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Anesth Analg 2006;102:1333-1340 © 2006 International Anesthesia Research Society doi: 10.1213/01.ane.0000202464.06660.66
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Abstract |
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In this study we evaluated, in 10 sevoflurane-anesthetized pigs undergoing abdominal surgery, different techniques for measuring autonomic nervous system (ANS) activity: ANSiscopeTM index, spectral analysis of heart-rate variability, hemodynamic variables, and plasma catecholamines and cortisol levels. Animals underwent a 120-min anesthesia during which unilateral ovariectomy was performed. Cardiovascular and respiratory responses were monitored. ANSiscopeTM indices (ANSindexTM sympathetic, ANSindexTM parasympathetic and balANSindexTM) were used to monitor ANS activity. Spectral analysis was performed using an autoregressive model with a parametric method. The low frequency (LF) and high frequency (HF) components were used to interpret the power spectral density of short-term electrocardiograms (ECGs). The relationship LF/(LF+HF) reflects sympathetic activity, HF/(LF+HF) indicates parasympathetic activity, and the LF/HF ratio gives the predominance of the system. Plasma concentrations of adrenaline, noradrenaline, and cortisol were determined at different times. Correlation (P < 0.01) was found between the balANSindexTM and adrenaline levels and between LF/HF ratio and plasma adrenaline concentrations. Moreover, a significant (P < 0.01) correlation was found between the balANSindexTM and LF/HF ratio. However, no correlation was seen between the registered ANSiscope indices and hemodynamic variables. The correlation seen in this study suggests that the balANSindexTM could be a useful tool to monitor ANS activity during anesthesia and surgery.
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Introduction |
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A variety of techniques have been used to assess sympathetic nervous system (SNS) activity, but in many cases the assessment is indirect and often obtained in the absence of related functional information. Probably the most widely used indicator of SNS activity is the measurement of plasma catecholamine concentrations (1).
Attenuation of sympathetic nerve activity during anesthesia is usually assessed by monitoring cardiovascular reactions. The beat-to-beat fluctuation in heart rate (HR) is closely linked to the activity of autonomic nerves. In the past 2 decades, spectral analysis of HR variability (HRV) has enabled continuous noninvasive quantification of cardiac autonomic function (2,3). Previous analysis indicates that HRV may be a useful tool for evaluating autonomic functions (4) or stress responses (5).
A new system for representing and measuring the autonomic nervous system (ANS), the ANSiscopeTM (Dyansys, Inc., Burlingame, California), has been devised. It is based on a discriminating analysis of fractal characteristics found in the time-series between R wave intervals of the electrocardiogram (ECG). The system discriminates the component resulting from the activity of the sympathetic subsystem from the component resulting from the parasympathetic subsystem.
The ANSiscopeTM computes a trajectorial representation of the sympathovagal balance named the balANSindexTM. From this representation, the center of gravity can be computed (balANSindexTM corresponding to the distance from the origin), and it allows measurement of sympathetic or parasympathetic predominance. This balANSindexTM has values comprised between –50 and 50, negative values indicating a predominance of parasympathetic activity and positive values a predominance of sympathetic activity. A healthy volunteer at rest will have a balANSindexTM around –15, showing a predominance of parasympathetic activity.
The ANSiscopeTM has shown promise in diabetes-related disorders (6).
ANS monitoring using the ANSiscopeTM may allow the anesthesiologist to better determine correct drug dosage. The ANSiscopeTM shows the state of the sympathovagal balance and thus may be used in the operating room to monitor the effectiveness of anesthesia in real time.
The aim of this pilot study was to compare different available methods to monitor ANS activity in sevoflurane-anesthetized animals undergoing abdominal surgery. We investigated the relationship between plasma catecholamines and cortisol levels, which are related to sympathetic activation, ANSiscopeTM indices and spectral analysis of HRV, as a reflection of ANS activity, and hemodynamic variables of the subject's physiological responses to surgery.
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Methods |
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The experimental protocol was approved by the Institutional Ethical Committee for Animal Research. Ten healthy female Large White pigs were used. Their mean weight was 21.0 ± 1.4 kg.
One day before the experimental anesthetic episode, each pig was anesthetized with sevoflurane and a 20-gauge catheter was placed in the external iliac artery through a femoral approach (7) and fixed to the skin. Similarly, on that same day a vascular sheath was placed in the jugular vein using the Seldinger technique.
The ANSiscopeTM monitoring system has a single 3-lead ECG. Electrodes for the ECG module were placed on each pig in accordance with a standard (i.e., lead-III) configuration. The ECG signal is digitized with a sampling rate of 200 Hz. The QRS complex detection is performed leading to the RR-intervals signal. From this RR-intervals chaotic time-series, a phase-space is reconstructed in which changes in the state of the ANS become explicit as a velocity from negative to positive values, from parasympathetic predominance (manifested by slow HR) to sympathetic predominance (manifested by rapid HR). This reconstruction takes advantage of changes on multiple time scales. The obtained phase space describes the force of change applied (constant times of the acceleration) as a function of this velocity. Points reached in this two-dimensional space together form the sympathovagal balANSTM, it expresses the global ANS outcome. To acquire independent measurements of sympathetic and parasympathetic activities, the following equation is solved with every point obtained at the time of the latest heart beat:
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where SP and PSP are respectively the sympathetic and parasympathetic local degrees of activity, S and D are respectively the sum and difference of values for the last two heart beats, and C and D are constants to be defined. This equation expresses a summation law, i.e., how the two activities of the ANS subsystems add up to one global predominance for the ANS, with the overall antagonism of these subsystems respected. This approach of extraction of autonomic information from the interval tachogram represents scale-covariance, is non-model driven, and belongs essentially to the time-domain. The SP and PSP degrees of activity are termed ANSindicesTM, and the balANS indexTM corresponds here to the distance from the points' center of gravity to the origin.
The ANSindexTM sympathetic, ANSindexTM parasympathetic and balANSindexTM computed at each R wave were recorded continuously beginning during the conscious state and continuing through induction, maintenance, and recovery from anesthesia.
Spectral analysis of HRV using an autoregressive model with a parametric method was performed as described by Malik et al. (8).
For each event time, we have taken 300 RR intervals just after the event. In a spectrum calculated from that short term recording of 300 RR intervals, 3 main spectral components are distinguished: very low frequency (LF), LF, and high frequency (HF) components. The very LF component should be avoided when interpreting the power spectral density of short-term ECGs. Vagal activity is the major contributor to the HF component (9). Previous studies suggest that LF is a quantitative marker of sympathetic activity (9). The LF/HF ratio is considered by some investigators to mirror the sympathovagal balance or to reflect sympathetic modulators (9).
Animals were premedicated with IM diazepam (Valium; Roche Pharma, Madrid, Spain) (0.1 mg/kg) and ketamine (Ketolar; Pfizer, Madrid, Spain) (10 mg/kg). Anesthesia was induced with sevoflurane (5%) in oxygen (5 L of oxygen/min). When lack of jaw tone, loss of swallowing, lack of head shaking, loss of palpebral and pain reflexes, and ventromedial rotation of the eyes were all detected, an endotracheal tube was inserted. The tube was then connected to a semiclosed circular anesthetic circuit attached to a ventilator (Ventilator 7800; Ohmeda, Madrid, Spain). Sevoflurane (Sevorane; Abbott Laboratories, Madrid, Spain) administration started at 5%, which enabled us to rapidly achieve 1.25 MAC (1 MAC = 2.66%) (10) with an oxygen flow rate of 3 L/min. Once 1.25 MAC was reached (3.3% end-tidal sevoflurane), the vaporizer setting was adjusted as needed to maintain this concentration. Muscle relaxation was obtained by injection of vecuronium (0.1 mg/kg) (Norcuron, Organon Española, Barcelona Spain) every 30 min.
Intermittent positive pressure ventilation was used during the procedure to maintain the end-tidal CO2 concentration between 35 and 40 mm Hg.
The pigs were placed in dorsal recumbence, and unilateral ovariectomy was performed through a midline approach with a 10-cm long infraumbilical incision. This procedure was always performed by the same surgeon using the same technique to achieve reproducible stimulation.
During surgery, continuous infusion of physiologic saline solution at a rate of 10 mL · kg–1 · h–1 was administered. At the end of surgery, the vaporizer was switched off and fresh gas flow rate was increased to 10 L/min of 100% oxygen. Tracheal extubation was done when pigs regained swallowing reflexes and were considered recovered and fully conscious by the ability to stand and walk.
Bispectral index (BIS) (A-1050TM, version 3.05.05; Aspect Medical Systems, Newton, MA) was registered using gel-coated disposable silver-silver-chloride electrodes (Zipprep; Aspect Medical Systems) located according to a previously described montage (11). ECG was performed (model 86S; Hewlett-Packard, Geneva, Switzerland) (lead II) with the electrodes placed in the interdigital spaces of all 4 limbs and pulse-oximetry with a probe (Clip Tip sensor, Oximeter Sensor; Datex-Ohmeda, Louisville, CO) placed on the tongue. Other variables registered were rectal temperature, tidal volume, end-tidal concentration of sevoflurane, end-tidal CO2 concentration, and respiratory rate (Ohmeda RGM 5250; Ohmeda, Madrid, Spain). Muscle relaxation was observed and monitored by train-of-four (TOF-Guard, Biometer International A/S, Odense, Denmark).
Arterial blood pressure, central venous pressure, and HR were also measured using a blood pressure module (Press M 1006B; Hewlett-Packard) connected to a system for monitoring hemodynamic variables.
Arterial blood pressure was obtained by connecting the catheter previously inserted in an external iliac artery to the monitoring system via a transducer (Ohmeda transducer DT-XX; Ohmeda).
Under sterile conditions a 7F Swan-Ganz catheter (CritiCathTM SP5107, Becton Dickinson Infusion Therapy Systems Inc., Singapore) was placed through a femoral vein approach. The placement of the tip of the Swan-Ganz catheter was confirmed through monitoring of pressure waveforms. Pulmonary artery occlusion pressure (wedged pressure), cardiac output calculated by thermodilution, and central venous pressure were measured.
Through the jugular sheath, venous blood was sampled at different times. At each interval, 5 mL of blood was collected using a cold syringe. Venous blood samples were collected in tubes containing EDTA.
Tubes of blood were centrifuged immediately at 4°C, and plasma was harvested, frozen, and stored at –20°C until hormone assays.
The plasma cortisol concentration was measured using radio-immunoassay. For plasma cortisol, intra-assay variation ranged between 3 and 5%, inter-assay variation ranged from 4% to 5.2%, with a detection limit of 5.52 nmol/L.
Plasma concentrations of adrenaline and noradrenaline were measured by enzyme immunoassay (Immuno-Biological Laboratories Hamburg, Germany). The sensitivity of the adrenaline assay was 10 pg/mL. Intra-assay variation ranged between 4.1 and 8.3% and inter-assay variation ranged from 12.4% to 16%. For plasma noradrenaline, intra-assay variation ranged between 4.8 and 10% and inter-assay variation ranged from 12% to 16.5%, with a detection limit of 20 pg/mL.
All the recorded data were computerized and means were calculated for the following times: baseline (conscious state) (T1); immediately after anesthetic induction (T2); immediately after tracheal intubation (T3); 30 s before skin incision (T4); during skin incision (T5); during ovarian pedicle traction (maximal nociceptive stimulus) (T6); during peritoneum closure (T7), and at the end of surgery and cessation of anesthetic administration (T8). The ANSiscopeTM indices were also measured 24 h after the end of surgery (T9).
Plasma hormone concentrations were measured at baseline (conscious state), 30 s after induction, during skin incision, during ovarian pedicle traction, during peritoneal closure, and 24 h after the end of surgery.
Statistical analysis was performed with the SPSS 10.0 statistical package for Windows (SPSS Inc, Chicago, IL). Results were expressed as mean ± sd. A Kolmogorov-Smirnov test (13) was used to determine that data were normally distributed. Changes in BIS, ANSiscopeTM indices, hemodynamic variables, and hormone concentrations at each time point were analyzed using one-way analysis of variance for repeated measures followed by the Tukey test to examine deviation from control values. A Bonferroni procedure for multiple comparisons was conducted to minimize the possibility of finding significant results by chance. Stepwise multiple-regression analysis was performed to evaluate the relationship between the ANSiscopeTM indices and hemodynamic variables, the ANSiscopeTM indices and hormone concentrations, the LF/HF ratio and BalANSindexTM, and between the LF/HF ratio and hormone concentrations. Values of P < 0.05 were considered significant.
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Results |
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Temperature was maintained stable as was Petco2 between 35–40 mm Hg and Spo2 was > 97% in all pigs. Blood loss was minimal for all procedures.
A significant (P < 0.001) decrease in BIS was detected after anesthetic induction, but no further significant changes were seen during anesthetic maintenance (Table 1). No movements were observed in any pig during anesthesia. Anesthetic depth, as determined by clinical observation was consistent with a surgical plane of anesthesia.
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The changes observed in all the measured variables are reflected in Tables 1–3. In brief, these changes are summarized below.
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Before Surgery (Times 1 to 4)
The ANSindexTM sympathetic, balANSindexTM, and LF/(LF+HF) increased significantly (P < 0.001)and the HF/(LF+HF) quotient decreased significantly after sevoflurane induction, but hemodynamic variables, cortisol, and catecholamine concentrations did not change significantly. The LF/HF ratio increased significantly after tracheal intubation.
During Surgery (Times 5 to 8)
The ANS indexTM sympathetic and the quotient LF/(LF+HF) remained increased through the surgery. The HF/(LF+HF) quotient remained decreased from baseline through the whole procedure. The LF/HF ratio increased significantly during skin incision, ovarian pedicle traction, and during peritoneum closure. BalANSindexTM values increased significantly (P < 0.001) during skin incision. Similarly, a significant (P < 0.001) increase in plasma cortisol, adrenaline, and noradrenaline was seen immediately after incision, with the maximum hormone values being found at the moment of ovarian pedicle traction.
No significant changes were detected in hemodynamic variables during skin incision or during maximal nociceptive stimulus throughout the surgical procedure, except for a significant increase noted in wedged pulmonary pressure (P < 0.001) during abdominal incision. This high value was maintained all through surgery.
Time 9
The ANSindexTM sympathetic and the balANSindexTM remained significantly higher than baseline 24 h after surgery whereas the ANSindexTM parasympathetic stayed significantly lower. Catecholamine levels remained high but cortisol levels reverted to normal.
No correlation was detected in this study among any of the registered ANS indicesTM and hemodynamic variables. A significant (P < 0.01) correlation was found, however, between the balANSindexTM and plasma adrenaline concentrations (Fig. 1) but not between balANSindexTM and cortisol concentration (Table 4). The same tendency was seen at all studied intervals between balANSindexTM and catecholamines concentrations.
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A significant (P < 0.01) correlation was found between the balANSindexTM and LF/HF ratio and between LF/HF ratio and plasma adrenaline concentrations but not between LF/HF ratio and noradrenaline and cortisol concentrations (Table 4, Figs. 1 and 2).
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Moreover a significant (P < 0.01) correlation was observed between the ANSindexTM sympathetic and adrenaline plasma levels, whereas no correlation was found between this index and noradrenaline and cortisol values. On the other hand, a correlation was found between ANSindexTM parasympathetic and plasma noradrenaline (P < 0.01) (Table 4).
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Discussion |
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The present study detected a correlation between the balANSindexTM and catecholamine concentrations and between the balANSindexTM and HF/LF ratio during anesthesia.
On the other hand, no correlation was seen between both indexes and cortisol concentrations. The endocrine rapid response to stress is mainly associated with activation of the adrenal medulla and the SNS, with increased catecholamine levels, whereas stimulation of the pituitary-adrenocortical system and cortisol release represent a slower reaction (1). The balANSindexTM could be an earlier marker of sympathetic activity than changes in cortisol concentration.
In our opinion, the increase in hormone concentrations, ANS indexTM sympathetic, HF/LF ratio, and balANSindexTM during surgery were related to the surgical trauma, (14) and they were accompanied by a substantial ANS activation secondary to either a stress response or pain. Values for the ANS indexTM, spectral analysis variables, and hormone concentrations obtained at that time reflect the fact that the anesthetic protocol we used was not successful in minimizing stress responses of the ANS to the surgery. Similarly, the increases shown in catecholamines, ANSindexTM sympathetic and balANSindexTM during recovery of consciousness reflect a significant activation of the ANS during anesthetic recovery. However, this increase in the indices and in catecholamine concentrations was not followed by clinical signs suggestive of stress or pain during surgery or anesthetic recovery, nor did we detect hemodynamic changes at these times. This supports the assumption that HR and clinical signs are not good indicators of ANS stimulation during anesthesia, and these data are therefore not sufficient to determine the degree of stress in patients.
These results are consistent with prior studies in the same setting (15). It has been proposed (16) that HRV modifications can be used as an indicator of postoperative recovery.
The similarity between ANS indices during ovarian pedicle traction and 24 hours after surgery may be explained by considering that during surgical stimulus the animal was anesthetized and 24 hours later the measurements were taken in conscious animals with a surgical wound.
A slight increase in catecholamine levels was seen in this study immediately after induction, along with an increase on the balANSindexTM, and a concurrent increase in the ANS indexTM sympathetic, LF/(LF+HF) and HF/LF ratio. At the same time HF/(LF+HF) decreased. These changes suggest that sevoflurane anesthetic induction causes a sympathomimetic activation (9). The results obtained in the present study are in accordance with other studies conducted while inducing anesthesia with isoflurane (17). The sympathoadrenal activation shown by ANSiscopeTM and spectral analysis of HRV were not associated in this study to a hemodynamic response, in contrast with the data reported for isoflurane and desflurane (18). In humans, the initial administration of desflurane prompts a transitory, but substantial, increase in HR and arterial blood pressure (19) that is associated with sympathetic stimulation. The changes observed in ANSiscopeTM indices, hormones levels, and spectral analysis after induction may be associated with the administration of ketamine as a preanesthetic medication. This drug has a sympathomimetic action, thus decreasing the variability of R-R intervals. Theoretically, administration of ketamine should have caused an increase in the ANSindexTM sympathetic and in the LF/(LF+HF), so the increase observed in this index between baseline (registered in the conscious animal and before any preanesthetic medications) and immediately after anesthetic induction (i.e., after administration of ketamine), may have been related to this premedication (20). In our opinion this may reflect that ANSiscopeTM does not only reflect the sympathetic activation caused by the external stimulus but it also reflects the sympathetic activation caused by drugs.
Our study did not reveal a correlation between ANSiscopeTM indices and hemodynamic variables. Previous studies conducted with a different, early version of the monitor that also measured the reactivity of the ANS in real time through fractal analysis of HRV (15,21)1 reflected that the measured index could be a marker of stress responses to a nociceptive stimulus that would be evident sooner than changes in HR or arterial blood pressure. The period that elapses between changes in the proprietary index and hemodynamic changes may account for the lack of correlation in our study. In our opinion, this difference in the time frame between changes in the proprietary index and hemodynamic changes may make the ANSiscopeTM a valuable therapeutic tool. It is possible that the anesthetic protocol used, given the known cardiovascular effects of sevoflurane, could have masked any HR and arterial blood pressure changes in response to surgery.
In our opinion, the main limitations of this pilot study are that despite having found significant correlations among several of the studied variables (Table 4), these correlations are weak as indicated by the R2 values. Moreover, further studies including direct measurements of ANS activities are needed to fully determine the clinical usefulness of the monitor.
In the study reported here, we used an electrode configuration for BIS that is normally used in human medicine (11). Our clinical experience with this electrode arrangement has always yielded good-quality recordings in pigs. BIS data have not been validated in animals and hence the interpretation of these data must extrapolate from human data.
In a previous study performed by our group (12), BIS was useful for predicting changes in anesthetic depth at clinically used dosages of sevoflurane at varying MAC concentrations.
We used intermittent positive-pressure ventilation in all pigs to avoid chemoreflex activation secondary to hypoventilation-induced hypercapnia and hypoxemia. Moreover, variables were measured as soon as possible after anesthetic induction (i.e., a time when capnic changes are minimal). Variables of mechanical ventilation (tidal volume and respiratory rate) were set near values observed for conscious pigs. In conscious subjects, reduction of tidal volume is associated with a reduction in HF spectral energy and, through a complex dynamic interaction, causes an increase in the LF components (22). This implies that changes in HRV during induction of anesthesia depend on drug-induced modifications of ANS activity as well as their effects on respiration.
In the pilot study reported here, the correlations seen suggest that the balANSindexTM could be a useful tool to monitor ANS activity during anesthesia and surgery. However, we did not detect a correlation between hemodynamic variables and the ANSindexTM. To fully validate this monitoring system further studies are needed, using the technique described by Ebert and Muzi (23) that obtain direct measurements of SNS and parasympathetic nervous systems activity. In this way the sensitivity and the specificity of the ANSindicesTM could be verified.
The authors thank Marion Genoulaz, researcher at Dyansys, Inc., USA for technical assistance.
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Footnotes |
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1Vibe K, Courvoisier J, Cohen-Laroque ES, et al. Decreased reactivity of the autonomic nervous system during induction of general anesthesia [abstract]. Schweiz Med Wochenschr 1999; 129(suppl 112): 9S.
Accepted for publication December 12, 2005.
Supported by Consejería de Sanidad y Consumo. Junta de Extremadura, Spain. Reference No. 03/85.
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