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Ann Thorac Surg 2004;78:1999-2003
© 2004 The Society of Thoracic Surgeons

Original article: cardiovascular

Impaired Endothelial Function of the Umbilical Artery After Fetal Cardiac Bypass

Yasuhisa Oishi, MDa, Munetaka Masuda, MDa,*, Toru Yasutsune, MDa, Noriko Boku, MDa, Shigehiko Tokunaga, MDa, Shigeki Morita, MDa, Hisataka Yasui, MDa

a Department of Cardiovascular Surgery, Research Institute of Angiocardiology, Faculty of Medicine, Kyushu University, Fukuoka, Japan

Accepted for publication May 19, 2004.

* Address reprint requests to Dr Masuda, Department of Cardiovascular Surgery, Research Institute of Angiocardiology, Faculty of Medicine, Kyushu University, 3–1–1 Maidashi, Higashi-ku, Fukuoka, 812–8582, Japan
masudam{at}heart.med.kyushu-u.ac.jp


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Recently, endothelial dysfunction as a result of fetal cardiac bypass has been reported. Here, the effect of fetal cardiac bypass on the endothelial function of the umbilical artery was investigated by a tension study.

METHODS: Fourteen fetal lambs were divided into a control group (n = 7) and a pump group (n = 7). In the pump group, cardiac bypass was maintained for 30 minutes using a low-volume priming circuit with a centrifugal pump. Hemodynamic measurements and blood gas analyses were performed before, during, and 30 and 60 minutes after cardiac bypass. The umbilical artery was harvested 60 minutes after cessation of cardiac bypass. Endothelium-dependent relaxation (bradykinin, calcium ionophore A23187) and endothelium-independent relaxation (sodium nitroprusside) were measured after smooth muscle contraction by 60 mmol/L potassium or serotonin and compared between the two groups.

RESULTS: The umbilical artery flow and aortic pressure of the fetus were significantly decreased at 30 and 60 minutes after cardiac bypass. Hypoxia and hypercapnia were recognized during and after cardiac bypass. Metabolic acidosis progressed during and after cardiac bypass. Endothelium-dependent relaxation was impaired in the pump group compared with the control group (bradykinin: 43.6% ± 6.4% in the control group, 18.9% ± 2.5% in the pump group, p < 0.01; A23187: 37.8% ± 4.6% in the control group, 19.6% ± 3.9% in the pump group, p < 0.01). Meanwhile, endothelium-independent relaxation was preserved in both groups.

CONCLUSIONS: Fetal cardiac bypass caused endothelial dysfunction of the umbilical artery and hemodynamic deterioration as a result of metabolic acidosis. Prevention of endothelial damage and metabolic acidosis could be the main target for successful fetal cardiac surgery.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
As a result of the development of fetal echocardiography, congenital cardiac anomalies can be precisely diagnosed prenatally. Certain lesions that are present at birth with complex morphologic cardiac defects are considered to be the result of a relatively simple primary lesion that subsequently develops complex secondary lesions during gestation. This hypothesis is based on the "flow-related theory of cardiac development" [1]. In some congenital heart lesions, intervention in utero may result in better outcomes than current neonatal or infant repair procedures. However, it is necessary to establish the safety of fetal cardiac bypass to perform surgical repair on fetuses.

Since the first report of fetal cardiac bypass by Bradley and colleagues in 1992 [2], several investigators have tried to elucidate the pathophysiologic responses of the fetal circulation. Fetal cardiac bypass induces placental dysfunction, which is characterized by elevation of the fetal partial carbon dioxide pressure (PCO2), progressive acidosis, and elevation of placental vascular resistance. Some investigators have tried to improve the hemodynamics and gas exchange after fetal cardiac bypass using several interventions [3–8]. Recently, the role of the endothelium of the fetal vasculature has been reported [9, 10]. Reddy and colleagues [9] showed that the response of the umbilical arterial flow to direct vasodilator injection deteriorated after fetal cardiac bypass. Vedrinne and colleagues [10] reported that pulsatile bypass flow preserved endothelial nitric oxide (NO) synthesis more efficiently than nonpulsatile flow. Both studies suggested that impairment of the endothelium resulted in deterioration of the fetal circulation; however, this has not yet been fully elucidated. Thus, we investigated whether the endothelium of the umbilical artery was impaired by fetal cardiac bypass using a vessel tension study method, which has previously been used to investigate the function of the endothelium [11–13].


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Animal Care
Fourteen pregnant ewes between 120 and 136 days' gestation were used in the present study. The protocols were reviewed by the Ethics Committee on Animal Experiments in the Faculty of Medicine, Kyushu University, and carried out under the Guidelines for Animal Experimentation in the Faculty of Medicine, Kyushu University and in accordance with the law (No.105) and notification (No.6) of the Japanese government.

Maternal Anesthesia and General Preparation
Ewes were anesthetized with ketamine (Ketaral; Sankyo, Tokyo, Japan; 10 mg/kg intramuscularly). After endotracheal intubation, ewes were artificially ventilated with 100% oxygen. The minute volume of ventilation was adjusted to maintain the maternal arterial PCO2 between 35 and 45 mm Hg. Anesthesia was maintained with inhaled isoflurane (Forane; Abbott, North Chicago, IL). A double-lumen catheter was inserted into the jugular vein for intravenous infusion. After the cannulation, ritodrine hydrochloride (Utemerin; Kissei, Nagano, Japan) was dripped at a dose of 3 mg/h to prevent excess movement of the uterus during the experiment. An arterial catheter was inserted into the carotid artery to monitor the arterial pressure and to take blood samples for analysis of blood gases, electrolytes, and pH.

Fetal Surgical Procedure and Cardiac Bypass
After exposure of the uterus through a midline laparotomy, a longitudinal hysterotomy was performed. A 14-mm ultrasonic flow probe connected to a flowmeter (model T106; Transonic Systems, Inc, New York, NY) was positioned around the umbilical artery. Twenty-two-gauge catheters were inserted into the jugular vein for intravenous infusion and the common carotid artery for blood pressure monitoring and blood sampling. After a midline sternotomy and longitudinal pericardiotomy, the heart was exposed. Systemic heparin (approximately 300 U/kg) was administered to the fetus. The pulmonary artery trunk was cannulated with an 8Fr straight arterial cannula (RMI FEM; Medtronic, Minneapolis, MN). The right atrium was cannulated with a 16Fr angled-tip venous cannula (Stöckert, Munich, Germany).

The bypass circuit in the present study consisted of a low-priming centrifugal pump (HPM-24; NIKKISO, Tokyo, Japan), a soft venous reservoir (priming volume, 20 mL; Senko Medical, Tokyo, Japan), and a 1/4-inch diameter tube. The total priming volume was 200 mL. A heat exchanger was not used to minimize the priming volume. Instead, a halogen heater was used to maintain the body temperature of the fetuses. The circuit was primed with acetate Ringer's solution (Veen D; Nikken Medical, Tokyo, Japan) and heparin. No maternal blood was transfused to the fetus during the experiment.

Protocol 1: Measurement of Hemodynamics and Blood sample Analyses
Fourteen fetal lambs were used for protocol 1. Arterial pressure and umbilical artery flow were continuously monitored. After arterial and venous cannulation, baseline blood sampling was performed. The fetuses were then divided into two groups. Seven animals served as the control group. The control fetuses were sacrificed just after cannulations. The remaining 7 animals underwent cardiac bypass (pump group). Cardiac bypass was conducted for 30 minutes, and bypass flow was maintained at 1 L/min (approximately 300 mL · kg–1 · min–1). This flow rate was chosen on the basis of previous reports to maintain the placental oxygenating function [5, 6].

Blood sampling from the carotid artery for measuring arterial oxygen saturation (SaO2), arterial PCO2, and plasma lactate concentration was performed at 15 and 30 minutes during cardiac bypass, and at 30 and 60 minutes after cessation of cardiac bypass. We did not perform any substitution administration including calcium chloride and sodium bicarbonate during the protocol.

Protocol 2: Endothelial Function
After completion of protocol 1, we immediately isolated the umbilical artery and preserved it in ice-cold modified Krebs solution (pH 7.4). The composition of modified Krebs solution was as follows (in mmol/L): NaCl, 121.3; KCl, 4.7; NaHCO3, 24.7; KH2PO4, 1.2; MgSO4, 1.2; CaCl2, 1.25; D-glucose, 5.8. Arterial segments were cleaned of adherent connective tissue and opened longitudinally. The segments were cut into 1- to 2-mm wide strips. The endothelium was left intact, and each strip was mounted in an individual 30-mL isolated organ chamber filled with 37°C Krebs solution. The strip was connected to an isometric force transducer (NEC, Tokyo, Japan), and the contractile response was recorded with a MacLab 8E (ADInstruments Pty Ltd, Castle Hill, NSW, Australia) and stored on a Power Macintosh 5300C computer (Apple Computers Inc, Cupertino, CA). After equilibration in the organ chamber, each strip was stretched to the optimal resting tension as determined by the tension that developed in response to 60 mmol/L potassium (K) added at each stretch level. For relaxation studies, the strips were precontracted with 60 mmol/L K or serotonin (5-HT, 10–6 M), and then bradykinin (BK, 10–6 M), calcium ionophore (A23187, 10–6 M), and sodium nitroprusside (SNP, 10–6 M) were applied individually. The concentrations of vasodilators were determined from previous reports [11, 12] and our preliminary study to obtain the maximum relaxation response.

Statistical Analysis
Data are presented as the mean ± standard error of the mean. Intragroup comparisons were achieved using the Student's t test or one-way analysis of variance followed by the Dunnett test. A p value less than 0.05 was considered statistically significant. Statistical analysis was performed using the StatView 5.0 software package (SAS Institute, Cary, NC).


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
During fetal cardiac bypass, umbilical artery flow, mean arterial pressure, and heart rate were well maintained. However, these were significantly decreased at 60 minutes after cardiac bypass compared with their baseline values (umbilical artery flow, 100 to 22.1% ± 11.4%; mean arterial pressure, 59.8 ± 4.4 to 22.0 ± 7.5 mm Hg; heart rate, 178.5 ± 11.5 to 96.4 ± 43.7 beats/min; Fig 1).



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  		Fig 1. Changes in (a) umbilical artery flow (UAF), (b) mean aortic pressure (mAoP), and (c) heart rate (HR). The percent changes in umbilical artery flow, mean aortic pressure, and heart rate are maintained during fetal cardiac bypass, but all the variables are significantly decreased at 30 and 60 minutes after cessation of cardiac bypass. *p < 0.01 versus baseline; #p < 0.05 versus baseline.

 
Hypoxia and hypercapnia occurred during cardiac bypass despite mechanical flow support. These deterioration responses progressed after cessation of cardiac bypass (Fig 2). Metabolic acidosis was recognized during and after cardiac bypass, which was manifested by the decline in pH and base excess (Fig 2). Plasma lactate level was gradually elevated during and after cardiac bypass, and reached statistical significance between baseline and after cardiac bypass (24.4 ± 3.0 mg/dL at baseline to 77.4 ± 10.7 mg/dL at 30 minutes and 95.3 ± 5.3 mg/dL at 60 minutes after cardiac bypass; Fig 2).



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  		Fig 2. Changes in pH, partial carbon dioxide pressure (PCO2), partial oxygen pressure (PO2), arterial oxygen saturation (SaO2), base excess (BE), and plasma lactate level in the fetuses in the pump group. *p < 0.01 versus baseline; #p < 0.05 versus baseline.

 
The tension study revealed impairment of the endothelium-dependent response of the umbilical artery after fetal cardiac bypass. The percent relaxation induced by BK during 60 mmol/L K-induced or 5-HT-induced contraction was significantly decreased after cardiac bypass (60 mmol/L K: control group 42.7% ± 3.7%, pump group 23.0% ± 3.6%, p = 0.0023; 5-HT: control group 43.6% ± 6.4%, pump group 18.9% ± 2.5%, p = 0.0022; Fig 3). The percent relaxation induced by A23187 during contraction by 60 mmol/L K or 5-HT was also significantly decreased after cardiac bypass (60 mmol/L K: control group 53.8% ± 6.9%, pump group 20.9% ± 3.6%, p = 0.0011; 5-HT: control group 37.8% ± 1.5%, pump group 19.6% ± 3.9%, p = 0.0093; Fig 3). On the other hand, the percent relaxation induced by SNP during contraction by 60 mmol/L K or 5-HT was not impaired after fetal cardiac bypass (60 mmol/L K: control group 104.8% ± 2.6%, pump group 95.5% ± 3.7%; 5-HT: control group 96.3% ± 3.7%, pump group 89.7% ± 5.6%; Fig 3).



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  		Fig 3. (Top) Percent relaxation induced by bradykinin, calcium ionophore (A23187), and sodium nitroprusside (SNP) after contraction by potassium chloride (KCl, 60 mmol/L) in the control group (black bars) and the pump group (gray bars). (Bottom) Percent relaxation induced by bradykinin, calcium ionophore, and sodium nitroprusside after contraction by serotonin (5-HT) in the control group (black bars) and the pump group (gray bars).

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
It is well known that fetal cardiac bypass induces placental dysfunction, which is manifested by hypercapnia and metabolic acidosis of the fetus [2–10, 14–19]. The mechanism of placental dysfunction has been discussed in several studies, for example, shortage of placental blood flow [5], hypothermia [14], cytokines [20], neutrophils [21], NO [3, 10, 16, 18], and endothelin-1 [9, 10]. Recently, impairment of the vascular endothelium has been reported. Reddy and colleagues [9] showed that the response of the umbilical artery to an endothelium-dependent vasodilator deteriorated after fetal cardiac bypass, by direct injection of vasodilators. On the other hand, the response to an endothelium-independent vasodilator was not altered. Vedrinne and colleagues [10] reported that a pulsatile bypass flow preserved endothelial NO synthesis more efficiently than a steady flow. They suggested that the NO biosynthetic mechanism played an important role in fetal circulation. Both studies suggested that endothelial damage could be an important mechanism of placental dysfunction after fetal cardiac bypass, although this remained speculative.

We used a tension study to determine whether the endothelium was impaired after fetal cardiac bypass. This is a well-established method for investigating vascular endothelial function [11–13]. Bradykinin induces receptor-dependent NO release from the endothelium and causes endothelium-dependent relaxation of the vascular smooth muscle [22]. On the other hand, A23187 induces receptor-independent NO release and endothelium-dependent relaxation [11]. In the present study, both BK-induced and A23187-induced relaxations were impaired after fetal cardiac bypass. These findings support the hypothesis that the reduced NO release response is caused by impairment of the endothelium itself. Champsaur and associates [18] and Vedrinne and colleagues [10] suggested the contribution of impaired NO release as an important mechanism of hemodynamic deterioration after fetal cardiac bypass. We directly proved the contribution of NO and endothelial damage to the fetal circulation as a result of fetal cardiac bypass in this tension study.

We determined the bypass flow rate (300 mL ·kg–1 · min–1) on the basis of a previous report [5, 6], which did not affect placental function during cardiac bypass. In the present study, we could maintain the umbilical artery flow during cardiac bypass at the baseline level. However, hypercapnia, hypoxia, metabolic acidosis, and lactate elevation were recognized, even during cardiac bypass. This implies that the bypass flow rate itself cannot be the cause of the placental dysfunction after fetal cardiac bypass. This flow rate was possibly insufficient to maintain placental function.

It is well known that cardiac bypass itself can induce several inflammatory responses. Parry and coworkers [21] and Reddy and colleagues [20] reported increases in fetal plasma C3a and IL-6, respectively, after fetal cardiac bypass. In addition, it was reported that indomethacin [7] and high-dose steroids [8] could suppress placental dysfunction after fetal bypass. We speculate that inflammatory responses induced by cardiac bypass could cause the vascular endothelial dysfunction of the fetoplacental system. This endothelial damage could cause impairment of NO synthesis, which induces the increase in placental vascular resistance and may decrease umbilical artery flow. Such a response of the fetoplacental unit could lead to fetal hypoxia and acidosis. Further studies avoiding the inflammatory response and endothelial dysfunction during fetal cardiac bypass are necessary.

We gave ritodrine hydrochloride to the ewe as a uterine relaxant. Ritodrine hydrochloride is known to have some effects on fetal hemodynamics. Rasanen [23] reported that ritodrine hydrochloride increased fetal heart rate; however, it did not cause any unfavorable changes in fetal myocardial function and blood flow in the umbilical artery. Thus, we decided to use ritodrine hydrochloride to avoid unfavorable contraction of the uterus. We thought that the effect of ritodrine on the fetus in this study was less than the effect of cardiac bypass.

We used acetate Ringer's solution for priming of the circuit because fetal hemoglobin is different from adult hemoglobin in its affinity for oxygen. In fact, the hemoglobin level was decreased to 80% of baseline values after cardiac bypass (11.2 ± 0.5 g/dL to 9.0 ± 0.6 g/dL). Mari and colleagues [24] reported that intravascular transfusion to human fetuses with severe red-cell alloimmunization increased fetal hematocrit and flow velocity of the umbilical artery. We have no data concerning the effect of hemodilution in the level of our study. In the clinical situation, development of fetal blood transfusion might be important.

This study has some important limitations. In the present study, we used single doses of BK, A23187, and SNP rather than constructing dose-response curves. The concentrations of A23187 and SNP were based on previous reports [11, 12], which induced sufficient relaxations of the ovine uterine and human umbilical arteries. The concentration of BK was determined to induce maximum relaxation of the ovine umbilical artery in our preliminary study (data not shown).

In conclusion, the present study demonstrated fetal hemodynamic deterioration and placental dysfunction after fetal cardiac bypass. Such responses could be the result of impairment of the endothelium, which induces a decrease in NO release. Avoidance of the inflammatory response during fetal cardiac bypass would be a key to improving the results of this procedure.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This study was supported by a Grant-in-Aid for Scientific Research (13671868) from the Ministry of Education, Science and Culture of Japan. The authors thank Emi Takayama and Aki Takao for valuable technical assistance.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Hanley FL. Fetal cardiac surgery. Adv Card Surg. 1994;5:47–74[Medline]
  2. Bradley SM, Hanley FL, Duncan BW, et al. Fetal cardiac bypass alters regional blood flows, arterial blood gases, and hemodynamics in sheep. Am J Physiol. 1992;263:H919–928[Medline]
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