Circulation. 1999;100:II-151-II-156
(Circulation. 1999;100:II-151.)
© 1999 American Heart Association, Inc.
Surgery for Congenital Heart Disease |
Effect of Accessory Pulmonary Blood Flow on Survival After the Bidirectional Glenn Procedure
Richard D. Mainwaring, MD;
John J. Lamberti, MD;
Karen Uzark, PhD;
Robert L. Spicer, MD;
Mark W. Cocalis, MD;
John W. Moore, MD
From the Cardiac Institute, Childrens HospitalSan Diego,
San Diego, Calif.
Correspondence to Richard D. Mainwaring, MD, Alfred I. duPont Hospital for Children, Nemours Cardiac Center, 1600 Rockland Rd, Wilmington, DE 19803. E-mail rmainwar{at}nemours.org
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Abstract
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BackgroundThe bidirectional
Glenn procedure (BDG) is
used in the staged surgical management of
patients with a functional
single ventricle. Controversy exists
regarding whether accessory
pulmonary blood flow (APBF) should
be left at the time of BDG
to augment systemic saturation or be
eliminated to reduce volume
load of the ventricle. The present
study was a retrospective
review of patients undergoing BDG that was
conducted to assess
the influence of APBF on survival rates.
Methods and ResultsFrom 1986 through 1998, 149 patients have
undergone BDG at our institution. Ninety-three patients had elimination
of all sources of APBF, whereas 56 patients had either a shunt or a
patent right ventricular outflow tract intentionally left
in place to augment the pulmonary blood flow provided by the
BDG. The operative mortality rate was 2.2% without APBF and 5.4% with
APBF. The late mortality rate was 4.4% without APBF and 15.1% with
APBF. Actuarial analysis demonstrates a divergence of the
Kaplan-Meier curves in favor of patients in whom APBF was eliminated
(P<0.02). One hundred seven patients have subsequently
undergone completion of their Fontan operation, so the actuarial
analysis includes the operative risk of this second
operation.
ConclusionsThe results suggest that the elimination of APBF at
the time of BDG may confer a long-term advantage for patients with a
functional single ventricle.
Key Words: blood flow Fontan procedure mortality morbidity
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Introduction
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The bidirectional Glenn procedure (BDG) is used as the
first
of 2 operations to achieve separation of the systemic and
pulmonary
circulations in patients with a functional single
ventricle.
1 This 2-staged approach to Fontan completion
has resulted in
a significant reduction in mortality rates during the
past decade.
2 3 4 The original premise for this approach
was based on the
elimination of ventricular volume work at
an early age and the
stepwise accommodation of ventricular
geometry to the reduction
in volume load.
5 6 Other factors
that have favorably influenced
outcome include the earlier elimination
of systemicpulmonary
artery shunts
7 and the
influence of interventional cardiology
techniques.
8 Improved results have made BDG an integral
part of the management
of single-ventricle patients.
9
A number of controversies remain regarding the BDG, including the
timing of the procedure and the interval to Fontan completion. In
addition, there exists a controversy regarding the use or elimination
of accessory pulmonary blood flow (APBF). Advocates for the
provision of APBF cite more "physiological"
levels of oxygen saturation, inhibition of arteriovenous malformations,
and the potential to decrease the development of pulmonary
arterial collateral vessel development.10 It
has also been proposed that APBF may stimulate pulmonary artery
growth, resulting in patients being better candidates for the Fontan
procedure.11 Conversely, advocates for the elimination of
APBF emphasize the importance of eliminating volume loads to allow the
remodeling of the ventricle that occurs after this procedure. The
elimination of APBF results in a degree of hypoxemia that is usually
well tolerated in infancy and permits adequate growth of the
pulmonary arteries to allow completion of the Fontan procedure.
However, as a consequence of these divergent opinions and observations,
there remain a variety of algorithms that have evolved regarding the
management of single-ventricle patients and the use of APBF at the time
of BDG.
We previously reported our experience with the BDG and the influence of
APBF.12 This report, in which we evaluated 92 patients
through mid-1994, reported that the incidence of effusions and the
likelihood of prolonged hospital stay were higher when APBF was used.
Actuarial analysis did not reveal a statistical difference in
survival rates for the 2 groups; however, there was a trend toward
improved survival rates in the patients without APBF. The purpose of
this update was to evaluate the effect of APBF on survival rates after
BDG in a larger cohort of patients and with a longer duration of
follow-up.
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Methods
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This study is a retrospective review of our experience with
BDG
in patients with a functional single ventricle. The medical
records
were reviewed, and 2 groups were formulated based on
the presence or
absence of APBF, which is defined as either
a
systemicpulmonary artery shunt or a patent right
ventricular
outflow tract. Aortopulmonary
collaterals are not included in
this definition of APBF.
From 1986 through August 1998, 149 patients underwent BDG at
Childrens HospitalSan Diego as part of the staged surgical
management leading to Fontan completion. Excluded from this
analysis were 4 patients (2 with and 2 without APBF) in whom
surgery failed to achieve pulmonary blood flow to both lungs
secondary to technical considerations. (Details for these 4 patients
are given in our previous report.12 ) In addition, there
were 8 patients who underwent BDG as part of a one and one-half
ventricle approach. This cohort was also excluded from this study
because they were not patients with a functional single ventricle in
whom Fontan completion was contemplated.
Figure 1
shows the number of BDGs
performed annually and delineates those with and without APBF.
Fifty-six of the 149 patients had inclusion of APBF. The median age of
these patients at time of surgery was 10 months (range, 2.5 to 195
months), and the median weight was 7.1 kg (range, 3.9 to 37 kg). The
median year of surgery was 1991. Ninety-three patients had no APBF at
the time of BDG; the median age for these patients was 8 months (range,
2.2 to 46 months), and the median weight was 6.1 kg (range, 3.9 to 15.8
kg). The median year of surgery for patients without APBF was 1994. The
diagnoses and ventricular morphology for the 2 groups are
listed in Table 1
.

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Figure 1. BDG procedures performed at the Childrens
HospitalSan Diego from February 1986 through August 1998. Filled
column represents number of patients who underwent BDG with
APBF. Hatched column represents number of patients who
underwent BDG as sole source of pulmonary blood flow.
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Pleural effusions were defined as the need for chest tube drainage for
>7 days. Prolonged hospitalization was defined as a length of stay of
>14 days.
Results of this study are reported as either the mean±SEM value or the
median and range values. Statistical comparison of the 2 groups was
performed with the use of 2-tailed log-rank analysis.
Kaplan-Meier survival curves were constructed using the
product-limit method. A comparison of the Kaplan-Meier curves was
performed using Fishers exact test. A P value of <0.05
was considered significant.
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Results
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There were 5 operative deaths, for an overall early mortality
rate
of 3.3%. Three of these early deaths occurred in patients
with APBF
(5.4%), and 2 occurred in patients without APBF (2.2%).
One hundred
forty-four patients underwent successful BDG; this
total included 53
with APBF and 91 without APBF. The incidence
of pleural effusions was
16% with APBF and 2% without APBF.
The length of hospital stay for
the 2 groups is shown in Figure
2

; the
median length of stay was 8 days for both groups. Prolonged
hospital
stay occurred in 13 patients (24%) with APBF and 7
patients (8%)
without APBF (
P<0.05); the causes for prolonged
hospital
stay are listed in Table 2

.

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Figure 2. Length of hospital stay for patients
undergoing BDG with and without APBF. Filled column represents
number of patients who underwent BDG with APBF. Hatched column
represents number of patients who underwent BDG as sole source
of pulmonary blood flow.
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Of the 144 patients who underwent successful BDG, 142 have been
followed for an average duration of 70±12 months (Figure 3
). There were 2 patients who were lost
to follow-up (1 in 1990 and 1 in 1992); both were from the APBF group.
These 2 patients have been dropped from the actuarial curve at the
point of last contact.
There were 12 late deaths: 8 patients (15.1%) with APBF and 4 patients
(4.4%) without APBF. Seven of these deaths occurred in the interim
between BDG and the Fontan procedure. The remaining 5 deaths either
occurred perioperatively at the time of Fontan
completion or were late deaths after the Fontan procedure. The causes
of early and late deaths are summarized in Table 3
.
Actuarial analysis was performed for patients undergoing BDG
with and without APBF. Figure 4
demonstrates the actuarial survival curves when the operative mortality
rate of the procedure is included. A comparison of these 2 curves
demonstrates a survival advantage in the patients in whom APBF was
eliminated (P<0.02). Figure 5
demonstrates the actuarial survival curves when operative mortality is
excluded, again demonstrating improved survival without APBF
(P<0.04).

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Figure 4. Actuarial analysis of patients undergoing
BDG with and without APBF. This analysis includes operative
mortality rate at time of BDG.
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Figure 5. Actuarial analysis of patients undergoing
BDG with and without APBF when operative mortality rate is
excluded.
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One hundred thirty-five patients in this series (149 minus 5 operative
deaths, 7 interim deaths, and 2 lost to follow-up) were potentially
eligible for Fontan completion. Of these patients, 25 (9 with and 16
without APBF) have had BDG relatively recently (average follow-up, 6±1
month) and, therefore, have not had their Fontan evaluation. Three
patients (2 with and 1 without APBF) in this series were deemed
unsuitable candidates for Fontan completion due to elevated
pulmonary vascular resistance; these 3 patients remain alive in
a palliated state. One hundred seven patients have undergone completion
of their Fontan procedure; this includes 36 patients with APBF (77% of
surviving cohort) and 71 patients without APBF (81% of survivors in
this cohort). There were 3 early deaths after the Fontan
procedure, which were attributed to low cardiac output in 2 patients
and a cerebrovascular accident in 1. There also were 2 late deaths
after the Fontan procedure; both were related to progressive hypoxemia
and pulmonary dysfunction. The probability of undergoing BDG
and ultimately achieving Fontan success was 74% with APBF and 92%
without APBF (P<0.01) (Figure 6
).

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Figure 6. Probability of achieving Fontan survival based on
presence or absence of APBF at time of BDG.
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Discussion
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The purpose of this report was to evaluate the effect of APBF
on
survival after BDG. One hundred forty-nine BDGs were performed
at our
institution from 1986 to 1998. The early mortality rate
was 5.4% with
APBF and 2.2% without APBF, and the late mortality
rate was 15.1%
with and 4.4% without APBF. These data suggest
that the elimination of
APBF may confer a survival advantage
in patients undergoing BDG.
The reasons for the divergence of the survival curves in this series
remain uncertain. The BDG results in an immediate decrease in both
preload and afterload, as well as favorable alterations in
ventricular geometry. It has been hypothesized that these
changes may have long-term beneficial effects on the preservation of
myocardial performance.13 14 The inclusion of APBF
will increase the volume work of the ventricle, thereby mollifying the
beneficial effects seen in the absence of APBF. The inclusion of APBF
may also have an adverse effect on pulmonary vasculature,
because it represents a high-pressure source of
pulmonary blood flow that may lead to alterations in
pulmonary vascular resistance.7 The elimination of
APBF may result in an improvement in both myocardial
performance and pulmonary vascular resistance, which
may confer advantages not only at the time of Fontan but also in the
long term. In our series, the incorporation of APBF resulted in a
combined early and late mortality rate that was significantly greater
than that seen in patients without APBF. Some of the late deaths were
cardiac related (eg, Fontan mortality), whereas others were clearly not
related to cardiac issues (eg, tracheal complication). The disparity
between the actuarial curves continues to widen during the first 2
years, suggesting that APBF may have adverse effects that manifest well
after the perioperative time period.
The incidence of pleural effusions requiring chest tube drainage for
>7 days was 8-fold higher in patients with APBF than in those without
APBF, an observation that we and others have previously
reported.12 15 Similar observations relating the incidence
of effusions to the presence of significant aortopulmonary
artery collateral vessels have been made in patients undergoing the
Fontan procedure.16 The cause of effusions after BDG and
Fontan procedures remains uncertain, but the incidence clearly
increases in the presence of left-to-right shunts. In theory, APBF or
aortopulmonary collaterals provide competitive flow to the
lungs and may increase pressures in the systemic venous pathways. Also,
these additional sources of pulmonary blood flow
represent a "steal" from the systemic circulation and thus
may contribute to the incidence of low cardiac output and the
endocrinologic changes that have been associated with pleural
effusions.17 Because the presence of effusions is a
principal determinant of length of stay for this operation, it is not
surprising that patients with APBF had longer lengths of stay in the
hospital.
Oxygen saturation levels are typically in the 80% range for most
infants undergoing BDG without APBF. However, saturation levels may be
considerably <80% in patients <4 months old or in children >4 or 5
years old. It remains unclear why pediatric patients at either
end of the age spectrum have marked differences in their physiology
compared with those in the middle of the spectrum. These observations
suggest that APBF may be both beneficial and necessary at the age
extremes. From an institutional standpoint, we have performed most of
our BDGs when the children were 6 to 12 months old. We then proceeded
with Fontan completion
1 year later. By establishing this
programmatic approach, we have largely avoided the extreme hypoxemia
that may be seen in very young infants or in older children.
Advocates for the inclusion of APBF suggest that the increase in
pulmonary blood flow will result in higher levels of
oxygenation and thus obviate excessive
hypoxemia.18 Any benefit of improved
oxygenation must offset the increase in
ventricular volume work attendant to this approach. An
inherent difficulty of including APBF is the regulation of flow through
that additional source, because excessive pulmonary blood flow
may have all of the adverse effects noted above. Because the eventual
goal in these patients is to separate their systemic and
pulmonary circulations, it seems that success in achieving this
would be a logical end point. The present series provides midterm
follow-up of the BDG and suggests that survival is appreciably higher
in patients in whom APBF is eliminated.
Pulmonary artery growth patterns have been a theoretical
concern in terms of the interim between the BDG and completion of the
Fontan procedure.19 20 It is not surprising that
pulmonary artery growth is diminished after BDG, because the
pulmonary-to-systemic flow ratio is appreciably
<1.21 Pulmonary artery growth patterns are
improved when APBF is included,11 and this has been
presented as a plausible argument for APBF. Some reports have
correlated pulmonary artery size with successful Fontan
outcome,22 whereas others have found it not to be
predictive of operative survival.23 24 If
pulmonary artery size were universally accepted as an indicator
of survival, then inclusion of APBF would be a way to achieve this end.
In our experience, 97% of the patients who were evaluated for
completion of their Fontan procedure subsequently underwent this
operation with a <3% operative mortality rate. None of our patients
have been turned down for Fontan completion due to pulmonary
artery size criteria; therefore, our experience suggests that
pulmonary artery growth is satisfactory for Fontan completion
regardless of whether APBF is used.
The development of pulmonary arteriovenous malformations (AVMs)
has been another theoretical concern after BDG. Pulmonary AVMs
have been seen after a classic Glenn shunt and after the Kawashima
operation. Both of these procedures exclude hepatic venous circulation
to the lungs on the first pass, suggesting a "hepatic factor" in
the cause of pulmonary AVMs.25 Advocates for APBF
have suggested that the accessory source will allow sufficient hepatic
venous blood to pass through the lungs to prevent pulmonary AVM
formation.11 However, we have seen the development of
pulmonary AVMs only in the setting of heterotaxy with
interrupted vena cava and azygous continuation (eg, polysplenia or left
isomerism). There were 4 patients in our series with this
anatomy, 2 of whom subsequently developed pulmonary
AVMs. One of these 2 patients had APBF, indicating that a source of
APBF may not protect from AVM formation. More importantly, none of our
BDG patients with situs solitus have developed pulmonary AVMs
detectable either clinically or with
echocardiography and pulmonary angiography,
which were routinely performed before Fontan completion. It is
conceivable that the presence of small AVMs could have been overlooked
in this evaluation, but none have surfaced during follow-up of the
Fontan patients. Thus, we believe that pulmonary AVM formation
is not an indication for inclusion of APBF.
One limitation of this study relates to the retrospective and
nonrandomized design. This study format may always be subject to
criticism insofar as there is the potential for a selection process or
learning curve that could bias the results. The inclusion of APBF was
our preferred surgical approach from 1986 to 1990, whereas from 1991 to
1998, we have usually, but not always, eliminated APBF. Since 1991, the
use of APBF has related to referral source (eg, cardiologist
preference) rather than to patient diagnosis or physiology. The 2
groups were similar with regard to age and weight at surgery, duration
of follow-up, and percentage of patients who have completed their
Fontan procedure. The groups were dissimilar in the year of surgery,
because the group with APBF tended to be earlier in the series. There
also was some dissimilarity with regard to diagnoses, because most of
our experience with hypoplastic left heart accrued in the 1990s. As a
consequence, the group without APBF had a disproportionate number of
patients with hypoplastic left heart syndrome and a higher percentage
of patients with right ventricular morphology. This
dissimilarity potentially may have favored the group with APBF, because
hypoplastic left heart syndrome and right ventricular
morphology have been considered risk factors in some studies. All of
the procedures (149 BDG and 107 Fontan) were performed by the 2
surgeons (R.D.M. and J.J.L.); we believe that the disparity between the
actuarial curves is indicative of the effect of APBF on survival and
not a function of the study design. The only way to prove this point
would be to embark on a prospective, multi-institutional trial. This
type of study not only could evaluate the influence of APBF on survival
but also could assess some of the factors that may ultimately
contribute to survivability, such as the effect of APBF on
ventricular cavity size, pressure, and wall thickness and
the influence of APBF on native aortopulmonary collateral
vessel development.
In summary, the results of this study demonstrate a significant
survival advantage when APBF is eliminated at the time of BDG. In
addition, the probability of continuing to a successful Fontan
procedure completion was higher in the patients without APBF. We
postulate that this survival advantage may be based on improvement in
pulmonary resistance and ventricular function. It
is our belief that the elimination of APBF at the time of BDG will
improve the long-term outlook after Fontan procedure completion.
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