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Ann Thorac Surg 2005;80:1592-1596
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

Pulmonary Arteriovenous Malformations in Children After the Kawashima Operation

John W. Brown, MD * , Mark Ruzmetov, MD, PhD, Palaniswamy Vijay, PhD, Mark D. Rodefeld, MD, Mark W. Turrentine, MD

Section of Cardiothoracic Surgery, Indiana University School of Medicine, and James Whitcomb Riley Hospital for Children, Indianapolis, Indiana

Accepted for publication April 25, 2005.

* Address correspondence to Dr Brown, Section of Cardiothoracic Surgery, Indiana University School of Medicine, 545 Barnhill Dr, EH 215, Indianapolis, IN 46202-5123; (Email: jobrown{at}iupui.edu).

Presented at the Poster Session of the Forty-first Annual Meeting of The Society of Thoracic Surgeons, Tampa, FL, Jan 24–26, 2005.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: Pulmonary arteriovenous malformations are a major cause of progressive late cyanosis in patients treated with cavopulmonary anastomoses. Previous experience suggests that exclusion of the hepatic venous effluent from the pulmonary circulation may cause the development of pulmonary arteriovenous malformations after the Kawashima operation in children with interrupted inferior vena cava with azygous continuation.

METHODS: From January 1990 to November 2004, 21 children (median age, 2 years) with heterotaxy syndrome and interrupted inferior vena cava with azygous continuation underwent Kawashima operation. The average preoperative arterial oxygen saturation was 76% ± 7% (range, 64% to 90%).

RESULTS: Follow-up was complete in all survivors except 1 at a median duration of 4.5 years. Pulmonary arteriovenous malformations were diagnosed at a median of 5 years after Kawashima operation in 11 patients (58%). Completion Fontan operation has been performed in 15 (79%). Five children who underwent a completion Fontan procedure 1 to 1.5 years after Kawashima operation did not have pulmonary arteriovenous malformations. There were 2 late deaths due to chronic congestive heart failure 4 months and 7 years after Kawashima operation. Overall survival at 10 years is 90%. Univariate and multivariate analysis demonstrated presence of bilateral superior vena cavae (p = 0.002) and interval longer than 2 years between Kawashima operation and completion Fontan operation (p = 0.04) as predictors of developing pulmonary arteriovenous malformations.

CONCLUSIONS: In most patients with heterotaxy and interrupted inferior vena cava with azygous continuation, clinical evidence of pulmonary arteriovenous malformations will develop after Kawashima operation if they are followed up long enough. Early redirection of the hepatic venous effluent to the pulmonary arterial circulation may prevent or lead to regression of pulmonary arteriovenous malformations, with low mortality and morbidity.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Surgical connection of the superior vena cava (SVC) to the right pulmonary artery as classically described by Glenn was initially considered a satisfactory means of palliation for various forms of cyanotic congenital heart disease. Substantial morbidity and mortality from the late onset of ipsilateral pulmonary arteriovenous malformations (PAVMs), however, contributed to modification of the originally described procedure as a destination therapy. Use of various other modifications of superior cavopulmonary artery connections (bidirectional Glenn, hemi-Fontan procedures) subsequently evolved for palliation of single-ventricle anomalies in the first year of life [1–3]. Although physiologically similar to the classic Glenn operation, current techniques of bidirectional cavopulmonary anastomosis (BCPA) have been shown to cause bilateral rather than ipsilateral PAVMs under certain conditions, but at a lower incidence [3, 4]. The main reason for the lower incidence may be that the BCPA is usually performed as part of a two-stage approach, with most patients proceeding relatively quickly to incorporation of inferior vena caval (IVC) and hepatic venous flow into the pulmonary circulation, namely, completion Fontan operation.

A notable exception to the two-stage strategy for total cavopulmonary diversion has been in children with polysplenia syndrome with interruption of the IVC when there is azygous continuation of the IVC to the SVC. In this situation, only the hepatic venous effluent remains to drain directly into the atrium, bypassing the pulmonary vascular bed. Bidirectional cavopulmonary anastomosis alone in these patients incorporates most (85%) of the systemic venous return into the pulmonary circulation, excluding coronary sinus and hepatic venous flow. Kawashima and colleagues [1, 5] in 1984 described BCPA in this group of patients. This procedure typically results in arterial oxygen saturations in the range of 85% to 90% and was initially believed to obviate the need for further operation. However, a high incidence of PAVM development was subsequently recognized in patients with polysplenia who have had the Kawashima operation alone as their definitive procedure [6–10]. This report reviews our experience with the development of PAVMs after the Kawashima operation in patients with polysplenia syndrome and interruption of the IVC with azygous continuation to the SVC.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Three-hundred eleven patients have undergone Fontan palliation for single-ventricle physiology at Riley Children's Hospital in Indianapolis. One hundred nine patients had a single-stage Fontan repair without an antecedent Glenn shunt before 1990. One hundred fifty-one have had a two-stage Fontan repair and 51 additional patients have had a BCPA but have not yet undergone a completion Fontan operation. Twenty-one children (21 of 311, 7%) presented with polysplenia syndrome with interruption of the IVC with azygous continuation to the SVC. In these patients, a bidirectional Glenn anastomosis was performed incorporating IVC flow through the azygous vein into the SVC in the Kawashima operation.

Medical charts, echocardiograms, and catheterization data were reviewed retrospectively with close attention paid to possible diagnoses of PAVMs and the patterns of hepatic and pulmonary blood flow. Follow-up data were obtained from hospital charts, correspondence with referring physicians, and from a computerized institutional database. Of the 21 patients who underwent Kawashima operation, 17 of 21 (81%) had single-ventricle physiology with morphologic right ventricle anatomy and 4 had morphologic left ventricle anatomy. Ten patients had unbalanced atrioventricular septal defects. Ten patients had bilateral SVCs, 6 patients had only a right SVC, and 5 had only a left SVC. The average preoperative arterial oxygen saturation was 76% ± 17% (range, 64% to 90%). Eighteen of the 21 patients (86%) had undergone 1 to 3 prior palliative procedures (Table 1). Before performing the Kawashima operation, no patient had hemodynamic, echocardiographic, or angiographic findings at cardiac catheterization that indicated the presence of clinically significant PAVMs. Our standard current regimen for postoperative anticoagulation after either a staged or nonstaged Fontan procedure includes aspirin 10 mg/kg per day and warfarin 0.5 to 1 mg/kg per day (for 1 year).


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  		Table 1. Previous Cardiac Procedures
 
Method of Kawashima Operation
Patients underwent the Kawashima operation at a median age of 2 years (range, 8 months to 9 years) and at a median weight of 11.2 kg (range, 8.5 to 51 kg). Concomitant procedures are summarized in Table 2. The Kawashima operation consisted of division and end-to-side anastomosis of the proximal SVC with a branch pulmonary artery, occlusion of the SVC stump into the atrium, and augmentation of the confluence of the branch pulmonary arteries, if necessary. Among 10 patients who had bilateral SVC's, 9 underwent bilateral bidirectional Glenn shunts and 1 had division of a diminutive right SVC.


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  		Table 2. Concomitant Cardiac Procedures
 
Diagnosis of Pulmonary Arteriovenous Malformations
The diagnosis of PAVMs was suspected when there was (1) detection of progressive resting systemic arterial oxygen desaturation by pulse oximetry, without any evidence of parenchymal lung disease; (2) arterial oxygen saturation of 80% or less in room air during cardiac catheterization; and (3) one or more positive results of the three following diagnostic modalities: (a) chest roentgenogram, (b) contrast echocardiogram, and (c) pulmonary angiogram. We considered PAVMs to be resolved when, on cardiac catheterization, arterial oxygen saturation was greater than 90% in room air and when a normal pulmonary arterial-to-venous transit time was observed on pulmonary angiography. Diagnostic cardiac catheterization was performed at a median duration of 5.1 years (range, 10 months to 13 years) after the Kawashima operation.

Method of Hepatic Vein Inclusion Into the Pulmonary Circulation
In 10 patients, connection of the hepatic veins to the pulmonary arteries was accomplished with a polytetrafluoroethylene (PTFE [Gore-Tex; W.L. Gore & Associates, Newark, DE]) extracardiac conduit. The hepatic veins were taken off of the atrium with a cuff of atrial tissue, and the atrium was closed primarily with a running suture. A PTFE vascular graft (13 mm to 18 mm diameter) was attached to the hepatic vein cuff with running 6-0 Gore-Tex suture. The other end of the conduit was anastomosed to the underside of the ipsilateral pulmonary artery. In the remaining 5 patients, the hepatic venous effluent was brought to the pulmonary arteries using a lateral caval tunnel constructed with a PTFE patch.

Statistical Analysis
The SPSS statistical program for Windows version 10 (SPSS, Chicago, Illinois) was used to perform the data analysis. Data are expressed as mean, median, and range. Actuarial estimates of freedom from postoperative events were accomplished with Kaplan-Meier methods, and p values for differences between distributions were obtained by log-rank testing. Event-free rates are presented with +1 SE of the estimate. Factors evaluated in multivariate analysis for risk of developing of PAVMs included age, weight, sex, date of operation, cardiac diagnosis, previous cardiac operations, concomitant cardiac operations, interval between the Kawashima operation and completion Fontan procedure (more or less than 2 years), and type of Kawashima operation (unilateral or bilateral BCPA). The analyses were performed with Cox proportional hazards regression. A forward step-wise selection method was used to add variables to the model, requiring significance at p less than 0.10 for entry and p less than 0.05 for retention. Early death is defined as death in the hospital or death within 30 days of discharge after the Kawashima operation. All other deaths are considered late.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Survival
There were no operative or early deaths in the series, but there were 2 late deaths. Overall survival estimated by the Kaplan-Meier method was 95% at 5 years and 90% at 7 and 10 years after the Kawashima operation (Fig 1). The first late death occurred in a 2-year-old child with heterotaxy syndrome with polysplenia, levocardia, double-outlet right ventricle, hypoplastic left ventricle, pulmonary stenosis, congenital complete heart block, bilateral SVCs, interrupted IVC with azygous continuation to a left SVC, and duodenal atresia. He underwent pacemaker implantation at 2 days of age, duodenal atresia repair at 1 week of age, and the Kawashima operation at 2 years of age. He did well initially after his Kawashima operation, but later had difficulty weaning from the ventilator with CO2 retention. He was discharged 48 days postoperatively with arterial oxygen saturation of 90%, but died of chronic heart failure and sepsis 4 months later.



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  		Fig 1. Overall survival estimated by the Kaplan-Meier method.

 
The second late death occurred in a child with polysplenia syndrome, unbalanced atrioventricular septal defect, double-outlet right ventricle, hypoplastic left ventricle, bilateral SVCs, and interrupted IVC with azygous continuation to the left SVC. He underwent right modified Blalock-Taussig shunt at 3 weeks of age and the Kawashima operation at 6 years of age. Subsequent serial follow-up revealed an asymptomatic child developing normally with pulse oximetry measuring 91%. Seven years after the Kawashima operation, he exhibited deteriorating physical activity and cyanosis. Pulse oximetry measured 78% and hemoglobin concentration measured 17.8 mg/dL. Transthoracic echocardiogram revealed intrapulmonary shunting consistent with PAVMs. Pulmonary angiography revealed prompt filling of the pulmonary veins, confirming the presence of bilateral PAVMs. The patient was taken to the operating room and underwent lateral caval tunnel modification of Fontan procedure with connection of the hepatic vein confluence to the pulmonary arterial circulation. The patient died because of low cardiac output 4 days after surgery.

A postoperative complication occurred in a child with dextrocardia, D-transposition of the great arteries, double-outlet right ventricle, pulmonary atresia, large ventricular septal defect, bilateral SVCs, and azygous continuation of the left sided IVC. This patient underwent a palliative Blalock-Taussig shunt during infancy and then subsequently underwent a Kawashima operation. Four years later the family noticed her to have some increased fatigue, shortness of breath, and cyanosis. Her saturation on room air was 79%. Pulmonary angiography revealed prompt filling of the pulmonary veins, confirming the presence of bilateral PAVMs. A lateral caval tunnel connection was performed. She returned 2 weeks later with pericardial effusions. She subsequently developed protein losing enteropathy, chronic lower extremity edema, and ascites. Orthotopic heart transplantation was performed 3 years after the completion Fontan procedure.

Follow-up was complete in 20 of 21 patients (95%) and ranged from 4 months to 14 years (median, 4.5 years; mean, 5.5 ± 4.0). One patient was lost to follow-up. Nineteen patients were assessed for PAVMs (2 children were excluded: 1 late death and 1 lost to follow-up; Fig 2).



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  		Fig 2. Distribution and disposition of patients with Kawashima operation. (PAVM = pulmonary arteriovenous malformation; pt = patient.)

 
Eleven patients (58%) were found to have developed bilateral PAVMs in a median time interval of 5 years after the Kawashima operation (mean, 5.7 ± 3.1 years; range, 2 to 11; Fig 3). The median arterial oxygen saturation was 75% (range, 64% to 85%), the median hemoglobin concentration was 17 mg/dL (range, 10.2 to 18.5 mg/dL), and the median mean pulmonary arterial pressure was 13 mm Hg (range, 10 to 20 mm Hg). Progressive cyanosis was noted in all patients in this group at a median duration of 32 months (range, 19 to 52) after the Kawashima operation.



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  		Fig 3. Freedom from pulmonary arteriovenous malformations estimated by the Kaplan-Meier method.

 
Ten patients with PAVMs have undergone a completion Fontan procedure (6 extracardiac and 4 lateral caval tunnel). One patient in whom PAVMs developed is awaiting completion Fontan surgery. Two patients had postoperative complications after their completion Fontan procedure: 1 patient died because of low cardiac output, and another underwent orthotopic heart transplantation 3 years later owing to protein-losing enteropathy and congestive heart failure.

Nine patients with PAVMs who underwent a completion Fontan procedure (including patients after heart transplantion) were assessed for PAVMs and only 2 had attributes of PAVMs during the first year of follow-up (9 months and 1 year after a completion Fontan). At last follow-up (mean, 4.1 ± 2.3 years; range, 1 to 7), none of the 9 has developed evidence of PAVMs by echocardiogram and contrast angiogram. The mean arterial oxygen saturation in those patients was 95% ± 2% (range, 93% to 98%).

Eight patients (42%) had cyanosis but did not develop PAVMs during a median 2-year follow-up (mean, 3.2 ± 4.0 years; range, 1 to 13). The median arterial oxygen saturation was 82% (range, 80% to 90%; p = 0.02), the median hemoglobin concentration was 12.4 mg/dL (range, 9.0 to 15.3 mg/dL; p = 0.01), and the median mean pulmonary artery pressure was 16 mm Hg (range, 14 to 22 mm Hg; p = 0.08).

In the group of patients who did not develop PAVMs (n = 8), 5 underwent a completion Fontan procedure (4 extracardiac conduit and 1 lateral caval tunnel) in a median of 1.5 years (range, 1 to 2; p = 0.001). Three patients (2, 3, and 13 years after the Kawashima operation), have not shown evidence of PAVMs by echocardiogram and contrast angiogram.

Finally, 15 of 19 patients (79%) underwent a completion Fontan procedure, and 4 patients are awaiting completion Fontan. All 18 current survivors are in New York Heart Association functional class I or II.

Univariate and multivariate analysis showed the presence of bilateral SVCs (p = 0.002), and an interval between the Kawashima operation and completion Fontan operation of more than 2 years (p = 0.04) as the most sensitive predictors of development of PAVMs after the Kawashima operation.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Pulmonary arteriovenous malformations develop embryologically owing to incomplete development of the pulmonary capillary system and are characterized by greatly increased numbers of nonessential pulmonary blood vessels that do not serve a critical gas exchange function but cause arteriovenous shunting. The existence of PAVMs in normal lungs has been verified by several investigators [7]. Under certain physiologic conditions these vascular channels may become dilated and more numerous. Related to congenital cardiopulmonary disease, the association of PAVMs with anomalous systemic venous drainage was described in 1965 [11]. Pulmonary arteriovenous malformation development after the classic Glenn shunt in the ipsilateral lung was initially thought to be due to overperfusion of the lower lobe or lack of pulsatile flow in the pulmonary arteries [12, 13]. Moore and colleagues [4] demonstrated PAVMs after the BCPA, firmly establishing a link between superior cavopulmonary shunts and subsequent PAVM formation.

It was not until 1994 when Srivastava and coworkers [7] conclusively demonstrated that PAVMs were due to an absence of a "hepatic factor" or "mesenteric factor" [7, 14] and that an unidentified element in the hepatic venous drainage inhibited the recruitment and dilatation of preexisting pulmonary arteriovenous connections. Duncan and Desai [15] further elaborated the mechanisms for the etiology of PAVMs and demonstrated that they were likely due to greatly increased numbers of abnormal and dilated channels and suggested an angiogenic process, as well as recruitment of preexisting channels that dilated when there was an absence of hepatic venous return to the pulmonary circulation. Alternately, these authors hypothesized that the liver may be responsible for the degradation of an angiogenic substance which is not removed after BCPA.

Clinically important PAVMs may develop in as many as 28% of patients within 3 to 5 years after the Kawashima operation and can cause clinically severe arterial oxygen desaturation and heart failure. Kawashima [5] demonstrated that subclinical PAVMs were present in nearly all patients with BCPA when elicited by contrast echocardiography. Shah and colleagues [9] and Duncan and Desai [15] corroborated these findings and showed that PAVMs would regress within 7 months after completion Fontan. Our experience with the Kawashima operation for complex single ventricle with azygous continuation of the IVC dates to 1990 when we, like Kawashima and others, assumed that BCPA would adequately palliate this complex group of children.

It was not until the mid to late 1990s that we noted clinically important PAVMs in 11 of our 21 patients in this series (52%). All had regression of their PAVMs after completion Fontan. Five of the most recent patients after the Kawashima operation have undergone a completion Fontan within 18 months and no evidence of PAVMs has developed. Analysis of this series demonstrated that bilateral SVCs and an interval of more than 2 years were independent risk factors for the development of PAVMs after the Kawashima operation. We now perform completion Fontan within 2 years of the BCPA in all patients with single-ventricle physiology with or without azygous continuation of the IVC.

Although all of our completion Fontans after the Kawashima operation have been performed by diverting the hepatic veins directly to the pulmonary arteries with an extracardiac conduit or lateral caval tunnel, other authors have shown that a connection of the hepatic veins to the azygous vein serves that same purpose and may be technically simpler in some patients [16–19].

In summary, clinically important PAVMs will likely form over time in the majority of patients who do not have their hepatic venous drainage diverted to the pulmonary circulation. The PAVMs appear within weeks of BCPA or the Kawashima operation and can be demonstrated earliest by contrast echocardiography. The PAVMs after the Kawashima operation or BCPA appear to be due to dilations, recruitment, and possibly angiogenesis in preexisting pulmonary venous connections. The early development of PAVMs in our Kawashima operation series and the potential development in patients undergoing BCPA as an intermediate step has led us to adopt early (less than 2 years) completion of the Fontan connection in patients who are on a pathway to single-ventricle palliation.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

  1. Kawashima Y, Kitamura S, Matsuda H, Shimazaki Y, Nakano S, Hirose H. Total cavopulmonary shunt operation in complex cardiac anomaliesa new operation. J Thorac Cardiovasc Surg 1984;87:74-81.[Abstract]
  2. Freedom RM, Hamilton R, Yoo S-J, et al. The Fontan procedureanalysis of cohorts and late complications. Cardiol Young 2000;10:307-331.[Medline]
  3. Lamberti JJ, Spicer RI, Waldman JD, et al. The bidirectional cavopulmonary shunt J Thorac Cardiovasc Surg 1990;100:22-30.[Abstract]
  4. Moore JW, Kirby WC, Madden WA, Gaither NS. Development of pulmonary arteriovenous malformations after modified Fontan operations J Thorac Cardiovasc Surg 1989;98:1045-1050.[Abstract]
  5. Kawashima Y. Cavopulmonary shunt and pulmonary arteriovenous malformations Ann Thorac Surg 1997;63:930-932.[Free Full Text]
  6. Matsuda H, Kawashima Y, Hirose H, Nakano S, Kishimoto H, Sano T. Evaluation of total cavopulmonary shunt operation for single ventricle with common atrioventricular valve and left isomerism Am J Cardiol 1986;58:180-182.[Medline]
  7. Srivastava D, Preminger T, Lock JE, et al. Hepatic venous blood and the development of pulmonary arteriovenous malformations in congenital heart disease Circulation 1995;92:1217-1222.[Abstract/Free Full Text]
  8. Kim SJ, Bae EJ, Cho DJ, et al. Development of pulmonary arteriovenous fistulas after bidirectional cavopulmonary shunt Ann Thorac Surg 2000;70:1918-1922.[Abstract/Free Full Text]
  9. Shah MJ, Rychik J, Fogel MA, Murphy JD, Jacobs ML. Pulmonary AV malformations after superior cavopulmonary connectionresolution after inclusion of hepatic veins in the pulmonary circulation. Ann Thorac Surg 1997;63:960-963.[Abstract/Free Full Text]
  10. Baskett RJF, Ross DB, Warren AE, Sharratt GP, Murphy DA. Hepatic vein to the azygous vein anastomosis for pulmonary arteriovenous fistulae Ann Thorac Surg 1999;68:232-233.[Abstract/Free Full Text]
  11. Anabtawi IN, Elliso RG, Ellison LT. Pulmonary arteriovenous aneurysm and fistulasanatomical variations, embryology, and classification. Ann Thorac Surg 1965;1:277-285.
  12. Cloutier A, Ash JM, Smallhorn JF, et al. Abnormal distribution of pulmonary blood flow after the Glenn shunt or Fontan procedurerisk of development of arteriovenous fistulae. Circulation 1985;72:471-479.[Abstract/Free Full Text]
  13. Kopf GS, Laks H, Stansel HC, et al. Thirty-year follow-up of superior vena cava-pulmonary artery (Glenn) shunts J Thorac Cardiovasc Surg 1990;100:662-671.[Abstract]
  14. Uemura H, Yagihara T, Hattori R, Kawahira Y, Tsukano S, Watanabe K. Redirection of hepatic venous drainage after total cavopulmonary shunt in left isomerism Ann Thorac Surg 1999;68:1731-1735.[Abstract/Free Full Text]
  15. Duncan BW, Desai S. Pulmonary arteriovenous malformations after cavopulmonary anastomosis Ann Thorac Surg 2003;76:1759-1766.[Abstract/Free Full Text]
  16. Steinberg J, Alfieris GM, Brandt III B, et al. New approach to the surgical management of pulmonary arteriovenous malformations after cavopulmonary anastomosis Ann Thorac Surg 2003;75:1640-1642.[Abstract/Free Full Text]
  17. Lee J, Menkis AH, Rosenberg HC. Reversal of pulmonary arteriovenous malformation after diversion of anomalous hepatic drainage Ann Thorac Surg 1998;65:848-849.[Abstract/Free Full Text]
  18. Pike NA, Vricella LA, Feinstein JA, Black MD, Reitz BA. Regression of severe pulmonary arteriovenous malformations after Fontan revision and "hepatic factor" rerouting Ann Thorac Surg 2004;78:697-699.[Abstract/Free Full Text]
  19. Schneider DJ, Banerjee A, Mendelsohn AM, Norwood WI. Hepatic venous malformation after modified Fontan procedure with partial hepatic vein exclusion Ann Thorac Surg 1997;63:1177-1179.[Abstract/Free Full Text]



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