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Anesth Analg 2008; 106:164-170
© 2008 International Anesthesia Research Society
doi: 10.1213/01.ane.0000289531.18937.0a
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TECHNOLOGY, COMPUTING, AND SIMULATION

Real-Time Heart Rate Variability and Its Correlation with Plasma Catecholamines During Laparoscopic Adrenal Pheochromocytoma Surgery

Musa Sesay, MD*, Patrick Tauzin-Fin, MD*, Philippe Gosse, MD{dagger}, Philippe Ballanger, MD{ddagger}, and Pierre Maurette, MD*

From the *Department of Anesthesiology, Centre Hospitalier Universitaire Pellegrin, Place Amélie Raba Léon, 33076 Bordeaux, France; {dagger}Department of Cardiology, Centre Hospitalier Universitaire Sainte Andrée, Cours d’Albret, 33076 Bordeaux, France; and {ddagger}Department of Urology, Centre Hospitalier Universitaire Pellegrin, Place Amélie Raba Léon, 33076 Bordeaux, France.

Address correspondence and reprint requests to Musa Sesay, MD, Department of Anesthesiology, Centre Hospitalier Universitaire Pellegrin, Place Amélie Raba Léon, 33076 Bordeaux, France. Address e-mail to musa.sesay{at}chu-bordeaux.fr.


   Abstract
Top
 Abstract
Introduction
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 APPENDIX: THE MAXIMUM ENTROPY...
 REFERENCES
 
BACKGROUND: We studied sympathovagal activity using real-time heart rate variability (HRV) and determined its relationship with plasma catecholamines to characterize short-term cardioregulatory mechanisms during laparoscopic adrenal pheochromocytoma surgery.

METHODS: We recruited 20 patients with pheochromocytoma (Group P) and 20 with incidentaloma (Group I). HRV, systolic blood pressure and heart rate were continuously monitored. The low frequency and high frequency spectra denoted, respectively, sympathetic and parasympathetic activity. The low frequency/high frequency (LF/HF) ratio represented sympathovagal balance. Blood samples for epinephrine and norepinephrine assays were collected before, during, and after surgery. After log transformation of the repeated measures, a linear regression model was applied on their mean values. The correlation coefficients among variables were calculated using the Spearman rank test.

RESULTS: No significant changes were observed in Group I. In Group P, epinephrine and norepinephrine increased in all patients during peritoneal insufflation and tumor resection. In 16 patients, systolic blood pressure, heart rate, low frequency, and LF/HF ratio increased concurrently. In four patients, low frequency and LF/HF ratio decreased. Three of these patients had normal systolic blood pressure and heart rate, and the fourth patient had hypotension and tachycardia. The high frequency component was enhanced in 15 patients and was stable in five. Low frequency was correlated with norepinephrine (r = 0.68, P < 0.001), systolic blood pressure (r = 0.66, P < 0.01), and heart rate (r = 0.62, P < 0.05).

CONCLUSION: This study demonstrated a strong correlation between low frequency HRV, plasma norepinephrine, arterial blood pressure, and heart rate during pheochromocytoma surgery.


   Introduction
Top
 Abstract
 Introduction
METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 APPENDIX: THE MAXIMUM ENTROPY...
 REFERENCES
 
Pheochromocytoma tumors affect cardiovascular function through the catecholamines they secrete into the circulation.1–4 Excessive catecholamine release can cause malignant hypertension, arrhythmia, myocardial hypertrophy, and heart failure.5–7 Conversely, some patients remain asymptomatic even though they harbor active catecholamine-secreting tumors.8–11 These varying hemodynamic responses to increased catecholamines have been attributed to cardiac sympathovagal modulation.5

Most data on hemodynamic response are obtained from experimental or pre- and postoperative clinical studies.12–16 Intraoperative care of these patients is complicated by catecholamine release during tumor resection.17–19 Heart rate variability (HRV), microneurography,12 and scintigraphy20 have been used to evaluate sympathetic activity during pheochromocytoma resection. HRV is a noninvasive marker of cardiac sympathovagal activity21,22 that provides quantitative beat-to-beat assessment of cardiovascular control.23,24 Improvements in computer technology have now made it possible to calculate HRV in real-time.

The goal of this study was 1) to assess the cardiac sympathovagal activity, using real-time HRV and 2) to determine the relationship between HRV and plasma catecholamine release during laparoscopic adrenalectomy for pheochromocytoma.


   METHODS
Top
 Abstract
 Introduction
 METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 APPENDIX: THE MAXIMUM ENTROPY...
 REFERENCES
 
Preoperative Preparation
After IRB approval and written informed consent, we recruited 20 patients with adrenal pheochromocytoma (Group P) and 20 age-matched patients with clinically unapparent adrenal mass (or incidentaloma: Group I) scheduled for laparoscopic surgery. Patients with diabetes, heart disease, or neurological diseases were excluded. Coffee, alcohol consumption, cigarette smoking, and tricyclic antidepressants were stopped 1 wk before surgery. The diagnosis of pheochromocytoma was established on clinical, biochemical, and radiological criteria. Clinical criteria included headache, sweating, palpitation, and hypertension. Biochemical criterion consisting of 24-h urinary metanephrine was >2 mg (normal value: 0.14–0.93 mg). Radiological criteria consisted of computed tomographic scan and 131I-metaiodobenzylguanidine scintigraphy identifying adrenal tumors of 3–5 cm. The preoperative echocardiogram excluded dilated cardiomyopathy and the 60°/10 min head-upright tilt-table testing demonstrated no orthostatic hypotension.25

Preoperative preparation of Group P was started 15 days before surgery using oral prazosin (5 mg/d) and bisoprolol (10–20 mg/d). Three days before surgery these drugs were replaced by a continuous IV infusion of urapidil (10–15 mg/h), which was maintained until ligation of the adrenal vein. All patients were within our target systolic blood pressure range of 100–150 mm Hg before surgery. The operations were performed between 7 and 11 am by the same surgeon (PB).

Anesthetic Protocol
After fasting overnight, patients were premedicated 1 h before surgery with 5 mg of oral midazolam. A patch containing an eutectic mixture of prilocaine (2.5 mg/g) and lidocaine (2.5 mg/g) (EMLA®) was applied over the radial arteries of the wrists. Heart rate, arterial blood pressure, and pulse oximetry were monitored (Datex AS/3TM, Helsinki, Finland) on admission to the operating room. A standard lead II electrocardiogram (ECG) was used for heart rate. The radial artery was cannulated for continuous arterial blood pressure assessment. Anesthesia depth was monitored by the electroencephalogram-Bispectral Index (BIS Version 3.4, Aspects Medical Systems, Spacelab, MA).

General anesthesia induced with propofol 2–2.5 mg/kg and sufentanil 0.8 µg/kg. Muscle relaxation was provided with cisatracurium 0.15 mg/kg. Anesthesia was maintained with sevoflurane 2.5%, and continuous infusions of sufentanil 30–40 µg/h and cisatracurium 30 mg/h. The BIS was maintained between 40 and 60 using 0.1%–0.2% adjustments in inspired sevoflurane concentration. After tracheal intubation, the patients were mechanically ventilated with 100% oxygen. The respiratory rate was 16 breaths per min at a tidal volume of 7 mL/kg. The latter was adjusted (100–200 mL up/down) to keep the end-tidal Pco2 between 35 and 45 mm Hg. Isotonic saline solution was infused intraoperatively at a rate of 10–15 mL · kg–1 · h–1. Systolic blood pressure variation during mechanical ventilation was used to detect hypovolemia and guide fluid replacement. Patients were placed in the full lateral position with the operative side uppermost. The pneumoperitoneum with CO2 was produced with the intraabdominal pressure maintained between 12–14 mm Hg. Three to five trocars were used for the operation.

HRV and Catecholamine Measurements
A laptop computer running the HRV software (MemCalc/TawaraTM; Suwa Trust, Tokyo, Japan) was connected to the Datex monitor via a 12-bit, ±10 V, 10 ms, analog/digital card (ContecTM, Osaka, Japan). The ECG was recorded by the monitor at a sampling rate of 250 Hz and transferred to the computer with an analog output of 1 V/1 mV, resolution of 1 bpm and averaging time of 10 s. The analog signal was converted to a readable digital signal by the computer. Real-time spectral analysis was performed using the maximum-entropy method with high resolution and automatic elimination of artifacts and ectopic beats (Appendix 1,22,24). The area under the curve of the spectral peaks within the ranges of 0.003–0.04 Hz (very low frequency), 0.04–0.15 Hz (low frequency), and 0.15–0.4 Hz (high frequency) were calculated on 30-s epochs of the ECG RR interval data with automatic update of each RR interval. Output data were averaged every 10 s. The low frequency and high frequency component were expressed both in absolute units of power (ms2) of power and normalized units (nu). The latter are defined as the relative value of low frequency or high frequency power to total power, minus the very low frequency power.21 The low frequency component is thought to primarily reflect sympathetic activity and, to a lesser extent, parasympathetic activity, the high frequency component, parasympathetic activity, and the low frequency/high frequency ratio, sympathovagal balance.21 The HRV indices and cardiorespiratory variables were continuously recorded. Event markers on the computer and the ECG monitor were set at 30 s before induction of anesthesia, after the induction, at laryngoscopy, after peritoneal insufflation, at onset of tumor resection, after tumor resection, and in the recovery room after tracheal extubation. Blood samples for catecholamine assays were simultaneously collected at these time points. Additional blood samples were collected any time we observed an abrupt and isolated change in systolic blood pressure or heart rate. Samples were transferred immediately into ice cold tubes. They were centrifuged at 4°C and plasma separated for storage at –80°C until assayed. Plasma concentrations of epinephrine, norepinephrine, and dopamine were determined using a high performance liquid chromatography method with electrochemical detection.26

Statistical Analysis
Data were analyzed using the Systat® version 12 and Sigmaplot version 10 statistical packages (Systat Software, Point Richmond, CA). The distribution of each variable was checked for normality using the Kolmogorov–Smirov test. HRV, in normalized units, satisfied the assumption of normality and formed the basis of our sample size calculation. However, the natural logarithm was used for all the figures to facilitate comparisons. A formal sample size determination was impossible because no reference data were available at the inception of this study. Therefore, we assumed that a 10% change in low frequency and a standard deviation of 8%, relative to the baseline value, would be clinically relevant. For a given {alpha} = 0.05, a β = 0.1 (power: 90%), we estimated that a minimum of 15 patients would be needed in each group using the unpaired t-test. Categorical data were compared using {chi}2 and Fisher’s exact tests where appropriate. The Kruskall–Wallis rank ANOVA and Dunn’s post hoc tests were used for comparisons within groups. Comparisons between groups were done by a Student’s t-test or the Mann–Whitney test where appropriate. The relationship among variables was evaluated by linear regression using the mean values of the repeated measures.27


   RESULTS
Top
 Abstract
 Introduction
 METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 APPENDIX: THE MAXIMUM ENTROPY...
 REFERENCES
 
The demographic data of the two groups were similar but surgery was longer in Group P (Table 1). The estimated delay between the first symptoms and surgery in Group P was 10–720 days (Table 2). Anesthesia was stable (BIS: 40–60) during surgery in all the patients.


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  		Table 1. Demographic Data and Duration of Surgery in the Two Groups

 

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  		Table 2. Major Characteristics of the Patients with Adrenal Pheochromocytoma Tumors

 

The major changes in plasma catecholamines, HRV indices, and cardiovascular variables are presented in Table 3. Plasma dopamine levels were <30 pg/mL (normal values <50 pg/mL) throughout the study in both groups. The changes in Group I were not statistically significant. In Group P, insufflation of the pneumoperitoneum and adrenal gland resection were associated with high levels of plasma norepinephrine and epinephrine in all the patients.


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  		Table 3. Perioperative Differences in Plasma Catecholamine, Heart Rate Variability (HRV) and Hemodynamic Levels of the Two Groups

 

Hypertensive peaks were treated with IV boluses of nicardipine 2–4 mg to maintain systolic blood pressure between 120 and 150 mm Hg. IV boluses of esmolol 1–1.5 mg/kg were used when the heart rate exceeded 100 bpm. The hypotensive episodes were treated with IV boluses of ephedrine and the infusion of hydroxyethyl starch colloid (Voluven® 500 mL) when systolic variation with ventilation exceeded 10 mm Hg. The injection of esmolol and nicardipine produced a 5% reduction in low frequency power, which was statistically insignificant.

The postoperative period was uneventful. The patients remained normotensive with normal catecholamine levels. The patients were discharged on postoperative day 3 (Group I) and day 5 (Group P) without medication. Histological confirmation of pheochromocytoma was obtained after surgery in all Group P patients.

Linear regression analysis indicated that low frequency power was strongly correlated with norepinephrine (Fig. 1), systolic blood pressure, and heart rate (Fig. 2). No significant correlation was observed among the other variables.


Figure 131
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  		Figure 1. Relationship between heart rate variability (HRV) and plasma catecholamine levels during pheochromocytoma surgery. ln = natural log; LF = low frequency denotes sympathetic activity; HF = high frequency or parasympathetic activity; LF/HF = sympathovagal balance.

 

Figure 231
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  		Figure 2. Effects of catecholamines or heart rate variability (HRV) on heart rate and systolic blood pressure variation during pheochromocytoma surgery. ln = natural log; LF = low frequency denotes sympathetic activity; HF = high frequency or parasympathetic activity; LF/HF = sympathovagal balance.

 


   DISCUSSION
Top
 Abstract
 Introduction
 METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 APPENDIX: THE MAXIMUM ENTROPY...
 REFERENCES
 
We used real-time HRV based on a maximum entropy method to assess short-term cardiac sympathovagal control systems28 during pheochromocytoma surgery. We assessed the relationship among the different variables (HRV, catecholamines, systolic blood pressure, and heart rate) to depict the cardioregulatory control mechanisms during pheochromocytoma surgery. Our study detected a strong correlation between low frequency power and plasma norepinephrine, systolic blood pressure, and heart rate. No correlation was found between circulating catecholamines and hemodynamic changes during surgery.

The catecholamine levels in all 20 patients undergoing pheochromocytoma resection were very high. However, four patients were either hypotensive (No. 17) or normotensive (No. 18, 19, and 20). How is this possible, given the suggestion by Ito et al.3 that plasma catecholamine levels directly increase arterial blood pressure in patients with pheochromocytoma? One of our patients (No. 17) was hypotensive even though her epinephrine levels were very high during surgery. This is consistent with two cases of epinephrine-producing tumors that were nearly asymptomatic reported by Lipsic et al.29 Other authors demonstrated that a large proportion of catecholamine secretion in patients with pheocyromocytoma originates from sympathetic nerve endings.3 This suggests that varying hemodynamic presentation of pheochromocytoma mostly reflects sympathovagal modulation,5,30,31 explaining why previous authors found little correlation between arterial blood pressure and circulating catecholamines, similar to our findings.

HRV detected a significant reduction in low frequency power during surgery in our study. We observed increased low frequency power in the 16 patients who became hypertensive during tumor administration (No. 1–16), whereas patients with suppressed low frequency power were hypotensive (No. 17) or normotensive (No. 18–20). However, HRV remains controversial. There is strong evidence that vagal activity is the major contributor to the high frequency component. There is disagreement with respect to the low frequency component. Some studies suggest that the low frequency power is a quantitative marker of sympathetic modulation, consistent with our finding that low frequency power correlated with plasma norepinephrine concentrations (the intrinsic marker of sympathetic activity). Other studies suggest low frequency power reflects both sympathetic activity and vagal activity. In their special report concerning the standards of measuring HRV, the Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology did not provide any specific recommendation for the interpretation of low frequency power.21

Our study is consistent with previous studies showing that neither preoperative adrenergic blockade nor anesthesia can completely prevent the hemodynamic crisis during surgery.18,32 Our study also confirms previous reports that catecholamine and hemodynamic surges occur often during the creation of the pneumoperitoneum and tumor manipulation.33

Limitations and Perspectives
We calculated HRV using the MemCalc/Tawara program. This program overcomes limitations of conventional Fourier transform methods (e.g., poor frequency resolution of short data segments, spectral leakage and the assumption of data stationarity).34,35 The MemCalc/TawaraTM program does not distort the power calculation even if the underlying variation is changed, e.g., change in respiration.

Our study depicted only a small aspect of the complex pathophysiology of pheochromocytoma disease. Several questions remained unanswered. First, we did not measure sympathetic and parasympathetic activity per se. Second, we did not assess the role of HRV in predicting hemodynamic crisis. In an off-line study, Dabrowska et al.16 reported that HRV preceded sudden arterial blood pressure increases or complex cardiac arrhythmias in pheochromocytoma.


   CONCLUSION
Top
 Abstract
 Introduction
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
APPENDIX: THE MAXIMUM ENTROPY...
 REFERENCES
 
The present study clarifies the role of sympathetic activity on systolic blood pressure and low frequency heart rate variations during pheochromocytoma surgery. The study did not assess the ability of HRV to predict hemodynamic crisis, which might be a clinically valuable use of HRV in anesthesia practice.


   ACKNOWLEDGMENTS
 
The authors would like to thank Professor Guy Simmonet for his assistance, particularly in the measurement of the plasma and urinary catecholamine concentrations.


   APPENDIX: THE MAXIMUM ENTROPY METHOD FOR REAL-TIME SPECTRAL ANALYSIS OF HEART RATE VARIABILITY (HRV)
Top
 Abstract
 Introduction
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 APPENDIX: THE MAXIMUM ENTROPY...
REFERENCES
 
Entropy is a measure of randomness. The maximum entropy method (MEM) is a spectral estimation program based on the parametric autoregressive model. The MEM involves the ranking of probability distribution, the highest (maximum) rank being given to the least biased distribution. The algorithm is suitable for analyzing short blocks of nonstationary data. Its principle assumes that the underlying varia-tion of the time series, Xuv (t), encodes a linear combination of sine and cosine functions:



Formula 1

Where a0 is a constant that indicates the mean value of the time series, Np is the total number of components, an and bn are the amplitudes and fn is the frequency of the nth periodic component. The value of fn is determined by the peaks in the power spectral density or P(f), expressed as:



Formula 2

Where Pm is the output power of the prediction error filter of the order m, and {gamma}m,k is the corresponding filter coefficient, m = 0, 1, 2, . . ., M (M = optimal filter order). Pm and {gamma}m are determined by Yule–Walker equation using Burg’s algorithm.36 M can be determined from Eq. A1 using a filter order >1/fmin where fmin is the minimum central frequency component. The MEM software (MemCalc/TawaraTM, Suwa Trust, Tokyo, Japan) uses the nonlinear least squares method for fitting the electrocardiogram R–R interval series. It needs only 30 s for estimation of HRV with minimum distortion. M is automatically updated each time a new R–R interval is available.37 Output data can be averaged every 10 s, 1 min, 2 min, 5 min, and 10 min depending on the clinical context. However, real-time HRV has not yet been validated by a task force. Hence further research is mandatory, particularly comparative studies on HRV techniques.


   Footnotes
 
Accepted for publication September 4, 2007.

The study was presented in part at the 2005 ASA Meeting in Atlanta, Georgia.


   REFERENCES
Top
 Abstract
 Introduction
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 APPENDIX: THE MAXIMUM ENTROPY...
 REFERENCES
 

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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins with the assistance of Stanford University Libraries' HighWire Press®. Copyright 2006 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press