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Single-breath vital capacity high concentration sevoflurane induction in children: with or without nitrous oxide?
British Journal of Anaesthesia 110 (1): 81–6 (2013) Advance Access publication 17 September 2012 . doi:10.1093/bja/aes319
PAEDIATRICS
Single-breath vital capacity high concentration sevoflurane induction in children: with or without nitrous oxide? S. Y. Lee*, S. L. Cheng, S. B. Ng and S. L. Lim Department of Paediatric Anaesthesia, KK Women’s and Children’s Hospital, 100 Bukit Timah Road, Children’s Tower Level 2, Singapore 229899, Singapore * Corresponding author. E-mail: [email protected]
† This study found that for single-breath vital capacity inhalation induction with high concentration sevoflurane in children, the addition of N2O resulted in faster loss of consciousness and reduced excitatory movements. † Differences in the time to return of ‘regular breathing’ and ‘conjugate gaze’ were not statistically significant. † Patients receiving N2O had less excitatory movements.
Background. Single-breath vital capacity inhalation induction with high concentration sevoflurane (SBVC-HC) is a rapid and ‘needleless’ technique, preferred and well tolerated in the cooperative child. The addition of nitrous oxide may speed up induction by its second gas effects. Previous studies done in children looking at the effect of N2O on this technique lacked power and showed conflicting results. This study aims to investigate the effect of N2O on induction time for SBVC-HC sevoflurane induction in children. Methods. Eighty unpremedicated, ASA I and II children, aged 5–15 yr having elective surgical procedures under general anaesthesia, were recruited and randomized to: Group A: 8% sevoflurane in O2 6 litre min21, and Group B: 8% sevoflurane in N2O 4 litre min21 and O2 2 litre min21. The primary outcome was the time to ‘loss of eyelash reflex’. The time to return of ‘regular respiration’ and ‘conjugate gaze’ were also noted. Results. The difference in the ‘time to loss of eyelash reflex’ was small but statistically significant. Group B: mean duration 53.6 s, standard deviation (SD) 16.1, compared with Group A: 63.5 s, SD 16.1 (mean difference 9.9, 95% confidence interval 2.5–17.3, P¼0.01). Differences in the time to return of ‘regular breathing’ and ‘conjugate gaze’ were not statistically significant. Patients receiving N2O had less excitatory movements (P¼0.007), but incidence of other adverse events was low and did not differ significantly between both groups. More than 94% of children would choose this method of induction again in both groups. Conclusions. We conclude that for SBVC-HC sevoflurane induction in children, the addition of N2O resulted in faster loss of consciousness and reduced excitatory movements. Keywords: anaesthesia, paediatric; anaesthetics gases, nitrous oxide; anaesthetics volatile, sevoflurane; inhalation anaesthesia Accepted for publication: 23 July 2012
Inhalation induction offers the possibility of ‘needleless induction’; hence, it is a preferred technique by many children,1 especially when cannulation is difficult. Paediatric anaesthetists use different strategies for inhalation induction, which can vary from volatile agents delivered in a high inspired concentration or incrementally,2 – 4 by having the child to take a single vital capacity breath5 or normal tidal volume (TV) breaths.6 The introduction of sevoflurane,5 7 with its low solubility and good acceptability even at high concentrations (HCs), has popularized the single-breath technique. It has been shown that single-breath vital capacity HC (SBVC-HC) inhalation induction with sevoflurane is more rapid and better tolerated by the cooperative child, compared with the conventional TV technique.2 6
As with any other drug, nitrous oxide has its advantages and disadvantages. Despite its long history, there have been increasing concerns8 of its possible adverse effects on both patients9 10 and the environment.11 12 More recently, it has been implicated in contributing to increased postoperative nausea/ vomiting, pulmonary complications,9 and possibly apoptosis in the developing brain13 (in animal studies). Previously associated with increased spontaneous abortions in the prescavenging era,14 it is still considered a potential health hazard to healthcare staff, as prolonged exposure may have repercussions on the reproductive, neurological, and haematological systems, by inhibition of methionine synthesis.15 On the environmental aspect, nitrous oxide also contributes to the greenhouse effect.16
& The Author [2012]. Published by Oxford University Press on behalf of the British Journal of Anaesthesia. All rights reserved. For Permissions, please email: [email protected]
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Editor’s key points
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Methods After ethics committee approval, informed written consent was obtained from the parent or legal guardian, and written assent from the child, if old enough. Eighty unpremedicated, ASA I and II paediatric patients, aged 5 –15 yr undergoing elective day surgery procedures, for example, circumcision, herniotomy, and orchidopexy, under general anaesthesia, were recruited. Patients with a history of malignant hyperthermia, reactive airway disease, upper respiratory tract infection, or full stomach were excluded. Patients who preferred an i.v. induction or who could not tolerate the facemask were also not included. Upon recruitment, each child was taught the SBVC inhalation technique. He/she was instructed to take a vital capacity breath, and then breathe out fully, at the end of which, a facemask was applied; and the child was then told to inhale maximally and hold his/her breath for at least 20 s. This was practiced until the child was confident, in performing the technique. Once ready, the child was brought to the operating theatre and arterial pressure, ECG. and pulse oximetry monitoring were applied. Induction was performed using a circle-absorber breathing circuit primed with sevoflurane 8% with 6 litre min21 of fresh gas flow (FGF). Recruited patients were randomized into two groups by sealed envelope assignment: Group A without nitrous oxide (8% sevoflurane in O2 6 litre min21), and Group B with
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nitrous oxide (8% sevoflurane in N2O 4 litre min21and O2 2 litre min21). The Datex-Ohmeda (GE) Aespire 700 anaesthetic machine (breathing system volume of 2.7 litre), with integrated haemodynamic and airway gas monitor system, was used in all cases. Before the facemask was placed on the patient’s face at the end of exhalation, the circle-absorber breathing circuit was primed with the required gas mixture by completely emptying the reservoir bag, and flushing the circuit with 6 litre min21 of FGF and 8% sevoflurane delivered by a Datex Ohmeda Tec 7 vaporiser, with the patient’s Y piece occluded. The volatile concentration was monitored by a Datex Ohmeda (GE) infra-red multi-gas analyser, with side-stream sampling at 200 ml min21, from the Y piece at the patient’s end. A constant sevoflurane concentration of .7% with FGF 6 litre min21 was ensured before proceeding. For our study, the endpoints chosen were the loss of eyelash reflex, establishment of regular breathing, and return of conjugate gaze. The loss of eyelash reflex is most commonly used to identify the loss of consciousness and induction of anaesthesia, whereas regular tidal breathing and the return of conjugate gaze, in combination with other clinical signs such as heart rate (HR) and arterial pressure, are used to gauge the depth of anaesthesia. Based on experience, these endpoints are chosen because they are useful in identifying time to certain events during a paediatric inhalation induction. For example, it may be timely to send a parent out of the induction room with the ‘loss of eyelash reflex’. I.V. cannulation, jaw manipulation, and insertion of airway device30 may be timed with the establishment of ‘regular respiration’ and ‘return of conjugate gaze’. For our study, three endpoints were chosen. The primary outcome was the time (in seconds) to ‘loss of eyelash reflex’, and secondary outcomes were the time to ‘return of regular breathing’ and ‘return of conjugate gaze’. Outcomes were assessed by an independent observer, familiar with the identification of all three endpoints and blinded to the gas mixture delivered. The ‘loss of eyelash reflex’ was assessed every 5 s by gentle brushing of the eyelashes of one eyelid with a finger. Breathing was considered regular once five regular tidal breaths were captured on capnography, in the absence of breathholding or apnoea. Conjugate gaze was assessed by lifting the eyelids to observe for centralization of pupils. All timings were measured from the time the facemask (connected to the primed circuit) was applied onto the child’s face (i.e. at the start of maximal inspiration from residual volume). The onset of anaesthesia was taken as the time when eyelash reflex was lost. Therefore, the time to ‘loss of eyelash reflex’ defined induction time. Vital signs such as systolic arterial pressure (SAP), HR, saturation (SpO2 ), inspired sevoflurane concentration (FISevo), ′ and end-tidal sevoflurane concentration (ESevo ) were recorded just before induction, then at 1 min intervals. Adverse events such as excitatory movements, coughing, laryngospasm, breath-holding/apnoea, and the presence of secretions were also noted with graded severity (0, none; 1, mild; 2, moderate; 3, severe). In addition, desaturation
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Conversely, as an analgesic and weak anaesthetic, nitrous oxide is a useful adjunct to other anaesthetic agents, reducing their consumption, and saving costs. Its anaestheticsparing effect also results in a faster recovery.15 The addition of nitrous oxide can increase the rate of alveolar–capillary uptake of the volatile agent, and also oxygen,17 by the concentration18 and second gas effect.19 20 During inhalation induction, it may contribute to a smoother and marginally quicker induction, as shown by Hall and colleagues.21 This is especially useful in anaesthetizing children,22 23 even the uncooperative ones.3 While this theoretical advantage has not been demonstrated in some adult studies,24 25 the uptake of anaesthetic gas in children differs from the adult, due to a larger ratio of alveolar ventilation to functional residual capacity, a larger fraction of cardiac output being delivered to vessel-rich organs,26 and different blood gas partition coefficients for inhaled anaesthetics.27 28 Responses to inhalation induction may also differ due to higher MAC requirements in children.29 The assessment of concentrating and second gas effects of nitrous oxide may have been underestimated in the past20 (as end-expired concentrations rather than arterial partial pressures were used). Moreover, previous studies3 5 6 22 done in children included only small numbers and were not powered to evaluate the effect of nitrous oxide on SBVC-HC method of induction with sevoflurane. We decided to investigate the hypothesis that the concentrating and second gas effects of nitrous oxide can hasten, smoothen, or both this inhalation induction technique in children.
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N2O for SBVC-HC sevoflurane induction in children
Table 2 Incidence of adverse events during SBVC-HC sevoflurane induction Group A ‘no nitrous’ (n537)
Group B ‘with nitrous’ (n538)
Excitatory movements
0.007
None
40.5% (15)
Mild
29.7% (11)
13.2% (5)
Moderate
24.3% (9)
7.9% (3)
78.9% (30)
Severe
5.4% (2)
0% (0)
83.8%
92.1%
Cough None
0.489
Mild
8.1%
5.3%
Moderate
8.1%
2.6%
None
100%
97.4%
Mild
0%
2.6%
None
100%
97.4%
Mild
0%
2.6%
None
100%
97.4%
Mild
0%
2.6%
0%
0%
Laryngospasm
0.321
Breathholding
0.321
Secretions
Results A total of 75 patients completed the study. Five patients (three in Group A, two in Group B) dropped out due to anxiety (three) and mask refusal upon reaching the operating theatre (two). Baseline characteristics were similar in both Groups A and B (Table 1), and between patients who completed the study and those who did not complete the study. The ‘time to loss of eyelash reflex’ was significantly shorter for the nitrous group (Group B) with a mean duration of 53.6 s (SD 16.1), compared with Group A which was 63.5 s (SD 16.1). This gave a mean difference of 9.9 s [95% confidence interval (CI) 2.5–17.3], P¼0.01. Differences in secondary endpoints were not statistically significant. The time to return of regular breathing in Group A was 90.1 s (SD 18.4) and Group B was 81.5 s (SD 20.5), with a mean difference of 8.6 s (95% CI 20.4 to 17.7), P¼0.06.
Desaturation
P-value
0.321
Male
78.4%
78.9%
Female
21.6%
21.1%
The time to return of conjugate gaze in Group A was 160.6 s (SD 32.0) and Group B was 153.6 s (SD 41.3), with a mean difference of 7.0 s (95% CI 210.1 to 24.1), P¼0.42. Patients receiving nitrous oxide (Group B) had less excitatory movements (P¼0.007) (Table 2). The incidence of other adverse events (i.e. cough, laryngospasm, breathholding, secretions, desaturation) was low and did not differ significantly between the groups. ′ Changes in FISevo and ESevo recorded every minute from the start of induction were similar between both groups. The FISevo at baseline 0 min was .7% in all patients and notably higher in the non-nitrous Group A (mean inspired Sevo 8.08%, SD 0.53) compared with the nitrous Group B (mean inspired Sevo 7.64%, SD 0.49), with a mean difference of 0.44% (95% CI 0.20 –0.18), P¼0.001. Changes in vital signs such as SAP and HR after SBVC-HC induction did not differ significantly between the two groups (Table 3). Only two out of 37 patients in Group A required ‘rescue’ i.v. agents. More than 94% of children in both groups indicated that they would choose SBVC-HC inhalation induction again. The difference between the two groups was not significant, with 94.7% of children in Group B and 94.3% of children in Group A (P¼1.0) reporting that they would choose the same method of induction again.
Circumcision
48.6%
55.3%
Discussion
Others
51.4%
44.7%
Table 1 Patient characteristic data. Data for age are shown as mean (range) Group A ‘no nitrous’ (n537) Age (yr)
9.14 (5– 15)
Group B ‘with nitrous’ (n538) 9.50 (6– 15)
ASA I
86.5%
78.9%
II
13.5%
21.1%
Gender
Surgery
We found that the addition of nitrous oxide to the gas mixture hastened and smoothened SBVC-HC sevoflurane
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SpO2 ,94% and the need for rescue i.v. induction drugs was noted. Observations were made until the last endpoint ‘return of conjugate gaze’ was reached. All timings were recorded using the same stopwatch each time. The primary and secondary endpoints were defined as above. The severity of excitatory movements were defined as (0, none; 1, mild, inconsequential; 2, moderate, more movement but does not interfere with induction; 3, severe, interferes with induction, requiring restraint). On return to the day surgery ward, the patients were asked if they were satisfied with the technique and whether they would choose the same type of induction again. Based on a local study31 where the mean SB-VC induction time was 50 s (SD 14), a 10 s difference in induction time was presumed significant, and a sample size of 62 (31 in each group) calculated, using a two-tailed test with a-value of 0.05 and b of 0.2. SPSS version 16 was used for statistical analysis, where unpaired t-test and x 2/Fisher’s exact tests were used for continuous variables and categorical variables, respectively. P,0.05 was presumed as significant.
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Table 3 Changes in inspired sevoflurane (FISevo), expired sevoflurane (E′Sevo), SAP, and HR during SBVC-HC induction, with and without nitrous oxide Variables
Time from start of induction (min) 0
1
2
3
4
FISevo (%) (SD) Group A
8.08 (0.53)
7.67 (0.84)
7.33 (0.79)
6.44 (1.54)
5.30 (1.73)
Group B
7.64 (0.49)
7.46 (0.59)
7.28 (0.59)
6.57 (1.02)
5.07 (1.72)
Group A
3.60 (3.85)
5.85 (1.41)
5.93 (1.04)
5.45 (1.13)
4.59 (1.39)
Group B
3.67 (3.95)
5.50 (1.62)
6.08 (1.09)
5.64 (0.87)
4.59 (1.38)
Group A
99.06 (1.37)
99.37 (1.22)
99.71 (0.94)
99.60 (1.27)
99.79 (0.49)
Group B
98.11 (4.98)
99.05 (1.29)
99.32 (1.29)
99.22 (1.46)
99.47 (1.16)
Group A
86.95 (14.22)
97.78 (16.60)
104.25 (21.97)
103.62 (28.71)
94.61 (23.04)
Group B
88.97 (16.54)
92.89 (17.07)
95.84 (20.87)
93.18 (23.45)
88.58 (24.32)
E′Sevo (%) (SD)
SAP (mm Hg) (SD)
induction in children. This supports our hypothesis that the concentration18 and second gas19 20 effects of nitrous oxide makes it an effective adjunct16 in improving the rate and quality of inhalation induction in children. First described by Lamberty32 in 1988, the single-breath induction technique has been much evaluated in both adults and children, using HC administration of various types of volatile agents, for example, halothane5 or sevoflurane, delivered via carrier gas (with or without nitrous oxide). Studies have consistently shown that the SBVC6 33 34-HC2 3 technique results in faster induction of anaesthesia than incremental TV technique, in both adults and children. The SBVC-HC sevoflurane technique has been shown to be an efficient and well-accepted technique in children as young as 4 yr old, with an acceptance rate up to 95% in older children.35 It is associated with few haemodynamic side-effects or airway complications,35 36 and it remains very popular with paediatric anaesthetists.37 However, the effect of nitrous oxide in the gas mixture remained equivocal. In our study, SBVC-HC inhalation induction using a circle system primed with .7% sevoflurane delivered by 6 litre min21 FGF yielded an approximate induction time of 53.6 s with nitrous oxide, and 63.5 s without nitrous oxide. Similar induction timings were reported by Dubois and colleagues22 and Ho and colleagues.31 Two other paediatric studies5 6 found shorter induction times, probably because patients were premedicated, and noncircle delivery systems with higher gas flows, such as the Ayre’s T-piece, were used. Despite presenting a lower sevoflurane concentration in the nitrous oxide group, our study consistently showed a small but statistically significant faster induction time when nitrous oxide was used as a carrier gas using an SBVC-HC technique. This was also shown by Dubois and colleagues,22 although the TV technique was used in her study. These findings are in contrast to three adult studies by Yurino and Kimura38 (SBVC), Siau and Liu,25 and O’Shea and colleagues24
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(TV technique for both), which failed to show a difference in time to induction of anaesthesia, although ‘motor endpoints’ (time taken for the outstretched arm to drop, and cessation of finger tapping) were used in the latter two studies. The discrepancy may be due to different endpoints being chosen. The effects of nitrous oxide on the incidence of excitation and involuntary limb movement in our study also differed from other studies. Fernandes and colleagues39 and O’Shea and colleagues24 found that excitation was more frequent in adults receiving nitrous oxide than those receiving oxygen only. Siau and Liu25 reported nitrous oxide conferred no benefit in the reduction in involuntary movements, whereas Dubois and colleagues22 found that nitrous oxide reduced the incidence of excitation. Our study found that the addition of nitrous oxide resulted in a smoother induction and a decreased incidence of excitatory movements. The difference between adult and paediatric studies may be explained by the fact that the minimum alveolar concentration (MAC) requirements decreases with age.29 At a similar end-tidal concentration of inhaled anaesthetic agent, a child may still be in stage 2, the excitatory stage of anaesthesia, when compared with an adult. Hence the addition of nitrous oxide, which allows a more rapid achievement of a higher MAC, would result in a smoother induction with less time in stage 2 of anaesthesia. The use of nitrous oxide has been challenged due to its postulated deleterious effects on the haematological system and cardiovascular system after prolonged exposure, especially in patients at risk.40 The effects of raised plasma homocysteine levels after nitrous oxide anaesthesia in children warrant further investigation.41 However, we found that nitrous oxide still has significant advantages as a co-induction agent for sevoflurane inhalation induction using the SBVC-HC technique in children, resulting in a faster and smoother induction. This was achieved using a circle system with efficient scavenging, hence reducing theatre and environmental pollution. At the recommended
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HR (beats min21) (SD)
N2O for SBVC-HC sevoflurane induction in children
Declaration of interest None declared.
Funding This study was self-funded by departmental funds.
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10 Baum VC. When nitrous oxide is no laughing matter: nitrous oxide and pediatric anesthesia. Paediatr Anaesth 2007; 17: 824–30 11 Byhahn C, Strouhal U, Westphal K. Exposure of anesthetists to sevoflurane and nitrous oxide during inhalation anesthesia induction in pediatric anesthesia. Anaesthesiol Reanim 2000; 25: 12– 6 12 Wood C, Ewen A, Goresky G, et al. Exposure of operating room personnel to nitrous oxide during paediatric anaesthesia. Can J Anaesth 1992; 39: 682–6 13 Schmitt EL, Baum VC. Nitrous oxide in pediatric anesthesia: friend or foe? Curr Opin Anaesthesiol 2008; 2: 356–9 14 Boivin JF. Risk of spontaneous abortion in women occupationally exposed to anaesthetic gases: a meta-analysis. Occup Environ Med 1997; 54: 541–8 15 Smith I. Nitrous oxide in ambulatory anaesthesia: does it have a place in day surgical anaesthesia or is it just a threat for personnel and the global environment? Curr Opin Anaesthesiol 2006; 19: 592– 6 16 Sherman SJ, Cullen BF. Nitrous oxide and the greenhouse effect. Anesthesiology 1988; 68: 816–7 17 Peyton PJ, Stuart-Andrews C, Deo K, et al. Persisting concentrating and second gas effects on oxygenation during N2O anaesthesia. Anaesthesia 2006; 61: 322– 9 18 Goldman LJ. Anesthetic uptake of sevoflurane and nitrous oxide during an inhaled induction in children. Anesth Analg 2003; 96: 400–6 19 Taheri S, Eger EI. A demonstration of the concentration and second gas effects in humans anesthetized with nitrous oxide and desflurane. Anesth Analg 1999; 89: 774– 80 20 Peyton PJ, Fortuin M, Robinson GJ, et al. The rate of alveolarcapillary uptake of sevoflurane and nitrous oxide following anaesthetic induction. Anaesthesia 2008; 63: 358–63 21 Hall JE, Stewart JIM, Harmer M. Single-breath inhalation induction of sevoflurane anaesthesia with and without nitrous oxide: a feasibility study in adults and comparison with an intravenous bolus of propofol. Anaesthesia 1997; 52: 410– 15 22 Dubois MC, Piat V, Constant I, et al. Comparison of three techniques for induction of anaesthesia with sevoflurane in children. Paediatr Anaesth 1999; 9: 19– 23 23 Kihara S, Yaguchi Y, Inomata S, et al. Influence of nitrous oxide on minimum alveolar concentration of sevoflurane for laryngeal mask insertion in children. Anesthesiology 2003; 99: 1055–8 24 O’Shea H, Moultrie S, Drummond GB. Influence of nitrous oxide on induction of anaesthesia with sevoflurane. Br J Anaesth 2001; 87: 286– 8 25 Siau C, Liu EHC. Nitrous oxide does not improve sevoflurane induction of anesthesia in adults. J Clin Anesth 2002; 14: 218– 22 26 Rusy L, Usaleva E. Paediatric anaesthesia review. Update Anaesth 1998; 8: Article 2 27 Lerman J, Schmitt-Bantel BI, Gregory GA, et al. Effect of age on the solubility of volatile anesthetics in human tissues. Anesthesiology 1986; 65: 307– 11 28 Lerman J, Gregory GA, Willis MM, et al. Age and solubility of volatile anesthetics in blood. Anesthesiology 1984; 61: 139– 43 29 Stoelting RK, Hillier SC. Pharmacology and Physiology in Anesthetic Practice, 4th Edn. Lippincott: Williams and Wilkins, 2006; 34– 5 30 Wappler F, Frings DP, Scholz J, et al. Inhalational induction of anaesthesia with 8% sevoflurane in children: conditions for endotracheal intubation and side-effects. Eur J Anaesthesiol 2003; 20: 548–54 31 Ho K, Chua WL, Lim S, et al. A comparison between single-and double-breath vital capacity inhalation induction with 8% sevoflurane in children. Paediatr Anaesth 2004; 14: 457– 61
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occupational exposure limits, there is no conclusive evidence for reproductive, genetic, haematological, or neurological occupational toxicity from nitrous oxide exposure.40 Nitrous oxide remains to be a useful inhalation analgesic and sedative that is cheap and has a long history of use in various clinical settings. Further research is needed to weigh the risk –benefit ratio of using this agent for anaesthesia in the paediatric population. In conclusion, we found that the addition of nitrous oxide resulted in less excitation and marginally faster induction times, as defined by the time to loss of eyelash reflex. Overall, we also established that the SBVC-HC sevoflurane technique was pleasant with most children choosing to have it again. Despite movement away from the use of nitrous oxide, it may still have a beneficial role in SBVC-HC sevoflurane induction in children. Further studies need to be done to evaluate if short exposure to nitrous oxide during induction alone has the same adverse effects as when used for a longer period during maintenance of anaesthesia, to the patients and healthcare personnel.
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BJA 32 Lamberty J. Single breath induction. Anaesthesia 1988; 43: 160. 33 Martı´n-Larrauri R, Gilsanz F, Rodrigo J, et al. Conventional stepwise vs. vital capacity rapid inhalation induction at two concentrations of sevoflurane. Eur J Anaesthesiol 2004; 21: 265– 71 34 Yurino M, Kimura H. A comparison of vital capacity breath and tidal breathing techniques for induction of anaesthesia with high sevoflurane concentrations in nitrous oxide and oxygen. Anaesthesia 1995; 50: 308–11 35 Fernandez M, Lejus C, Rivault O, et al. Single-breath vital capacity rapid inhalation induction with sevoflurane: feasibility in children. Paediatr Anaesth 2005; 15: 307–13 36 Nishiyama T, Aibiki M, Hanaoka K. Haemodynamic and catecholamine changes during rapid sevoflurane induction with tidal volume breathing. Can J Anaesth 1997; 44: 1066– 70
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37 Lerman J. Inhalation agents in pediatric anaesthesia—an update. Curr Opin Anaesthesiol 2007; 20: 221– 6 38 Yurino M, Kimura H. Comparison of induction time and characteristics between sevoflurane and sevoflurane/nitrous oxide. Acta Anaesthesiol Scand 1995; 39: 356–8 39 Fernandes CR, Gomes JM, Cordeiro RA, et al. Assessment of the cognitive effects of inhalational induction with sevoflurane associated or not with nitrous oxide: a comparative study in adult volunteers. Rev Bras Anestesiol 2007; 57: 237– 46 40 Sanders RD, Weimann J, Maze M. Biologic effects of nitrous oxide. A mechanistic and toxicologic review. Anesthesiology 2008; 109: 707– 22 41 Pichardo D, Luginbuehl IA, Shakur Y, et al. Effect of nitrous oxide exposure during surgery on the homocysteine concentrations of children. Anesthesiology 2012; 117: 15 –21
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Handling editor: M. M. R. F. Struys
PAEDIATRICS
Single-breath vital capacity high concentration sevoflurane induction in children: with or without nitrous oxide? S. Y. Lee*, S. L. Cheng, S. B. Ng and S. L. Lim Department of Paediatric Anaesthesia, KK Women’s and Children’s Hospital, 100 Bukit Timah Road, Children’s Tower Level 2, Singapore 229899, Singapore * Corresponding author. E-mail: [email protected]
† This study found that for single-breath vital capacity inhalation induction with high concentration sevoflurane in children, the addition of N2O resulted in faster loss of consciousness and reduced excitatory movements. † Differences in the time to return of ‘regular breathing’ and ‘conjugate gaze’ were not statistically significant. † Patients receiving N2O had less excitatory movements.
Background. Single-breath vital capacity inhalation induction with high concentration sevoflurane (SBVC-HC) is a rapid and ‘needleless’ technique, preferred and well tolerated in the cooperative child. The addition of nitrous oxide may speed up induction by its second gas effects. Previous studies done in children looking at the effect of N2O on this technique lacked power and showed conflicting results. This study aims to investigate the effect of N2O on induction time for SBVC-HC sevoflurane induction in children. Methods. Eighty unpremedicated, ASA I and II children, aged 5–15 yr having elective surgical procedures under general anaesthesia, were recruited and randomized to: Group A: 8% sevoflurane in O2 6 litre min21, and Group B: 8% sevoflurane in N2O 4 litre min21 and O2 2 litre min21. The primary outcome was the time to ‘loss of eyelash reflex’. The time to return of ‘regular respiration’ and ‘conjugate gaze’ were also noted. Results. The difference in the ‘time to loss of eyelash reflex’ was small but statistically significant. Group B: mean duration 53.6 s, standard deviation (SD) 16.1, compared with Group A: 63.5 s, SD 16.1 (mean difference 9.9, 95% confidence interval 2.5–17.3, P¼0.01). Differences in the time to return of ‘regular breathing’ and ‘conjugate gaze’ were not statistically significant. Patients receiving N2O had less excitatory movements (P¼0.007), but incidence of other adverse events was low and did not differ significantly between both groups. More than 94% of children would choose this method of induction again in both groups. Conclusions. We conclude that for SBVC-HC sevoflurane induction in children, the addition of N2O resulted in faster loss of consciousness and reduced excitatory movements. Keywords: anaesthesia, paediatric; anaesthetics gases, nitrous oxide; anaesthetics volatile, sevoflurane; inhalation anaesthesia Accepted for publication: 23 July 2012
Inhalation induction offers the possibility of ‘needleless induction’; hence, it is a preferred technique by many children,1 especially when cannulation is difficult. Paediatric anaesthetists use different strategies for inhalation induction, which can vary from volatile agents delivered in a high inspired concentration or incrementally,2 – 4 by having the child to take a single vital capacity breath5 or normal tidal volume (TV) breaths.6 The introduction of sevoflurane,5 7 with its low solubility and good acceptability even at high concentrations (HCs), has popularized the single-breath technique. It has been shown that single-breath vital capacity HC (SBVC-HC) inhalation induction with sevoflurane is more rapid and better tolerated by the cooperative child, compared with the conventional TV technique.2 6
As with any other drug, nitrous oxide has its advantages and disadvantages. Despite its long history, there have been increasing concerns8 of its possible adverse effects on both patients9 10 and the environment.11 12 More recently, it has been implicated in contributing to increased postoperative nausea/ vomiting, pulmonary complications,9 and possibly apoptosis in the developing brain13 (in animal studies). Previously associated with increased spontaneous abortions in the prescavenging era,14 it is still considered a potential health hazard to healthcare staff, as prolonged exposure may have repercussions on the reproductive, neurological, and haematological systems, by inhibition of methionine synthesis.15 On the environmental aspect, nitrous oxide also contributes to the greenhouse effect.16
& The Author [2012]. Published by Oxford University Press on behalf of the British Journal of Anaesthesia. All rights reserved. For Permissions, please email: [email protected]
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Editor’s key points
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Methods After ethics committee approval, informed written consent was obtained from the parent or legal guardian, and written assent from the child, if old enough. Eighty unpremedicated, ASA I and II paediatric patients, aged 5 –15 yr undergoing elective day surgery procedures, for example, circumcision, herniotomy, and orchidopexy, under general anaesthesia, were recruited. Patients with a history of malignant hyperthermia, reactive airway disease, upper respiratory tract infection, or full stomach were excluded. Patients who preferred an i.v. induction or who could not tolerate the facemask were also not included. Upon recruitment, each child was taught the SBVC inhalation technique. He/she was instructed to take a vital capacity breath, and then breathe out fully, at the end of which, a facemask was applied; and the child was then told to inhale maximally and hold his/her breath for at least 20 s. This was practiced until the child was confident, in performing the technique. Once ready, the child was brought to the operating theatre and arterial pressure, ECG. and pulse oximetry monitoring were applied. Induction was performed using a circle-absorber breathing circuit primed with sevoflurane 8% with 6 litre min21 of fresh gas flow (FGF). Recruited patients were randomized into two groups by sealed envelope assignment: Group A without nitrous oxide (8% sevoflurane in O2 6 litre min21), and Group B with
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nitrous oxide (8% sevoflurane in N2O 4 litre min21and O2 2 litre min21). The Datex-Ohmeda (GE) Aespire 700 anaesthetic machine (breathing system volume of 2.7 litre), with integrated haemodynamic and airway gas monitor system, was used in all cases. Before the facemask was placed on the patient’s face at the end of exhalation, the circle-absorber breathing circuit was primed with the required gas mixture by completely emptying the reservoir bag, and flushing the circuit with 6 litre min21 of FGF and 8% sevoflurane delivered by a Datex Ohmeda Tec 7 vaporiser, with the patient’s Y piece occluded. The volatile concentration was monitored by a Datex Ohmeda (GE) infra-red multi-gas analyser, with side-stream sampling at 200 ml min21, from the Y piece at the patient’s end. A constant sevoflurane concentration of .7% with FGF 6 litre min21 was ensured before proceeding. For our study, the endpoints chosen were the loss of eyelash reflex, establishment of regular breathing, and return of conjugate gaze. The loss of eyelash reflex is most commonly used to identify the loss of consciousness and induction of anaesthesia, whereas regular tidal breathing and the return of conjugate gaze, in combination with other clinical signs such as heart rate (HR) and arterial pressure, are used to gauge the depth of anaesthesia. Based on experience, these endpoints are chosen because they are useful in identifying time to certain events during a paediatric inhalation induction. For example, it may be timely to send a parent out of the induction room with the ‘loss of eyelash reflex’. I.V. cannulation, jaw manipulation, and insertion of airway device30 may be timed with the establishment of ‘regular respiration’ and ‘return of conjugate gaze’. For our study, three endpoints were chosen. The primary outcome was the time (in seconds) to ‘loss of eyelash reflex’, and secondary outcomes were the time to ‘return of regular breathing’ and ‘return of conjugate gaze’. Outcomes were assessed by an independent observer, familiar with the identification of all three endpoints and blinded to the gas mixture delivered. The ‘loss of eyelash reflex’ was assessed every 5 s by gentle brushing of the eyelashes of one eyelid with a finger. Breathing was considered regular once five regular tidal breaths were captured on capnography, in the absence of breathholding or apnoea. Conjugate gaze was assessed by lifting the eyelids to observe for centralization of pupils. All timings were measured from the time the facemask (connected to the primed circuit) was applied onto the child’s face (i.e. at the start of maximal inspiration from residual volume). The onset of anaesthesia was taken as the time when eyelash reflex was lost. Therefore, the time to ‘loss of eyelash reflex’ defined induction time. Vital signs such as systolic arterial pressure (SAP), HR, saturation (SpO2 ), inspired sevoflurane concentration (FISevo), ′ and end-tidal sevoflurane concentration (ESevo ) were recorded just before induction, then at 1 min intervals. Adverse events such as excitatory movements, coughing, laryngospasm, breath-holding/apnoea, and the presence of secretions were also noted with graded severity (0, none; 1, mild; 2, moderate; 3, severe). In addition, desaturation
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Conversely, as an analgesic and weak anaesthetic, nitrous oxide is a useful adjunct to other anaesthetic agents, reducing their consumption, and saving costs. Its anaestheticsparing effect also results in a faster recovery.15 The addition of nitrous oxide can increase the rate of alveolar–capillary uptake of the volatile agent, and also oxygen,17 by the concentration18 and second gas effect.19 20 During inhalation induction, it may contribute to a smoother and marginally quicker induction, as shown by Hall and colleagues.21 This is especially useful in anaesthetizing children,22 23 even the uncooperative ones.3 While this theoretical advantage has not been demonstrated in some adult studies,24 25 the uptake of anaesthetic gas in children differs from the adult, due to a larger ratio of alveolar ventilation to functional residual capacity, a larger fraction of cardiac output being delivered to vessel-rich organs,26 and different blood gas partition coefficients for inhaled anaesthetics.27 28 Responses to inhalation induction may also differ due to higher MAC requirements in children.29 The assessment of concentrating and second gas effects of nitrous oxide may have been underestimated in the past20 (as end-expired concentrations rather than arterial partial pressures were used). Moreover, previous studies3 5 6 22 done in children included only small numbers and were not powered to evaluate the effect of nitrous oxide on SBVC-HC method of induction with sevoflurane. We decided to investigate the hypothesis that the concentrating and second gas effects of nitrous oxide can hasten, smoothen, or both this inhalation induction technique in children.
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N2O for SBVC-HC sevoflurane induction in children
Table 2 Incidence of adverse events during SBVC-HC sevoflurane induction Group A ‘no nitrous’ (n537)
Group B ‘with nitrous’ (n538)
Excitatory movements
0.007
None
40.5% (15)
Mild
29.7% (11)
13.2% (5)
Moderate
24.3% (9)
7.9% (3)
78.9% (30)
Severe
5.4% (2)
0% (0)
83.8%
92.1%
Cough None
0.489
Mild
8.1%
5.3%
Moderate
8.1%
2.6%
None
100%
97.4%
Mild
0%
2.6%
None
100%
97.4%
Mild
0%
2.6%
None
100%
97.4%
Mild
0%
2.6%
0%
0%
Laryngospasm
0.321
Breathholding
0.321
Secretions
Results A total of 75 patients completed the study. Five patients (three in Group A, two in Group B) dropped out due to anxiety (three) and mask refusal upon reaching the operating theatre (two). Baseline characteristics were similar in both Groups A and B (Table 1), and between patients who completed the study and those who did not complete the study. The ‘time to loss of eyelash reflex’ was significantly shorter for the nitrous group (Group B) with a mean duration of 53.6 s (SD 16.1), compared with Group A which was 63.5 s (SD 16.1). This gave a mean difference of 9.9 s [95% confidence interval (CI) 2.5–17.3], P¼0.01. Differences in secondary endpoints were not statistically significant. The time to return of regular breathing in Group A was 90.1 s (SD 18.4) and Group B was 81.5 s (SD 20.5), with a mean difference of 8.6 s (95% CI 20.4 to 17.7), P¼0.06.
Desaturation
P-value
0.321
Male
78.4%
78.9%
Female
21.6%
21.1%
The time to return of conjugate gaze in Group A was 160.6 s (SD 32.0) and Group B was 153.6 s (SD 41.3), with a mean difference of 7.0 s (95% CI 210.1 to 24.1), P¼0.42. Patients receiving nitrous oxide (Group B) had less excitatory movements (P¼0.007) (Table 2). The incidence of other adverse events (i.e. cough, laryngospasm, breathholding, secretions, desaturation) was low and did not differ significantly between the groups. ′ Changes in FISevo and ESevo recorded every minute from the start of induction were similar between both groups. The FISevo at baseline 0 min was .7% in all patients and notably higher in the non-nitrous Group A (mean inspired Sevo 8.08%, SD 0.53) compared with the nitrous Group B (mean inspired Sevo 7.64%, SD 0.49), with a mean difference of 0.44% (95% CI 0.20 –0.18), P¼0.001. Changes in vital signs such as SAP and HR after SBVC-HC induction did not differ significantly between the two groups (Table 3). Only two out of 37 patients in Group A required ‘rescue’ i.v. agents. More than 94% of children in both groups indicated that they would choose SBVC-HC inhalation induction again. The difference between the two groups was not significant, with 94.7% of children in Group B and 94.3% of children in Group A (P¼1.0) reporting that they would choose the same method of induction again.
Circumcision
48.6%
55.3%
Discussion
Others
51.4%
44.7%
Table 1 Patient characteristic data. Data for age are shown as mean (range) Group A ‘no nitrous’ (n537) Age (yr)
9.14 (5– 15)
Group B ‘with nitrous’ (n538) 9.50 (6– 15)
ASA I
86.5%
78.9%
II
13.5%
21.1%
Gender
Surgery
We found that the addition of nitrous oxide to the gas mixture hastened and smoothened SBVC-HC sevoflurane
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SpO2 ,94% and the need for rescue i.v. induction drugs was noted. Observations were made until the last endpoint ‘return of conjugate gaze’ was reached. All timings were recorded using the same stopwatch each time. The primary and secondary endpoints were defined as above. The severity of excitatory movements were defined as (0, none; 1, mild, inconsequential; 2, moderate, more movement but does not interfere with induction; 3, severe, interferes with induction, requiring restraint). On return to the day surgery ward, the patients were asked if they were satisfied with the technique and whether they would choose the same type of induction again. Based on a local study31 where the mean SB-VC induction time was 50 s (SD 14), a 10 s difference in induction time was presumed significant, and a sample size of 62 (31 in each group) calculated, using a two-tailed test with a-value of 0.05 and b of 0.2. SPSS version 16 was used for statistical analysis, where unpaired t-test and x 2/Fisher’s exact tests were used for continuous variables and categorical variables, respectively. P,0.05 was presumed as significant.
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Table 3 Changes in inspired sevoflurane (FISevo), expired sevoflurane (E′Sevo), SAP, and HR during SBVC-HC induction, with and without nitrous oxide Variables
Time from start of induction (min) 0
1
2
3
4
FISevo (%) (SD) Group A
8.08 (0.53)
7.67 (0.84)
7.33 (0.79)
6.44 (1.54)
5.30 (1.73)
Group B
7.64 (0.49)
7.46 (0.59)
7.28 (0.59)
6.57 (1.02)
5.07 (1.72)
Group A
3.60 (3.85)
5.85 (1.41)
5.93 (1.04)
5.45 (1.13)
4.59 (1.39)
Group B
3.67 (3.95)
5.50 (1.62)
6.08 (1.09)
5.64 (0.87)
4.59 (1.38)
Group A
99.06 (1.37)
99.37 (1.22)
99.71 (0.94)
99.60 (1.27)
99.79 (0.49)
Group B
98.11 (4.98)
99.05 (1.29)
99.32 (1.29)
99.22 (1.46)
99.47 (1.16)
Group A
86.95 (14.22)
97.78 (16.60)
104.25 (21.97)
103.62 (28.71)
94.61 (23.04)
Group B
88.97 (16.54)
92.89 (17.07)
95.84 (20.87)
93.18 (23.45)
88.58 (24.32)
E′Sevo (%) (SD)
SAP (mm Hg) (SD)
induction in children. This supports our hypothesis that the concentration18 and second gas19 20 effects of nitrous oxide makes it an effective adjunct16 in improving the rate and quality of inhalation induction in children. First described by Lamberty32 in 1988, the single-breath induction technique has been much evaluated in both adults and children, using HC administration of various types of volatile agents, for example, halothane5 or sevoflurane, delivered via carrier gas (with or without nitrous oxide). Studies have consistently shown that the SBVC6 33 34-HC2 3 technique results in faster induction of anaesthesia than incremental TV technique, in both adults and children. The SBVC-HC sevoflurane technique has been shown to be an efficient and well-accepted technique in children as young as 4 yr old, with an acceptance rate up to 95% in older children.35 It is associated with few haemodynamic side-effects or airway complications,35 36 and it remains very popular with paediatric anaesthetists.37 However, the effect of nitrous oxide in the gas mixture remained equivocal. In our study, SBVC-HC inhalation induction using a circle system primed with .7% sevoflurane delivered by 6 litre min21 FGF yielded an approximate induction time of 53.6 s with nitrous oxide, and 63.5 s without nitrous oxide. Similar induction timings were reported by Dubois and colleagues22 and Ho and colleagues.31 Two other paediatric studies5 6 found shorter induction times, probably because patients were premedicated, and noncircle delivery systems with higher gas flows, such as the Ayre’s T-piece, were used. Despite presenting a lower sevoflurane concentration in the nitrous oxide group, our study consistently showed a small but statistically significant faster induction time when nitrous oxide was used as a carrier gas using an SBVC-HC technique. This was also shown by Dubois and colleagues,22 although the TV technique was used in her study. These findings are in contrast to three adult studies by Yurino and Kimura38 (SBVC), Siau and Liu,25 and O’Shea and colleagues24
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(TV technique for both), which failed to show a difference in time to induction of anaesthesia, although ‘motor endpoints’ (time taken for the outstretched arm to drop, and cessation of finger tapping) were used in the latter two studies. The discrepancy may be due to different endpoints being chosen. The effects of nitrous oxide on the incidence of excitation and involuntary limb movement in our study also differed from other studies. Fernandes and colleagues39 and O’Shea and colleagues24 found that excitation was more frequent in adults receiving nitrous oxide than those receiving oxygen only. Siau and Liu25 reported nitrous oxide conferred no benefit in the reduction in involuntary movements, whereas Dubois and colleagues22 found that nitrous oxide reduced the incidence of excitation. Our study found that the addition of nitrous oxide resulted in a smoother induction and a decreased incidence of excitatory movements. The difference between adult and paediatric studies may be explained by the fact that the minimum alveolar concentration (MAC) requirements decreases with age.29 At a similar end-tidal concentration of inhaled anaesthetic agent, a child may still be in stage 2, the excitatory stage of anaesthesia, when compared with an adult. Hence the addition of nitrous oxide, which allows a more rapid achievement of a higher MAC, would result in a smoother induction with less time in stage 2 of anaesthesia. The use of nitrous oxide has been challenged due to its postulated deleterious effects on the haematological system and cardiovascular system after prolonged exposure, especially in patients at risk.40 The effects of raised plasma homocysteine levels after nitrous oxide anaesthesia in children warrant further investigation.41 However, we found that nitrous oxide still has significant advantages as a co-induction agent for sevoflurane inhalation induction using the SBVC-HC technique in children, resulting in a faster and smoother induction. This was achieved using a circle system with efficient scavenging, hence reducing theatre and environmental pollution. At the recommended
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HR (beats min21) (SD)
N2O for SBVC-HC sevoflurane induction in children
Declaration of interest None declared.
Funding This study was self-funded by departmental funds.
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10 Baum VC. When nitrous oxide is no laughing matter: nitrous oxide and pediatric anesthesia. Paediatr Anaesth 2007; 17: 824–30 11 Byhahn C, Strouhal U, Westphal K. Exposure of anesthetists to sevoflurane and nitrous oxide during inhalation anesthesia induction in pediatric anesthesia. Anaesthesiol Reanim 2000; 25: 12– 6 12 Wood C, Ewen A, Goresky G, et al. Exposure of operating room personnel to nitrous oxide during paediatric anaesthesia. Can J Anaesth 1992; 39: 682–6 13 Schmitt EL, Baum VC. Nitrous oxide in pediatric anesthesia: friend or foe? Curr Opin Anaesthesiol 2008; 2: 356–9 14 Boivin JF. Risk of spontaneous abortion in women occupationally exposed to anaesthetic gases: a meta-analysis. Occup Environ Med 1997; 54: 541–8 15 Smith I. Nitrous oxide in ambulatory anaesthesia: does it have a place in day surgical anaesthesia or is it just a threat for personnel and the global environment? Curr Opin Anaesthesiol 2006; 19: 592– 6 16 Sherman SJ, Cullen BF. Nitrous oxide and the greenhouse effect. Anesthesiology 1988; 68: 816–7 17 Peyton PJ, Stuart-Andrews C, Deo K, et al. Persisting concentrating and second gas effects on oxygenation during N2O anaesthesia. Anaesthesia 2006; 61: 322– 9 18 Goldman LJ. Anesthetic uptake of sevoflurane and nitrous oxide during an inhaled induction in children. Anesth Analg 2003; 96: 400–6 19 Taheri S, Eger EI. A demonstration of the concentration and second gas effects in humans anesthetized with nitrous oxide and desflurane. Anesth Analg 1999; 89: 774– 80 20 Peyton PJ, Fortuin M, Robinson GJ, et al. The rate of alveolarcapillary uptake of sevoflurane and nitrous oxide following anaesthetic induction. Anaesthesia 2008; 63: 358–63 21 Hall JE, Stewart JIM, Harmer M. Single-breath inhalation induction of sevoflurane anaesthesia with and without nitrous oxide: a feasibility study in adults and comparison with an intravenous bolus of propofol. Anaesthesia 1997; 52: 410– 15 22 Dubois MC, Piat V, Constant I, et al. Comparison of three techniques for induction of anaesthesia with sevoflurane in children. Paediatr Anaesth 1999; 9: 19– 23 23 Kihara S, Yaguchi Y, Inomata S, et al. Influence of nitrous oxide on minimum alveolar concentration of sevoflurane for laryngeal mask insertion in children. Anesthesiology 2003; 99: 1055–8 24 O’Shea H, Moultrie S, Drummond GB. Influence of nitrous oxide on induction of anaesthesia with sevoflurane. Br J Anaesth 2001; 87: 286– 8 25 Siau C, Liu EHC. Nitrous oxide does not improve sevoflurane induction of anesthesia in adults. J Clin Anesth 2002; 14: 218– 22 26 Rusy L, Usaleva E. Paediatric anaesthesia review. Update Anaesth 1998; 8: Article 2 27 Lerman J, Schmitt-Bantel BI, Gregory GA, et al. Effect of age on the solubility of volatile anesthetics in human tissues. Anesthesiology 1986; 65: 307– 11 28 Lerman J, Gregory GA, Willis MM, et al. Age and solubility of volatile anesthetics in blood. Anesthesiology 1984; 61: 139– 43 29 Stoelting RK, Hillier SC. Pharmacology and Physiology in Anesthetic Practice, 4th Edn. Lippincott: Williams and Wilkins, 2006; 34– 5 30 Wappler F, Frings DP, Scholz J, et al. Inhalational induction of anaesthesia with 8% sevoflurane in children: conditions for endotracheal intubation and side-effects. Eur J Anaesthesiol 2003; 20: 548–54 31 Ho K, Chua WL, Lim S, et al. A comparison between single-and double-breath vital capacity inhalation induction with 8% sevoflurane in children. Paediatr Anaesth 2004; 14: 457– 61
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occupational exposure limits, there is no conclusive evidence for reproductive, genetic, haematological, or neurological occupational toxicity from nitrous oxide exposure.40 Nitrous oxide remains to be a useful inhalation analgesic and sedative that is cheap and has a long history of use in various clinical settings. Further research is needed to weigh the risk –benefit ratio of using this agent for anaesthesia in the paediatric population. In conclusion, we found that the addition of nitrous oxide resulted in less excitation and marginally faster induction times, as defined by the time to loss of eyelash reflex. Overall, we also established that the SBVC-HC sevoflurane technique was pleasant with most children choosing to have it again. Despite movement away from the use of nitrous oxide, it may still have a beneficial role in SBVC-HC sevoflurane induction in children. Further studies need to be done to evaluate if short exposure to nitrous oxide during induction alone has the same adverse effects as when used for a longer period during maintenance of anaesthesia, to the patients and healthcare personnel.
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37 Lerman J. Inhalation agents in pediatric anaesthesia—an update. Curr Opin Anaesthesiol 2007; 20: 221– 6 38 Yurino M, Kimura H. Comparison of induction time and characteristics between sevoflurane and sevoflurane/nitrous oxide. Acta Anaesthesiol Scand 1995; 39: 356–8 39 Fernandes CR, Gomes JM, Cordeiro RA, et al. Assessment of the cognitive effects of inhalational induction with sevoflurane associated or not with nitrous oxide: a comparative study in adult volunteers. Rev Bras Anestesiol 2007; 57: 237– 46 40 Sanders RD, Weimann J, Maze M. Biologic effects of nitrous oxide. A mechanistic and toxicologic review. Anesthesiology 2008; 109: 707– 22 41 Pichardo D, Luginbuehl IA, Shakur Y, et al. Effect of nitrous oxide exposure during surgery on the homocysteine concentrations of children. Anesthesiology 2012; 117: 15 –21
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Handling editor: M. M. R. F. Struys