8%) and five newborns in the control group (6%) died during their first two weeks of life, while one newborn in the SLI group (1%) and four in the control group (5%) died subsequently. In the SLI group fewer infants than in the control group required intubation in the delivery room (5 of 78 [6%] vs 16 of 78 [21%]; p = 0.009; odds ratio (OR) = 0.27; confidence interval (CI) = 0.09–0.77). Infants

2.2. Resuscitation maneuvers in the delivery room Newborns in the SLI group received only one 25 cm H2O pressure controlled inflation for 15 s using a face mask of appropriate size for each of them and a T-piece ventilator [5,6,10]. If required, after SLI, infants were resuscitated according to the maneuvers required by the American Heart Association (AHA) 2010 neonatal resuscitation guidelines [6] or received a 4 cm H2O continuous positive airway pressure (CPAP) [4]. Newborns in the control group received conventional resuscitation maneuvers which consist in a first initial inflation of 30– 40 cm H2O, followed by insufflations not exceeding 20 cm H2O, with a rate of 60 per minute and a PEEP of 5 cm H2O using a face mask of appropriate size and a T-piece ventilator (Neopuff). Positive pressure ventilation was started with FiO2 at 21% [7,10]. FiO2 was subsequently incremented if necessary [7]. In both groups newborns were intubated and mechanically ventilated if, despite the correct resuscitation maneuvers, the heart rate did not increase above 100 beats per minute, if breathing was absent, if cyanosis persisted or dyspnea occurred [6]. All infants, after stabilization and an

Table 1 Demographic characteristics.

Gestational age, mean (SD), wk Birth weight, mean (SD), g Male gender, n (%) Twin, n (%) Cesarean birth, n (%) PROM, n (%) Chorionamionite, n (%) Prenatal steroids, n (%) IUGR, n (%) Cordonal pH, mean (SD) 5′ Apgar score b 6, n (%) 5′ Apgar score, median Growth, median Died b2 weeks old, n (%)

Sustained (N = 78)

Conventional (N = 78)

30.4 (±2,6) 1335 (±376) 39 (50) 40 (51) 65 (83) 12 (15) 9 (12) 65 (83) 4 (5) 7.25 (±0,20) 5 (6) 8 22 6 (8)

30.5 (±3.1) 1371 (±411) 38 (49) 24 (31) 66 (85) 15 (19) 8 (10) 63 (81) 5 (6) 7.23 (±0.22) 16 (21) 8 21 5 (6)

IUGR, intrauterine growth restriction; n, number; PROM, premature rupture of membrane; SD, standard deviation; wk, weeks.

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who received SLI had less need of intubation and invasive mechanical ventilation than infants in the conventional group (11 of 78 [14%] vs 43 of 78 [55%]; p ≤ 0.001; OR = 0.13; CI = 0.06–0.29). Regarding non-invasive ventilation, there was no statistically significant difference in the number of children that received ventilation with n-CPAP between the sustained group 65 [82%] and conventional group 60 [77%] (p = 1.43; OR = 1.37; CI = 0.63–3.00) (Fig. 1A). The mean duration of ventilation was shorter in the SLI group than in the control group (9.1 days vs 13.8 days; p ≤ 0.001) (Fig. 1B). Thirty-one of 78 [40%] infants in the SLI group received INtubation, a dose of SURfactant and shortly after Extubation (INSURE) versus 23 of 78 [29%] infants in the control group (p = 0.17; OR = 1.58; CI = 0.81–3.07). Between the two groups there was a significant difference in the number of newborns who received a first dose of surfactant (42 of 78 [54%] vs 66 of 78 [85%], p ≤ 0.001; OR = 0.21; CI = 0.10–0.45), and in those patients who needed subsequent doses (24 of 78 [31%] vs 39 of 78 [50%], p = 0.01; OR = 0.44; CI = 0.23–0.86) (Fig. 1C). There were no differences in signs of severe respiratory distress as seen at the X-ray (15 of 78 [19%] vs 16 of 78 [21%]; p = 0.84; OR = 0.92; CI = 0.42–2.03); bronchopulmonary dysplasia (9 of 78 [12%] vs 12 of 78 [15%]; p = 0.48; OR = 0.72; CI = 0.28–1.81); periventricular leukomalacia (2 of 78 [3%] vs 5 of 78 [6%]; p = 0.25; OR = 0.38; CI = 0.07–2.04); severe retinopathy of prematurity (5 of 78 [6%] vs 6 of 78 [8%]; p = 0.75; OR = 0.82; CI = 0.24–2.81); pneumothorax (1 of 78 [1%] vs 2 of 78 [3%]; p = 0.56; OR = 0.49; CI = 0.04–5.56); and necrotizing enterocolitis (1 of 78 [1%] vs 1 of 78 [1%]; p = 1; OR = 1; CI = 0.06–16.28). There was no statistically significant difference in the number of patients with patent ductus arteriosus requiring surgical or pharmacological intervention (PDA) (14 of 78 [18%] vs 10 of 78 [13%], p = 0.37; OR = 1.49; CI = 0.62–3.59) (Table 2). With regard to the intraventricular hemorrhage (IVH), even if there were no statistically significant differences between the two groups (p = 0.46), there were more children with IVH in the group treated with SLI than in the control group (22 of 78 [28%] vs 18 of 78 [23%]; OR = 1.31; CI = 0.64–2.69); this concerned more mild IVH (grades I– II) (18 of 78 [23%] vs 11 of 78 [14%]; p = 0.15; OR = 1.83; CI = 0.80– 4.18) than severe ones (grades III–IV) (4 of 78 [5%] vs 6 of 78 [8%]; p = 0.51; OR = 0.65; CI = 0.18–2.39) (Fig. 2). There was no statistically significant difference in average growth between the two groups (22 g per day (median 22) vs 21 g per day (median 20); p ≤ 0.0548, z = −1.59). 4. Discussion The effects of Sustained Lung Inflation in preterm babies are still under discussion. The beneficial effects of SLI were not confirmed by Lindner's randomized work of 2005, any differences between newborns who received SLI and newborns who received intermittent mandatory ventilation with a nasopharyngeal tube were not found [13]. The same for Harling's work that did not prove any benefits from the use of Sustained Lung Inflation in very preterm newborns [3]. But Harling did not study a true SLI: as demonstrated, recruitment takes a minimum of 10 s and continues beyond 30 s while in his study he applied inflation just for 5 s. Several more recent studies as te Pas' randomized trial of 2007 [4] and Lista's work of 2011 [2] proved that the application of a peak pressure of 25– 30 cm H2O for 10–20 s in preterm newborns at birth, followed by the application of continuous PEEP of 5 cm H2O improves the achievement of an adequate functional residual capacity (FRC) and correlates to a reduction of the need and duration of mechanical ventilation [2–5,14,15]. A trial of Dani et al. is currently ongoing to compare the need for MV in the first 72 h of life in infants born at 25 + 0 to 28 + 6 weeks' gestation who received the SLI maneuver in the delivery room or not [16]. Data obtained in our study are consistent with the most recent data reported in literature: infants who received SLI followed by CPAP showed less need of intubation in the delivery room, of mechanical invasive ventilation and needed a shorter duration of ventilation. The

Fig. 1. A. Need for invasive and not invasive ventilation in infants resuscitated with Sustained Lung Inflation (SLI) or with conventional maneuvers. B. Duration of invasive ventilation in infants resuscitated with Sustained Lung Inflation (SLI) or with conventional maneuvers. C. Need for surfactant administration divided in first, subsequent doses or Intubation, surfactant and Extubation (INSURE), in infants resuscitated with Sustained Lung Inflation (SLI) or with conventional maneuvers.

reduction in the necessity of intubation is very significant because it allows the use of nasal CPAP as the first-line respiratory support [17]. It may also contribute to the reduction of the risk of volutrauma, barotrauma and of the bronchopulmonary dysplasia (BPD) without increasing the mortality [18,19]. According to te Pas' and Lista's studies, as in our study, SLI is related with a reduced demand of surfactant but not of the INSURE treatment

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Table 2 Outcomes.

Intubation delivery room, n (%) Radiological severe chest, n (%) INSURE, n (%) Surfactant N1 dose, n (%) Duration of ventilation, mean (SD) Bronchopulmonary dysplasia, n (%) Patent ductus arteriosus (treated), n (%) Retinopathy of prematurity (III–IV plus), n (%) Pneumothorax, n (%) Necrotizing enterocolitis, n (%) Mild intraventricular hemorrhage, n (%) Severe intraventricular hemorrhage, n (%) Periventricular leukomalacia, n (%) Died N2 weeks old, n (%)

Sustained (N = 78)

Conventional (N = 78)

p value

OR value (CI)

5 (6) 15 (19) 31 (40) 24 (31) 9.1 (±15.8) 9 (12) 14 (18) 5 (6) 1 (1) 1 (1) 18 (23) 4 (5) 2 (3) 1 (1)

16 (21) 16 (21) 23 (29) 39 (50) 13.8 (±29.8) 12 (15) 10 (13) 6 (8) 2 (3) 1 (1) 11 (14) 6 (8) 5 (6) 4 (5)

b0.009 0.84 0.17 0.01 b0.001 0.48 0.37 0.75 0.56 1 0.15 0.51 0.25 0.17

0.27 (0.09–0.77) 0.92 (0.42–2.03) 1.58 (0.81–3.07) 0.44 (0.23–0.86) – 0.72 (0.28–1.81) 1.49 (0.62–3.59) 0.82 (0.24–2.81) 0.49 (0.04–5.56) 1 (0.06–16.28) 1.83 (0.80–4.18) 0.65 (0.18–2.39) 0.38 (0.07–2.04) 0.24 (0.03–2.20)

INSURE, INtubation, a dose of SURfactant and Extubation; n, number; OR, odds ratio; CI, 95% confidence interval.

[2–4]. We found a statistically significant reduction in the number of children who needed both the first and the second dose of surfactant in the SLI group compared to the control group. The limit given by the need of prophylactic surfactant treatment [20] has been exceeded by the most recent studies: they affirm that the use of prophylactic surfactant was not superior to the nCPAP and to the early selective surfactant in decreasing the need of mechanical ventilation and in improving of the outcomes of preterm infants [12]. te Pas and Walther showed an increase of severe intraventricular hemorrhage, although without a statistically significant difference, in infants who were treated with SLI at birth [4]. These data were not confirmed by the most recent study which stated that sustained ventilation did not induce evident adverse effects [2]. In our study we didn't find any differences in the outcome except for a slight not significant increase of the mild form of IVH (I–II grades) in the group treated with SLI. We also found a statistically significantly improved growth (grams per day) in newborns who received SLI. Hemodynamic effects of SLI are still being studied. The most recent animal studies do not prove the presence of adverse circulatory events linked to the Sustained Lung Inflation at birth and we didn't find any significant difference in hemodynamically relevant patent ductus arteriosus [21,22]. Studies on newborns are limited, even for the extreme difficulty to design and to perform them, and although the SLI seems to have no evident adverse events [2,23,24], the most recent data affirm that the

hemodynamic effects of SLI are still uncertain and should be better studied by clinical large trials [23]. 5. Conclusions The execution of Sustained Lung Inflation (SLI) in the delivery room is an easier maneuver to perform, it requires only one operator and reduces the percentage of children who necessitate of more complicated maneuvers such as intubation and invasive ventilation. Thereby the incidence of volotrauma and barotrauma and risk of infection are reduced. Infants who received SLI followed by CPAP showed less need of intubation in the delivery room, mechanical invasive ventilation and a shorter duration of ventilation without statistically evident adverse effects. In the SLI group there was also less requirement of surfactant which is very important since the use of prophylactic surfactant is no longer indicated. Even if our study is retrospective, with the limitations of any retrospective cohort comparison, we think that our experience could be useful to improve current knowledge about Sustained Lung Inflation and to encourage more randomized studies to confirm the importance of Sustained Lung Inflation at birth in very pre-term infants. It would also be interesting to investigate the correlation between SLI, cerebral bleedings and their pathogenesis. Authors' contributions Conception and design: Pietro Sciacca and Pasqua Betta. Collection and assembly of data: Chiara Grasso, Valentina Giacchi, Caterina Carpinato, Carmine Mattia and Grazia Maria Palano. Analysis and interpretation of data: Chiara Grasso and Pasqua Betta. Draft of the manuscript: Chiara Grasso, Pasqua Betta and Pietro Sciacca. Critical revision of the manuscript and important intellectual content: Pasqua Betta and Pietro Sciacca. Final approval: Pasqua Betta and Pietro Sciacca. Conflict of interests The authors declare that they have no competing interests. Acknowledgment

Fig. 2. Incidence of all intraventricular hemorrhages (IVHs), and incidence of mild (I–II) and of severe (III–IV) ones in infants resuscitated with Sustained Lung Inflation (SLI) or with conventional maneuvers.

We acknowledge the excellent technical assistance of Nicola Bonanno of the Department of Pediatrics of the University of Catania, Italy. We also acknowledge our secretary Concetta Scuderi for her collaboration in collecting data.

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