Ultrasound assessment of the gastric contents for the guidance of the anaesthetic strategy in infants with hypertrophic pyloric stenosis: a prospective cohort study

Ultrasound assessment of the gastric contents for the guidance of the anaesthetic strategy in infants with hypertrophic pyloric stenosis: a prospective cohort study

British Journal of Anaesthesia, 116 (5): 649–54 (2016) doi: 10.1093/bja/aew070 Paediatrics PA E D I AT R I C S cohort study A.-C. Gagey1, M. de Quei...

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British Journal of Anaesthesia, 116 (5): 649–54 (2016) doi: 10.1093/bja/aew070 Paediatrics

PA E D I AT R I C S

cohort study A.-C. Gagey1, M. de Queiroz Siqueira1, F.-P. Desgranges1, S. Combet1, C. Naulin2, D. Chassard1,3 and L. Bouvet1,4,* 1

Department of Anaesthesia and Intensive Care, Hospices Civils de Lyon, Femme Mère Enfant Hospital, 59, boulevard Pinel, 69500 Bron, France, 2Department of Anaesthesia and Intensive Care, Centre Hospitalier de Villefranche-sur-Saône, Plateau d’Ouilly Gleizé, 69655 Villefranche-sur-Saône, France, 3University of Lyon, Claude Bernard Lyon 1 University, 43 boulevard du 11 Novembre 1918, 69100 Villeurbanne, France, and 4Inserm, U1032, LabTau, 151, cours Albert Thomas, 69003 Lyon, France

*Corresponding author. E-mail: [email protected]

Abstract Background: Evacuation of gastric content through a nasogastric tube, followed by rapid sequence induction, is usually recommended in infants undergoing pyloromyotomy. However, rapid sequence induction may be challenging, and is therefore controversial. Some anaesthetists regularly perform classical non-rapid induction technique, after blind aspiration of the gastric contents, although this aspiration may have been incomplete. This prospective observational study aimed to assess whether the ultrasound monitoring of the aspiration of the stomach contents, may be useful to appropriately guide the choice of the anaesthetic induction technique, in infants undergoing pyloromyotomy. Methods: Infants undergoing pyloromyotomy were consecutively included. Ultrasound assessment of the antrum was performed before and after the aspiration of the gastric contents through a 10 French gastric tube. The stomach was defined as empty when no content was seen in both supine and right lateral positions. The correlation between antral area and the aspirated gastric volume was also tested. Results: We analysed 34 infants. Ultrasound examination of the antrum failed in three infants. The stomach was empty in 30/34 infants (nine before aspiration, 21 after aspiration), allowing to perform a non-rapid induction technique in 88.2% of the infants. There was a significant correlation between antral area measured in right lateral decubitus and the aspirated gastric volume. Conclusions: Our results suggest that the qualitative ultrasound assessment of the antral content may be a simple and useful point-of-care tool, for the choice of the most appropriate anaesthetic technique for pyloromyotomy according to the estimated risk of pulmonary aspiration of gastric contents. Key words: infant; anesthesia, general; stomach; pyloric antrum; ultrasound

Accepted: February 7, 2016 © Crown copyright 2016.

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Ultrasound assessment of the gastric contents for the guidance of the anaesthetic strategy in infants with hypertrophic pyloric stenosis: a prospective

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Editor’s key points • Pulmonary aspiration is a potential risk in induction of anaesthesia for pyloromyotomy. • Ultrasound measurement of gastric contents was used in pyloromyotomy to guide anaesthetic technique. • Antral cross sectional area and gastric volume, in lateral decubitas position, were strongly correlated. • Further studies are needed of ultrasound assessment of gastric volume in guiding anaesthetic technique.

Protection des Personnes Sud Est III, Groupement Hospitalier Est, Lyon, Chairperson Prof. F Chapuis, on December 4th, 2012). This single site study was performed in our university hospital (Hôpital Femme Mère Enfant, Bron, France) from January to October 2013. Patients were recruited according to operators′ availability (three physicians, MDQS, SC and CN, with a practice of at least 50 gastric ultrasounds). Parents received information about the study during the preoperative visit. They gave their written consent to the anaesthetist on arrival of their infant in the operating theatre.

Patients

Methods Study design This prospective observational cohort study received approval (n°2012-043B) from the local ethics committee (Comité pour la

All infants undergoing pyloromyotomy during the study period were consecutively included. Exclusion criteria were parental refusal and any contraindication to insert an oro-gastric tube. Once hypertrophic pyloric stenosis was diagnosed, the infant remained fasting, and an eight French enteral feeding tube (Entral™, Maxter Catheters, Marseille, France) was inserted in order to provide passive draining of the gastric contents. Dehydration and electrolyte imbalance were corrected appropriately before surgical repair, which was performed the day after the diagnosis.

Ultrasound examination of the antrum An ultrasound device (SonoSite S-Nerve™, Inc., Bothell, WA) fitted with a linear high-frequency transducer ( probe HFL38, 10–13 MHz) was used to obtain a sagittal cross-section of the antrum, in a plane including the left lobe of the liver and either the aorta or the inferior vena cava, as previously described.15 16 19 All examinations were performed with the infant placed first in supine and then in right lateral decubitus position. During each examination, qualitative assessment of the gastric antrum contents was performed. An ‘empty’ stomach was defined by the absence of any hypoechoic fluid contents seen in the antrum, in both supine and right lateral positions, corresponding to a grade 0 according to the Perlas′s three-point grading scale.14 A ‘full’ stomach was defined by the visualization of hypoechoic fluid contents into the antrum, either in right lateral decubitus only, or in both supine and right lateral positions, corresponding to a Perlas grade 1 or 2, respectively.14 The calculation of the antral cross-sectional area was performed by measuring the longitudinal diameter (D1) and the antero-posterior diameter (D2) of the antrum between antral contractions, from serosa to serosa, using the following formula: Antral area ¼ ðπ × D1 × D2Þ=4:

Protocol A first ultrasound examination of the antrum, including qualitative assessment of the gastric content and measurement of the antral cross-sectional area, was performed at the arrival of the infant in the operating theatre. For all infants, the eight French enteral feeding tube was removed immediately after this first ultrasound examination, and a 10 French PVC multiorifice gastric tube (Salem Sump™, Covidien, Mansfield, MA, USA) was inserted. The gastric contents was gently aspirated, into 60-ml syringes, with the infant installed in supine and then in right lateral decubitus position, by a nurse not aware of the result of the first ultrasound assessment of the gastric contents. A second qualitative ultrasound examination of the antrum was performed

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Hypertrophic pyloric stenosis is one of the most frequent gastrointestinal diseases requiring surgery in infancy.1 Because of potentially large gastric volume resulting from gastric outlet obstruction, infants with pyloric stenosis are considered as being at increased risk of pulmonary aspiration of the gastric contents when performing general anaesthesia for pyloromyotomy. Consequently, blind aspiration of the gastric contents through a gastric tube before induction of anaesthesia, followed by rapid anaesthesia sequence induction, are usually recommended in infants with pyloric stenosis.2 3 However, the systematic achievement of rapid sequence induction after the prior evacuation of the gastric contents remains controversial.2 3 In fact, rapid sequence induction is challenging in infants because of possible increased difficulty for tracheal intubation induced by cricoid pressure,4 5 and an increased risk of hypoxaemia after the 60 s period of apnoea.6 7 Thus, in clinical practice, various induction techniques are performed by paediatric anaesthetists, after pre-induction evacuation of the gastric contents has been done.2 8–10 However, in some infants, the residual gastric fluid volume may remain >1.5 ml kg−1 after blind gastric evacuation, leading to potential increased risk for pulmonary aspiration of the gastric contents if inappropriate induction technique is performed.11 Ultrasound examination of the antrum is a non-invasive and easy-to-perform tool that may allow reliable assessment of the gastric contents in both adults and children.12–17 Particularly, the gastric fluid volume may be estimated by using a three-point grading system, based on the qualitative assessment of the antrum performed in supine and right lateral position.14 18 Furthermore, linear mathematical models were constructed in adults and in children, for the prediction of the gastric volume, according to the antral cross-sectional area measured in right lateral decubitus, and the patients′ age, with R 2 ranging from 0.6 to 0.73.15 18 Thus, one can assume that the ultrasound examination of the antrum could be useful for ascertaining that the gastric contents was totally emptied from the stomach, during the preoperative gastric suction in infants undergoing pyloromyotomy, allowing then to undergo safe non-rapid sequence induction when appropriate. The aim of this prospective observational study was to assess whether the ultrasound monitoring of the aspiration of the stomach contents may be useful to guide the choice of the anaesthetic induction technique in infants undergoing pyloromyotomy. The second aim of this study was to test the correlation between the measurement of antral area and the aspirated gastric volume in those infants.

Ultrasound-guided anaesthesia for pyloromyotomy

immediately after the aspiration of the gastric contents, by the same physician who performed the first ultrasound examination, not blinded to the result of the gastric aspiration. If the stomach was totally emptied (Perlas grade 0), a non-rapid induction sequence (inhalation induction technique) was allowed and performed. If a fluid content was seen either in right lateral decubitus only, or in both right lateral decubitus and supine positions, or if ultrasound examination of the antrum failed, a standard rapid sequence induction was performed. Patient characteristic data, data from the ultrasound examinations performed before and after aspiration through the gastric tube, volumes of aspirated gastric contents, and complications such as regurgitation and pulmonary aspiration occurring during induction and recovery period, were recorded.

Statistical analysis was performed using MedCalc® version 12.1.4.0 (Mariakerke, Belgium). After a Shapiro-Wilk′s W test for normality of distribution of the data, continuous data were expressed as median (interquartile range) or median (min - max). Incidence data were expressed as number ( percentage) and compared using Fisher′s exact test. The median volume suctioned in patients with a ‘full’ stomach according to the first ultrasound examination, was compared with the median volume suctioned in patients with an ‘empty’ stomach, using the Mann-Whitney U test. A linear regression analysis was performed between the antral cross-sectional area and the aspirated gastric volume, with calculation of the Pearson correlation coefficient. A stepwise linear multiple regression was used to model the relation between suctioned volume, antral cross-sectional area, infants′ age and weight. For each test, P<0.05 was considered as statistically significant. We assumed that the second qualitative ultrasound assessment of the gastric contents would allow concluding that rapid sequence induction could be avoided in 40% of the infants, while rapid sequence induction would have been performed in the absence of any ultrasound examination for all infants. According to this hypothesis, the inclusion of 28 infants was

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required, to show a reduction of 40% of the requirement for rapid sequence induction thanks the use of the ultrasound monitoring of the suction of gastric contents, with a significance level of 0.05 and a power of 0.99. Because of foreseeable failures of ultrasound examination, we decided to perform this study over 10 months, in order to include at least 30 infants.

Results Thirty-five infants were undergoing pyloromyotomy during the study period. One infant was not enrolled because of operator unavailability for ultrasound examination. A total of 34 infants were enrolled and included. The median (interquartile range) age was five (4–6) weeks and the median (interquartile range) weight was 3.85 (3.60–4.40) kg. All infants were admitted in operating room within 48 h after the diagnosis of hypertrophic pyloric stenosis. For three patients (8.8%), the first ultrasound assessment of antral area failed, because of either significant amount of gas in the stomach (n=2), or infant agitation (n=1). Among the 31 remaining patients, nine (29%) had an ‘empty’ stomach and 22 (71%) had a ‘full’ stomach, during the first ultrasound examination of the antrum. The median (interquartile range) aspirated gastric volume was 2.2 (0.4–4.3) ml kg−1. In the nine infants with an ‘empty’ stomach during the first ultrasonography, the median (min – max) aspirated gastric fluid volume was 0.26 (0–0.59) ml kg−1, while the median (min – max) aspirated volume was 2.89 (0.86– 12.2) ml kg−1 in the 22 infants with a ‘full’ stomach during the first ultrasound examination (P<0.0001). No ultrasound examination failed after aspiration of gastric contents. After this aspiration, 21/22 (95.5%) infants with a ‘full’ stomach during the first ultrasound had an ‘empty’ stomach during the second examination, and all the infants with an ‘empty’ stomach during the first ultrasound also had an empty stomach during the second examination. Figure 1 shows an example of the change in the antrum before and after aspiration of the gastric content in one infant. Gastric fluid content was seen in right lateral decubitus after gastric aspiration in 1/22 (4.5%) infant. Non-rapid sequence induction was performed in 30/34 (88.2%) infants, while rapid sequence induction would have been performed for all infants, in the absence of any ultrasound examination of the gastric contents (P<0.0001). In the present study,

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Fig. 1 Sonographic images of the antrum, before () and after () aspiration of the gastric contents through a 10 French nasogastric tube in one infant with pyloric stenosis.

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Statistical analysis

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Aspirated volume (ml)

35 30 25 20 15 10 Y=–6.5+4x 5

R=0.83; P<0.0001

0 0

2 4 6 8 Antral area measured in right lateral decubitus (cm²)

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sectional area measured in right lateral decubitus.

Table 1 Regression model statistics for the aspirated gastric volume. Adjusted R 2=0.69 Independent variables Intercept Antral area in RLD (cm2) Weight (kg) Age (weeks)

Coefficient Std. Error 1.4183 4.1805 −0.6524 −1.2387

t

P value

0.6473 6.458 <0.0001 2.1877 −0.298 0.7694 1.0631 −1.165 0.2610

rapid sequence induction was performed in the infant with gastric fluid content still visualized after gastric aspiration, and in the three infants for which ultrasound examination of the antrum failed during the first ultrasonography. The aspirated gastric volume significantly correlated to the antral cross sectional area measured in right lateral position, as set out in Fig. 2. The Pearson correlation coefficient was 0.83 (95% confidence interval: 0.62–0.93; P<0.0001). However, no linear correlation was found between the antral cross sectional area measured in supine position and the suctioned gastric volume (correlation coefficient: 0.20). According to the stepwise linear multiple regression analysis, the prediction of gastric contents was: VolumeðmlÞ ¼ 1:42 þ 4:18 × ðAntral area in RLD ½cm2   1:24 × ðAge ½weeksÞ  0:65 × ðWeight½kgÞ Regression model statistics for the aspirated gastric volume are summarized in Table 1. The adjusted R 2 value was 0.69 for this linear model.

Discussion In this observational prospective study, ultrasound examination of the gastric contents was successfully performed in 31/34 (91.1%) of the infants suffering from hypertrophic pyloric stenosis, enabling the anaesthetists to choose the most appropriate anaesthetic technique, according to the potential risk of pulmonary aspiration of gastric contents: non-rapid induction technique

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Fig. 2 Correlation of the aspirated gastric content with the antral cross-

in 30/34 infants, and standard rapid sequence induction in 4/34 infants. Preoperative evacuation of gastric contents is recommended before induction of general anaesthesia for pyloromyotomy, in order to reduce the gastric volume and, consequently, to minimize the risk of pulmonary aspiration of gastric contents.2 CookSather and colleagues11 previously reported that 83% of the infants undergoing pyloromyotomy had a gastric fluid volume >1.25 ml kg−1, independently of the preoperative fasting duration and of the preoperative nasogastric passive suction. In our study, ultrasound examination of the antrum allowed visualization of a gastric fluid contents in 22/31 (71%) of the infants before the aspiration of the stomach. For these infants, the median aspirated volume was large, >1.25 ml kg−1, while infants with an ‘empty’ stomach during the first ultrasound had a low gastric fluid volume, similar to this reported in adults with Perlas grade 0.18 Hence, the qualitative ultrasound diagnosis of an ‘empty’ stomach could allow the avoidance of insertion of gastric tube for preoperative aspiration of gastric contents before performing a non-rapid sequence induction technique. This could strongly reduce the stress of infants with an ‘empty’ stomach when arriving in the operating theatre,20 without compromising their safety. The ultrasound examination of the antrum performed after the evacuation of the gastric contents through a 10 French orogastric catheter, showed that 21/22 (95.5%) infants had an ‘empty’ stomach. Similarly, Cook-Sather and colleagues11 previously reported that the blind aspiration technique performed through a larger (14 French) multiorifice orogastric catheter was effective, for the almost complete evacuation of the fluid gastric contents assessed by gastroscopy in children, suffering from hypertrophic pyloric stenosis. Gastric contents during pyloric stenosis is mainly related to gastric secretions, and is then composed of clear fluids, that may easily be removed from the stomach during preoperative aspiration, through an appropriate multiorifice gastric tube. Further studies are required to assess whether smaller gastric tube (e.g. eight French tube) could also be used for achieving complete aspiration of the gastric content in infants with pyloric stenosis. After blind aspiration of the gastric content, the choice of the anaesthetic induction technique for pyloromyotomy remains controversial.2 3 21 Rapid sequence induction with cricoid pressure has some inconveniences and may be particularly challenging in infants,4 5 22 23 leading a part of the anaesthetists to routinely avoid cricoid pressure with performing gentle mask ventilation before tracheal intubation,9 or to perform classical non-rapid gaseous induction technique for pyloromyotomy.10 24 In infants with pyloric stenosis, ultrasound examination of gastric content may therefore be a useful point-of-care tool for the guidance of the most appropriate anaesthetic technique, according to the benefits/risks ratio of each technique: rapid sequence induction whenever a gastric content is visualized or when ultrasound examination failed, and non-rapid (inhalation or i.v.) induction whenever the stomach is empty (i.e. for most of the infants included in the present study). In our study, the aspirated gastric content highly correlated with the antral cross sectional area, measured in right lateral decubitus, while antral area measured in supine position poorly correlated to the gastric fluid volume, as previously described.15 25 The P values for age and weight were >0.05 in the mathematical model for the calculation of the gastric volume according to the antral area measured in right lateral position, the patient′s age and weight, probably because of the low dispersion of both weight and age of the infants with pyloric stenosis. Hence, the model can be reduced to the linear correlation between antral

Ultrasound-guided anaesthesia for pyloromyotomy

Authors’ contributions Study design/planning: D.C. Study conduct: M.D.Q.S., S.C., C.N. Data analysis: L.B. Writing paper: A.C.G., L.B. Revising paper: all authors

Declaration of interest None declared.

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5. Landsman I. Cricoid pressure: indications and complications. Paediatr Anaesth 2004; 14: 43–7 6. Hardman JG, Wills JS. The development of hypoxaemia during apnoea in children: a computational modelling investigation. Br J Anaesth 2006; 97: 564–70 7. Xue FS, Luo LK, Tong SY, Liao X, Deng XM, An G. Study of the safe threshold of apneic period in children during anesthesia induction. J Clin Anesth 1996; 8: 568–74 8. Cook-Sather SD, Tulloch HV, Cnaan A, et al. A comparison of awake versus paralyzed tracheal intubation for infants with pyloric stenosis. Anesth Analg 1998; 86: 945–51 9. Neuhaus D, Schmitz A, Gerber A, Weiss M. Controlled rapid sequence induction and intubation - an analysis of 1001 children. Paediatr Anaesth 2013; 23: 734–40 10. Scrimgeour GE, Leather NW, Perry RS, Pappachan JV, Baldock AJ. Gas induction for pyloromyotomy. Paediatr Anaesth 2015; 25: 677–80 11. Cook-Sather SD, Tulloch HV, Liacouras CA, Schreiner MS. Gastric fluid volume in infants for pyloromyotomy. Can J Anaesth 1997; 44: 278–83 12. Bouvet L, Mazoit JX, Chassard D, Allaouchiche B, Boselli E, Benhamou D. Clinical assessment of the ultrasonographic measurement of antral area for estimating preoperative gastric content and volume. Anesthesiology 2011; 114: 1086–92 13. Perlas A, Chan VW, Lupu CM, Mitsakakis N, Hanbidge A. Ultrasound assessment of gastric content and volume. Anesthesiology 2009; 111: 82–9 14. Perlas A, Davis L, Khan M, Mitsakakis N, Chan VW. Gastric sonography in the fasted surgical patient: a prospective descriptive study. Anesth Analg 2011; 113: 93–7 15. Spencer AO, Walker AM, Yeung AK, et al. Ultrasound assessment of gastric volume in the fasted pediatric patient undergoing upper gastrointestinal endoscopy: development of a predictive model using endoscopically suctioned volumes. Paediatr Anaesth 2015; 25: 301–8 16. Schmitz A, Thomas S, Melanie F, et al. Ultrasonographic gastric antral area and gastric contents volume in children. Paediatr Anaesth 2012; 22: 144–9 17. Van de Putte P, Perlas A. Ultrasound assessment of gastric content and volume. Br J Anaesth 2014; 113: 12–22 18. Perlas A, Mitsakakis N, Liu L, et al. Validation of a mathematical model for ultrasound assessment of gastric volume by gastroscopic examination. Anesth Analg 2013; 116: 357–63 19. Cubillos J, Tse C, Chan VW, Perlas A. Bedside ultrasound assessment of gastric content: an observational study. Can J Anaesth 2012; 59: 416–23 20. Carbajal R, Rousset A, Danan C, et al. Epidemiology and treatment of painful procedures in neonates in intensive care units. JAMA 2008; 300: 60–70 21. Neilipovitz DT, Crosby ET. No evidence for decreased incidence of aspiration after rapid sequence induction. Can J Anaesth 2007; 54: 748–64 22. Eich C, Timmermann A, Russo SG, et al. A controlled rapid-sequence induction technique for infants may reduce unsafe actions and stress. Acta Anaesthesiol Scand 2009; 53: 1167–72 23. Engelhardt T. Rapid sequence induction has no use in pediatric anesthesia. Paediatr Anaesth 2015; 25: 5–8 24. Stoddart PA, Brennan L, Hatch DJ, Bingham R. Postal survey of paediatric practice and training among consultant anaesthetists in the UK. Br J Anaesth 1994; 73: 559–63 25. Tomomasa T, Tabata M, Nako Y, Kaneko H, Morikawa A. Ultrasonographic assessment of intragastric volume in neonates: factors affecting the relationship between intragastric

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area measured in right lateral decubitus and the aspirated gastric volume, with a high correlation coefficient (r=0.83). This high relationship between the antral area and the aspirated gastric fluid volume, contributes to confirm that the aspiration of gastric fluid volume was nearly optimal for each infant, and that the qualitative interpretation of the ultrasound examination of the antrum was therefore relevant. Our study has several limitations. Firstly, the ultrasound assessments of gastric contents were performed by three operators. Nevertheless, high intra- and inter-rater reliabilities of both ultrasound measurement and qualitative assessment of the antrum were previously reported in adult patients.26 27 Secondly, the assessment of the gastric fluid content was not corroborated using another method. In fact, the use of either a gastroscopy or a non-invasive technique for estimating gastric volume (gastric tomodensitometry or magnetic resonance imaging) was not feasible in this clinical context. In our study, empty stomach was defined using a qualitative ultrasound score that has been validated in both adults and children.15 18 Thirdly, we could not assess whether this ultrasound-guided anaesthetic strategy would improve the patient outcome, by avoiding the potential complications related to rapid sequence induction without increasing the incidence of pulmonary aspiration of the gastric content. Fortunately, pulmonary aspiration of gastric content is a relatively rare complication related to general anaesthesia,28 and the inclusion of more than 10 000 infants would be required, in order to assess the clinical impact of ultrasound-guided anaesthetic technique strategy, on the risk of pulmonary aspiration in infants undergoing pyloromyotomy. The clinical benefit of the avoidance of rapid sequence induction guided by gastric ultrasound in such infants would be more easily assessed in further studies. In conclusion, our results suggest that the qualitative ultrasound assessment of the antral content may be a simple and useful point-of-care tool for the choice of the most appropriate anaesthetic technique for pyloromyotomy, according to the estimated risk of pulmonary aspiration of gastric contents. Further studies are required in order to assess the clinical benefit of such strategy on patient outcome.

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volume and antral cross-sectional area. Pediatr Radiol 1996; 26: 815–20 26. Arzola C, Cubillos J, Perlas A, Downey K, Carvalho JC. Interrater reliability of qualitative ultrasound assessment of gastric content in the third trimester of pregnancy. Br J Anaesth 2014; 113: 1018–23

27. Kruisselbrink R, Arzola C, Endersby R, Tse C, Chan V, Perlas A. Intra- and interrater reliability of ultrasound assessment of gastric volume. Anesthesiology 2014; 121: 46–51 28. Warner MA, Warner ME, Warner DO, Warner LO, Warner EJ. Perioperative pulmonary aspiration in infants and children. Anesthesiology 1999; 90: 66–71 Handling editor: L. Colvin

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