Laparoscopic surgery is increasingly performed in children (1). CO2 is the insufflation gas of first choice and peritoneal CO2 absorption may cause hypercapnia. The effects of CO2 pneumoperitoneum on cerebral hemodynamics have been investigated in adults (2–4) and animals (5–7), but not in children. In adults, CO2 pneumoperitoneum-induced hypercapnia causes an increase in cerebral blood volume (CBV) (2) and cerebral blood flow velocity (CBFV) (3), whereas maintaining normocapnia and positioning of the patient in the head-up position during laparoscopic cholecystectomy, CO2 insufflation causes a decrease in CBV (4). Increasing the intraabdominal pressure (IAP) during CO2 pneumoperitoneum and maintaining normocapnia in animals causes an increase in intracranial pressure (ICP) (5–7). A small increase in Paco2 in preterm and term artificially ventilated infants caused an increase in CBV, and data obtained by Wyatt et al. (8) suggest that full-term infants have a much greater cerebrovascular sensitivity to Paco2 than preterm infants. We evaluated the effects of low-pressure CO2 pneumoperitoneum on regional cerebral oxygenation and CBV in children scheduled for laparoscopic fundoplication, superimposed on a baseline of moderate hypocapnia.
Materials and Methods
The protocol was approved by the Hospital Ethics Committee, and written informed parental consent was obtained in all cases. Fifteen children (ASA physical status I–III) at least 53 wk postconception scheduled for laparoscopic fundoplication for treatment of primary or secondary gastroesophageal reflux were investigated. Children with significant cardiovascular diseases, children with clinical signs of pulmonary disease without adequate treatment, and children with increased ICP or decreased intracranial compliance were excluded. In all cases, a low-pressure CO2 pneumoperitoneum (5–8 mm Hg) was applied.
No premedication was used. When the patient or the parents preferred IV induction of anesthesia or when an IV infusion was already present, the child was induced with preoxygenation, thiopentone 5 mg/kg, sufentanil 0.2 μg/kg, and atracurium 0.5 mg/kg. When unconscious, the child was manually ventilated with oxygen/air (Fio2 0.40) and isoflurane (Fi 1%). Otherwise, general anesthesia was induced by face mask, using oxygen, nitrous oxide, and halothane. After induction, an IV line was inserted and atracurium 0.5 mg/kg and sufentanil 0.2 μg/kg were given IV. The administration of nitrous oxide and halothane was discontinued and the child was manually ventilated with oxygen/air (Fio2 0.4) and isoflurane (Fi 1%). Nitrous oxide is not used during the laparoscopic guided surgery because of its potential for flammability and dilation of the bowel. After orotracheal intubation, continuous infusions of atracurium 0.5 mg · kg−1 · h−1 and sufentanil 0.5 μg · kg−1 · h−1 were started, and the operating table was positioned in the head-up position (10°). This position was maintained during the entire study period. The child was mechanically ventilated (Cicero; Dräger, Lübeck, Germany) with oxygen/air (Fio2 0.4) and isoflurane (Fi 1%). This level of isoflurane was kept constant during the study period. Tidal volume was set at 10 mL/kg, whereas respiratory rate was adjusted to achieve a mild hypocapnia (end-tidal CO2 between 25 and 33 mm Hg) before insufflation. Thereafter, these ventilatory settings remained unchanged during the operation. An IV infusion of glucose 2.5% NaCl 0.45% 10 mL · kg−1 · h−1 was started. A urinary catheter, a large-bore gastric tube, and a radial arterial line were inserted. Arterial pressure was measured with the transducer at mid-thoracic level. Before the start of operation, an extra bolus of sufentanil 0.1 μg/kg IV was given to prevent any hemodynamic response to surgical stimulation. CO2 was insufflated by using an electronic laparoflator (Type 26430020; Karl Storz, Tuttlingen, West Germany). After desufflation, the continuous infusions of atracurium and sufentanil were discontinued. The administration of isoflurane was stopped after the last measurement and the patient was weaned from ventilation and extubated when consciousness had returned.
Near-Infrared Spectroscopy (NIRS)
The regional cerebral oxygen saturation (ScO2) was assessed with NIRS (INVOS®-3100A; Somanetics Inc., Troy, MI). A patch containing a light emitter and two receivers was placed over the right side of the forehead and secured with a stretch bandage. The INVOS measurement is referred to as a regional oxygen saturation index (“rSO2 index”), as displayed on the monitor. Changes in the rSO2 index should be considered to correspond to changes in ScO2. The INVOS 3100A NIRS device is a trend instrument and mea-sures changes in ScO2 and CBV from an unknown baseline. Changes in CBV were calculated by subtracting deep and shallow density signals at 805 nm. This results in a linearly proportional unscaled number, representing the changes in total hemoglobin (Hb). CBV is expressed in arbitrary units (AU). Both ScO2 and CBV are expressed as percentages of baseline in the Results, Discussion, and Figures as rScO2 (relative ScO2) and rCBV (relative CBV), respectively.
With the patient in the head-up position, all variables were recorded before insufflation, 30, 60, and 90 min after the start of CO2 insufflation, and 10 min after desufflation. Variables measured were heart rate (HR), mean arterial blood pressure (MAP), peak inspiratory pressure (PIP), end-tidal CO2 (Petco2), partial pressure of CO2 in arterial blood (Paco2), pH, arterial oxygen saturation (SaO2), and ScO2. Arterial blood gas samples were collected at each time point. The initial target IAP was 5 mm Hg, but after the seventh patient, the surgeons decided to increase target IAP to 8 mm Hg to obtain a better view of the region of interest.
All results were expressed as mean ± sd. Analysis of variance (ANOVA) for repeated measurements was performed to test for time effects. Post hoc paired samples t-tests were performed to determine whether monitored variables obtained 30 min after the start of CO2 insufflation were significantly different from baseline, whether monitored variables obtained 10 min after desufflation were significantly different from monitored variables obtained 90 min after the start of CO2 insufflation, and whether monitored variables obtained 10 min after desufflation were significantly different from baseline. Bonferroni correction was applied by multiplying the P value with 3. Linear regression analysis was used to test whether there was a relation between Paco2 and rScO2 or rCBV. Further analyses were performed to evaluate whether the magnitude of IAP influenced the hemodynamic and cerebral changes after insufflation. The Student’s independent samples t-test was used to compare both groups of IAP (5 versus 8 mm Hg). ANOVA for repeated measurements was performed to analyze whether the changes in ScO2 and CBV during low-pressure pneumoperitoneum were statistically significant, with the level of IAP as a factor. A P value < 0.05 was considered statistically significant. The SPSS program (version 9.0; SPSS, Chicago, IL) was used for all statistical analyses.
Patient characteristics are presented in Table 1. All patients but one had a mask induction. Figure 1 shows the time course of changes in ScO2, CBV, and Petco2 in one patient. PIP increased from 17 ± 3 cm H2O at baseline to 20 ± 4 cm H2O (P < 0.001) 30 min after the start of CO2 insufflation. PIP decreased from 22 ± 4 cm H2O 90 min after the start of CO2 insufflation to 19 ± 5 cm H2O after desufflation. Insufflation of CO2 resulted in an increase in Petco2 in all patients, and there was a concomitant and evident increase in ScO2 and a less evident increase in CBV. Insufflation of CO2 increased Petco2 from 30.0 ± 2.8 to 38.3 ± 5.1 mm Hg (P < 0.001) and Paco2 from 32.0 ± 4.7 to 40.4 ± 5.9 mm Hg (P < 0.001). Desufflation resulted in decreases in Petco2 and Paco2, but end-tidal and arterial values did not return to the preinsufflation values. Arterial blood gases are summarized in Table 2. No significant changes were observed in Pao2, SaO2, and HCO3−. Figure 2 shows changes in hemodynamic variables during insufflation and after desufflation. Insufflation of CO2 increased MAP from 59 ± 7 to 72 ± 12 (21% increase) (P < 0.01) and HR from 97 ± 22 to 116 ± 24 (21% increase) (P < 0.001), but these hemodynamic variables remained increased after desufflation. Figure 3 shows the changes in NIRS variables induced by CO2 insufflation. ScO2 increased from 61 ± 9 to 70 ± 9 AU (P < 0.001) and rScO2 increased 15.7% ± 8.8% (P < 0.001). In two patients, it was not possible to calculate CBV and/or rCBV because of a hardware problem of the NIRS monitor. CBV increased from 123 ± 66 to 128 ± 66 AU (P = 0.048) and rCBV increased 4.6% ± 8.8% (P = 0.297). These values decreased again after desufflation. All parameters mentioned above remained increased during insufflation of CO2. Linear regression analysis of the results before and 30 min after the start of CO2 insufflation showed a strong correlation between the increase in Paco2 and the increase in rCBV (r = 0.748, P = 0.003). There was a correlation between the increase in rCBV and the increase in rScO2 (r = 0.631, P = 0.021). There was no significant correlation between the increase in Paco2 and the increase in rScO2 (r = 0.354, P = 0.195).
There were no significant baseline differences between Group I (IAP = 5 mm Hg) and Group II (IAP = 8 mm Hg) for age, weight, height, body surface area, sex, HR, MAP, PIP, Petco2, Paco2, ScO2, rScO2, CBV, rCBV, and pH before insufflation. ANOVA for repeated measurements showed no significant differences between groups during CO2 insufflation.
This is the first study that attempted to quantify the effects of CO2 insufflation on cerebral oxygenation and CBV in children. During CO2 insufflation, significant increases in Petco2 and Paco2 were observed and this resulted in significant increases in HR, MAP, ScO2, and CBV. After desufflation, Petco2 and Paco2 decreased, but were still higher than preinsufflation values. Hemodynamic variables remained increased. ScO2 and CBV decreased and rCBV decreased to a value less than the preinsufflation state.
Insufflation of CO2 during laparoscopy causes both mechanical and pharmacologic effects on the cardiorespiratory system. Hypercapnia, resulting from CO2 absorption into peritoneal blood vessels, causes an increase in HR and MAP via increased catecholamine release. After desufflation, MAP and HR remained increased which might have been caused by a delay in the decrease in CO2 level because of a release of CO2 out of CO2 buffers and a delay in CO2-mediated hormonal effects (catecholamine release).
Cerebral changes were assessed using NIRS, which is a noninvasive optical method for the bedside monitoring of cerebral oxygenation (9). This tool quantifies the oxyhemoglobin fraction within superficial layers of the cerebral cortex. The displayed value represents the algebraic sum of intravascular arterial, capillary, and venous Hb. Intersubject variability in NIRS monitoring of ScO2 originates in part from emitter-detector spacings, biologic variations in transcranial optical path length and cerebral Hb concentration, SaO2, and cerebral blood flow (9). In our study, we were mainly interested in relative changes in ScO2 and CBV, rather than in estimation of absolute values. In 1996, Daubeney et al. (10) found that there was a good correlation between regional cerebral oxygenation and jugular bulb venous saturation in children aged between 2 weeks and 14.5 years undergoing pediatric cardiac operations. They concluded that the NIRS device cannot reliably measure absolute values, but can track trends accurately. ScO2 gives online information about local cerebral perfusion, mainly in the territory of the anterior cerebral artery, if the sensor is applied on the forehead of the patient. During laparoscopic surgery in children, gross abnormalities of the cerebral circulation as a result of cerebral infarction or vasospasm and changes in Hb concentration or hematocrit are not expected.
Kitajima et al. noted in two studies (2,4) in adult patients scheduled for laparoscopic cholecystectomy that the oxidized cytochrome aa3 in their studies remained constant during CO2 insufflation. That suggests that cerebral oxygen metabolism remains constant during CO2 insufflation. Hypercapnia causes moderate vasodilation of arterioles in most tissues and a marked vasodilation in the brain (11). To prevent cerebral vasodilation, we hyperventilated our patients to obtain mild hypocapnia before insufflation. Baseline ScO2 and CBV were obtained at hypocapnia, which means that both were decreased compared with normocapnia. Significant increases in ScO2 and CBV were observed during CO2 insufflation. An increase in Paco2 from hypocapnia to normocapnia as a result of CO2 insufflation changes the vasomotor tone of cerebral blood vessels. The increase in ScO2 is likely caused by an increase in oxygen delivery, resulting from a CO2-induced increase in CBF, rather than a decrease in cerebral oxygen metabolism during CO2 insufflation. ScO2 and CBV may have simply returned to normal after CO2 insufflation. After desufflation, Paco2, ScO2, and CBV decreased. The cerebral responses during CO2 insufflation have been studied previously in adults (2,4). An increase in Petco2 induced by CO2 insufflation during laparoscopic cholecystectomy (operating table in the supine position) resulted in a change from normocapnia to hypercapnia with a concomitant increase in CBV (2) and CBFV (3), whereas a decrease in CBV was noted during laparoscopic cholecystectomy with constant Petco2 and moving the patient in the head-up position. A hydrostatic displacement of venous blood to the lower part of the body seems to be the explanation for the decrease in CBV (4). CBV is affected by the head-up position (4), CBF (12), ICP (13,14), Paco2(2), pneumoperitoneum (2), nitrous oxide (15), anesthetics (15), and blood pressure. Isoflurane has dose-dependent cerebral vasodilatory effects and causes dose-dependent increases in CBF (14–17). However, in concentrations <1 MAC, these effects of isoflurane are modest and isoflurane is frequently used during neurosurgical procedures. To prevent changes in isoflurane concentrations that might be reflected in rScO2 and rCBV, we strictly maintained isoflurane at 1% inspired during the entire study period. In our study, children were placed in the head-up position and hyperventilated to mild hypocapnia before CO2 insufflation to counteract the consequences of CO2 absorption on the cerebral circulation. During subsequent insufflation of CO2, Paco2 and Petco2 increased to normocapnic levels and a significant increase in CBV was observed. The sensitivity of the cerebrovascular system may vary with age. Wyatt et al. (8) noted that a small increase in Paco2 in preterm and term infants, ventilated in a neonatal intensive care, caused an increase in CBV. They suggested that full-term infants have a much greater cerebrovascular sensitivity to Paco2 than preterm infants. Because we did not measure CBFV with transcranial Doppler, we cannot comment on the different cerebrovascular reactivity at the various age groups. To establish whether CO2 insufflation might result in undesired increases in ICP in very young children, CBF or transcranial Doppler studies are needed.
Comparing the results of previous studies and the present study, it is possible to arrive at recommendations for preventing inadvertent increases in CBV during laparoscopic surgery. Moving the child in the head-up position and hyperventilation before CO2 insufflation may not be sufficient to prevent any increase in CBV. Because all children in our study had normal intracranial compliance, it is unlikely that the magnitude of the increases in CBV and ScO2 were such that an increase in ICP occurred. However, it is conceivable that in children with intracranial mass lesions, in which compensatory mechanisms are exhausted, insufflation of CO2, even at low IAPs, might cause a further increase in ICP. In these patients, more aggressive hyperventilation under arterial blood gas monitoring during prolonged laparoscopic procedures may protect them from significant increases in CBV.
In conclusion, we have demonstrated that insufflation of CO2 at low IAPs (IAP ≤8 mm Hg) in children causes considerable increases in Petco2 and Paco2, that are reflected in increases in ScO2 and CBV, even when superimposed on a baseline of mild hypocapnia. These changes are likely caused by a CO2-mediated increase in CBF. To counteract these CO2-induced cerebral effects, it may be advisable to hyperventilate more aggressively during CO2 insufflation.
The authors are grateful for the cooperation and support of Dr. Nicolaas M. A. Bax, MD, PhD, professor of pediatric surgery, and Dr. David C. van der Zee, MD, PhD, pediatric surgeon.
1. Lugo-Vicente HL. Impact of minimally invasive surgery in children. Bol Asoc Med P R 1997; 89: 25–30.
2. Kitajima T, Shinohara M, Ogata H. Cerebral oxygen metabolism measured by near-infrared laser spectroscopy during laparoscopic cholecystectomy with CO2
-insufflation. Surg Laparosc Endosc 1996; 6: 210–2.
3. Fujii Y, Tanaka H, Tsuruoka S, et al. Middle cerebral arterial blood flow velocity increases during laparoscopic cholecystectomy. Anesth Analg 1994; 78: 80–3.
4. Kitajima T, Okuda Y, Yamaguchi S, et al. Response of cerebral oxygen metabolism in the head-up position during laparoscopic cholecystectomy. Surg Laparosc Endosc 1998; 6: 449–52.
5. Josephs LG, Este-McDonald JR, Birkett DH, Hirsch EF. Diagnostic laparoscopy increases intracranial pressure. J Trauma 1994; 36: 815–9.
6. Este-McDonald JR, Josephs LG, Birkett DH, Hirsch EF. Changes in intracranial pressure associated with apneumic retractors. Arch Surg 1995; 130: 362–6.
7. Halverson A, Buchanan R, Jacobs L, et al. Evaluation of mechanism of increased intracranial pressure with insufflation. Surg Endosc 1998; 12: 266–9.
8. Wyatt JS, Edwards AD, Cope M, et al. Response of cerebral blood volume to changes in arterial carbon dioxide tension in pre-term and term infants. Pediatr Res 1991; 29: 553–7.
9. Kurth CD, Uher B. Cerebral hemoglobin and optical pathlength influence near-infrared spectroscopy measurement of cerebral oxygen saturation. Anesth Analg 1997; 84: 1297–305.
10. Daubeney PEF, Pilkington SN, Janke E, et al. Cerebral oxygenation measured by near-infrared spectroscopy: comparison with jugular bulb oximetry. Ann Thorac Surg 1996; 61: 930–4.
11. Guyton AC, Hall JE, eds. Textbook of medical physiology. Philadelphia: WB Saunders, 1996:207.
12. Grubb RL, Raichle ME, Eichling JO, Ter-Pogossian MM. The effects of changes in Pa co2
on cerebral blood volume, blood flow and vascular transit time. Stroke 1974; 5: 630–9.
13. Rosner MJ, Coley IB. Cerebral perfusion pressure, intracranial pressure and head elevation. J Neurosurg 1986; 65: 636–41.
14. Smelt WLH, de Lange JJ, Booij LHDJ. Cardiorespiratory effects of the sitting position in neurosurgery. Acta Anaesthesiol Belg 1988; 39: 223–31.
15. Hansen TD, Warner DS, Todd MM, Vust LJ. Effects of nitrous oxide and volatile anaesthetics on cerebral blood flow. Br J Anaesth 1989; 63: 290–5.
16. Matta BF, Mayberg TS, Lam AM. Direct cerebrovasodilatory effects of halothane, isoflurane, and desflurane during propofol-induced isoelectric encephalogram in humans. Anesthesiology 1995; 83: 980–5.
© 2002 International Anesthesia Research Society
17. Matta BF, Heath KJ, Tipping K, Summors A. Direct cerebral vasodilatory effects of sevoflurane and isoflurane. Anesthesiology 1999; 91: 677–80.