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Anesth Analg 2001;93:1121-1126
© 2001 International Anesthesia Research Society

CARDIOVASCULAR ANESTHESIA

The Effects of Vasoactive Drugs on Hepatic Blood Flow Changes Induced by CO2 Laparoscopy: An Animal Study

Mercè Agustí, MD*, J. Ignasi Elizalde, MD{dagger}, Ramon Adàlia, MD*, Graciela Martínez-Pallí, MD*, Juan C. García-Valdecasas, MD{ddagger}, Josep M. Piqué, MD{dagger}, and Pilar Taurà, MD*

Departments of *Anesthesia (URSC), {dagger}Gastroenterology, and {ddagger}Digestive Surgery (IMD), Hospital Clínic, Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain

Address correspondence and reprint requests to Pilar Taurà, MD, Anesthesiology Department, Hospital Clínic, Villarroel 170, 08036 Barcelona, Spain. Address e-mail to 29272mal{at}comb.es


   Abstract
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 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Laparoscopic surgery is associated with systemic and splanchnic hemodynamic alterations. Recent data suggest that small-dose dobutamine may attenuate the reduction in splanchnic blood flow associated with increments in intraabdominal pressure. We conducted this study to analyze the effects of dopamine and dobutamine on the hepatic circulation in this setting. Twenty-one pigs were anesthetized and mechanically ventilated. A flow-directed pulmonary artery and carotid artery catheters were inserted. Perivascular flowprobes were placed around the main hepatic artery and the portal vein. CO2 was insufflated into the peritoneal cavity to reach an intraabdominal pressure of 15 mm Hg. After 60 min, animals received dopamine (5 µg · kg-1 · min-1; n = 8), dobutamine (5 µg · kg-1 · min-1; n = 8), or saline (n = 5) for 30 min. Pneumoperitoneum induced significant increases in heart rate, mean arterial pressure, and systemic vascular resistance, with decreases in cardiac output and hepatic artery and portal vein blood flows. Dobutamine infusion, in contrast to dopamine, corrected, at least in part, cardiac output, systemic vascular resistance, and hepatic artery blood flow alterations, but neither drug restored total hepatic blood flow.

IMPLICATIONS: Hepatic blood flow decreases during laparoscopic surgery. A small-dose infusion of neither dobutamine nor dopamine corrects the total hepatic blood flow impairment, but the former is able to restore the hepatic arterial blood supply in an animal model mimicking this condition.


   Introduction
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 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
In the last decade, laparoscopic techniques have become the standard surgical approach for several gastrointestinal and gynecologic disorders. Even working with small pressures, peritoneal gas insufflation induces many splanchnic hemodynamic changes related to both the direct mechanical compression of intraabdominal vessels and to the systemic hemodynamic and acid-base effects derived from increased intraabdominal pressure and from carbon dioxide absorption (1). Several experimental and human studies have revealed that such moderate increases in intraabdominal pressure are associated with a reduction in liver blood flow, an effect that is usually devoid of overt complications (2,3). However, laparoscopy is performed increasingly in older and often more unfit patients, in whom the procedure may take considerably longer. In those settings, clinical impairments in hepatic and renal function have been described (4), but until now, pharmacologic approaches to override these possible complications of transient increased intraabdominal pressure have not been extensively investigated.

We recently provided evidence that small-dose dobutamine can restore gut mucosal perfusion in animals submitted to moderate increases in intraabdominal pressure, similar to those used for laparoscopic surgical approaches in the clinical setting (5). We hypothesized that those effects of small-dose dobutamine would also correct changes in liver blood flows and, therefore, we assessed the effects of dopamine and dobutamine on laparoscopy-induced changes in hepatic arterial (HABF) and portal vein (PVBF) blood flows in pigs.


   Methods
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 Abstract
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 Methods
Results
 Discussion
 References
 
All experimental procedures were conducted conforming to the Guiding Principles in the Care and Use of Animals as approved by the Council of the American Physiologic Society and received the approval of the Animal Care Committee of the Hospital Clínic of Barcelona.

After an overnight fasting, with free access to water, 21 Yorkshire pigs of either sex (30–35 kg) were premedicated with IM azaperon (10 mg/kg, Stresnil; Lab Dr. Esteve, Barcelona, Spain). Sixty minutes later, anesthesia was induced with an IV bolus of thiopental (20 mg/kg). The trachea was intubated with a cuffed tube, and the lungs were ventilated with a fraction of inspired oxygen of 0.5 and a tidal volume that maintained PaCO2 within 40 ± 5 mm Hg at a rate of 12 to 14 breaths/min. Anesthesia was maintained with 1% inhaled isoflurane. Pancuronium (1 mg/h, IV) was administered to prevent incremental increases in intraabdominal pressure (IAP) derived from muscle contraction. All animals received IV 0.9% sodium chloride and 5% dextrose solutions at a rate of 2 mL · kg-1 · h-1 each. Central temperature was monitored throughout the experiments and was kept between 36.5°C and 37.5°C by means of heating lamps and warmed IV fluid administration, if needed. Once anesthetized, animals were maintained in a supine position for all the experiments to avoid changes derived from body position.

After careful dissection, a 16-gauge catheter was inserted into the right carotid artery for continuous monitoring of mean arterial pressure (MAP; mm Hg) and blood sampling. A 7F flow-directed pulmonary catheter was advanced into the pulmonary artery through the right external jugular vein to measure cardiopulmonary pressures and cardiac output (CO; L/min), and to draw mixed venous blood samples. The position of the tip of the catheter was confirmed by the pressure tracing.

A midline celiotomy was performed, and the hepatic artery and portal vein were carefully dissected from the surrounding tissue. The gastroduodenal and right gastric arteries were ligated to ensure that all the blood flowing through the common hepatic artery supplied the liver. Taking special care not to disturb perivascular structures, ultrasonic flowprobes (H3SB878; Transonic Systems, Ithaca, NY) of appropriate sizes to ensure a snug fit were placed around the vessels and connected to a blood flowmeter (HT107; Transonic Systems) to continuously monitor HABF and PVBF (mL/min). This technique allows for continuous measurements of blood flow in discrete vessels and has been extensively validated (6). To ensure optimal blood flow measurements, 200–300 mL of warm sterile saline solution was instilled into the peritoneal cavity. Liver blood flow was calculated as the sum of HABF and PVBF.

Finally, a 5-mm-diameter Veress needle (HS Surgical Corp, Norwalk, CT) was inserted through a small incision in the left flank and connected to an insufflator (Electronic Laparoflator; Storz Endoscope, Schaffhausen, Switzerland), and the laparotomy incision was closed in two layers to effect a watertight seal. Additional silk sutures were performed during the experiments if an excess intraperitoneal gas escape was detected.

After surgery, animals were allowed to stabilize for 30 min. Thereafter, systemic and hepatic hemodynamic and respiratory variables, as well as venous and arterial blood samples, were obtained, and IAP was increased in a 5- to 10-min period by means of CO2 insufflation (at a rate of 0.5–1 L/min) until an intraperitoneal pressure of 15 mm Hg was obtained. This level of IAP was sustained for the whole experiment, with automatic additional gas insufflation on demand. Measurements were repeated at 30 and 60 min, a time at which a dopamine (5 µg · kg-1 · min-1; n = 8), dobutamine (5 µg · kg-1 · min-1; n = 8), or saline (n = 5) infusion was started. Randomization was performed by using sealed opaque envelopes that contained the group assignment according to a previously computer-generated random list. Hemodynamic and respiratory variables were reassessed 30 min after starting drug infusion and again 30 min after drug discontinuation. Finally, the animals were killed by an overdose of anesthesia.

MAP, right atrial pressure (RAP; mm Hg), mean pulmonary arterial pressure (MPAP; mm Hg), pulmonary wedge pressure (PWP; mm Hg), and CO were recorded with a Hewlett-Packard 68S monitor (Hewlett-Packard, Andover, Germany) by using standard techniques. CO (L/min, thermal dilution) was measured in triplicate at each experimental time point. Heart rate was derived from continuously electrocardiographic monitoring. Systemic vascular resistance (SVR; dynes · s · cm-5) was calculated as (MAP - RAP) x 80/CO, in which RAP is measured in millimeters of mercury and CO is measured as liters per minute. Pulmonary vascular resistance (dynes · s · cm-5) was calculated as (MPAP - PWP) x 80/CO. Arterial and mixed venous blood samples were drawn for determinations of blood gases at fixed time points and immediately analyzed.

Results are expressed as mean ± SEM. The effects of pneumoperitoneum and drug infusion on hemodynamic variables were evaluated by analysis of variance (ANOVA) for repeated measures by using the SPSS 6.1.3 statistical package software (SPSS Inc., Chicago, IL). Duncan’s test was used as a post hoc test when group differences were detected by ANOVA. Statistical significance was established at a P value of <0.05.


   Results
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 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Peritoneal insufflation with CO2 prompted a significant increase (P < 0.05) in HR, MAP, and RAP during the entire experience in all groups of animals, whereas neither MPAP nor PWP showed any significant variation in any treatment group (Table 1). Similarly, pulmonary vascular resistance did not show any significant variation from baseline at any of the analyzed time points.


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  		Table 1. Effects of Dopamine and Dobutamine on Systemic Hemodynamics in Pigs Submitted to CO2 Peritoneal Insufflation
 
Sixty minutes after CO2 insufflation, SVR increased significantly in all groups of animals, and this effect reached maximal values after 1 h in animals receiving dopamine and in control pigs (P < 0.01). Conversely, dobutamine administration was followed by a full restoration of SVR to baseline values (Table 1).

Early after gas insufflation (30 min), there was a slight CO decrease (P < 0.05) in all animal groups, an effect that progressed with time in animals thereafter receiving saline and that was kept stable when dopamine was infused (Fig. 1). In contrast, dobutamine administration prompted a full restoration of this variable 30 min after starting the drug infusion (P < 0.05 with respect to Saline and Dopamine groups). Drug retrieval was followed by a rapid decrease in CO in either group of animals receiving ß-adrenergic drugs, reaching values comparable to those observed in control animals 30 min later.



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  		Figure 1. Changes in cardiac output induced by laparoscopic CO2 insufflation (15 mm Hg) in pigs. Sixty minutes after peritoneal insufflation, dopamine, dobutamine or saline was administered for 30 min. Results are expressed as percentage of baseline values (mean ± SEM; T0 = baseline; T1 = 30 min after peritoneal insufflation; T2 = 60 min after peritoneal insufflation; T3 = 30 min after starting drug infusion; T4 = 30 min after drug discontinuation; *P < 0.05 and **P < 0.01 with respect to baseline values; {dagger}P < 0.05 with respect to the remaining groups).

 
PaCO2 increased during the entire experience in all animal groups, both in arterial as well as in venous samples (Table 2). These variations were associated with a sustained trend to decreasing pH values in arterial and mixed venous blood samples along with time.


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  		Table 2. Effects of Dopamine and Dobutamine on Acid-Base Variables in Pigs Submitted to Peritoneal Insufflation
 
A marked and sustained decrease in PVBF, appearing as early as 30 min after peritoneal insufflation, was observed in control animals. PVBF changes induced by laparoscopy in animals receiving dopamine or dobutamine infusion paralleled those observed in the Control group (Fig. 2A).



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  		Figure 2. Changes in portal vein (A), hepatic artery (B), and total hepatic (C) blood flow induced by laparoscopic CO2 insufflation (15 mm Hg) in pigs. Sixty minutes after peritoneal insufflation, dopamine, dobutamine, or saline was administered for 30 min. Results are expressed as percentage of baseline values (mean ± SEM; T0 = baseline; T1 = 30 min after peritoneal insufflation; T2 = 60 min after peritoneal insufflation; T3 = 30 min after starting drug infusion; T4 = 30 min after drug discontinuation; *P < 0.05 and **P < 0.01 with respect to baseline values; {dagger}P < 0.05 with respect to the remaining groups).

 
A significant decrease in HABF was also noted after 30 min of peritoneal insufflation (Fig. 2B). This impairment in hepatic arterial perfusion remained during the whole experiment in animals receiving saline. Conversely, dobutamine infusion prompted an increase in this variable, which showed a trend toward restoration to baseline values. When dobutamine infusion was stopped, HABF values decreased again to values similar to those of control animals at the same time point. Dopamine administration did not exert any significant effect on this variable, because the decrease in HABF paralleled that observed in saline-treated animals.

Total hepatic blood flow, being the sum of PVBF and HABF, decreased significantly early after peritoneal gas insufflation, which progressed with time in animals subsequently receiving either saline or dopamine infusions (Fig. 2C). During drug infusion, animals allocated to receive dobutamine experienced a trend toward a restoration of this variable, but this effect did not reach statistical significance.


   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
The results of this investigation show that small-dose dobutamine, unlike small-dose dopamine, can restore the hepatic arterial blood supply in animals submitted to CO2 pneumoperitoneum. Peritoneal gas insufflation for laparoscopic procedures results in increased IAP, leading to many hemodynamic, respiratory, metabolic, neurologic, and humoral effects (7,8), depending on the insufflating agent (e.g., CO2), the IAP, and the length of the procedure (6,9). In that regard, there is a large body of evidence indicating that peritoneal insufflation, even at small pressures, induces a significant decrease in blood perfusion of intraabdominal organs (5,6,10,11). Whereas the overt clinical relevance for such disturbances is likely to be small for individuals without underlying diseases, several studies have revealed that hepatic function abnormalities after laparoscopy are frequent (12,13), especially in the elderly (14). Because laparoscopy is performed increasingly in older and often more un-fit patients in whom the procedure may take considerably longer, development of strategies to counterbalance its systemic and splanchnic hemodynamic side effects, thus enhancing the safety profile of minimally invasive abdominal surgery, would be desirable.

ß-Adrenergic agonists (i.e., dopamine and dobutamine) have been largely used to manage systemic hemodynamic impairments perioperatively and in the intensive care unit setting, but until now, the effects of these drugs on splanchnic hemodynamics have been largely unknown. ß-Adrenergic receptor agonists improve splanchnic oxygenation in sepsis (15,16). The rationale for such an effect is based on their inotropic properties as well as on the expression of ß2 and dopaminergic receptors in the vessels of the gastrointestinal tract. A selective vasodilatory effect of dopamine within the intestinal mucosa, which is mediated by postsynaptic vascular dopamine-1 receptors, occurs (17). Dobutamine, being primarily a potent ß1-adrenergic receptor agonist, also has some ß2-adrenergic receptor agonist properties within the peripheral vasculature. The pharmacologic effects mediated by the various receptor types are overlapping and dependent on the dose of dopamine or dobutamine given. Theoretically, both small-dose dopamine and dobutamine can induce vasodilation in the splanchnic area, but there is some evidence suggesting that dobutamine might be better than dopamine at improving gastrointestinal perfusion both in sepsis and in conditions associated with intraabdominal hyperpressure (5,18,19). Most of the aforementioned studies have focused on gut mucosal blood flow, and investigations assessing the effects of ß-adrenergic agonists on liver perfusion are limited, but both drugs increase total liver blood flow under certain circumstances (20–22).

The results of this investigation confirm previous investigations indicating that CO2 peritoneal insufflation induces sustained decreases in both HABF and PVBF, resulting in a marked reduction in total liver blood flow (6,14). Even though dobutamine administration failed to restore total liver blood flow to baseline values, it was able, whereas dopamine was not, to increase HABF and, accordingly, it significantly blunted the impairment in liver perfusion induced by laparoscopic insufflation. Perhaps an earlier or more prolonged drug administration or at larger doses could have been more beneficial. Moreover, the effect of these effects on endothelial, Kupffer, or parenchymal liver cell function (12,13) was not addressed in this study and will require further investigation. In fact, dobutamine may increase splanchnic metabolic demands, an effect that could counterbalance the hemodynamic benefits derived from its administration. However, Ensinger et al. (23) suggest that the splanchnic hemodynamic amelioration induced by dobutamine is devoid of this unwanted metabolic effect. As for the data obtained in dopamine-treated animals, contrasting with the results obtained by Fujita et al. (24), we did not observe any splanchnic hemodynamic benefits derived from dopamine administration in this or in previous investigations, but considering the number of animals studied, we cannot completely exclude the possibility of a type II error (5). Differences in CO2 insufflation pressure or drug dosing could be responsible for these diverging results. In addition, the large variability of dopamine pharmacokinetics, even in healthy subjects (25), may also account, at least in part, for these apparent discrepancies.

This investigation was conducted to elucidate whether blood flow improvements obtained with dobutamine in the gut mucosal layer (5) are also extended to hepatic perfusion in an animal model, mimicking the usual conditions of human laparoscopic surgery. Our results indicate that small-dose infusion of neither dobutamine nor dopamine corrects the total hepatic blood flow impairment, but the former partially restores the hepatic arterial blood supply induced by CO2 peritoneal insufflation. These results provide preclinical evidence suggesting that pharmacologic approaches could be helpful for preventing the splanchnic hemodynamic side effects of laparoscopic insufflation, which would allow expansion of the indications for minimally invasive abdominal surgery to more un-fit patients. It is noteworthy that this investigation was conducted in healthy animals, contrasting with the clinical scenario in which the underlying patient’s condition (sepsis or cardiac or liver failure) might modify drug responses because of vascular hyporeactivity or CO redistribution. Moreover, even though significant splanchnic hemodynamic alterations have not been documented after open abdominal surgery (26), we cannot completely exclude that laparotomy modified the hemodynamic responses in this series of experiments. Therefore, additional experimental work further exploring this and other aspects should be performed before assessing the possible clinical usefulness of this pharmacologic approach.


   Acknowledgments
 
Supported by a grant from Fondo de Investigaciones Sanitarias de la Seguridad Social of Spain (FISss 97/0838). MA was supported by a research fellowship grant from Hospital Clínic de Barcelona.


   References
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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Accepted for publication June 6, 2001.




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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins and Stanford University Libraries' HighWire Press®. Copyright 2001 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press