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Ann Thorac Surg 1999;68:1336-1342
© 1999 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Effects of perfusion mode on regional and global organ blood flow in a neonatal piglet model

^a Congenital Heart Surgery Service, Texas Children’s Hospital, Department of Surgery, Baylor College of Medicine, and Cullen Cardiovascular Surgical Research Laboratories, Texas Heart Institute, Houston, Texas, USA

Address reprint requests to Dr Ündar, Congenital Heart Surgery Service, Texas Children’s Hospital, 6621 Fannin St, MC 1-2285, Houston, TX 77030-2399
e-mail: aundar{at}bcm.tmc.edu

Presented at the Thirty-fifth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 25–27, 1999.

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. Organ injury (brain, kidney, and heart) has been reported in up to 30% of pediatric open heart surgery patients after conventional hypothermic non-pulsatile cardiopulmonary bypass (CPB) support with or without deep hypothermic circulatory arrest (DHCA). The effects of pulsatile (with a Food and Drug Administration approved modified roller pump) versus non-pulsatile perfusion on regional and global cerebral, renal, and myocardial blood flow were investigated during and after CPB with 60 minutes of DHCA in a neonatal piglet model.

Methods. Piglets, mean weight 3 kg, were used in both pulsatile (n = 7) and non-pulsatile (n = 7) groups. After initiation of CPB, all animals were subjected to hypothermia for 25 minutes, reducing the rectal temperatures to 18°C, 60 minutes of DHCA followed by 10 minutes of cold reperfusion and 40 minutes of rewarming with a pump flow of 150 mL/kg/min. During cooling and rewarming, alpha-stat acid-base management was used. Differently labeled radioactive microspheres were injected pre-CPB, on normothermic CPB, pre-DHCA, post-DHCA, and after CPB to measure the regional and global cerebral, renal, and myocardial blood flows.

Results. Global cerebral blood flow was significantly higher in the pulsatile group compared to the non-pulsatile group at normothermic CPB (100.4 ± 6.3 mL/100 gm/min versus 70.2 ± 8.1 mL/100 gm/min, p < 0.05) and pre-DHCA (77.2 ± 5.2 mL/100 gm/min versus 56.1 ± 6.7 mL/100 gm/min, p < 0.05). Blood flow in cerebellum, basal ganglia, brain stem, and right and left cerebral hemispheres had an identical pattern with the global cerebral blood flow. Renal blood flow appeared higher in the pulsatile group compared to the non-pulsatile group during CPB, but the results were statistically significant only at post-CPB (94.8 ± 9 mL/100 gm/min versus 22.5 ± 22 mL/100 gm/min, p < 0.05). Pulsatile flow better maintained the myocardial blood flow compared to the non-pulsatile flow after CPB (316.6 ± 45.5 mL/100 gm/min versus 188.2 ± 19.5 mL/100 gm/min, p < 0.05).

Conclusions. Pulsatile perfusion provides superior vital organ blood flow compared to non-pulsatile perfusion in this model.

	Introduction

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Organ injury after hypothermic cardiopulmonary bypass (CPB) with conventional non-pulsatile perfusion with or without deep hypothermic circulatory arrest (DHCA) is still a significant clinical problem in children [1–4]. Although the mechanisms of organ injury (cerebral, renal, and myocardial) are not fully understood, the mode of perfusion (pulsatile versus non-pulsatile) may have significant impact on this process. Several investigators have demonstrated the physiologic benefits of pulsatile perfusion in neonates, infants, and small children, as well as in animal models, compared to the conventional non-pulsatile flow during and after CPB [5–7]. To date, however, pulsatile perfusion has received only limited acceptance in clinical pediatric cardiac surgery [8].

Although several pulsatile pumps (modified roller, piston actuated ventricle pumps, hydraulically driven pumps, and flat-plate compression pumps) have been designed for CPB support, only a few have been approved for clinical use [9]. Currently, a roller pump with a pulsatile module is the only type of pump used for clinical pulsatile CPB support in the United States. To date, there has been no investigation of the impact of the perfusion mode on regional and global vital organ blood flow with the Food and Drug Administration (FDA) approved pulsatile roller pump using microspheres during and after cardiopulmonary bypass in an infant model.

The purpose of this study was to investigate the effects of pulsatile (with an FDA approved modified roller pump) versus non-pulsatile flow on regional and global cerebral, renal, and myocardial blood flow using radionuclide-labeled microspheres, during and after cardiopulmonary bypass and deep hypothermic circulatory arrest, in a neonatal piglet model.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
Piglets, mean weight 3 kg, were used in pulsatile (n = 7) and non-pulsatile (n = 7) groups. All the animals received humane care as described in the "Guide for the Care and Use of Laboratory Animals" of the National Academy of Sciences, published by the National Institute of Health (NIH Publication No. 85–23, 1985). The Texas Heart Institute’s Institutional Animal Care and Use Committee has approved the research protocol for this study. St. Luke’s Episcopal Hospital’s Radiation Safety Committee has also approved the use of radiolabeled isotopes for this study. All experiments were performed at the Cullen Cardiovascular Surgical Research Laboratories of the Texas Heart Institute.

Animals were premedicated with intramuscular ketamine hydrochloride (20 mg/kg) and acepromazine maleate (1 mg/kg). After establishing an intravenous line, a 3 mm endotracheal tube was inserted for mechanical ventilation. Intravenous boluses of fentanyl citrate (100 µg/kg) and pancuronium bromide (0.3 mg/kg) were given. Anesthesia was maintained by a continuous fentanyl infusion at a rate of 100 µg/kg/hr and isoflurane (1% to 4%) through oxygenator gas inflow. After median sternotomy, the ascending aorta and the right atrium were cannulated with a 10 French DLP aortic cannula (Model #70010, DLP, Inc, Grand Rapids, MI) and 21 French single-stage venous cannula (Polystan A/S, Varlose, Denmark), respectively. The extracorporeal circuit was primed with heparinized fresh blood from a donor pig and Plasma-Lyte A solution (Baxter Healthcare Corporation, Deerfield, IL). Hematocrit was maintained at 20% to 25% during bypass. In addition to the Stöckert Caps non-pulsatile heart–lung machine (Stöckert, Munich, Germany), a pulsatile roller pump (Stöckert S3, Stöckert), a Capiox SX10 hollow fiber membrane oxygenator (Terumo Corp, Tokyo, Japan) and a Pall pediatric arterial filter (LPE-1440, Fajarou, Puerto Rico) were used. Pump rate was kept constant at 150 beats per minute (bpm) during pulsatile CPB. Pump base flow was set 30% (70% pulsatile and 30% non-pulsatile flow) and pump run time was maintained at 55% in all pulsatile experiments. Pump flow rate was maintained at 150 mL/kg/min in both pulsatile and non-pulsatile groups. An ultrasonic flow probe (T109, Transonic Systems, Inc, Ithaca, NY) was placed after the oxygenator to measure the blood flow. Arterial pH and PCO₂ were maintained at 7.35 to 7.45 and 35 to 45 mm Hg, respectively. In all experiments, phenoxybenzamine (1 mg/kg), a potent vasodilator and alpha-adrenergic blocker, was used at pre-CPB. During CPB, mean arterial pressures were maintained at 45 to 50 mm Hg by adding isoflurane through oxygenator gas inflow in both groups. A 40 cc dose of crystalloid cardioplegia (modified Kirklin solution) was manually administered into the ascending aorta at the beginning of DHCA. Animals were euthanized with intravenous boluses of Beuthanasia-D (0.22 mg/kg) at the end of each experiment.

Experimental design
After initiation of CPB, all animals were subjected to 25 minutes of hypothermia reducing the rectal temperature to 18°C, followed by 60 minutes of DHCA, then 10 minutes of cold reperfusion, and finally 40 minutes of rewarming. Animals were maintained on CPB a total of 100 minutes in addition to the 60 minutes of DHCA. Alpha-stat acid-base management technique was used during cooling and rewarming.

The radionuclide labeled microsphere technique was used to measure regional and global organ blood flows. Differently labeled isotopes with a 15 micron diameter (⁵¹Cr, ⁹⁵Nb, ¹⁴¹Ce, ⁸⁵Sr, ⁴⁶Sc, NEN Life Science Products, Boston, MA) were injected at pre-CPB (after heparin), on normothermic CPB (10 min on pump), pre-DHCA (18°C), post-DHCA (after 10 minutes of cold reperfusion and 40 minutes of rewarming), and finally post-CPB (30 minutes off pump) to measure organ blood flows. Before the injection of the microspheres, a vortex mixer (American Scientific Products, McGaw Park, IL) was also used to agitate the microsphere vial vigorously for 4 minutes. To break up the aggregations, the vial was then sonicated for 2 minutes. Then, the vial was agitated again for another minute, and 1 mL of microsphere suspension (~1 million microspheres) was withdrawn into a syringe for injection. A reference blood sample was withdrawn using a syringe pump (Model 351, Orion Research Inc, Boston, MA) starting 10 seconds before each injection for 2 minutes with a pump flow rate of 2 mL/min. Microspheres were injected into the left atrial catheter 15 minutes before and 30 minutes after CPB, and into the site of the arterial line 18 inches (40 cm) proximal to the aortic cannula during CPB. All animals were weaned from CPB. After the animals were euthanized, the entire brain, left kidney, and the heart were removed. The brain was dissected into cerebellum, basal ganglia and thalmus, brain stem, and right and left hemispheres, and placed into pre-weighted special tubes for gamma counting. Left ventricle and kidney were also separated and placed into pre-weighted tubes for gamma counting. Finally, all results were transferred to a personal computer via Excel 7.0 software (Microsoft Corp, Redmond, WA) for regional and global organ blood flow calculations.

Data acquisition
Waveforms were obtained for arterial pressure, pre-aortic cannula extracorporeal circuit pressure (ECCP), and pump flow at pre-CPB, on-CPB, pre-DHCA, post-DHCA, and post-CPB. At each data sampling point, recordings were made for 15 seconds at a rate of 360 samples per second. Data were obtained via WINDAQ data acquisition software (DATAQ Instruments, Akron, OH). Then, data were analyzed for systolic, diastolic, and mean arterial pressures, flow, pulse pressure, pre-aortic cannula ECCP, and pressure across the aortic cannula. Pressure drop across the aortic cannula was calculated by the subtraction of arterial pressure from pre-cannula extracorporeal circuit pressure.

Statistical analysis
The two-sided ANOVA with repeated measures was used for statistical analysis between pulsatile and non-pulsatile groups at five different stages. A p value less than 0.05 was considered statistically significant. All regional and global cerebral, renal, and myocardial blood flows were expressed as mean ± standard error of mean (SEM).

	Results

Top Abstract Introduction Material and methods Results Comment References

 
Piglet weights in both groups were 2.9 ± 0.1 kg. There were no differences in mean arterial pressure (MAP) pre-CPB, on-CPB, pre-DHCA, and post-DHCA periods. However, MAP was higher in the non-pulsatile group than in the pulsatile group after CPB (61.8 ± 2.9 mm Hg versus 48 ± 6.4 mm Hg, p = 0.08). Hemodynamic data of both pulsatile and non-pulsatile groups (mean arterial pressure, pulse pressure, pre-cannula extracorporeal circuit pressure, and the pressure drop of the aortic cannula) are presented in Table 1 and Figures 1 and 2. There were no differences between groups in temperature, arterial oxygen tension, arterial carbon dioxide tension, and hematocrit at any of the experimental stages.

View larger version (19K): [in this window] [in a new window]   Fig 1. Femoral artery pressure, pre-cannula extracorporeal circuit pressure, and pump flow during pulsatile cardiopulmonary bypass in a neonatal piglet.

View larger version (15K): [in this window] [in a new window]   Fig 2. Femoral artery pressure, pre-cannula extracorporeal circuit pressure, and pump flow during non-pulsatile cardiopulmonary bypass in a neonatal piglet.

Regional and global cerebral blood flow
There were no differences in regional or global cerebral blood flow at pre-CPB. Left and right cerebral hemisphere blood flows were significantly better maintained in the pulsatile group compared to the non-pulsatile group on normothermic CPB stage (on-CPB) and pre-DHCA. Both right and left cerebral hemisphere blood flows were higher after 60 minutes of circulatory arrest (post-DHCA) and after cardiopulmonary bypass in the pulsatile group than in the non-pulsatile group. Basal ganglia and thalmus, brain stem, and cerebellum blood flows were also significantly higher in the pulsatile group than in the non-pulsatile group at normothermic CPB and pre-DHCA. Blood flow in basal ganglia and thalmus, brain stem, and cerebellum was significantly diminished in the non-pulsatile group at normothermic CPB compared to the pre-CPB. However, pulsatile perfusion maintained very similar blood flows in these regions on normothermic CPB compared to the pre-CPB.

Regional cerebral blood flows were significantly diminished in both groups at pre-DHCA, post-DHCA, and post-CPB compared to the pre-CPB. Regional blood flows were not different at post-DHCA in either group. However, every region of the brain appeared to have higher blood flows in the pulsatile group than in the non-pulsatile group at post-CPB. A detailed analysis of these results is shown on Table 2.

View larger version (18K): [in this window] [in a new window]   Fig 3. Global cerebral blood flow during pulsatile versus non-pulsatile perfusion (mean ± SEM). *p < 0.05 pulsatile versus non-pulsatile groups; p < 0.05 versus pre-CPB within pulsatile group; p < 0.05 versus pre-CPB within non-pulsatile group. (CPB = cardiopulmonary bypass; DHCA = deep hypothermic circulatory arrest; NP = non-pulsatile; P = pulsatile).

View larger version (17K): [in this window] [in a new window]   Fig 4. Renal blood flow during pulsatile versus non-pulsatile perfusion (mean ± SEM). *p < 0.05 pulsatile versus non-pulsatile groups; p < 0.01 versus pre-CPB within pulsatile group p < 0.01 versus pre-CPB within non-pulsatile group. (CPB = cardiopulmonary bypass; DHCA = deep hypothermic circulatory arrest; NP = non-pulsatile; P = pulsatile).

View larger version (20K): [in this window] [in a new window]   Fig 5. Myocardial blood flow during pulsatile versus non-pulsatile perfusion (mean ± SEM). *p < 0.05 Pulsatile versus non-pulsatile groups; p < 0.05 versus pre-CPB within pulsatile group; p < 0.05 versus pre-CPB within non-pulsatile group. (CPB = cardiopulmonary bypass; DHCA = deep hypothermic circulatory arrest; NP = non-pulsatile; P = pulsatile).

	Comment

Top Abstract Introduction Material and methods Results Comment References

The membrane oxygenators and arterial cannulae also have significant effects on the quality of the pulsatility in neonatal models. It has been proven that the membrane structure of the oxygenator had a significant effect on the quality of the pulsatility. Flat-plate membrane oxygenators dampen the pulsatility more than hollow-fiber membrane oxygenators [15–17]. Since the aortic cannula diameter is smaller in neonates and infants, the geometry of the cannula is extremely important in producing adequate pulsatility. It has been shown that the shorter the tip of the cannula, the better the pulsatility [15]. The Capiox SX10 hollow fiber membrane oxygenator and a DLP short tip 10F aortic cannula were specifically chosen for this study because of their unique performance with pulsatile flow in our pilot experiments.

Several investigators have suggested that non-pulsatile perfusion is associated with microcirculatory dysfunction. Matsumoto and associates [18] has demonstrated that blood flow in capillaries was reduced with non-pulsatile perfusion compared with that which was obtained with pulsatile perfusion in dogs. They also noted that sludges in capillaries were always present when non-pulsatile flow was used. Takeda [19] has shown that pulsatile perfusion improved visceral microcirculation compared to the non-pulsatile perfusion in dogs. Lower total body oxygen consumption, lower pH, and greater base deficits were also observed with non-pulsatile flow [20]. Watanabe and associates [21] have proven that low-flow pulsatile CPB protects the brain better than non-pulsatile perfusion by increasing the safety margin of perfusion. It has also been shown that pulsatile perfusion improves cerebral blood flow, metabolism, oxygen delivery, and vascular resistance at 40 mm Hg of cerebral perfusion pressure (CPP) in neonatal piglets compared to the standard non-pulsatile perfusion after 60 minutes of DHCA [6]. However, there was no statistical significance in these parameters in either group when CPP was 55 mm Hg and 70 mm Hg. In a separate study, pulsatile flow with mean arterial pressures higher than 50 mm Hg improved myocardial blood flow after DHCA, but there were no differences in cerebral and renal blood flows between groups [7].

Chow and associates [22] could not show any benefits of pulsatile flow with three different pump rates in 40 children. During cardiopulmonary bypass, there were no differences in cerebral blood flow or hemoglobin concentration among groups. However, pulsatile flow was used only 15 minutes with three 5-minute intervals and different pump flow rates which was a limitation of the study. Hindman and associates have investigated the effects of the pulsatile perfusion during hypothermic CPB in a rabbit model [23]. No differences in regional brain perfusion were observed between pulsatile and non-pulsatile groups. However, the distal aorta was ligated and cannulated in a retrograde fashion. Hence, there was no visceral blood flow during CPB. Arterial pressures were also maintained above 70 mm Hg in the rabbit experiments. It has been proven that cerebral autoregulation is intact if the cerebral perfusion pressures are greater than 50 mm Hg [24]. Mean arterial pressures are significantly lower during clinical CPB in neonates and infants than in adults. Mean arterial pressures may be below 40 mm Hg during clinical hypothermic CPB in neonates and infants.

Although cerebral, renal, and myocardial blood flows were better maintained with this particular pulsatile roller pump than with a conventional non-pulsatile roller pump, the quality of the pulsatility with pulsatile roller pumps is significantly lower than other pulsatile pumps [25]. Currently, an experimental physiologic pulsatile pump (Medical Engineering Consultants, Bishop, CA) is being evaluated in our laboratory. This particular hydraulically driven dual-chamber physiologic pulsatile pump (without an FDA approval) produces physiologic pulsatile flow in our pilot experiments [26].

Future investigations are planned to compare the effects of the different pulsatile pumps and standard roller pumps on vital organ perfusion. In addition, different experimental protocols including pH-stat versus alpha-stat strategies and hypothermic CPB without a duration of circulatory arrest will also be performed in the near future.

In summary, pulsatile perfusion improves regional and global cerebral blood flow at normothermic CPB and pre-DHCA when compared to non-pulsatile perfusion at 45 to 50 mm Hg of mean arterial pressures. Renal blood flow was also preserved better with pulsatile perfusion during and post-CPB than in the non-pulsatile group. Pulsatile flow also improved myocardial blood flow at post-CPB. These data suggest that further investigation of the benefits of pulsatile perfusion in children is warranted.

	Acknowledgments

 
We thank William K. Vaughn, PhD, at the Texas Heart Institute for statistical analysis of these data. We also thank Maryann Mueller, CCP, Mary Claire McGarry, CCP, Rex Inman, BS, and Kathleen McKay for technical assistance during these experiments, and Betty Hornung and Harris Rose, BS, for their invaluable help during preparation of this manuscript.

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