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Ann Thorac Surg 2001;72:401-407
© 2001 The Society of Thoracic Surgeons
a Division of Pediatric Cardiothoracic Surgery, Children’s Hospital of Pittsburgh, University of Pittsburgh, Pittsburgh, Pennsylvania, USA
Address reprint requests to Dr Pigula, Pediatric Cardiothoracic Surgery, Room 2820, 2 Main, Children’s Hospital of Pittsburgh, Pittsburgh, PA 15213
e-mail: pigulaf{at}heart.chp.edu
Presented at the Thirty-seventh Annual Meeting of The Society of Thoracic Surgeons, New Orleans, LA, Jan 29–31, 2001.
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Abstract |
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Methods. Fifteen neonates undergoing arch reconstruction with regional perfusion were studied. Three techniques were used to assess somatic perfusion: abdominal aortic blood pressure, quadriceps blood flow (near-infrared spectroscopy), and gastric tonometry.
Results. Twelve patients required operation for hypoplastic left heart syndrome, and 3 required arch reconstruction with a biventricular repair. There was one death (7%). Abdominal aortic blood pressure was higher (12 ± 3 mm Hg versus 0 ± 0 mm Hg), and quadriceps blood volumes (5 ± 24 versus -17 ± 26) and oxygen saturations (57 ± 25 versus 33 ± 12) were greater during regional perfusion than during deep hypothermic circulatory arrest (p < 0.05). During rewarming, the arterial–gastric mucosal carbon dioxide tension difference was lower after circulatory arrest than after regional perfusion (-3.3 ± 0.3 mm Hg versus 7.8 ± 7.6 mm Hg, p < 0.05).
Conclusions. Regional low-flow perfusion provides somatic circulatory support during neonatal arch surgical procedures. Support of the subdiaphragmatic viscera should improve the ability of neonates to survive the postoperative period.
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Introduction |
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Material and methods |
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In the case of biventricular repairs, a graft (3.5-mm Gore-Tex; W. L. Gore and Associates, Flagstaff, AZ) is anastomosed to the innominate artery in a manner identical to that for placement of a Blalock-Taussig shunt. However, the shunt serves as the primary cannulation site and is unchanged for the duration of the operation. After separation of the patient from cardiopulmonary bypass, the graft is clipped flush with the innominate artery and the stump, oversewn.
All operations were performed using deep hypothermia (18°C) and alpha-stat management. The RLFP rate was guided by near-infrared spectroscopy (NIRS) with the goal of maintaining cerebral blood volumes at baseline levels (obtained on full-flow hypothermic cardiopulmonary bypass). Assessment of somatic perfusion was performed in three ways: abdominal aortic blood pressure was measured with an umbilical artery catheter; quadriceps muscle blood volumes and saturations were measured with NIRS; and visceral perfusion was assessed by measuring the arterial-mucosal carbon dioxide tension (PCO2) gradient (PCO2 gap) in the stomach using gastric tonometry.
Monitoring and data acquisition
Standard hemodynamic monitoring was applied to all children. Arterial blood pressure was measured simultaneously by a left radial artery catheter and an umbilical artery catheter (placed preoperatively for resuscitation and monitoring). After informed consent was obtained from the parents, all children underwent intraoperative monitoring of relative cerebral blood volumes and oxygen saturations using NIRS (INVOS 5100; Somanetics Corp, Troy, MI) [2]. These data have been reported previously and were used to guide the RLFP rate [2]. A NIRS sensor was placed on the quadriceps muscle to measure relative muscle oxygenation and relative quadriceps muscle blood volume index. Data were downloaded and stored for later analysis.
After the induction of anesthesia, a gastrointestinal tonometer catheter (Instrumentarium Corp, Helsinki, Finland) was placed in the stomach and attached to the tonometer (Tonometrics Corp, Helsinki, Finland). Gastric mucosal PCO2 was automatically measured at 10-minute intervals and recorded. Simultaneous arterial blood gases were obtained from the radial artery, and the arterial–gastric mucosal PCO2 gap was calculated.
Statistical analysis
Data are presented as the mean ± the standard deviation unless otherwise stated. Evaluation of continuous variables was performed using analysis of variance for repeated measures, and significance was assumed when the value of P was less than 0.05.
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Results |
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During RLFP, the mean left radial artery blood pressure was 29 ± 5 mm Hg, and the mean abdominal aortic blood pressure was 12 ± 3 mm Hg. Paired arterial blood gas data (obtained simultaneously from the radial and umbilical artery catheters) were comparable (radial: pH 7.4; PCO2, 29 mm Hg; oxygen tension, 194 mm Hg; the bicarbonate radical, 19.2; and lactate, 5.1 mmol/L; and umbilical: pH 7.39; PCO2, 29 mm Hg; oxygen tension, 133 mm Hg; the bicarbonate radical, 19.1; and lactate, 5.4 mmol/L).
Quadriceps data were obtained by NIRS for all 15 patients. Quadriceps muscle blood volumes and quadriceps saturations were measured on full-flow hypothermic cardiopulmonary bypass, during the brief period of DHCA required for atrial septectomy and shunt cannulation (for those children undergoing a Norwood operation), and during RLFP (Fig 1). The data showed a significant increase in both relative blood volume index and oxygenation in the quadriceps muscle during RLFP compared with values obtained during the short period of DHCA (mean duration, 9 ± 4 minutes). In fact they approximated the values obtained during full-flow hypothermic cardiopulmonary bypass (Table 2).
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Comment |
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Low-flow perfusion is one such alternative. Its advantages, identified in the Boston Circulatory Arrest Study [6], include better neurologic outcomes in neonates compared with the results in patients undergoing repair during DHCA. Low-flow perfusion, a well-described technique, has been applied during operations for other forms of congenital heart disease, such as tetralogy of Fallot, and has been important in the efforts to perform earlier anatomic cardiac repairs [7].
Regional low-flow perfusion differs from "conventional" low-flow perfusion, as described in the Boston study [6], in two important ways. First, cannulation is regional rather than central, and is accomplished through a perfusion conduit (shunt) anastomosed to the innominate artery. This is required in children with aortic arch hypoplasia, as the diminutive aorta precludes standard arterial cannulation. Second, whereas "conventional" low-flow perfusion maintains a cardiac index of 0.75 L · min-1 · m-2, the flow rates required to support the neonate using RLFP are substantially lower (cardiac index of 0.45 L · min-1 · m-2). This assertion is based on our earlier studies [2] showing baseline cerebral blood saturations and blood volumes are obtained at this flow rate. Because NIRS allows real-time assessment of the cerebral circulation, flows can be optimized to maintain those obtained at baseline (defined as full-flow cardiopulmonary bypass). Thus, the "incomplete ischemia" postulated to occur during "conventional" low-flow perfusion may be avoided [8].
During RLFP (30 to 40 mL · kg-1 · min-1 for a cardiac index of 0.45 L · min-1 · m-2), the mean left radial artery blood pressure was 29 mm Hg with a mean abdominal aortic blood pressure of 12 mm Hg. These findings support the speculation that in the neonate, there is an extensive network of vascular collaterals traversing the relatively short spatial distance between the supradiaphragmatic and subdiaphragmatic vasculature. These collaterals may include the internal mammary arteries and the intercostal arteries, as well as unnamed muscular and cutaneous connections. This degree of collateralization is clinically apparent by the extremely low incidence of paraplegia among neonates undergoing repair of aortic coarctation.
Near-infrared spectroscopy, a recent noninvasive technology capable of measuring tissue chromophores, exploits the differences in absorption peaks between oxygenated and deoxygenated hemoglobin and provides information on the changes in these compounds over time [9]. Thus, relative changes in oxygen saturations and blood volumes are obtainable [10]. In this study, we used NIRS to provide information on the relative blood volumes and saturations in the quadriceps muscle.
Validation of this technique in skeletal muscle has been pursued clinically and experimentally. Edwards and colleagues [11] reported a good correlation between NIRS and venous occlusion plethysmography in the human forearm. Experimentally, Tran and associates [12] performed a comparative analysis of nuclear magnetic resonance and NIRS measurements of intracellular oxygen tension in human skeletal muscle and reported that the NIRS signals closely match the desaturation kinetics of myoglobin. They concluded that skeletal muscle (gastrocnemius) NIRS largely reflects the change in oxymyoglobin and deoxymyoglobin rather than hemoglobin. This conclusion would do little to alter the interpretation of limb ischemia. Indeed, an assessment of tissue, rather than hemoglobin oxygenation, would provide a superior assessment of the adequacy of blood flow.
With this experience, the use of NIRS in the assessment of limb blood flow is increasingly common in the clinical setting [13]. Kooijman and coworkers [14] found that NIRS is an effective noninvasive method for assessing the oxygen debt in the lower extremities of patients with peripheral vascular disease. Komiyama and associates [15] recently suggested that NIRS grades the severity of intermittent claudication in diabetics more accurately than the ankle–brachial pressure index.
In this study, quadriceps NIRS recorded increasing muscle blood volumes and saturations about 5 minutes after the initiation of RLFP (see Fig 1). This delay probably represents the time required for blood to traverse the collateral vascular beds between the point of delivery (supradiaphragmatic) to the subdiaphragmatic aorta. These NIRS data are consistent with our observations of aortic backbleeding and a mean blood pressure of 12 mm Hg in the abdominal aorta during RLFP.
Finally, because the role of gastrointestinal ischemia in the development of sepsis and multiorgan dysfunction is well established, we thought it important to assess the physiological importance of splanchnic blood flow provided by RLFP. Gastric tonometry is a technique that measures the gastric mucosal PCO2 by way of a balloon-tipped catheter inserted into the stomach. There is evidence to suggest that increases in gastric mucosal PCO2 relative to arterial PCO2 (the PCO2 gap) are both sensitive and specific for the detection of gut ischemia [16, 17]. This phenomenon is thought to reflect two separate but related pathophysiological processes; carbon dioxide accumulation as a consequence of impaired blood flow or as a result of increased CO2 production under anaerobic conditions [18]. Although studies defining the precise PCO2 gap indicative of mucosal ischemia are lacking, Duke and associates [19] reported that among patients receiving pediatric extracorporeal membrane oxygenation, survivors had a significantly smaller PCO2 gap (-4.7) than did nonsurvivors (-24) (p = 0.003). Furthermore, animal studies [18] examining the linkage between blood flow reduction and PCO2 have shown that there appears to be a critical lower limit of blood flow (approximately a 60% reduction) below which there is a sudden rise in gastric mucosal PCO2.
Thus, we employed gastric tonometry to detect differences in gastric mucosal PCO2 after repair during DHCA or RLFP. Although the 3 patients having repair during DHCA presented with a slightly negative (gastric greater than arterial) PCO2 gap, it was mild (-0.5 mm Hg) and may reflect the fact that these tended to be older patients with medically refractory congestive heart failure. During cooling on bypass, the PCO2 gap was similar between the two groups. During rewarming, patients exposed to DHCA experienced a negative PCO2 gap (gastric mucosal PCO2 higher than arterial PCO2), whereas those having operation during RLFP did not (see Fig 2). Gastric mucosal hypercarbia identified in children undergoing repair during DHCA suggests an ischemic event not seen in patients supported with RLFP.
Although the value of statistical conclusions drawn from small samples is uncertain, we prefer to perform neonatal repairs during RLFP whenever possible. In practical terms, DHCA is now generally confined to the repair of obstructed total anomalous pulmonary venous return. Despite the small sample size, our data are consistent with the blood pressure and NIRS data and support the contention that RLFP provides significant subdiaphragmatic circulatory support during arch reconstruction.
Support of the subdiaphragmatic viscera would be noteworthy because substantial morbidity and mortality resulting from noncardiac-related organ failure or sepsis occur in the postoperative period. Poirier and coauthors [20] reported their experience with 59 neonates undergoing the Norwood operation for hypoplastic left heart syndrome or its variants. The median DHCA time was 37 minutes, and the early postoperative survival rate was 83%. Postoperative sepsis (not otherwise specified) occurred in 13 patients, necrotizing enterocolitis in 1 patient, and seizures in 1 patient. Clancy and colleagues [5] reported a survival rate of 84% among 318 neonates undergoing a variety of one- and two-ventricle repairs during DHCA. Among the 52 deaths, 24 (46%) occurred between 3 and 35 days postoperatively, when mortality is generally secondary to causes other than overt inadequacy of the hemodynamic repair. These studies would support the position that any postoperative organ dysfunction, be it renal, gut, or hepatic, can erode the already precarious clinical situation of a recovering neonate.
Overall survival (30-day and hospital discharge) for patients undergoing repair with RLFP was 93% (14/15). The subgroup of 12 neonates undergoing a Norwood operation with RLFP had a 92% survival rate (11/12), and all 3 children undergoing biventricular repair survived. The results in this small cohort compare favorably with those in published series, but factors other than the use of RLFP bear consideration [21, 22]. Postoperative management, directed at reducing fluctuations in pulmonary vascular resistance, may also be important.
From these data, we conclude that RLFP provides significant somatic circulatory support during neonatal aortic arch surgical procedures. Circulatory support of the subdiaphragmatic viscera should improve the ability of neonates to survive the postoperative period. These results complement those in our previous report [2] documenting cerebral circulatory support in neonates and justify the conclusion that RLFP truly reduces DHCA time during neonatal aortic arch operations. Furthermore, this modification of low-flow perfusion is applicable to most, if not all, forms of congenital heart disease.
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Discussion |
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What is very interesting in support of your findings is that when you remove the clamp from the descending thoracic aorta, you literally get flooded with backbleeding from the lower-body circulation.
My question is whether you have tried to quantify how much of the flow in the innominate artery reaches the cerebral circulation and how much ends up perfusing the lower body?
DR PIGULA: No, we have not done that, and actually we were talking about it last night. I suppose it is possible to get some idea if you can quantify the return from the inferior vera cava versus, the superior vera cava. That is manageable; we just have not pursued it.
DR TCHERVENKOV: The flow rates we have used clinically are somewhat higher than yours. They range from 0.23 to 1 L · min-1 · m-2, which works out to somewhere between 20 and 60 mL · kg-1 · min-1. I wonder if there is an upper limit of perfusion above which one might actually be doing damage to the brain. Do you have a sense of what the upper limit of regional perfusion flow is within the safe margin?
DR PIGULA: I do not have a sense of what the upper limit is, but I admit we have liberalized our flows a little bit. With flow at 30 to 40 mL · kg-1 · min-1, we check the left radial artery blood pressure often. I did not show those data. With this technique, when there is a descending aortic of 12 mm Hg, there is a left radial artery pressure of 25 mm Hg. So I usually try to maintain a mean left radial artery pressure of 25 to 30 mm Hg.
MR JAMES L. MONRO (Southampton, UK): Congratulations on a very nice study. It is important to know that the perfusion of the lower part of the body is good, but it is the brain about which we are particularly concerned.
If I understood correctly, 3 of your patients did not have a hypoplastic heart, and they had rather longer circulatory arrest times. Were you perfusing the right innominate artery? A trick my associates and I have used is to slide the aortic cannula up and snug it. When doing a hypoplastic correction, you use the shunt you have already placed. I do not understand how you did it in the 3 patients without a hypoplastic left heart.
DR PIGULA: With the biventricular repairs, I sewed a shunt to the innominate artery and cannulated that directly as the primary cannulation site. These 3 patients had longer circulatory arrest times because, at some points, it was more trouble technically doing the intracardiac portions of the repair and the ventricular septal defect closures in the operative field than I thought it was worth. So we did resort to some circulatory arrest time in those patients.
MR MONRO: As I understood it, you cannulated the innominate artery directly?
DR PIGULA: No, I sewed in a Gore-Tex graft, as in anticipation of a Blalock-Taussig shunt, and cannulate the Gore-Tex graft.
MR MONRO: But if you are not doing a shunt, my point is that you can use the DLP cannulas. You put one in the ascending aorta, and then when you want to do the anastomosis, you just slide it up and snug it.
DR ERLE H. AUSTIN (Louisville, KY): I enjoyed your presentation, and I thank you for helping introduce this technique of regional low-flow perfusion that allows us to do arch reconstruction without circulatory arrest. We have been using your technique for the past 2 years, and it has virtually eliminated the use of circulatory arrest in my practice.
However, a note of caution, based on my own anecdotal experience with this technique, is warranted. This note refers to the point of your presentation that suggests that during regional flow to the cerebral circulation, adequate flow is occurring to the subdiaphragmatic organs. In our experience, by placing one end of the shunt on the innominate artery prior to initiating bypass and using the shunt for all the arterial inflow, we were able to perform the operation without any period of circulatory arrest. We were comfortable with the technique but wondered whether or not we needed to cool the infant to 18°C. Therefore, for several patients, we decided to cool to no lower than 25°C to shorten the time it takes to rewarm. Doing this resulted in a relatively expeditious operation with good cerebral protection. However, we also noted that these patients had impaired, postoperative renal function with several days of oligúria that was unresponsive to diuretics, a situation that can be a problem postoperatively in such children.
After seeing this in 3 consecutive patients, we hypothesized that failing to cool the patient to less than 20°C may have contributed to the renal dysfunction. Subsequently, we have gone back to using deep hypothermic levels until reconstruction is completed and flow is restored to the descending aorta. Since then, we have noted no problems with postoperative renal function.
I recognize this is not very scientific, but I thought our experience might indicate that temperature is also an important factor in preserving the integrity of the subdiaphragmatic organs such as the kidneys.
DR PIGULA: I think that is a very important observation. Clearly, we are not providing physiologic blood flow necessarily, and we have to bear in mind that it is a supply–demand, issue. The demands at lower temperatures are much less than they are at the higher temperatures.
DR Tom R. KARL (Philadelphia, PA): I really enjoyed the presentation. This was a nicely thought-out strategy. As more of us adopt this technique, in your opinion, what sort of data should we be collecting prospectively to prove that it is better than circulatory arrest?
DR PIGULA: I have thought a bit about that. Mortality is a very crude assessment, and I think if we make a difference between an 80% survival rate and a 90% survival rate, it will take a lot of patients to try to prove a difference. In my estimation, the most important thing is to assess the developmental outcomes in these patients, even though new developmental assessments are fraught with difficulties.
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