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(Circulation. 1995;92:1217-1222.)
© 1995 American Heart Association, Inc.
Articles |
Hepatic Venous Blood and the Development of Pulmonary Arteriovenous Malformations in Congenital Heart Disease
From the Departments of Cardiology (D.S., T.P., J.E.L., J.F.K., P.J.S.), Radiology (V.M.), Cardiovascular Surgery (J.E.M.), and Pathology (H.K.), Children's Hospital, Harvard Medical School, 300 Longwood Ave, Boston, Mass.
Correspondence to Deepak Srivastava, MD, M.D. Anderson Cancer Center, Department of Biochemistry and Molecular Biology, 1515 Holcombe Blvd, Box 117, Houston, TX 77030.
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Abstract |
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 Top Abstract IntroductionMethods Results Discussion References |
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Background Pulmonary arteriovenous malformations (PAVMs) are a known complication after some types of cavopulmonary anastomoses (CVPAs). Their cause is unknown, but they may be related to the absence of pulsatile flow or the presence or absence of circulating factors. These PAVMs are diffuse and are presumed to be progressive and irreversible.
Methods and Results All patients with congenital heart disease (CHD) seen at Children's Hospital, Boston, Mass, between 1970 and 1993 were reviewed. We report on the 10 patients with CHD who were found to have developed PAVMs, as diagnosed by cardiac catheterization. Diagnoses included heterotaxy syndrome/polysplenia, with interrupted inferior vena cava and hepatic veins draining to the right atrium (n=6); heterotaxy/asplenia (n=1); corrected transposition with pulmonary stenosis (n=1); and biliary atresia and associated CHD (n=2). PAVMs were diagnosed 0.1 to 7.0 years (median, 3.5 years) after creation of a CVPA that resulted in exclusion of hepatic venous flow from one or both lungs in 8 of the 10 patients; the remaining 2 patients had normal drainage of hepatic veins to the lungs but had biliary atresia. In all, the common anatomic feature was the exclusion of normal hepatic venous return from the affected pulmonary arterial circulation. All patients with interrupted inferior vena cava, azygous continuation to the superior vena cava, and hepatic veins draining to the right atrium (polysplenia syndrome) were reviewed to determine the incidence of PAVMs in those with CVPA (ie, hepatic venous flow excluded from the pulmonary arteries) and without CVPA. Six of 28 (21%) of those with versus 1 of 56 (1.8%) of those without CVPA developed PAVMs (P=.004). The 1 patient without CVPA who had PAVMs also had biliary atresia. Among patients with CVPA, the probability of developing PAVMs was 15% and 28% at 3 and 5 years, respectively, after CVPA. The histological and angiographic appearances of PAVMs after CVPA are similar to those seen in PAVMs associated with hepatic cirrhosis.
Conclusions We postulate that PAVMs after CVPA are related to the diversion of normal hepatic venous flow from the pulmonary circulation. In this sense, these PAVMs may be analogous to those associated with liver disease, which have been found to resolve after liver transplantation. Redirection of hepatic flow to the pulmonary bed in some patients with CHD and PAVMs may lead to reversibility of the PAVMs.
Key Words: pulmonary heart disease • heart defects, congenital • anastomosis • liver
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Introduction |
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TopAbstractIntroductionMethods Results Discussion References |
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The development of pulmonary arteriovenous malformations (PAVMs) after the classic Glenn1 anastomosis (superior vena cava [SVC] to right pulmonary artery [PA]) is a previously described phenomenon with a reported incidence up to 25%.2 Although embolization therapy can successfully treat isolated PAVMs, effective therapy can be elusive when the disease is diffuse.3 4 The cause of the formation of these PAVMs remains unknown, but maldistribution of pulmonary blood flow to upper and lower lobes and nonpulsatile blood flow have been among the factors implicated in their pathogenesis.2 5 6 Angiographically, they appear as small, diffuse angiomatoid formations (Fig 1
)
and are similar in angiographic appearance to those
seen in cirrhotic liver disease.7 Rapid transit of
contrast media is seen from pulmonary
arterial-to-venous systems and is associated with
pulmonary venous desaturation. Histologically,
PAVMs associated with liver disease are characterized by diffuse
dilation of precapillary and capillary vessels.7 No
histological descriptions of PAVMs after
cavopulmonary anastomosis (CVPA) were found in our review
of the literature. The natural history of this condition is not well
described, but our experience is that it is a progressive and
irreversible condition leading to increasing cyanosis.
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In contrast to the experience with classic Glenn anastomoses, the reported incidence of PAVMs after other types of cavopulmonary anastomoses has been quite low. In the 1970s, the Fontan operation (atriopulmonary anastomosis)8 and later the modified Fontan operation,9 which incorporates almost all systemic venous return to the pulmonary arterial bed by the technique of total cavopulmonary anastomoses, became the palliative procedure of choice for most patients who had single ventricles and met the necessary anatomic and hemodynamic criteria. The distribution of pulmonary blood flow and the lack of pulsatile blood flow after the Fontan operation are similar to those noted after the Glenn anastomosis.10 However, PAVMs have not been reported after the Fontan operation and were absent in a series of Fontan patients examined specifically for the presence of PAVMs.2 The incidence of PAVMs after bidirectional cavopulmonary Glenn anastomoses (BDGs) has not been reported but also seems to be extremely low. However, this finding may be confounded by the short natural history of patients with a BDG, since the majority of such patients proceed to Fontan operations within 6 to 18 months after the creation of a BDG.
One exception to this sequence of BDG and early Fontan is patients with the polysplenia form of heterotaxy syndrome who have an interrupted inferior vena cava (IVC). In this form of heart disease, the IVC is interrupted, with only the hepatic veins entering the lower portion of the right atrium (RA). The remainder of the lower-body systemic venous return enters the SVC via the azygous system. Thus, in these cases, an SVC-to-PA anastomosis (BDG) directs all venous return to the pulmonary bed except for coronary sinus and hepatic venous blood. Two patients reported to have developed PAVMs after modified Fontan operations had similar anatomies and had BDG anastomoses that included all venous return except hepatic and coronary sinus blood.11
In this report, we describe all 10 patients with congenital heart disease (CHD) at our hospital who developed PAVMs as diagnosed by cardiac catheterization. A majority of these patients were diagnosed with a heterotaxy syndrome with interrupted IVC. This experience led to a review of all our patients with interrupted IVC, which is also included in this report. In all patients who developed PAVMs, the common anatomic feature was the exclusion of normal hepatic venous flow from the affected pulmonary vasculature. The angiographic and histological appearance of these PAVMs is similar to that seen in PAVMs associated with liver disease. We postulate that the occurrence of PAVMs in patients with CHD is related to the diversion of normal hepatic venous flow away from the pulmonary circulation. In this sense, PAVMs in CHD may be analogous to those associated with hepatic cirrhosis and may thus share a common pathogenesis.
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Methods |
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TopAbstractIntroductionMethods Results Discussion References |
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Data Collection
From the computerized cardiology data base at Children's Hospital, Boston, Mass, all patients diagnosed with both PAVMs and CHD between 1970 and 1993 were identified. Additionally, all patients with interrupted IVC anatomy were identified. Medical charts and echocardiographic and catheterization data were reviewed retrospectively, with close attention paid to the possible diagnoses of PAVMs and the patterns of hepatic and pulmonary blood flow. Follow-up data were obtained from charts and correspondence with the patients' referring physicians. All patients diagnosed with PAVMs were included in this study.
Diagnostic Criteria
The diagnosis of PAVM was made when there
was (1) resting
pulmonary venous desaturation without evidence of parenchymal
lung disease on chest roentgenogram and/or (2) demonstration of PAVMs
by selective pulmonary angiography. Pulmonary
arteriograms of patients presumed to have PAVMs and those without were
interpreted in a blinded fashion by two independent observers (V.M. and
J.F.K.).
Interpretation of Pulmonary Arteriograms
To confirm previous
diagnoses of PAVMs, pulmonary
arteriograms of patients with and without previous diagnoses of PAVMs
were interpreted in a blinded fashion by two independent observers.
Rapid arterial-to-venous transit time and a reticular
appearance of the lung parenchyma were used in establishing the
diagnosis (see Fig 1
). All patients with previous diagnoses of
PAVMs
were again thought to have PAVMs by both observers. Locations of PAVMs
are given in Table 1. PAVMs were seen in both the upper
and lower lobes of lungs. The classic reticular pattern was noted only
in the patients previously thought to have PAVMs. This pattern may
represent concomitant filling of arteries and veins. The
transit time from arterial to venous circulation was
assessed subjectively and was noted to be more rapid in all patients
with PAVMs. In addition, the lack of the capillary phase disappearance
of dye was noted only in patients thought to have PAVMs.
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Histological Studies
Autopsy slides were available in two
patients who had developed
PAVMs after CVPA and were reviewed with pathologists at our
institution. Evidence of abnormal pulmonary parenchymal and
vascular changes was noted compared with normal control subjects as
previously identified.12
Statistical Analysis
Actuarial survival curves were generated
for two groups of
patients with interrupted IVCs: those with CVPA and those without. A
log-rank test13 compared the probability of freedom from
PAVMs in patients with and without CVPA. In addition, Fisher's exact
test13 was used to compare the proportion of patients who
developed PAVMs in the two groups. Values of P<.05 were
considered statistically significant for both tests.
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Results |
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TopAbstractIntroductionMethods Results Discussion References |
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Patient Characteristics
Ten patients with CHD were found to have developed PAVMs over the 23-year period reviewed. Clinical characteristics of these patients, including anatomic arrangement, are shown in Table 1
. Six
patients had
heterotaxy syndrome with interrupted IVC, azygous continuation to the
SVC, and hepatic veins draining to the RA. Three of these patients
(patients 1 through 3) underwent anastomoses of the cranial end of the
SVC to the PA, ie, a BDG, as their definitive palliative procedure, and
they developed bilateral diffuse PAVMs between 3 and 4 years after
surgery. One patient (patient 4) had a left SVC anastomosed to the left
PA and the RA anastomosed to the right PA but had preferential blood
flow from the RA to the right PA, as demonstrated by angiography. This
patient developed PAVMs in the left lung only, whereas the right lung
(which continued to receive hepatic venous blood) remained unaffected.
Patient 5 had an interrupted IVC draining to a left SVC, and a left
classic Glenn procedure was performed because of pulmonary
vascular obstructive disease in the right lung after a Waterston shunt.
Hepatic veins drained to the RA, which then emptied into the systemic
arterial circulation. PAVMs developed in the left lung 4
years after the Glenn anastomosis, whereas the right lung was without
PAVMs. Patient 6 also had similar anatomy but underwent a
procedure that incorporated the hepatic veins into the
pulmonary circulation as well. Secondary to postoperative
complications, the patient was catheterized 1 month after surgery, and
it was found by contrast distribution that most, if not all, of the
hepatic venous flow was streaming to the right lung. PAVMs were noted
in the left lung only. The seventh patient had a bidirectional Glenn
anastomosis, and because of aortic oxygen saturations in the 85% to
90% range, a Fontan procedure was postponed. The IVC and hepatic veins
continued to drain to the RA. PAVMs were found bilaterally 3.5 years
after surgery. Patient 8 had a right classic Glenn shunt and developed
many small PAVMs in the right lung 4 years after surgery. The final 2
patients had complex CHD but did not undergo any type of CVPA. These
patients both had biliary atresia, and both developed bilateral PAVMs
that were angiographically similar to those seen in patients with
CVPAs. These developed despite normal anatomic and pulsatile flow of
hepatic venous blood to the lungs.
In summary, 4 patients developed
bilateral PAVMs after BDG; 2 patients
developed unilateral PAVMs after CVPAs that directed hepatic venous
flow to the contralateral lung; 2 patients were found to have
unilateral PAVMs after classic Glenn procedures to the ipsilateral
lung; and 2 patients had PAVMs associated with biliary atresia. As seen
in Table 1, the median time of diagnosis after surgery was 3.5
years.
Of note, 8 of 10 patients had the diagnosis made more than 2 years
after hepatic vein "diversion." The majority of patients were
diagnosed relatively recently, and follow-up has been brief, the median
follow-up being 0.7 years, with a range of 0.1 to 7.5 years.
Hemodynamic and Laboratory Data
Hemodynamic and laboratory
data at the time of
diagnosis are shown in Table 2. The median aortic
saturation was 77% (range, 50% to 90%), the median hemoglobin was
17.3 mg/dL (range, 9.0 to 18.9 mg/dL), and the median mean PA pressure
was 14 mm Hg (range, 10 to 20 mm Hg). Of note, 2 patients were found
to have PAVMs despite the presence of pulsatile flow in the PAs.
Pulmonary venous saturations were measured in 7 of 10 patients
(Table 2). Data on hepatic function were available in 8
patients.
Bilirubin levels ranged from 0.8 to 3.2 mg/dL, with a mean of 1.6 mg/dL
in the patients without biliary atresia. The 2 patients with biliary
atresia had significant elevation of serum bilirubin.
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Histology
Histological sections of the lungs were available
for study in 2 patients with PAVMs after CVPA, both deceased. The lungs
in patient 1 had a PA barium sulfate–gelatin injection under
nonstandard conditions, precluding vascular morphometric
analysis. Pulmonary arteries and veins were patent and
appeared to be of adequate caliber. The lungs in patient 6 were
examined after routine formalin fixation without injection of the PA
tree. The external diameter of respiratory and terminal bronchiolar
arteries and percentage medial wall thickness of PAs 200 to 300 µm in
diameter and septal veins 100 to 200 µm in diameter were determined
according to the method of Haworth and Hislop.12 The
respiratory bronchiolar arteries were dilated (95 µm observed, 64
µm expected), as were the terminal bronchiolar arteries (165 µm
observed, 120 µm expected) (Fig 2, top). The mean
percentage arterial wall medial thickness of arteries 200
to 300 µm in diameter was 5.9% and essentially similar to the
control value of 5.8%.12 The mean percentage wall
thickness of veins 100 to 200 µm in diameter was increased, with a
value of 6.6% compared with the control value of
4.3±1.4%.12 Some areas of pleura contained clusters of
predominantly thin-walled vessels of indeterminate origin showing a
thin elastic lamina and thin smooth-muscle-cell collar (Fig 2,
bottom).
Some ancient recanalized PA thromboemboli were present in the left
lung.
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Incidence of PAVM in Polysplenia
Given that 6 patients had
the common anatomy of
interrupted IVC with azygous continuation to the SVC and that a genetic
abnormality associated with heterotaxy syndrome has recently been
identified,14 we considered whether there might be an
association between heterotaxy syndrome and PAVMs. Therefore, we
reviewed all patients with interrupted IVC to determine whether this
anatomy alone promoted the development of PAVMs.
A total of 84 patients
were identified who had interrupted IVC
anatomy. Of the 84 patients, 56 (67%) did not have any type of
CVPA; only 1 of 56 (1.8%) of those without CVPA developed PAVMs. The 1
patient without CVPA who developed PAVMs also had biliary atresia. The
remaining 28 patients had CVPAs that excluded hepatic venous blood from
one or both lungs; 6 of 28 (21%) of these patients were found to have
PAVMs (P=.004) (Fig 3). Long-term clinical
follow-up was available for 55 of the 56 patients without CVPA (median,
8 years) and for 23 of the 28 with CVPA (median, 4 years). The
incidence of PAVMs in patients with long-term follow-up is 1 of 55
(1.8%) in those without CVPA and 6 of 23 (26%) in those with CVPA
(P=.004). Actuarial analysis of these patients (Fig
4, top) shows a 15% and 28% probability of developing
PAVMs 3 and 5 years, respectively, after CVPA. Fig 4, bottom,
compares
the development of PAVMs in interrupted IVC patients with and without
CVPA and shows a significant increase in probability for patients with
CVPAs (P=.002). Thus, in our series, patients with
interrupted IVC alone did not develop PAVMs but did have a higher
probability of PAVMs after exclusion of hepatic venous flow to the
lungs.
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Discussion |
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TopAbstractIntroductionMethods Results Discussion References |
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We have described a series of 10 patients with CHD who developed PAVMs and whose clinical description led to a common denominator: the exclusion of normal hepatic venous blood flow from the affected pulmonary circulation. Bilateral PAVMs were seen when both lungs were deprived of normal hepatic venous flow. In all cases in which one lung received hepatic venous blood and the remaining lung did not, only the latter developed PAVMs. The median duration from the time of CVPA to diagnosis of PAVM was 3.5 years. Two patients did show angiographic evidence of PAVMs less than 2 years after surgery, one with biliary atresia and a second at an early postoperative catheterization carried out because of an abnormal postoperative course. This patient died of a fatal arrhythmia soon after the catheterization.
Although the development of PAVMs was noted after the classic Glenn procedure, we found no reported cases of PAVMs after the Fontan operation, which directs hepatic and IVC blood, in addition to SVC blood, to the lungs. The majority of the patients in our series who developed PAVMs had a unique anatomic arrangement: heterotaxy/polysplenia syndrome having an interrupted IVC with azygous continuation to a SVC but hepatic veins still draining to the RA. Two patients with similar anatomy have been reported11 who developed diffuse, bilateral PAVMs after a "modified Fontan procedure," known as the Kawashima operation.15 The Kawashima procedure involves an anastomosis of the cranial end of the SVC to the PA (similar to a bidirectional Glenn procedure) and diverts all lower-body venous return to the PAs except hepatic venous return. These patients frequently have arterial oxygen saturations in the 85% to 90% range and have previously been thought to require no further intervention. In contrast, the long-term outcome after the usual type of BDG has been difficult to determine, since most patients with BDGs undergo subsequent completion to a Fontan type of circulation. In most patients who develop PAVMs after CVPA, detection is not for several years.
Although many patients with PAVMs after Glenn procedures have been reported, we have not found any histological descriptions of the pulmonary parenchyma in this condition. The pulmonary parenchymal changes associated with PAVMs in one of the patients in our series who had CVPA consisted of diffuse dilation of precapillary vessels. These resemble the "PAVMs" seen in patients with liver disease.7
A recent report of a patient with polysplenia who did not have a CVPA but did develop bilateral PAVMs raises the possibility of an inherent predisposition to PAVMs in patients with polysplenia.16 This patient had hypoplasia of the intrahepatic portal vein branches and a portal-to-systemic shunt; thus, mesenteric venous return bypassed the liver and went directly to the heart and lungs without metabolic reductions or additions. We nonetheless reviewed all our patients with polysplenia who did not have CVPA to determine whether polysplenia alone contributed to the development of PAVMs. However, only 1 of 56 patients with polysplenia syndrome but without CVPA developed PAVMs, and that patient had biliary atresia.
Although the first reported case of PAVMs was in 1897,17 the pathogenesis of PAVMs remains unclear. Hemodynamic alterations have been suggested, but in general, most intracardiac, PA (mean), and pulmonary capillary wedge pressures are normal.18 Normal hemodynamic findings were present in our series of patients as well. Maldistribution of pulmonary blood flow has been suggested as a possible cause of PAVMs.2 It has been shown that passive blood return to the lungs after a Glenn anastomosis results in flow to the lower lobes increased over normal compared with the upper lobes.2 Although this maldistribution is present in some patients after the Fontan operation,2 PAVMs have not been a complication of Fontan operations. Absence of pulsatile pulmonary blood flow has also been implicated in the development of PAVMs; however, our two patients with biliary atresia developed bilateral PAVMs in the presence of pulsatile blood flow.
These data strongly suggest that normal hepatic venous blood may play a role in the prevention of PAVMs. Patients with hepatic cirrhosis develop vascular dilations7 similar to those seen in our patients at the pulmonary precapillary and capillary levels,19 which are thought to cause diffusion-perfusion defects resulting in cyanosis. Pulmonary arteriograms in patients with liver disease and PAVMs are similar to the arteriograms in our patients. Although abnormal vasoactive agents have been found in hepatic venous blood in patients with cirrhosis,20 21 most of our patients had normal livers, thus implicating the absence of a normal factor rather than the presence of an abnormal one. Given the dilation of vessels seen histologically, the putative hepatic product may be involved in vasomotor control rather than angiogenic control. Since only the minority of patients with hepatic vein exclusion develop PAVMs, any causal relation between the former and latter must be complex, although it is possible that echocardiographic or radionuclide studies would reveal an even higher incidence of PAVMs. In a recent report, two patients with biliary atresia who had developed diffuse PAVMs underwent orthotopic liver transplantation and within 3 months were found to have resolution of intrapulmonary shunting,22 suggesting that return of normal hepatic blood flow to the lungs may reverse these lesions.
These data seem to permit several inferences. Angiographically, PAVMs should be suspected when pulmonary venous return is evident more rapidly than normal after contrast injection into the PAs. Patients with interrupted IVCs, and possibly others, who have had BDG-type operations diverting hepatic venous blood away from the lungs should be followed closely for the development of PAVMs. Patients who undergo BDG operations as a long-term palliation may benefit from adjunctive procedures that provide some source of normal hepatic blood to the lungs. The recent evidence of reversibility of PAVMs after liver transplantation in patients with cirrhosis raises the possibility that redirection of hepatic venous flow to the pulmonary bed in some patients with CHD and PAVMs may reverse the arteriovenous malformations.
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Acknowledgments |
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Deepak Srivastava, MD, is a fellow of the National Institutes of Health Pediatric Scientist Development Program. The authors would like to thank Lynne Reid, MD, Department of Pathology, Children's Hospital, for her review and consultation concerning the histological evaluation.
Received September 22, 1994; revision received February 15, 1995; accepted February 25, 1995.
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J. W. Brown, M. Ruzmetov, P. Vijay, M. D. Rodefeld, and M. W. Turrentine Pulmonary Arteriovenous Malformations in Children After the Kawashima Operation Ann. Thorac. Surg., November 1, 2005; 80(5): 1592 - 1596. [Abstract] [Full Text] [PDF]
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D. B. McElhinney, J. Kreutzer, P. Lang, J. E. Mayer Jr, P. J. del Nido, and J. E. Lock Incorporation of the Hepatic Veins Into the Cavopulmonary Circulation in Patients With Heterotaxy and Pulmonary Arteriovenous Malformations After a Kawashima Procedure Ann. Thorac. Surg., November 1, 2005; 80(5): 1597 - 1603. [Abstract] [Full Text] [PDF]
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D. B. McElhinney, A. C. Marshall, P. Lang, J. E. Lock, and J. E. Mayer Jr Creation of a Brachial Arteriovenous Fistula for Treatment of Pulmonary Arteriovenous Malformations After Cavopulmonary Anastomosis Ann. Thorac. Surg., November 1, 2005; 80(5): 1604 - 1609. [Abstract] [Full Text] [PDF]
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G. P. Georghiou, E. Erez, E. Bruckheimer, O. Dagan, B. A. Vidne, and E. Birk Anomalous Hepatic Venous Drainage Ann. Thorac. Surg., September 1, 2005; 80(3): 1113 - 1115. [Abstract] [Full Text] [PDF]
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 R Kaulitz and M Hofbeck Current treatment and prognosis in children with functionally univentricular hearts Arch. Dis. Child., July 1, 2005; 90(7): 757 - 762. [Abstract] [Full Text] [PDF]
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 G. P. Georghiou, E. Birk, and B. A. Vidne Is there a reversal of pulmonary arteriovenous malformation after redirection of anomalous hepatic venous flow to the lungs? Interactive CardioVascular and Thoracic Surgery, June 1, 2005; 4(3): 227 - 231. [Abstract] [Full Text] [PDF]
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A. Ikai, M. Shirai, K. Nishimura, T. Ikeda, T. Kameyama, K. Ueyama, and M. Komeda Maintenance of pulmonary vasculature tone by blood derived from the inferior vena cava in a rabbit model of cavopulmonary shunt J. Thorac. Cardiovasc. Surg., January 1, 2005; 129(1): 199 - 206. [Abstract] [Full Text] [PDF]
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 T. B. Kinane and S. J. Westra Case 31-2004 - A Four-Year-Old Boy with Hypoxemia N. Engl. J. Med., October 14, 2004; 351(16): 1667 - 1675. [Full Text] [PDF]
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 D. M. McMullan, F. L. Hanley, G. A. Cohen, M. A. Portman, and R. K. Riemer Pulmonary arteriovenous shunting in the normal fetal lung J. Am. Coll. Cardiol., October 6, 2004; 44(7): 1497 - 1500. [Abstract] [Full Text] [PDF]
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E. Aidala, E. Chiappa, M. T. Cascarano, A. Valori, and P. A. Abbruzzese Partial hepatic vein diversion in pulmonary arteriovenous malformations in congenital heart disease Ann. Thorac. Surg., September 1, 2004; 78(3): 1089 - 1090. [Abstract] [Full Text] [PDF]
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N. A. Pike, L. A. Vricella, J. A. Feinstein, M. D. Black, and B. A. Reitz Regression of severe pulmonary arteriovenous malformations after Fontan revision and "hepatic factor" rerouting Ann. Thorac. Surg., August 1, 2004; 78(2): 697 - 699. [Abstract] [Full Text] [PDF]
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A. Ikai, R. K. Riemer, X. Ma, O. Reinhartz, F. L. Hanley, and V. M. Reddy Pulmonary expression of the hepatocyte growth factor receptor c-Met shifts from medial to intimal layer after cavopulmonary anastomosis J. Thorac. Cardiovasc. Surg., May 1, 2004; 127(5): 1442 - 1449. [Abstract] [Full Text] [PDF]
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A. Ikai, M. Shirai, K. Nishimura, T. Ikeda, T. Kameyama, K. Ueyama, and M. Komeda Hypoxic pulmonary vasoconstriction disappears in a rabbit model of cavopulmonary shunt J. Thorac. Cardiovasc. Surg., May 1, 2004; 127(5): 1450 - 1457. [Abstract] [Full Text] [PDF]
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A. Dodge-Khatami, N. Sreeram, B.A.J.M. de Mol, and G.B.W.E. Bennink Systemic plasma vascular endothelial growth factor levels as a marker for increased angiogenesis during the single ventricle surgical pathway Interactive CardioVascular and Thoracic Surgery, December 1, 2003; 2(4): 458 - 461. [Abstract] [Full Text] [PDF]
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B. W. Duncan and S. Desai Pulmonary arteriovenous malformations after cavopulmonary anastomosis Ann. Thorac. Surg., November 1, 2003; 76(5): 1759 - 1766. [Abstract] [Full Text] [PDF]
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Y. Ootaki, M. Yamaguchi, N. Yoshimura, S. Oka, M. Yoshida, and T. Hasegawa Vascular endothelial growth factor in children with congenital heart disease Ann. Thorac. Surg., May 1, 2003; 75(5): 1523 - 1526. [Abstract] [Full Text] [PDF]
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J. Steinberg, G. M. Alfieris, B. Brandt III, F. Smith, C. J. Byrum, G. W. Fink, and J. Halter New approach to the surgical management of pulmonary arteriovenous malformations after cavopulmonary anastomosis Ann. Thorac. Surg., May 1, 2003; 75(5): 1640 - 1642. [Abstract] [Full Text] [PDF]
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 A. Mishra, S. R. Krishna Manohar, R. Sankar Kumar, and M. S. Valiathan Bidirectional Glenn Shunt For Right Ventricular Endomyocardial Fibrosis Asian Cardiovasc Thorac Ann, December 1, 2002; 10(4): 351 - 353. [Abstract] [Full Text] [PDF]
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 H Ashrafian and L Swan The mechanism of formation of pulmonary arteriovenous malformations associated with the classic Glenn shunt (superior cavopulmonary anastomosis) Heart, December 1, 2002; 88(6): 639 - 639. [Full Text] [PDF]
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 S. L. Starnes, B. W. Duncan, C. H. Fraga, S. Y. Desai, T. K. Jones, S. K. Mathur, G. L. Rosenthal, and F. M. Lupinetti Rat model of pulmonary arteriovenous malformations after right superior cavopulmonary anastomosis Am J Physiol Heart Circ Physiol, November 1, 2002; 283(5): H2151 - H2156. [Abstract] [Full Text] [PDF]
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S. P. Malhotra, V. M. Reddy, S. Thelitz, Y.-P. He, D. M. McMullan, F. L. Hanley, and R. K. Riemer The role of oxidative stress in the development of pulmonary arteriovenous malformations after cavopulmonary anastomosis J. Thorac. Cardiovasc. Surg., September 1, 2002; 124(3): 479 - 485. [Abstract] [Full Text] [PDF]
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S. P. Malhotra, V. M. Reddy, S. Thelitz, Y.-P. He, F. L. Hanley, S. Suleman, and R. K. Riemer Cavopulmonary anastomosis induces pulmonary expression of the angiotensin II receptor family J. Thorac. Cardiovasc. Surg., April 1, 2002; 123(4): 655 - 660. [Abstract] [Full Text] [PDF]
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Y. Kaneko, A. Murakami, T. Miyamoto, and S. Takamoto Hepatic vein-to-azygos vein connection in a patient with interrupted inferior vena cava Eur. J. Cardiothorac. Surg., March 1, 2002; 21(3): 582 - 584. [Abstract] [Full Text] [PDF]
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J. M. Chu, Q. Y. Wu, and W. M. Wang Pulmonary Blood Distribution After Total Cavopulmonary Connection Asian Cardiovasc Thorac Ann, December 1, 2001; 9(4): 282 - 285. [Abstract] [Full Text] [PDF]
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I. E. Konstantinov, F. J. Puga, and V. V. Alexi-Meskishvili Thrombosis of intracardiac or extracardiac conduits after modified Fontan operation in patients with azygous continuation of the inferior vena cava Ann. Thorac. Surg., November 1, 2001; 72(5): 1641 - 1644. [Abstract] [Full Text] [PDF]
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G. Agnoletti, A. Borghi, F. P. Annecchino, and G. Crupi Regression of pulmonary fistulas in congenital heart disease after redirection of hepatic venous flow to the lungs Ann. Thorac. Surg., September 1, 2001; 72(3): 909 - 911. [Abstract] [Full Text] [PDF]
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S. P. Malhotra, R. K. Riemer, S. Thelitz, Y.-P. He, F. L. Hanley, and V. M. Reddy Superior cavopulmonary anastomosis suppresses the activity and expression of pulmonary angiotensin-converting enzyme J. Thorac. Cardiovasc. Surg., September 1, 2001; 122(3): 464 - 469. [Abstract] [Full Text] [PDF]
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S. L. Starnes, B. W. Duncan, J. M. Kneebone, G. L. Rosenthal, K. Patterson, C. H. Fraga, K. M. Kilian, S. K. Mathur, and F. M. Lupinetti Angiogenic proteins in the lungs of children after cavopulmonary anastomosis J. Thorac. Cardiovasc. Surg., September 1, 2001; 122(3): 518 - 523. [Abstract] [Full Text] [PDF]
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S. J. Kim, E. J. Bae, D. J. Cho, I. S. Park, Y. M. Kim, W.-H. Kim, and S. H. Kim Development of pulmonary arteriovenous fistulas after bidirectional cavopulmonary shunt Ann. Thorac. Surg., December 1, 2000; 70(6): 1918 - 1922. [Abstract] [Full Text] [PDF]
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S. L. Starnes, B. W. Duncan, J. M. Kneebone, C. H. Fraga, S. States, G. L. Rosenthal, and F. M. Lupinetti Pulmonary microvessel density is a marker of angiogenesis in children after cavopulmonary anastomosis J. Thorac. Cardiovasc. Surg., November 1, 2000; 120(5): 902 - 908. [Abstract] [Full Text] [PDF]
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P. G. Walker, T. T. Howe, R. L. Davies, J. Fisher, and K. G. Watterson Distribution of hepatic venous blood in the total cavo-pulmonary connection: an in vitro study Eur. J. Cardiothorac. Surg., June 1, 2000; 17(6): 658 - 665. [Abstract] [Full Text] [PDF]
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M. L. Jacobs, K. K. Pourmoghadam, E. M. Geary, K. L. Wright, and V. R. Zales Pulmonary arteriovenous malformations after cavopulmonary connection Ann. Thorac. Surg., February 1, 2000; 69(2): 634 - 635. [Abstract] [Full Text] [PDF]
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 M J KROWKA Hepatopulmonary syndromes Gut, January 1, 2000; 46(1): 1 - 4. [Full Text] [PDF]
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E. A. Bacha, R. A. Jonas, J. E. Mayer Jr, S. Perry, and P. J. del Nido MANAGEMENT OF PULMONARY ARTERIOVENOUS MALFORMATIONS AFTER SURGERY FOR COMPLEX CONGENITAL HEART DISEASE J. Thorac. Cardiovasc. Surg., January 1, 2000; 119(1): 175 - 176. [Full Text] [PDF]
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R. D. Mainwaring, J. J. Lamberti, K. Uzark, R. L. Spicer, M. W. Cocalis, and J. W. Moore Effect of Accessory Pulmonary Blood Flow on Survival After the Bidirectional Glenn Procedure Circulation, November 9, 1999; 100 (2009): II-151 - II-156. [Abstract] [Full Text] [PDF]
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H. Uemura, T. Yagihara, R. Hattori, Y. Kawahira, S. Tsukano, and K. Watanabe Redirection of hepatic venous drainage after total cavopulmonary shunt in left isomerism Ann. Thorac. Surg., November 1, 1999; 68(5): 1731 - 1735. [Abstract] [Full Text] [PDF]
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A. C. Lardo, S. A. Webber, A. Iyengar, P. J. del Nido, I. Friehs, and E. G. Cape BIDIRECTIONAL SUPERIOR CAVOPULMONARY ANASTOMOSIS IMPROVES MECHANICAL EFFICIENCY IN DILATED ATRIOPULMONARY CONNECTIONS J. Thorac. Cardiovasc. Surg., October 1, 1999; 118(4): 681 - 691. [Abstract] [Full Text] [PDF]
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A. E. Ensley, P. Lynch, G. P. Chatzimavroudis, C. Lucas, S. Sharma, and A. P. Yoganathan Toward designing the optimal total cavopulmonary connection: an in vitro study Ann. Thorac. Surg., October 1, 1999; 68(4): 1384 - 1390. [Abstract] [Full Text] [PDF]
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R Premsekar, J L Monro, and A P Salmon Diagnosis, management, and pathophysiology of post-Fontan hypoxaemia secondary to Glenn shunt related pulmonary arteriovenous malformation Heart, October 1, 1999; 82(4): 528 - 530. [Abstract] [Full Text] [PDF]
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M. Remy-Jardin and J. Remy Spiral CT Angiography of the Pulmonary Circulation Radiology, September 1, 1999; 212(3): 615 - 636. [Abstract] [Full Text]
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R. J.F. Baskett, D. B. Ross, A. E. Warren, G. P. Sharratt, and D. A. Murphy Hepatic vein to the azygous vein anastomosis for pulmonary arteriovenous fistulae Ann. Thorac. Surg., July 1, 1999; 68(1): 232 - 233. [Abstract] [Full Text] [PDF]
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J. E. Mayer Jr Ann. Thorac. Surg., July 1, 1999; 68(1): 233 - 233. [Full Text] [PDF]
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U. M. Pandurangi, M. J. Shah, R. Murali, and K. M. Cherian Rapid onset of pulmonary arteriovenous malformations after cavopulmonary anastomosis Ann. Thorac. Surg., July 1, 1999; 68(1): 237 - 239. [Abstract] [Full Text] [PDF]
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R.-K. R. Chang, J. C. Alejos, D. Atkinson, R. Jensen, S. Drant, A. Galindo, and H. Laks Bubble contrast echocardiography in detecting pulmonary arteriovenous shunting in children with univentricular heart after cavopulmonary anastomosis J. Am. Coll. Cardiol., June 1, 1999; 33(7): 2052 - 2058. [Abstract] [Full Text] [PDF]
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M. G. Kiaffas, R. Van Praagh, C. Hanioti, and D. W. Green The modified Fontan procedure: morphometry and surgical implications Ann. Thorac. Surg., June 1, 1999; 67(6): 1746 - 1753. [Abstract] [Full Text] [PDF]
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A. Gerdes, J. Kunze, G. Pfister, and H.-H. Sievers Addition of a small curvature reduces power losses across total cavopulmonary connections Ann. Thorac. Surg., June 1, 1999; 67(6): 1760 - 1764. [Abstract] [Full Text] [PDF]
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B. W. Duncan, J. M. Kneebone, E. Y. Chi, V. Hraska, F. F. Isik, G. L. Rosenthal, T. K. Jones, S. L. Starnes, and F. M. Lupinetti A DETAILED HISTOLOGIC ANALYSIS OF PULMONARY ARTERIOVENOUS MALFORMATIONS IN CHILDREN WITH CYANOTIC CONGENITAL HEART DISEASE J. Thorac. Cardiovasc. Surg., May 1, 1999; 117(5): 931 - 938. [Abstract] [Full Text] [PDF]
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A. R. Mott, T. L. Spray, and N. D. Bridges Heart/single-lung transplant for a ""failed Fontan"" with pulmonary A-V malformation Ann. Thorac. Surg., March 1, 1999; 67(3): 841 - 843. [Abstract] [Full Text] [PDF]
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S. M. Marianeschi, D. B. McElhinney, and V. M. Reddy Pulmonary arteriovenous malformations in and out of the setting of congenital heart disease Ann. Thorac. Surg., August 1, 1998; 66(2): 688 - 691. [Abstract] [Full Text] [PDF]
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J. Lee, A. H. Menkis, and H. C. Rosenberg Reversal of Pulmonary Arteriovenous Malformation After Diversion of Anomalous Hepatic Drainage Ann. Thorac. Surg., March 1, 1998; 65(3): 848 - 849. [Abstract] [Full Text] [PDF]
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L. Mace, P. Dervanian, J. Losay, T. A. Folliguet, J.-M. Grinda, S. Abdelmoulah, J.-F. Verrier, F. Santoro, and J.-Y. Neveux Bidirectional Inferior Vena Cava-Pulmonary Artery Shunt Ann. Thorac. Surg., May 1, 1997; 63(5): 1321 - 1325. [Abstract] [Full Text]
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Y. Kawashima Cavopulmonary Shunt and Pulmonary Arteriovenous Malformations Ann. Thorac. Surg., April 1, 1997; 63(4): 930 - 932. [Full Text]
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M. J. Shah, J. Rychik, M. A. Fogel, J. D. Murphy, and M. L. Jacobs Pulmonary AV Malformations After Superior Cavopulmonary Connection: Resolution After Inclusion of Hepatic Veins in the Pulmonary Circulation Ann. Thorac. Surg., April 1, 1997; 63(4): 960 - 963. [Abstract] [Full Text]
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D. J. Schneider, A. Banerjee, A. M. Mendelsohn, and W. I. Norwood Jr Hepatic Venous Malformation After Modified Fontan Procedure With Partial Hepatic Vein Exclusion Ann. Thorac. Surg., April 1, 1997; 63(4): 1177 - 1179. [Abstract] [Full Text]
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T. C. Koutlas, J. K. Harrison, T. M. Bashore, M. P. O'Laughlin, M. E. Tripp, and J. W. Gaynor Late Conduit Occlusion After Modified Fontan Procedure With Classic Glenn Shunt Ann. Thorac. Surg., July 1, 1996; 62(1): 258 - 261. [Abstract] [Full Text]
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