British Journal of Anaesthesia

BJA Advance Access originally published online on May 23, 2006
British Journal of Anaesthesia 2006 97(2):215-219; doi:10.1093/bja/ael134

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© The Board of Management and Trustees of the British Journal of Anaesthesia 2006. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

Absorption of carbon dioxide during laparoscopy in children measured using a novel mass spectrometric technique

M. Pacilli¹, A. Pierro¹, C. Kingsley¹, J. I. Curry¹, J. Herod² and S. Eaton^1,*

¹ Department of Surgery, Institute of Child Health, Great Ormond Street Hospital for Children London, UK
² Department of Anaesthetics, Institute of Child Health, Great Ormond Street Hospital for Children London, UK

^*Corresponding author: Department of Paediatric Surgery, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK. E-mail: s.eaton{at}ich.ucl.ac.uk

Accepted for publication April 23, 2006.

	Abstract

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Background. Carbon dioxide (CO₂) is absorbed during pneumoperitoneum and may cause adverse haemodynamic effects. The aim of this study was to measure the elimination of exogenous CO₂ during laparoscopy in children.

Methods. Ten children [27.6 (56.5) months; mean (SD)] undergoing laparoscopic and nine [24.5 (17.3) months] undergoing open surgery were studied. Breath samples were collected at the line for end-tidal CO₂ and analysed for ¹³CO₂/¹²CO₂ ratio expressed as PDB (difference from standard), by isotope-ratio mass spectrometry. The proportion of absorbed CO₂ was calculated comparing exhaled ¹³CO₂/¹²CO₂ before and during CO₂ pneumoperitoneum.

Results. ¹³CO₂/¹²CO₂ in medical CO₂ was –32.7 (2.1) PDB. ¹³CO₂/¹²CO₂ in breath of patients undergoing open procedures was –24.3 (2.4) PDB at the start of operation and did not change during the operation (P > 0.2). ¹³CO₂/¹²CO₂ in breath of patients undergoing laparoscopy was –21.5 (5.4) PDB at the start of insufflation, and decreased during pneumoperitoneum by 2.5 (1.6) PDB, indicating absorption of exogenous CO₂. The percentage of expired CO₂ absorbed rose to 15.5 (7.7)% after 30 min of pneumoperitoneum and decreased rapidly after desufflation.

Conclusion. After 10 min of laparoscopy 10–20% of expired CO₂ derives from the exogenous CO₂. CO₂ absorption can be measured using a simple mass spectrometric technique.

Keywords: carbon dioxide, absorption; pneumoperitoneum; procedure, mass spectrometry; surgery, laparoscopy

	Introduction

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Carbon dioxide (CO₂) is commonly used for pneumoperitoneum in adults and children, as it is non-combustible, inexpensive and least likely to cause embolism. Laparoscopy can result in haemodynamic changes¹ and may lead to adverse effects on the cardiovascular system requiring increasing minute ventilation by 20–30% to prevent hypercarbia.^{2 3} Previously, we have demonstrated that small children eliminate relatively more CO₂ (measured as VCO₂ by indirect calorimetry) during laparoscopy⁴ and thus require scrupulous anaesthetic management, particularly in the presence of pre-existing pathological conditions.^{5 6} End-tidal CO₂ () is commonly monitored during laparoscopy in children and minute ventilation is accordingly adjusted in order to avoid hypercapnia. However, some authors suggested that the is not a reliable measure of arterial CO₂ pressure.^{7 8} Furthermore, measures total CO₂ elimination and does not allow quantification of the absorption of CO₂ from the peritoneum. Infants and children undergoing laparoscopy are hypermetabolic⁹ and the increased elimination of CO₂ during laparoscopy may be metabolic in origin and not arise from the absorption of CO₂ from the pneumoperitoneum; thus changes in VCO₂ measured by indirect calorimetry are not a reliable measure of absorbed CO₂. Development of a method to specifically measure the amount of CO₂ absorbed from the peritoneum during laparoscopy would allow comparison of the amount of CO₂ absorbed from the peritoneum between different surgical or anaesthetic management protocols.

The aim of this study was to determine absorption of exogenous CO₂ in expired breath during laparoscopy in children independently of metabolic CO₂ using a novel isotope-ratio mass spectrometry method. There are two naturally occurring stable isotopes of carbon, ¹²C and ¹³C. Of these, ¹²C makes up about 99%. An ideal way to study CO₂ absorption from pneumoperitoneum would be to insufflate with ¹³CO₂ and measure appearance of ¹³CO₂ in breath; however, this would be prohibitively expensive at the flow rates of 1–2 litre min^–1 during pneumoperitoneum. There are very small differences in ¹³C/¹²C ratio in different naturally occurring carbon sources, and this is reflected in a range of % ¹³C from 1.0563 to 1.1222. These differences are usually represented as ¹³C relative to PDB (Pee Dee Belemnite), the international standard for ¹³C/¹²C. Interestingly, exhaled breath has a rather different ¹³C/¹²C ratio from medical CO₂, reflected by their different ¹³C values: breath has of between –11 and –24 compared with PDB, whereas medical CO₂ has a PDB value of –32 to –34. Hence the absorbed, exhaled medical CO₂ causes the overall ¹³C/¹²C ratio in CO₂ breath to alter, enabling absorption of CO₂ to be measured using a mass spectrometric technique.

	Methods

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Ten children undergoing laparoscopic surgery and nine children undergoing open surgery were enrolled in this prospective non-randomized study. The study was approved by the Research Ethics Committee at the Institute of Child Health and Great Ormond Street Hospital for Children and written consent was obtained for each patient.

Anaesthesia
All patients were anaesthetized in a standard manner with either 8% sevoflurane in oxygen or 2–5 mg kg^–1 propofol. After induction, atracurium (0.5 mg kg^–1) was administered and the trachea intubated with an oral tracheal tube of age appropriate size with minimal leak present. was measured on a continuous basis using a positive sampling system (Hewlett Packard, Boeblingen, Germany). All patients were ventilated throughout the procedure with a mixture of air, oxygen and isoflurane to an level of between 4.5 and 6.0 kPa depending upon the pre-existing pulmonary function.

Paralysis was maintained with boluses of atracurium and intraoperative analgesia achieved with fentanyl up to 5 µg kg^–1 in increments plus acetaminophen 30 mg kg^–1 per rectum and diclofenac 1 mg kg^–1 for those patients over 10 kg. At the end of surgery up to 2 mg kg^–1 bupivacaine were infiltrated at the trocars' insertion sites and the patients were extubated and breathing spontaneously before going to the recovery room.

Laparoscopy
A Hasson cannula was inserted under direct vision just above the umbilicus and unheated (room temperature) CO₂ was used to establish a pneumoperitoneum with a pressure of 10–15 mm Hg, according to the surgeon's preference, and a maximum flow rate of 4 litre min^–1. Laparoscopic procedures were performed using standard techniques. Five patients had an open procedure after the end of the laparoscopic procedure.

Sample collection and analysis
Breath samples were collected at 5 min intervals using a 10 ml syringe connected to a 3-way valve at the sampling line for measurement of . The air was aspirated into a 10 ml syringe and transferred into 10 ml vacuum test tubes (Labco Limited, High Wycombe, UK) for the analysis. Samples were collected after the patient was intubated and before the start of the operation, during the operation, during pneumoperitoneum, after pneumoperitoneum in patients having open procedure after laparoscopy, and after the end of the operation until the patient was extubated. In addition, samples of air used for ventilation and of medical CO₂ used for the pneumoperitoneum were obtained for each operation. and body core temperature were recorded at each sampling point.

Sample analysis
Breath CO₂ was analysed for ¹³CO₂/¹²CO₂ enrichment by gas chromatography on a CP-Poraplot-Q column (Varian Inc., Oxford, UK) followed by isotope-ratio mass spectrometry on a Thermo Finnigan Delta-XP (Thermo Finnigan, Bremen, Germany). Sample ¹³CO₂/¹²CO₂ enrichment was standardized against a CO₂ cylinder (5.0 grade, BOC Special Gases, Guildford, Surrey, UK), which had been calibrated against the international standard PDB (Iso-Analytical, Sandbach, Cheshire, UK). Using the ¹³CO₂/¹²CO₂ of the medical CO₂ used for insufflation to represent 100% of exhaled CO₂ originating from pneumoperitoneum and baseline breath ¹³CO₂/¹²CO₂ to represent 0%, the percentage of exhaled CO₂ originating from the pneumoperitoneum at time x was calculated as:

Statistical analysis
Data are given as mean (SD) or median (range) and were compared by paired and unpaired t-tests, and by linear regression analysis, using Prism 4 software (GraphPad Software Inc., San Diego, USA). Results with a P-value of <0.05 were considered significant, and results were corrected for multiple comparisons by Bonferroni's correction where appropriate.

	Results

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Age at operation was comparable between the two groups, median 8 months (range, 1 month–15 yr) for the laparoscopic group and 24 months (3 months–4.5 yr) for the open group (P=0.7). Weight at operation was 11.1 (8.6) kg and 11.8 (4.0) kg in the laparoscopic and open groups, respectively (P=0.7). The surgical procedures performed in each group are listed in Table 1. Core temperature did not show any significant variation and remained within a normal range during the surgical procedure in all patients.

View this table: [in this window] [in a new window]   Table 1 Surgical procedures performed in each group. PEG, percutaneous endoscopic gastrostomy; PSARP, posterior sagittal anorectoplasty

 
¹³CO₂/¹²CO₂ in medical CO₂ was –32.7 (2.1) PDB. ¹³CO₂/¹²CO₂ in exhaled breath of patients undergoing open procedures was –24.3 (2.4) PDB at the start of operation and did not change significantly during the operation (P>0.2) (Fig. 1A). ¹³CO₂/¹²CO₂ in exhaled breath of patients undergoing laparoscopy was –21.5 (5.4) PDB at the start of insufflation, similar to baseline ¹³CO₂/¹²CO₂ of patients undergoing open surgery (P=NS). ¹³CO₂/¹²CO₂ progressively decreased during pneumoperitoneum, reducing by 2.5 (1.6) to –24.1 (4.1) PDB (P=0.0015 vs baseline by paired t-test with Bonferroni correction) at the end of pneumoperitoneum in each patient [35.0 (19.9) min, range 10–75 min], indicating absorption of exogenous CO₂ (Fig. 1B). The percentage of expired CO₂ absorbed rose to 16.4 (8.6)% after 30 min of pneumoperitoneum (P=0.012), and then decreased rapidly after discontinuing the CO₂ insufflation (desufflation) (Fig. 2). As five patients received open procedure after laparoscopy, we were able to obtain additional CO₂ samples before extubation, thus establishing that ¹³CO₂/¹²CO₂ returns to baseline 30 min after the end of pneumoperitoneum (Figs 1B and 2). After the end of pneumoperitoneum, ¹³CO₂/¹²CO₂ returned towards baseline, but required approximately 30 min to return to baseline values (Fig. 1B).

View larger version (9K): [in this window] [in a new window]   Fig 1 13CO2/12CO2 vs PDB in exhaled breath of patients undergoing open procedures (A) and in patients undergoing laparoscopy (B). Results are shown as changes from the baseline in each patient and are expressed as mean (SD). *Significantly different from baseline.

 

View larger version (11K): [in this window] [in a new window]   Fig 2 Percentage of exhaled CO2 originating from the peritoneum during laparoscopic procedure. Results are expressed as mean (SD). *Significantly different from baseline.

 
No patients in either group experienced cardiovascular or respiratory compromise during or after surgery and all had an uncomplicated postoperative recovery.

	Discussion

Top Abstract Introduction Methods Results Discussion References

 
Laparoscopy introduces new variables into anaesthetic management: effects of elevated intraabdominal pressure, effects of intraperitoneal gas insufflation and alterations caused by differences in patient positioning. As CO₂ is highly soluble, it is easily absorbed through the peritoneum. Experimental models in animals have documented CO₂ absorption during pneumoperitoneum, causing acidaemia, hypercarbia and depressed haemodynamic function.¹⁰–¹² Absorption of CO₂ through the peritoneal surface is also documented in adults, resulting in an increase in .¹³–¹⁷ Although this can lead to a decrease in blood pH,¹⁸ in otherwise healthy patients undergoing laparoscopic surgery, this CO₂ load does not produce a clinically significant respiratory or metabolic challenge^{19 20} and is usually adequately dealt with by an increase in minute ventilation. Several studies in adults have examined the time course of CO₂ elimination by indirect calorimetry, and although some authors have suggested that the rate of CO₂ elimination reaches a plateau within 15–40 min of pneumperitoneum,^{3 14 16 17 21} others have documented increases up to 2 h.²² These discrepancies could be related to differences in insufflation pressure, alterations in absorption of CO₂ from injured and non-injured peritoneum,^{15 23} or to hypercapnia and CO₂ retention in the body. However, in studies using indirect calorimetry³ or respiratory mass spectrometry^{15 16} to measure total CO₂ elimination as the difference between inspired and expired CO₂ (VCO₂), it is difficult to distinguish between metabolically produced CO₂ and CO₂ absorbed through the peritoneum. As substrate utilization and metabolic CO₂ production may well change during surgery,²⁴ the time to achieve plateau VCO₂ may vary in different studies depending on metabolic changes, and the estimation of absorbed CO₂ is not accurate as it depends on the assumption that metabolic CO₂ production is unchanged during the laparoscopic procedure.

Few studies have investigated the pathophysiological effects of laparoscopy in children and results have been extrapolated from studies conducted in adults. Similarly to adults, CO₂ absorption does not appear to be a problem in patients with normal cardiovascular function and healthy children undergoing short laparoscopic procedures have minimal adverse effects.^{25 26} However, an increase in minute ventilation is usually required to prevent hypercarbia.^{2 3} In previous studies, we have shown, using indirect calorimetry, that children increase VCO₂ during laparoscopy and that younger children eliminate relatively more CO₂ compared with older children.⁴ However, we have also shown that children undergoing laparoscopic procedures are hypermetabolic and would therefore be expected to have an increase in metabolic CO₂ production, and an increase in CO₂ absorption from the peritoneum.⁹ In order to accurately determine the timecourse of CO₂ absorption in children undergoing laparoscopic procedures, we aimed to develop an unambiguous method to quantify the absorption of exogenous CO₂, and to use this method to accurately determine the time course of CO₂ absorption during laparoscopy in children.

The high precision of isotope-ratio mass spectrometry enabled us to utilize the small differences in natural carbon abundance in different sources (i.e. CO₂ metabolically produced from the patient and CO₂ used for pneumoperitoneum). Using this technique, we have estimated that 10–20% of CO₂ eliminated during laparoscopy in children is derived from absorption through the peritoneum. The variability observed in our study may be related to different insufflation pressures.²⁷ Minute ventilation was adjusted by the anaesthetist throughout the pneumoperitoneum to maintain between 4 and 6 kPa and none of the patients in the laparoscopic group required desufflation of the pneumoperitoneum and conversion to an open procedure. CO₂ absorption reached a plateau after 20–25 min of pneumoperitoneum, a finding comparable with several of the adult studies based on VCO₂ measurement.^{3 14 16 17} At plateau, 10–20% of exhaled CO₂ originated from the pneumoperitoneum, comparable with the 18% estimated by Kazama and colleagues¹⁶ in adults, but somewhat lower than the 30% estimated by Mullet and colleagues.¹⁷ Differences between all these studies may be related to different intraabdominal pressures.²⁷ This amount of CO₂ could potentially cause significant acidosis if not corrected by increased minute ventilation, suggesting that although arterial blood gas analysis is not routinely performed because of its invasive nature, it may be a useful precaution in children with suspected significant arterial CO₂– gradients^{7 8} or with pulmonary or cardiovascular compromise. In addition, as absorbed CO₂ reached a plateau after about 20 min, any changes in subsequent to this are likely to be attributable to other reasons such as metabolic or haemodynamic alterations, or s.c. CO₂ emphysema. As several patients in our series required additional open procedures after the end of pneumoperitoneum, we were able to determine that absorbed CO₂ continued to be eliminated for 30 min after desufflation, very similar to the results of Katama and colleagues¹⁶ in adults. Although none of our patients experienced respiratory problems after extubation, the persistent elimination of the absorbed CO₂ after desufflation should be taken into account to prevent possible complication in children with pulmonary disease during recovery from anaesthesia.

In conclusion, CO₂ absorption from pneumoperitoneum can be measured using a new, simple method which does not require administration of labelled compounds. Using this method, we have demonstrated that in children after 10–20 min of laparoscopy, 10–20% of expired CO₂ is derived from the absorption of exogenous CO₂, and that exogenous CO₂ continues to be eliminated for up to 30 min after desufflation. Further studies using this technique may clarify the exact pathophysiological changes occurring during laparoscopy in children and adults.

	Acknowledgments

 
The authors are grateful to Fondazione Eugenio Litta for a grant to M.P. in support of this work, CHRAT for a summer studentship to C.K., and the Philip Ullman Trust for the isotope-ratio mass spectrometer.

	References

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This Article Abstract Full Text (PDF) All Versions of this Article: 97/2/215    most recent ael134v1 E-Letters: Submit a response to the article Alert me when this article is cited Alert me when E-letters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Archive Download to citation manager Search for citing articles in: ISI Web of Science (1) Request Permissions Disclaimer Google Scholar Articles by Pacilli, M. Articles by Eaton, S. Search for Related Content PubMed PubMed Citation Articles by Pacilli, M. Articles by Eaton, S. Social Bookmarking          What's this?

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