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Original Articles: Pediatric Cardiac

Can the Kawashima Procedure Be Performed in Younger Patients?

Division of Cardiothoracic Surgery, Childrens Hospital Los Angeles, Keck School of Medicine, University of Southern California, Los Angeles, California

Accepted for publication April 14, 2009.

^_* Address correspondence to Dr Wells, Childrens Hospital Los Angeles, Division of Cardiothoracic Surgery, 4650 Sunset Blvd, MS 66, Los Angeles, CA 90027 (Email: wwells{at}chla.usc.edu).

Presented at the Forty-fifth Annual Meeting of The Society of Thoracic Surgeons, San Francisco, CA, Jan 26–28, 2009.

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 
Background: The prudence of performing early palliative cavopulmonary connection that includes superior vena cava in association with azygous-hemiazygous continuation of the inferior vena cava, Kawashima procedure (KP), has been questioned. We document our experience with KP performed at a relatively younger age than usually reported.

Methods: A retrospective review of patients undergoing KP (October 2000 to April 2008) was done.

Results: Initial palliation was carried out in 13 of 15 patients. Age and weight at KP was 8.4 months (5.1 to 15.1) and 6.8 kg (4.6 to 11.0). The pre-KP catheterization showed the following: pulmonary artery pressure = 14.5 mm Hg (9 to 17); end-diastolic pressure of systemic ventricle = 8 (2 to 14); oxygenation saturation = 76% (63 to 82); and atrioventricular (AV) valve insufficiency moderate or greater in 5 patients. The post-KP characteristics included the following intubation = 1 day (0 to 19); nitric oxide = 4 patients; superior caval pressure = 14 mm Hg (6 to 18); inotrope score = 7.5 (2.5 to 14.3); intensive care unit stay = 3 days (1 to 9); hospital stay = 7 days (3 to 77); and oxygen saturation at discharge = 84% (76 to 90%). There was one hospital death that required takedown of KP. Fontan completion was performed in 8 patients at an interval of 2.7 years (1.8 to 5.8) after KP. There was one post-Fontan mortality from severe ventricular and AV valve dysfunction. Pulmonary arteriovenous malformations (PAVMs) were diagnosed in 4 patients with 3 resolving post-Fontan. With a median follow-up of 4.2 years (0.1 to 7.9), 13 of 15 remain alive yielding a series survival of 87%.

Conclusions: The Kawashima procedure can be safely performed at an earlier age than previously reported. The incidence of PAVMs after the KP appears to be similar to other reports where KP was performed at a later age.

	Introduction

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 
The Kawashima procedure (KP) provides palliation in cyanotic, single ventricle patients (usually with heterotaxy) who have an interrupted inferior vena cava (IVC) with azygous or hemiazygous continuation to the superior vena cava (SVC). The original description of the operation in 1984 [1] included 4 patients with a previous systemic to pulmonary shunt who underwent a bidirectional superior cavopulmonary connection, Blalock shunt takedown, and interruption of antegrade pulmonary flow. It is estimated that the KP diverts 80% to 85% of the systemic venous return to the lungs, excluding only the hepatic and coronary sinus drainage. Most current literature describes the KP as being performed in older children, typically around the age when a Fontan would be done [2–4]. Concern with an early operation reflects the thought that the volume loaded ventricle (after systemic to pulmonary shunt) may not tolerate the sudden change in preload that occurs with the "near Fontan" physiology of a KP [5].

Our current strategy has been to offer the KP at around the same age that a patient would usually undergo second-stage palliation for a single ventricle defect. To validate our practice, a study was designed to look at the outcomes of consecutive patients undergoing KP in our institution over the last 7.5 years. In addition to safety and efficacy issues we also had an interest in the incidence of pulmonary arteriovenous malformations (PAVMs) known to be potentially problematic in the post-KP population.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 
Demographics
A retrospective review of all patients less than 18 years of age undergoing a Kawashima procedure at Childrens Hospital Los Angeles from October 2000 to April 2008 was performed. Both inpatient and outpatient charts were reviewed following guidelines established by the Institutional Review Board. Demographic data regarding gender, cardiac morphology, presence of asplenia-polysplenia (based on spleen scan), and bilateral SVC and initial surgical palliation were tabulated.

Operative Description
Preoperative data utilized to determine feasibility of performing KP was tabulated. These included measurements of pulmonary artery pressure (PAP), end-diastolic pressure of the systemic ventricle, oxygenation saturation, ventricular function and presence of atrioventricular (AV) valve insufficiency, and antegrade pulmonary blood flow. At KP, age, weight, time from initial palliation, concurrent procedures, and cardiopulmonary bypass time were tabulated. Generally, KP patients in this series had the favorable hemodynamic characteristics that would be used to determine suitability for a bidirectional Glenn (PAP < 18 mm Hg, low transpulmonary gradient, good ventricular function). In general, a younger age patient with azygous or hemiazygous continuation of the IVC requiring an intervention because of falling saturations and who had marginal hemodynamics would undergo a repeat shunt operation.

All patients had their operation through a median sternotomy. Patients were placed on cardiopulmonary bypass and cardioplegic arrest was utilized as needed in cases where concurrent intracardiac defects were surgically addressed. The cavopulmonary anastomosis was performed with a continuous, monofilament suture technique. Essentially, the SVC (or both in those patients with bilateral SVC) was divided and an end-to-side anastomosis was fashioned to a pulmonary artery branch. The caudal or atrial end of the superior vena cava stump was closed in a running fashion.

At completing Fontan the incorporation of the hepatic effluent was performed by utilizing an extracardiac polytetrafluoroethylene (PTFE) conduit. An atrial cuff was created where the hepatic veins came into the atrium. This cuff was sewn end-to-end to the PTFE graft (usually 16 mm). The other end of the extracardiac conduit was sewn end-to-side to a branch of the pulmonary artery. Hence, the extracardiac conduit was routed from side of hepatic connection to the common atrium to its ipsilateral pulmonary artery.

Early Results
Cardiopulmonary support parameters were measured in the postoperative period. These included extubation time, use of inhaled nitric oxide, and superior caval pressure measurements. The inotrope score was calculated using the formula: dopamine + dobutamine + (epinephrine x 100) + (norepinephrine x 100) + (milrinone x 10) in micrograms per kilogram per minute [6]. Nitric oxide was generally implemented for cases of postoperative pulmonary arterial hypertension, manifest by oxyhemoglobin desaturation with elevated pressures within the cavopulmonary system. Usually, nitric oxide was implemented after other measures to control pulmonary arterial hypertension, such as increases in supplemental oxygen, adequate ventilation, sedation, or muscle relaxation, had failed. Nitric oxide was typically begun at 20 parts per million. In general, patients were maintained on the medication for 24 hours during which time inspired oxygen was decreased to a level below 0.6. At this point nitric oxide was gradually weaned. Sildenafil was usually started in advance of the nitric oxide wean and was maintained after coming off that medication.

In addition, the median time to chest tube removal, length of mechanical ventilation, and length of intensive care unit and hospital stay was identified. After KP completion, adverse outcomes including the presence of cardiac arrhythmias, persistent pleural effusions, persistent cyanosis, and mortality was tabulated. Hospital mortality was defined as any deaths that occurred prior to hospital discharge after KP or within 30 days of KP. The mode of death was also documented. Oxygenation saturations at discharge were measured.

Midterm Results
Outpatient charts were accessed from the patient's surgical and cardiology clinic visits to assess patient status. Complete follow-up was available in all 15 patients. Follow-up was considered complete when there was clinical and relevant echocardiographic and cardiac catheterization information within 6 months of data collection. The presence of PAVMs was suspected clinically based on oxygen saturations of less than 75% on room air. However, our criteria to assign a diagnosis of PAVMs required catheterization findings of rapid pulmonary artery-venous transit time or evidence of reticular or spongy markings in peripheral fields. Pulmonary venous blood sampling was sometimes, but not routinely, available and thus was not used as diagnostic criteria. Contrast (agitated saline) echocardiographic imaging, though often performed on study patients, was likewise not used as diagnostic criteria for PAVMs.

Cardiac catheterization was also performed as part of pre-Fontan evaluation and measurements of pulmonary artery pressure, end- diastolic pressure of the systemic ventricle, oxygenation saturation, ventricular function, and presence of AV valve insufficiency and antegrade pulmonary blood flow were tabulated. For the completion Fontan operation concurrent procedures and cardiopulmonary bypass times were tabulated. Midterm mortality was defined as any patient death after hospital discharge from KP. Resolution of PAVMs and need for cardiac reinterventions post-Fontan were noted.

Statistics
Data are presented as median and range. This is to provide a better representation of both the central tendency and the variability of this non-normally distributed data set.

	Results

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 
Demographics
Among the 15 patients that met criteria, 11 were male. All patients had heterotaxy and an unbalanced AV septal defect. Additional cardiology morphology for each patient is detailed in Table 1. Data with respect to splenic abnormalities, presence of bilateral SVC, and side of azygous continuation are shown in Table 1. As detailed in Table 1, 13 of 15 patients underwent initial palliation prior to KP. Of the 6 patients who underwent Blalock-Taussig (BT) shunt placement with restriction of antegrade pulmonary blood flow by pulmonary artery banding or ligation, 1 patient needed concomitant pacemaker placement for congenital heart block and another patient needed an atrial septectomy. Of the 3 patients listed as undergoing isolated BT shunt in Table 1, one patient had a right pulmonary arterioplasty for stenosis.

There was one hospital death. A 5.7-month-old male initially presented with heterotaxy, unbalanced atrioventricular septal defect, hypoplastic aortic arch, and obstructed total anomalous pulmonary venous return (TAPVR). Soon after birth, he underwent a BT shunt-Norwood with a TAPVR repair. At the time of KP, the patient concurrently underwent revision of TAPVR repair. In the postoperative period, the patient had persistent critical cyanosis and a few days after KP the cavopulmonary connection was taken down and a BT shunt was created. Ultimately, he expired in the hospital after a 2.5-month stay from sepsis. Significant morbidity was documented in 2 additional patients. An 8.8-month-old male developed pulmonary hypertension, seizures, cranial swelling, and pleural effusions. This necessitated a surgical intervention for pericardial stripping and interruption of persistent antegrade flow. The patient recovered without any further adverse events. A 5.4-month-old male had a phrenic nerve injury which necessitated unilateral plication of the diaphragm.

Midterm Results
The series follow-up was 4.2 years (0.1 to 7.9). At the completion of KP, antegrade pulmonary blood flow was present in 5 patients. Eight patients (53%) have undergone a Fontan completion. Cardiac catheterization was performed to ensure feasibility of directing hepatic effluent to the pulmonary circulation. Pulmonary artery pressure was 10 mm Hg (7 to 16), end-diastolic pressure of the systemic ventricle was 9 mm Hg (6 to 12), and oxygenation saturation was 82% (75 to 90). Moderate to severe AV valve insufficiency and markedly decreased ventricular function was present in 1 patient who was considered but found to be an unsuitable candidate for transplantation. The PAVMs were documented in 4 patients based on catheterization findings and pulmonary angiography.

At an interval of 2.7 years (1.8 to 5.8) from KP 8 patients underwent Fontan completion. Cardiopulmonary bypass was utilized in 7 patients for a duration of 58 minutes (22 to 105); in 1 patient, the procedure was done off-pump. There was one hospital death in a 3-year-old patient with poor ventricular function and AV valve insufficiency who was not a transplant candidate. At the time of Fontan completion, she had a concomitant AV valve repair. She had postoperative mediastinal hemorrhage requiring reoperation and extracorporeal membrane oxygenator support for ventricular dysfunction. She suffered a stroke and died 1 week after Fontan completion. Additional morbidity was documented in a 3.1-year-old male who had a phrenic nerve injury requiring diaphragm plication.

With a median follow-up of 4.2 years 13 of 15 patients remain alive yielding a series survival of 87%. Twelve patients remain without supplemental oxygen with a saturation of 89% (80 to 95). One patient requires oxygen for chronic lung disease.

Of 4 patients with PAVMs after KP, 3 had resolution of PAVMs after connection of the hepatic veins to the pulmonary arteries. A 6.1-year-old female with bilateral SVC developed bilateral PAVMs post-KP. After bidirectional hepatic venous connection to the left pulmonary artery (same side as KP), she had persistent PAVMs in the right lung with significant oxygen desaturations. This was believed to be secondary to a "streaming effect" with the hepatic effluent being preferentially directed toward the left lung. The pulmonary AVMs were not amenable to catheter-directed therapy. A surgical revision to redirect the hepatic flow to the right lung was undertaken 1.4 years after initial Fontan completion. Currently she has been followed for 6 months with improved saturations.

	Comment

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 
Appropriate Age for Kawashima
Many centers have demonstrated that the Kawashima procedure can be performed safely in patients who are more than 1 year of age [2, 3, 7]. A recent series from Indiana documented 21 patients undergoing their KP at a median age of 2 years and a median weight of 11.2 kg [2]. Similarly, in a large series from Boston, 36 patients underwent KP with one cohort of 16 patients (who subsequently developed post-KP PAVMs) undergoing their procedure at a median age of 10 months, while a second cohort with 20 patients (who did not develop post-KP PAVMs) underwent the procedure at a median age of 1.7 years [3]. While there are a few reports of younger patients undergoing KP [8], these have very small patient populations and limited follow-up. Our experience should therefore add important information on the outcome of earlier KP.

There are two principal concerns with performing KP at a younger age. The first is whether the potentially more reactive pulmonary bed will tolerate the diversion of roughly 80% of systemic venous return. Additionally the sudden change in preload seen by the previously volume-loaded systemic ventricle could be problematic. Our experience would suggest that these are not important issues. The second concern is whether PAVMs are more likely to develop in patients who undergo KP at a younger age. It has been suggested that the incidence of PAVMs appears to be higher in younger patients who undergo a standard bidirectional Glenn [5] and this finding was also noted among younger KP patients in the Boston report [3]. Our experience suggests that a relatively small percentage of patients develop important PAVMs even when KP is carried out at 8 months. However, we have used more rigid criteria for the presence of PAVMs by requiring angiographic evidence rather than an arbitrary level of desaturations.

To Fenestrate or Not to Fenestrate at KP
While it has been suggested that younger patients undergoing KP should be protected from the potential for low cardiac output by creating a fenestration [9, 10], our experience suggests this should rarely if ever be necessary. We found that the post-KP hemodynamics and hospital course were very similar to patients undergoing standard bidirectional Glenn.

Additional Pulmonary Flow After KP
We did not have a standardized approach to address this issue of antegrade pulmonary flow during the study period. Proponents of retaining additional pulmonary blood flow at the time of cavopulmonary connection believe that it may help to reduce the development of venovenous collaterals, improve oxygen saturations, and stimulate pulmonary artery growth [11–14]. Those opposed to leaving antegrade flow argue that there is a persistent volume load on the single ventricle (which may cause worsening atrioventricular valve regurgitation in some cases), increased central venous pressures in the upper body, and a higher risk of persistent pleural effusions [11, 13, 15]. In the KP population, some investigators suggest that preserved antegrade flow (with a competent pulmonary valve) may decrease the possibility of PAVM development as it allows a hepatic factor to enter the pulmonary circulation [9]. In our series, 5 patients maintained antegrade flow post-KP and none of these patients developed clinically significant PAVMs. However, given the small patient cohort we cannot draw conclusions from this experience. Our current institutional preference is to leave a small amount of antegrade flow whenever possible when performing KP.

Development of Pulmonary Arteriovenous Malformations
The PAVMs are thought to develop because the venous return from the liver (which is thought to contain a hepatic factor) does not reach the pulmonary circulation. It is known that patients with hepatopulmonary syndromes develop PAVMs that resolve subsequent to a liver transplant. This provides clinical support to the theory that there is a hepatic factor [16, 17]. In the laboratory, expression of vascular endothelial growth factor and hepatocyte growth factor has been implicated in the abnormal angiogenesis in PAVMs [18].

While PAVMs may be present in normal lung parenchyma [19], their incidence increases after completion of all types of cavopulmonary anastomosis [20, 21]. In animal models PAVMs have been shown to develop 8 weeks after cavopulmonary connection [18]. The incidence of clinically evident PAVMs after KP is thought to be about 21% [19]. The incidence ranges from 20% to 75% depending on which modality (contrast echocardiogram or pulmonary angiogram) is used to make the diagnosis [22, 23]. In one report of KP patients, contrast echocardiography demonstrated that subclinical PAVMs were present in nearly all patients [24]. In patients who undergo a standard bidirectional Glenn procedure, the incidence of clinically evident PAVMs is rather low provided that a total cavopulmonary connection is performed within 1 to 3 years of the Glenn [3]. Other investigators [3, 25, 26] have reported the incidence in this population to be higher and note that PAVMs can develop acutely as well.

A report from Boston [19] has detailed the effect of hepatic venous blood exclusion in the development of PAVMs. A report from Philadelphia [8] further noted the development and subsequent resolution of PAVMs with reintroduction of hepatic flow in the pulmonary circulation. In this study, 3 patients were suspected of having developed PAVMs 8 months after KP based on room air saturations of less than 75%. The diagnosis was confirmed on pulmonary angiography. After inclusion of hepatic venous blood, PAVMs resolved at a median of 7 months with resulting saturations of greater than 90% on room air [8].

Similar conclusions can be drawn from the more recent experience reported by the Indiana and Boston groups. In the Indiana experience [2], a cohort of 21 patients underwent KP and PAVMs were diagnosed in 11 patients. The diagnosis was based on clinical data such as oxygen saturations of less than 80% without evidence of parenchymal lung disease. Diagnosis was further validated by contrast echocardiograms and pulmonary angiograms; however, it is not clear for any given patient which modality was used to reach the diagnosis. The presence of bilateral SVC and waiting for more than 2 years to perform Fontan completion after KP were both associated with development of PAVMs. Subsequently 10 of the patients with bilateral PAVMs in this series had a Fontan procedure. Of these, 1 patient died and 1 needed heart transplantation. All remaining patients had resolution of PAVMs at last follow-up.

In the Boston experience [3], a more systematic investigation was used to determine if PAVMs resolved after hepatic flow was directed to the pulmonary circulation. In their report, 16 of 37 post-KP patients had significant PAVMs and underwent hepatic venous redirection to the pulmonary bed. The investigators' criteria for a PAVM diagnosis was angiographic evidence manifest by rapid pulmonary AV transit of contrast or reticular-spongy pattern peripherally and pulmonary venous desaturation (< 92%) in affected lung segments. A diagnosis of PAVMs was made at a median of 3.1 years post-KP. After completion Fontan, 11 of 16 patients had successful resolution of PAVMs.

In our series, PAVMs were evident in 4 of 14 patients post-KP. Based on clinical criteria they appear to have resolved in 3 patients post-Fontan. In 1 patient who had persistent desaturations and angiographic evidence of PAVMs post-Fontan, a surgical revision was needed to address the "streaming effect" which was creating unilateral PAVMs. The importance of flow streaming has been detailed in in-vitro models [27].

Limitations
This single-institution, observational study has a small patient population. There was no standard protocol for when KP was performed. There was also no standard protocol for when Fontan completion was carried out. While cardiac catheterization was utilized to diagnose PAVMs, the resolution of PAVMs was suspected based on improvement in clinical saturations but not confirmed with imaging modalities.

	Discussion

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 
DR S. TALWAR (New Delhi, India): I enjoyed your presentation. I have a couple of questions.

As you are aware there is lot of discussion about leaving the antegrade pulmonary blood flow to prevent development of pulmonary arteriovenous malformations. You had a group of patients who had interruption of the antegrade pulmonary blood flow and you have some patients who had antegrade pulmonary blood flow. So what in your experience are the criteria for interruption of anterior flow in these patients? That's the first question.

And second, did you notice any difference in proceeding to the next Fontan among these two groups of patients? What is your policy about timing of cardiac catheterization for completion Fontan in patients with or without antegrade pulmonary blood flow, and what was the difference in outcomes with the Fontan completion in either group?

DR NATH: During the study period we individualized decisions with regard to leaving antegrade flow at the time of KP [Kawashima procedure]. If patients had marginal saturations after weaning from bypass, we left antegrade flow if this was an option. There were 5 such cases among 15 patients.

The presence of antegrade pulmonary blood flow did not affect the feasibility of Fontan completion. We also noted that none of the patients with antegrade flow developed pulmonary AVMs [arteriovenous malformations] while these were present in 4 of the 10 patients without at least some hepatic factor getting to the lungs.

DR JAMES S. TWEDDELL (Milwaukee, WI): That was a nice presentation. When you have pulmonary arteriovenous malformations in a patient with bilateral superior vena cavas [SVCs] and azygous continuation of the inferior vena cava to the superior vena cava opposite the lung with pulmonary arteriovenous malformations, how did you revise the Fontan in order to resolve the arteriovenous malformations?

DR NATH: The patient in question had bilateral SVCs. At the time of Fontan completion, the hepatic veins were taken to the same side as the KP since they entered the common atrium on the same side as the hemiazygous continuation of the IVC [inferior vena cava]. The newly developed AVMs were in the lung on the opposite side to the KP. At the time of revision, we redirected hepatic flow to the PA [pulmonary artery] on the side of the AVMs using a new extracardiac conduit.

DR JOSEPH FORBESS (Dallas, TX): Do I understand that you revised the Fontan with a completely new extracardiac conduit?

DR NATH: We took down the previous extracardiac conduit and rerouted the hepatic veins to the contralateral side.

DR FORBESS: So it's not of a T-graft or the like?

DR NATH: No it was not a T-graft.

DR JOSEPH CASPI (New Orleans, LA): I saw in your preoperative evaluation the pulmonary artery pressure and the ventricular end diastolic pressure, but maybe I missed it. Was the size of the pulmonary arteries a factor that determined the suitability of these patients for the Kawashima? Because I have now two patients with aortic atresia; one after the Norwood and one after the hybrid procedure, and they are only 3 and 4 months, and we're debating whether the size of the branch pulmonary arteries is a factor for early Kawashima. Will you please comment on that.

DR NATH: We did not use size of the pulmonary arteries as a criteria for determining the suitability for proceeding with KP. In the past, we have found that contrast underfilling may lead to a miscalculation of PA size and thus we have relied more on hemodynamics in patient selection.

DR FORBESS: So what would you speculate would be your program's lower boundary for this procedure age wise? Because you don't always have the luxury of waiting the time frame that you're talking about here to do a bidirectional Glenn typically. We're putting in smaller shunts. There are more of these RV [right ventricle]-PA conduits being done, and the patients are blue, younger, and earlier. So how young is too young for the Kawashima procedure, would you guess?

DR NATH: We do not have the data to answer this important question but by way of speculation, a patient as young as 3 months who has suitable hemodynamics could be considered for a KP. Nitric oxide can be used to control the potential problem of pulmonary hypertension episodes that are likely to occur in a younger patient.

	References

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 

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