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Lung recruitment prevents collapse during laparoscopy in children

A randomised controlled trial

Acosta, Cecilia M.; Sara, Tomás; Carpinella, Martín; Volpicelli, Giovanni; Ricci, Lila; Poliotto, Sergio; Abrego, Diego; Gonorazky, Sergio; Böhm, Stephan H.; Tusman, Gerardo

European Journal of Anaesthesiology (EJA): August 2018 - Volume 35 - Issue 8 - p 573–580
doi: 10.1097/EJA.0000000000000761
Paediatric anaesthesia

BACKGROUND Capnoperitoneum and anaesthesia impair lung aeration during laparoscopy in children. These changes can be detected and monitored at the bedside by lung ultrasound (LUS).

OBJECTIVE The aim of our study was to assess the impact of general anaesthesia and capnoperitoneum on lung collapse and the potential preventive effect of lung recruitment manoeuvres, using LUS in children undergoing laparoscopy.

DESIGN Randomised controlled study.

SETTING Single-institution study, community hospital, Mar del Plata, Argentina.

PATIENTS Forty-two children American Society of Anesthesiologists I–II aged 6 months to 7 years undergoing laparoscopy.

INTERVENTIONS All patients were studied using LUS before, during and after capnoperitoneum. Children were allocated to a control group (C-group, n=21) receiving standard protective ventilation, or to a lung recruitment manoeuvre group (RM-group) (n=21), in which lung recruitment manoeuvres were performed after recording baseline LUS images before capnoperitoneum. Loss of aeration was scored by summing a progressive grading from 0 to 3 assigned to each of 12 lung areas, based on the detection of four main ultrasound patterns: normal aeration = 0, partial loss-mild = 1, partial loss-severe = 2, total loss-consolidation = 3.

MAIN OUTCOME MEASURES Lung aeration score and atelectasis assessed by ultrasound.

RESULTS Before capnoperitoneum and recruitment manoeuvres in the treated group the two groups presented similar ultrasound scores (5.95 ± 4.13 vs. 5.19 ± 3.33, P = 0.5). In the RM-group, lung aeration significantly improved both during (2.71 ± 2.47) and after capnoperitoneum (2.52 ± 2.86), compared with the C-group (6.71 ± 3.54, P < 0.001, and 8.48 ± 3.22, P < 0.001, respectively). There was no statistically significant difference in the percentage of atelectasis before capnoperitoneum and recruitment manoeuvres in the RM-group (62%) and in the C-group (47%, P = 0.750). However, during capnoperitoneum, only 19% of the RM-group had atelectasis compared with 80% in the C-group (P < 0.001).

CONCLUSION The majority of children undergoing laparoscopy have anaesthesia-induced atelectasis. In most cases, lung collapse due to capnoperitoneum could have been prevented by recruitment manoeuvres followed by positive-end expiratory pressure.


From the Department of Anaesthesiology, Hospital Privado de Comunidad, Mar del Plata, Argentina (CMA, TS, MC, GT), Department of Emergency Medicine, San Luigi Gonzaga University Hospital, Torino, Italy (GV), Department of Mathematics, Facultad de Ciencias Exactas, Universidad Nacional de Mar del Plata (LR), Department of Pediatric Surgery (SP, DA), Department of Clinical Research, Hospital Privado de Comunidad, Mar del Plata, Argentina (SG) and Hepa Wash GmbH, Munich, Germany (SHB)

Correspondence to Gerardo Tusman, MD, Department of Anaesthesiology, Hospital Privado de Comunidad, Mar del Plata, Argentina Tel: +54 223 4990074; fax: +54 223 4990099; e-mail:

Published online 22 December 2017

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In anaesthetised children, the incidence of lung collapse with episodes of hypoxaemia is high.1–5 Diaphragm dysfunction induced by general anaesthesia is one of the most important factors in the genesis of regional losses of lung aeration.1,2 The mass of the abdominal organs pushes the diaphragm cranially compressing the lungs in the most dependent areas. Such regional lung collapse may range from slight loss of aeration to complete atelectasis.6–11

Capnoperitoneum induced during laparoscopy may aggravate lung collapse as it generates a further increase in intra-abdominal pressure.12 Because the chest wall and abdomen work in series, impairment of abdominal compliance induced by capnoperitoneum may significantly influence thoracic compliance, causing changes in the pleural pressure.13 Neonates, infants and small children have in common low functional residual capacity, high pulmonary closing capacity and high oxygen consumption, and are especially prone to develop atelectasis and hypoxaemia during laparoscopic procedures.14,15

Lung recruitment manoeuvres have the potential to improve lung aeration and gas exchange in adults and children during nonlaparoscopic procedures.8,11,16 Laparoscopic studies have shown that recruitment manoeuvres successfully improved lung mechanics and atelectasis in adults, but similar data have not been obtained in children.17–19

Lung ultrasound (LUS) is a reliable and accurate noninvasive imaging tool for detecting anaesthesia-induced atelectasis.10 LUS has great potential for bedside assessment and monitoring of lung aeration particularly when the effect of therapeutic intervention is assessed in critically ill patients.20,21 It is a tool that appears suitable for use with children for observing changes in lung aeration during laparoscopy with general anaesthesia.

The aim of our study was to assess the impact of general anaesthesia and capnoperitoneum on lung collapse and the beneficial effect of recruitment manoeuvres, using LUS examinations of children undergoing laparoscopy. Our main hypothesis was that the loss of lung aeration during capnoperitoneum was higher in children ventilated with standard protective ventilation compared with those receiving similar ventilation preceded by recruitment manoeuvres.

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Ethical approval for this study (no. 2919/875/14) was provided by the Ethical Committee of Hospital Privado de Comunidad – CIREI, Mar del Plata, Argentina on 7 July 2014. The study started at the end of August 2014.

The current randomised controlled clinical trial (trial registration number NCT02824146) was performed in the operating theatre of a community hospital. After signed informed parental consent, we studied children aged 6 months to 7 years with a physical status classification [American Society of Anesthesiologists (ASA)] I–II, undergoing abdominal laparoscopic surgery. We excluded emergency and thoracic procedures, patients with abdominal distension or with significant pre-existing pulmonary, cardiac or chest wall diseases.

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Standard ECG, noninvasive mean systemic arterial pressure, time-based capnography and pulse oximetry were monitored by the S/5 device (Datex-Ohmeda, Helsinki, Finland). Anaesthesia was induced with Sevofluorane using the circle system of the GE Aespire workstation (GE Healthcare, Madison, Wisconsin, USA). Fentanyl 3 μg kg−1 and vecuronium 0.1 mg kg−1 were administered intravenously before intubation with a cuffed endotracheal tube of appropriate size. Anaesthesia was maintained with sevoflurane 0.7 minimum alveolar concentration and a remifentanil infusion (0.5 to 0.6 μg kg−1 min−1). All children were studied in the supine position.

The lungs were ventilated in a volume control mode using a tidal volume of 6 ml kg−1, a positive end-expiratory pressure (PEEP) of 5 cmH2O, an inspiratory: expiratory ratio of 1 : 1.5, respiratory rate between 20 and 25 breaths per minute and FIO2 of 0.5. Respiratory flow and pressure signals were obtained by a paediatric D-Lite adapter (GE-Datex Side Stream System, GE Healthcare, Madison, Wisconsin, USA) placed at the airway opening (S/5, Datex-Ohmeda). Tidal volume, PEEP and dynamic respiratory compliance [Cdyn (respiratory system dynamic compliance) = tidal volume/peak airway pressure − PEEP] were recorded on a chart at each protocol step.

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Lung ultrasound

LUS was performed with the portable device MicroMax (Sonosite, Bothell, Washington, USA) using a linear probe of 6 to 12 MHz. Each hemithorax was divided into six regions, as previously described, using three longitudinal lines (parasternal, anterior and posterior axillary) and two axial lines (one above the diaphragm and the other 1 cm above the nipples).10,22 Each hemithorax was assessed by placing the probe perpendicular to the ribs looking for the bat sign (the pleura and lung tissue between the acoustic shadows of two adjacent ribs).10,23 Once a complete hemithorax scan was performed, the probe was then placed in the oblique position between ribs in those areas in which the typical ultrasound patterns of atelectasis were detected. In general, the posterior areas are those with the highest incidence of anaesthesia-induced atelectasis.7–10 An aeration score previously described for adults was applied in our paediatric patients.20 Four LUS patterns were defined and assessed in each of the six thoracic areas per side:

Normal aeration (N): presence of lung sliding (the respiratory movement of the visceral pleura relative to the fixed parietal pleura) and A lines (repetitive horizontal reverberation artefacts generated by air within the lungs separated by regular intervals).

Moderate loss of lung aeration (B1): multiple and well defined B-lines (vertical, dynamic and laser-like echoic lines, originating from the pleural line or from small subpleural consolidations, reaching the lowest edge of the screen).

Severe loss of lung aeration (B2): multiple coalescent B-lines that occupy the whole lung image (the so-called white lung).

Complete loss of aeration (C): Anaesthesia-induced atelectasis was defined as localised sonographic consolidation (subpleural tissue-like pattern). Air bronchograms may be observed as bright echogenic branching structures within such consolidations.10

For a given thoracic area, points were allocated to the worst LUS pattern observed: N = 0, B1 = 1, B2 = 2 and C = 3. The sum of the points obtained in all the 12 lung areas defined the LUS aeration score, ranging from 0 to 36 for the whole thorax. This score is inversely proportional to the degree of lung aeration.

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The children were randomised into two groups before surgery, using a randomisation table, (StatsDirect versión 2.7.2; Altrincham, Cheshire, United Kingdom):

Control group (C-group): patients received the standard protective ventilatory setting as described in the anaesthesia section.

Lung recruitment manoeuvre group (RM-group): patients received a recruitment manoeuvre after baseline recordings and before the induction of capnoperitoneum. The recruitment manoeuvre was performed in a pressure-controlled mode with a constant driving pressure of 15 cmH2O. PEEP was increased in steps of 5 cmH2O, from 5 to 15 cmH2O, every three breaths. The target recruitment pressure of 30 cmH2O was maintained for 10 breaths, corresponding to approximately 30 s. The standard protective ventilatory settings were then applied with 8 cmH2O of PEEP, to keep the lungs open after lung recruitment. Recruitment manoeuvres were stopped immediately if mean arterial pressure and/or heart rate changed by at least 15% from baseline values.

Patients were studied in three consecutive steps:

Before capnoperitoneum: 5 min after anaesthesia induction. After baseline recordings, the recruitment manoeuvre was performed in the RM-group.

During capnoperitoneum: Capnoperitoneum pressure was kept at 1.3 kPa during the entire capnoperitoneum period (Endoflator; Karl Storz, Tuttlingen, Germany) and measurements were performed 20 min after starting the capnoperitoneum.

After capnoperitoneum: 5 min after the end of surgery.

The same investigator performed LUS at each time point of the study. Respiratory and cardiovascular data were collected during each protocol step.

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Statistical analysis

The null hypothesis was that atelectasis during the capnoperitoneum would be similar between the two groups and during the three episodes studied. Considering a beta-power of 80% and an alpha-error of 5%, the statistical power to reject this hypothesis was calculated assuming that atelectasis would be present in 90% of patients in the C-group and in only 45% of patients in the RM-group.10 A sample size of 21 patients per group was estimated. Descriptive data are presented as n (%) for proportions and mean ± SD or median for continuous variables.

Univariate comparisons between groups were performed for the three protocol episodes employing the t test for continuous variables (age, weight and duration of surgery) and the Fisher exact test for the remaining categorical variables. Within-group comparisons for the three episodes studied, for each of the two groups, were made using a t test for repeated measurements and a Bonferroni correction. Multiple linear mixed models were adjusted to examine the influence of recruitment manoeuvres, age and duration of surgery (covariates) on the aeration score and on each cardiovascular variable treating them as a triple-variate response (repeated measures). A second model, a generalised linear mixed model with an ordinal variable as the response, was fitted to analyse the influence of treatment and personal data on lung aeration during the three episodes studied.

A P value less than 0.05 was considered statistically significant. All calculations were performed using the R statistical package (R Core Team, 2015, Foundation for Statistical Computing, Vienna, Austria).

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We enrolled 47 children with ASA physical status I–II, aged 46 ± 27 months. Five patients were excluded (Fig. 1). All had similar personal characteristics and surgical duration (Table 1).

Fig. 1

Fig. 1

Table 1

Table 1

The aeration scores obtained in the two groups during the three steps of the study are illustrated in Fig. 2. After the induction of anaesthesia and before capnoperitoneum, the RM-group and C-group had similar scores for aeration (P = 0.514). The scores decreased in the RM-group during capnoperitoneum and after capnoperitoneum when compared with the C-group (both P < 0.001).

Fig. 2

Fig. 2

The generalised linear mixed model analysing the influence of treatment and personal data on the change in aeration across the three protocol steps, revealed an aeration trajectory in which weight (coefficient 0.073, P = 0.016), age (coefficient 0.043, P < 0.001) and recruitment manoeuvres (coefficient 0.879, P < 0.001) influenced lung aeration in the most dependent lung areas only.

Table 2 presents the incidence of a specific pattern for atelectasis in both groups. We found a significant difference in atelectasis during capnoperitoneum between the two groups (P < 0.001), and this difference was maintained to the end of anaesthesia (P < 0.001). Figure 3 and the Supplemental video, show examples of LUS images for one representative patient per group.

Table 2

Table 2

Fig. 3

Fig. 3

The recruitment manoeuvre was well tolerated haemodynamically and was not stopped in any of the children. Table 3 gives the cardiovascular variables and Cdyn. All variables remained stable in both groups, except for SpO2 and Cdyn. The latter was 23% higher in the RM-group than in the C-group after capnoperitoneum (P < 0.001).

Table 3

Table 3

The linear mixed models showed that the recruitment manoeuvre and age affected the trajectories of the aeration score (both, P < 0.001) and that age affected the trajectory of Cdyn (P < 0.001). The duration of surgery and all the other variables studied had no influence on the trajectories of aeration score.

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The current study documents the high incidence of lung collapse in anaesthetised children undergoing laparoscopy. The negative effect of anaesthesia and capnoperitoneum on lung aeration persisted in the children treated with standard protective ventilator strategy. In contrast, in most patients treated with a recruitment manoeuvre followed by 8 cmH2O of PEEP, the development of atelectasis was prevented during and after capnoperitoneum.

LUS has great potential as it represents a radiation-free, noninvasive and reliable tool for assessing lung aeration at the bedside.24,25 When compared with magnetic resonance imaging, LUS showed high sensitivity (88%), specificity (89%) and accuracy (88%) for diagnosing anaesthesia-induced atelectasis in children.10 These results were similar to those observed by Yu et al.26 in anesthetised adults, who showed good sensitivity (87%), specificity (92%) and accuracy (91%) in verifying the occurrence of atelectasis by LUS in comparison with computed tomography (CT)-scan as the reference method. The number of B-lines, well known LUS artefacts related to a deterioration in lung aeration, also correlated with the extent of parenchymal changes on CT scans in children.27 The LUS aeration score described by Soummer et al.20 and Bouhemad et al.24 is a well established and validated method for evaluating the condition of lung aeration and monitoring its changes over time. The same LUS method has already been tested in anaesthetised adults undergoing laparoscopy.19,21.

Lung collapse during anaesthesia ranges from slight loss in aeration to complete acinar collapse in the most dependent areas of the lungs.1,2,6–10 We found that the majority of our patients showed atelectasis immediately after the induction of anaesthesia. This high incidence of lung collapse is similar to that found in previous studies during nonlaparoscopic6–11 and laparoscopic21 procedures. We also observed that the aeration score and atelectasis increased during and after capnoperitoneum in the C-group but decreased in the RM-group (Table 2 and Fig. 2).

Our findings support the common belief that capnoperitoneum can increase atelectasis, possibly due to lung compression caused by a cranial shift of the diaphragm. Another possible explanation for this phenomenon of loss of aeration is the time effect. Lutterbey et al.9 described a 12% increase in the amount of atelectasis during 85 min of general anaesthesia. Indeed, in the C-group, we have observed that the extension of atelectasis doubled (23%) only 20 min after reaching the target capnoperitoneum pressure. It is probable that capnoperitoneum, rather than the time-effect, is the cause of loss of lung aeration in our children undergoing laparoscopy. Further support for this hypothesis comes from the generalised linear mixed model, as the development of aeration during the procedures was not affected by the time course of surgery.

The linear mixed model also revealed that age and body weight (related to age) affected the trajectory of lung aeration. This result is in agreement with the findings of other authors who showed that the severity of atelectasis induced by anaesthesia in children decreases with age.4,5,9,11

We performed the recruitment manoeuvre before capnoperitoneum, and not during laparoscopy, because the increase in intra-abdominal pressure generated by capnoperitoneum would have been transmitted, in part, to the pleural space,28,29 increasing the pulmonary plateau pressure beyond 30 cmH2O, the maximum pressure recommended for lung recruitment manoeuvres in children.

Following recruitment manoeuvres, the level of PEEP that prevents lung recollapse during capnoperitoneum in children is unknown. In anaesthetised children without capnoperitoneum, 5 cmH2O of PEEP applied after a recruitment manoeuvres kept the lungs open in some studies but failed to obtain similar beneficial effect in others.8,9 The current data suggest that a PEEP fixed at 8 cmH2O was not enough to prevent the lungs from recollapsing in all RM-group patients (Table 2 and Fig. 2). We hypothesise that PEEP levels higher than the usual 5 cmH2O applied in studies on anaesthetised patients would be required to preserve normal lung aeration during capnoperitoneum. It should be noted that the quoted studies were not intended to evaluate the best ventilator strategy to prevent the additional effects of capnoperitoneum.8,9

Following a recruitment manoeuvre, it is possible to personalise the PEEP level by using a PEEP titration trial, something that has been well described for experimental models and for anaesthetised adults.30–32 The level of PEEP to apply after a recruitment manoeuvre to achieve best lung function depends on individual and surgical factors. Thus, 5 cmH2O of PEEP was enough for paediatric and some adult patients without capnoperitoneum, but higher PEEP levels were necessary for thoracic procedures [10 ± 2 cmH2O] and the morbidly obese (15 to 16 cmH2O).16,31,32 To match PEEP to an anaesthetised child undergoing laparoscopy, a PEEP titration trial should be performed immediately after actively recruiting the lungs.

The clinical implication of our findings in children is that a recruitment manoeuvre can reduce the amount of lung collapse induced by the deleterious combination of general anaesthesia and capnoperitoneum. However, the transmission of pressure to the pleural space caused by capnoperitoneum probably demands a ventilator strategy based on higher PEEP levels than usual to maintain a beneficial recruitment effect. The optimisation of PEEP strategy based on a PEEP titration trial after a recruitment manoeuvres should be considered during laparoscopic procedures. Future studies should determine the point of lung recollapse and explore therapeutic PEEP levels in patients undergoing capnoperitoneum.

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Our study has some limitations. One pitfall in the protocol is the lack of baseline LUS images before induction of anaesthesia. The unlikely compliance of awake children in the stressful situation preceding surgery reduces the feasibility of a routine examination. We made the assumption that our children had normal lung aeration before anaesthesia because only the healthy were enrolled.

Another limitation of our study is the lack of LUS examination after recruitment manoeuvres and before capnoperitoneum in the treatment group. We limited the number of LUS examinations in an attempt to minimise the additional anaesthesia time created by our study. As a result, we are now unable to clarify whether the remaining atelectasis seen in this group was caused by inefficiencies of the recruitment manoeuvres, capnoperitoneum-induced additional lung collapse or a combination of both effects.

Our study lacks data on the interoperator variability in the assessment of LUS, but the ultrasound examinations were performed by an operator who might be considered an advanced expert in LUS. Accordingly, we cannot comment on the degree of variability of the technique. However, the ultrasound score used in the study relies on very basic and simple pattern recognition and previous reports have already demonstrated a low variability of the technique.

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Anaesthesia-induced atelectasis was present in the majority of children with healthy lungs. In most cases, additional lung collapse caused by capnoperitoneum may have been successfully prevented by recruitment manoeuvres and PEEP. This ventilatory strategy was haemodynamically well tolerated in children with normal lungs and cardiac function.

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Acknowledgements relating to this article

Assistance with the study: we thank Rita Ceschi for her technical assistance.

Financial support and sponsorship: local hospital resources.

Conflict of interest: none.

Presentation: none.

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