JRSSEM 2022, Vol. 01, No. 10, 1731 – 1741
E-ISSN: 2807 - 6311, P-ISSN: 2807 - 6494
DOI : 10.36418/jrssem.v1i10.183 https://jrssem.publikasiindonesia.id/index.php/jrssem/index
INCREASED MORTALITY RATE IN PATIENT WITH FROTHY
SPUTUM AFTER TOF TOTAL CORRECTION SURGERY
Suprayitno Wardoyo
1
Dhama Shinta Susanti
2
Aflah Dhea Bariz Yasta
3*
Rendy Agustian
4
Laksana Paduan Wilangsoka
5
Universitas Indonesia, Jakarta, Indonesia
e-mail: Supray1@yahoo.co.id
1
, drdhama2015@gmail.com
2
, aflahdheabariz@gmail.com
3
,
rendy.agustian.m.d@gmail.com
4
, laksanapaduan@gmail.com
5
*Correspondence: aflahdheabariz@gmail.com
Submitted: 27 April 2022, Revised: 09 May 2022, Accepted: 20 May 2022
Abstract. Tetralogy of Fallot (TOF) is the most common congenital heart disease. The most
common risk factor for TOF is Down syndrome(DS). There are two management approaches for
TOF: medication and operation. Operation/surgical treatment is consisted of palliative shunt and
definitive repair. In several case patients with TOF develop collaterals or major aortopulmonary
collateral arteries (MAPCAs), which can lung overflow can be initiated after surgery procedure was
completed. This causes the CPB time in the repair operation to be long so that the risk of RV/LV
dysfunction due to ischemic use of the CPB machine is very high. Frothy sputum is the one of signs
of lung injury that related to left and/or right ventricular dysfunction, it may increased mortality in
patients TOF repaired. The aim of this study was to identify frothy sputum associated with mortality
in patient repaired of TOF. This study is cross-sectional study. We collect data retrospectively
through medical record list from 2019 to 2020. In our study, there were 32 patients data included,
consisted with more dominant male (n = 22) compare to female (n = 10). It was found that 7 female
patients and 9 male patients experienced frothy sputum after TOF repair surgery. There are
association not only mortality (p-value 0.033) but also frothy sputum with pulmonary regurgitation
(p-value 0.049). Although any result of the study and weakness described previously, the study can
be as basis for futher research so that an appropiate guideline can be established to deal frothy
sputum in patients TOF repaired.
Keywords: frothy sputum; CHD; TOF; down syndrome; MAPCAs; myocardial dysfunction.
Suprayitno Wardoyo, Dhama Shinta Susanti, Aflah Dhea Bariz Yasta
Rendy Agustian,
| 1732
Laksana Paduan Wilangsoka
DOI : 10.36418/jrssem.v1i10.183 https://jrssem.publikasiindonesia.id/index.php/jrssem/index
INTRODUCTION
Tetralogy of Fallot is the most common
congenital heart disease (CHD) which
includes ventricular septal defect (VSD),
pulmonary stenosis (PS), right ventricular
hyperthropy (RVH) and overriding aorta
(Apandi et al., 2020); (Soebroto et al., 2020).
The most common risk factor for TOF and
other CHD is Down syndrome (DS)
condition (Quélin et al., 2009). Although,
TOF is categorized in cyanotic CHD not all
patients present with “bluish discoloration”
or sometimes referred to “pink TOF”. In
TOF, cyanosis is caused by limitation blood
to the lungs combined with VSD results in
oxygen-poor blood supply from rigth to
left shunt due to high pressure in right
ventricle from pulmonary stenosis. If the
pulmonary stenosis is mild with balance
shunting direction in the VSD, the clinical
presentation usually less cyanotic
(Siriapisith et al., 2010). There are two
management approaches for TOF:
medication and surgical repair. For medical
treatment, propanolol 0.5 – 2.0 mg/kg oral
is given every 6 hours to prevent hypoxic
spell. Surgical treatment is consisted of
palliative shunt and definitive repair.
Palliative surgical procedure such as Blaloq-
Taussiq shunt (BT shunt) is recommended in
several case such as TOF and pulmonary
atresia, infants with hypoplastic pulmonary
annulus, infants with hypoplastic arteries,
coronary artery anomalies, infants <3-4
months and hypoxic spells cannot be
treated medically and the baby’s body
weight is <2.5 kg
(Park, 2014). Primary
repair of tetralogy of Fallot has been
performed succesfully in young infants and
childrens for the last 45 years, with low
surgical mortality (<5%) and excellent
long-term result (Park & Salamat, 2020);
(Ma et al., 2018); (Makhija et al., 2018). In
several case patients with TOF develop
collaterals or major aortopulmonary
collateral arteries (MAPCAs) in response to
decreased pulmonary blood flow and
ongoing hypoxemia. This causes the CPB
time in the repair operation to be long so
that the risk of RV/LV dysfunction due to
ischemic use of the CPB machine is very
high (Liu et al., 2020).
Frothy sputum is the one of signs of
lung injury that related to left and/or right
ventricular dysfunction. It may be found in
patient post repair of TOF and associated
with increased mortality (Ovechkin et al.,
2007); (Yang et al., 2021). The aim of this
study was to identify frothy sputum
associated with increase mortality in
patient repaired of TOF.
METHODS
This study is a cross-sectional study in
the cardiovascular centre of Dr. Cipto
Mangunkusumo Hospital, Jakarta,
Indonesia. We collect data retrospectively
through medical record list from 2019 to
2020. The inclusion criteria used were all
patients who underwent tetralogy of Fallot
repair with frothy sputum and diagnostic
catheterization prior to surgery. Thirty-two
patients who met inclusion criteria were
enrolled in the study.
Population characteristic were listed
and grouped into before, during and after
surgery. Those included in preoperative
data were age at the time of surgery,
1733 | Increased Mortality Rate in Patient with Frothy Sputum After Tof Total Correction
Surgery
gender, baseline of saturation, follow up
duration, right pulmonary area size (mm),
left pulmonary area (mm), McGoon ratio
and we also assessed baseline laboratorium
such as Hb (gr/dL), hematocrite, leucocyte,
platelet, PT, APTT. The McGoon ratio was
calculated using the equation of left and
right pulmonary arterial diameter
summation divided by the aorta diameter
at diaphragm level. Right pulmonary area
and left pulmonary artery were measured
proximal to the first branching point of
each artery. Data included in the
perioperative group were cardiopulmonary
bypass time (minutes), aortic cross-clamp
time (minutes), length of stay in ICU, and
duration of intubation. After surgery, we
assessed frothy sputum with routine
suction.
The baseline data were described using
mean, median, or proportion as
appropriate. We performed bivariate
analysis using Chi-square test and
univariate analysis to determine the
association between each predictor.
RESULTS AND DISCUSSION
There were 32 patients data included,
consisted with more dominant male (n =
22) compare to female (n = 10). It was
found that 7 female patients and 9 male
patients experienced frothy sputum after
TOF repair surgery. All patients were not
diagnosed with DS. Two out of three
patients diagnosed with “pink TOF” had
frothy sputum (66.7%), while from sample
with “blue TOF”/cyanotic TOF, fourteen of
29 patients had frothy sputum (48.3%).
Based on the resected part of PS, there
were 17 infundibular type, 2 valvular type,
with 13 of them is combination of both.
Seven out of seventeen infundibular type
have frothy sputum (41.2%), similar to 7 out
of 13 mixture type (53.8%) while all valvular
type have frothy sputum. There were 3
samples with a history of previous BT shunt
surgery, one (33.3%) had frothy sputum
and 9 samples had MAPCAs findings and 4
(44.4%) had frothy sputum. In some
patients undergoing TOF repair surgery
procedure without patch, all of them had
frothy sputum, patients with TOF repair
procedure with transannular patch of 19
patients, 9 of whom had frothy sputum.
Patients with TOF repair and MPAP
procedures do not have frothy sputum, in
TOF repair with the Rastelly procedure,
there was no frothy sputum, while for the
intervention of the TOF repair monocusp
procedure, about 4 (44.4%) had frothy
sputum.
Table 1. Frothy Sputum results on categorical independent variables
Frothy Sputum
Frothy
Non Frothy
N
OR
95%CI
p-value
Gender
Female
Male
7(70%)
9(40.9%)
3(30%)
13(59.1%)
10
22
6.030
0.834-
43.574
0.075
Down
Suprayitno Wardoyo, Dhama Shinta Susanti, Aflah Dhea Bariz Yasta
Rendy Agustian,
| 1734
Laksana Paduan Wilangsoka
Frothy Sputum
Frothy
Non Frothy
N
OR
95%CI
p-value
syndome
Yes
No
0
16(50%)
0
16(50%)
0
32
-
-
-
Diagnosis
TOF (pink
Fallot)
TOF (blue)
2(66.7%)
14(48.3%)
1(33.3%)
15(51.7%)
3
29
0.992
0.056-
17.507
0.996
PS type
Infundibular
Valvular
Infundibular,
valvular
7(41.2%)
2(100%)
7(53.8)
10(58.8%)
0(0%)
6(46.2%)
17
2
13
0.556
0.217-1.426
0.222
Confluent
Confluent
Non
confluent
15(51.7%)
1(33.3%)
14(48.3%)
2(66.7%)
29
3
7.018
0.304-
162.087
0.224
Previous BT
shunt
Yes
No
1(33.3%)
15(51.7)
2(66.7%)
14(48.3%)
3
29
0.481
0.030-7.619
0.604
MAPCAs
Yes
No
4(44.4%)
12(52.2%)
5(55.6%)
11(47.8%)
9
23
0.835
0.147-4.735
0.839
Intervention
TOF repair
w/o patch
TOF repair
with TAP
TOF repair
with MPAP
TOF repair +
Rastelly
TOF repair
monocusp
2(100%)
9(47.4%)
0(0%)
1(100%)
4(44.4%)
0(0%)
10(52.6%)
1(100%)
0(0%)
5(55.6%)
2
19
1
1
9
1.588
0.798-3.162
0.188
Table 1. A table of frothy sputum results
on categorical independent variables. From
the table of sex for frothy sputum, p-value
is 0.075. In the "pink" and "blue" TOF
categories for frothy sputum, a p-value of
0.996 was obtained. In the PS type category
for frothy sputum, a p-value of 0.222 was
obtained. For the confluent and non-
1735 | Increased Mortality Rate in Patient with Frothy Sputum After Tof Total Correction
Surgery
confluent categories of frothy sputum, the
p-value was 0.604. In the category of
history of BT shunt and not for frothy
sputum, the p-value was 0.604. In the
MAPCAs category and not for frothy
sputum, the p-value was 0.839.
Intervention category for frothy sputum, p-
value 0.188. Based on the p-value, it can be
concluded that there is no significant
variable on frothy sputum, meaning that
there is no categorical independent
variable that does not affect frothy sputum.
Based on the OR value, patients with female
gender gave an effect of 6,030 times and
patients with pink fallot confluency had an
effect of 7,018 times on frothy sputum.
Table 2. Frothy Sputum results on numeric independent variables
Frothy Sputum
Mean
ST Deviation
OR
95%CI
p-value
Age (years)
4.03
5.270
1.546
0.772-3.097
0.219
Saturation (%)
80.97
8.567
1.048
0.893-1.229
0.568
PG (mmHg)
88.78
17.573
1.043
0.935-1.162
0.452
RPA size (mm)
490.578
223.021
0.346
0.070-1.696
0.191
LPA size (mm)
32.831
136.223
3.095
0.702-13.641
0.135
PV annulus
6.56
2.884
0.835
0.455-1.534
0.562
Mc Goon ratio
2.072
0.442
26.577
0.117-
6021.190
0.236
CPB time
(minutes)
107.687
34.106
1.083
0.970-1.210
0.156
Cross clamp
time (minutes)
39.937
20.463
0.834
0.658-1.057
0.134
Hb (g/dl)
16.668
3.516
0.634
0.169-2.375
0.499
Hematocrite
50.721
10.155
0.962
0.585-1.580
0.877
Leukocytes
8956.83
4161.89
1.000
0.999-1.000
0.161
Platelet (x10
9
)
272.46
98.46
1.002
0.982-1.021
0.877
PT
11.81
1.66
0.752
0.193-2.924
0.680
APTT
37.99
6.93
1.161
0.808-1.668
0.419
Table 2. Is a table of frothy sputum
results on numerical independent variables.
The table shows that age for frothy sputum
obtained p-value 0.219. The saturation of
frothy sputum shows a p-value of 0.568. For
pressure gradient (PG) obtained p-value of
0.452, RPA size (p-value 0.191), and LPA size
(p-value 0.135). PV annulus to obtained p-
value 0.562. For CPB time and cross clamp
time, respectively, p-values are 0.156 and
0.134. Likewise, the results of laboratory
examinations obtained p-value> 0.05. In
table 2 it can be seen that the p-value of all
variables is not below the value of 0.05, so
there are no significant variables. Based on
the OR value of the patient, the higher the
Suprayitno Wardoyo, Dhama Shinta Susanti, Aflah Dhea Bariz Yasta
Rendy Agustian,
| 1736
Laksana Paduan Wilangsoka
MC goon ratio, the greater the effect of
26,577 on frothy sputum.
Table 3. Mortality results on categorical independent variables
Mortality
Frothy
Non Frothy
N
OR
95%CI
p-value
Gender
Female
Male
7(70%)
4(18.2%)
3(30%)
18(81.8%)
10
22
1.608
0.223-11.584
0.637
Down
syndome
Yes
No
0
7(21.9%)
0
25(78.1%)
0
32
-
-
-
Diagnosis
TOF (pink
Fallot)
TOF (blue)
0(0%)
7(24.1%)
3(100%)
22(75.9%)
3
29
0.000
0.000
0.999
PS type
Infundibular
Valvular
Infundibular,
valvular
2(11.8%)
1(50%)
4(30.8)
15(88.2%)
1(50%)
9(69.2%)
17
2
13
0.500
0.170-1.468
0.207
Confluent
Confluent
Non confluent
6(20.7%)
1(33.3%)
23(79.3%)
2(66.7%)
29
3
0.988
0.060-16.397
0.993
Previous BT
shunt
Yes
No
0(0%)
15(51.7)
3(100%)
14(48.3%)
3
29
0.000
0.000
0.999
MAPCAs
Yes
No
1(11.1%)
12(52.2%)
8(88.9%)
11(47.8%)
9
23
0.356
0.029-4.336
0.418
Intervention
TOF repair w/o
patch
TOF repair with
TAP
TOF repair with
MPAP
TOF repair +
Rastelly
0(0%)
4(21.1%)
0(0%)
0(0%)
2(100%)
15(78.9%)
1(100%)
1(100%)
2
19
1
1
1.069
0.532-2.147
0.852
1737 | Increased Mortality Rate in Patient with Frothy Sputum After Tof Total Correction
Surgery
TOF repair
monocusp
3(33.3%)
6(66.7%)
9
Table 3 is a table of mortality results for
categorical independent variables. In the
gender category for mortality, a p-value of
0.637 was obtained. For pink TOF and blue
TOF, the p-value is 0.999. In PS type
category, p-value is 0.207, confluent
category p-value is 0.993. For BT shunt
obtained p-value 0.999. In the MAPCAs
category, the p-value is 0.418. Likewise
intervention, p-value >0.05. In Table 3. It
can be seen that the p-value of each
variable is above 0.05 so that there are no
significant variables. The OR value of the
variable that has a major influence only
reaches one-fold, namely on the gender
and intervention variables.
Table 4. Mortality result on numeric independent variables
It is a table of mortality results for the
numerical independent variables. Based on
the p-value, it can be concluded that there
are no variables that affect mortality,
because the p-value of each variable is
above 0.05. based on the OR value, age,
saturation, LPA size, and PT variables have
a big influence.
Mortality
Mean
ST Deviation
OR
95%CI
p-value
Age(years)
4.03
5.270
1650.76
0.000-
0.997
Saturation(%)
80.97
8.567
194.11
0.000-
0.995
PG(mmHg)
88.78
17.573
0.010
0.000-
0.996
RPA size(mm)
490.578
223.021
0.000
0.000-
0.996
LPA size(mm)
32.831
136.223
75277038.02
0.000-
0.996
PV annulus
6.56
2.884
0.000
0.000-
0.995
Mc Goon ratio
2.072
0.442
6.61E+24
0.000-
0.998
CPB
time(minutes)
107.687
34.106
0.119
0.000-
0.996
Cross clamp
time(minutes)
39.937
20.463
111.81
0.000-
0.994
Hb(g/dl)
16.668
3.516
4.483
0.000-
1.000
Hematocrite
50.721
10.155
1.491
0.000-
1.000
Leukocytes
8956.83
4161.89
0.998
0.037-27.196
0.999
Platelet(x10
9
)
272.46
98.46
0.894
0.000-
1.967E+27
0.997
PT
11.81
1.66
306076.49
0.000-
0.998
APTT
37.99
6.93
47.046
0.000-
0.997
Suprayitno Wardoyo, Dhama Shinta Susanti, Aflah Dhea Bariz Yasta
Rendy Agustian,
| 1738
Laksana Paduan Wilangsoka
Table 5. Effect of pulmonary valve on frothy sputum
Based on Table 5, the p-value obtained
is 0.049 which means that between
pulmonary valve(PV) and frothy sputum is
significant or PV has an effect on frothy
sputum. The resulting OR value shows that
PV has an effect of 45,549 times on frothy
sputum.
Table 6. Effect of Frothy Sputum on Mortality
Mortality
Yes
No
N
OR
95%CI
p-value
Frothy
sputum
Frothy
Non Frothy
6(37.5%)
1(40.9%)
10(62.5%)
15(59.1%)
16
16
9.000
0.936-86.522
0.033
Based on Table 6, the p-value obtained
is 0.033 which means that between frothy
sputum and significant mortality or frothy
sputum has an influence on mortality. The
resulting OR value indicates that frothy
sputum has a 9-fold effect on mortality.
Table 7. ICU stay and LOHS on Mortality
Mortality
Yes
No
N
OR
95%CI
p-value
Frothy
sputum
Frothy
Non Frothy
6(37.5%)
1(40.9%)
10(62.5%)
15(59.1%)
16
16
9.000
0.936-86.522
0.033
Based on Table 7, the characteristics of
ICU stay and LOHS are significant on
mortality, this can be seen in the p-value
which is less than 0.05, which means that
ICU stay and LOS stay have an effect on
mortality. The resulting OR value shows
that ICU stay has an effect of 2.236E+17
times on mortality and LOHS day has an
Frothy Sputum
Frothy
Non Frothy
N
OR
95%CI
p-value
Pulmonary
valve
Pulmonary
regurtitation
Pulmonary
stenosis
7(77.8%)
9(39.1%)
2(22.2%)
14(60.9%)
9
23
45.549
1.274-1628.222
0.049
1739 | Increased Mortality Rate in Patient with Frothy Sputum After Tof Total Correction
Surgery
effect of 244,317 times on mortality.
This study aims to find the association
of reverse complication after TOF repair
with frothy sputum. However, not all
studies investigate the association of the
effect frothy sputum to mortality.
Frothy sputum is the one of the signs of
lung injury that related to left ventricular
(LV) dysfunction or myocardial dysfunction.
It may be found in patient post repair of
TOF and increase significantly mortality TOF
repair was first described in 1955 by Lillehei
et all (Maddali et al., 2011). Timing of this
operation varies from instution to instution,
but early age surgery is generally preferred.
Total repair of the defect is carried out
under cardiopulmonary bypass, circulatory
arrest, and hypothermia. The procedure
includes stiches and/or patchs closure of
the VSD, preferably through transatrial and
transpulmonary artery approach, widening
of the right ventricular outflow tract (RVOT)
by division or resection of the infundibular
tissue, and pulmonary valvotomy, avoiding
placement of the fabric patch whenever
possible. However, if the pulmonary
annulus and main PA are hypoplastic,
transannular patch is unavoidable. For
patient with uncomplicated TOF, the
mortality rate is 2% to 3% during the first 2
years. During the last decades, it has been
well recognized that patients with repaired
TOF are at risk for exercise intolerance, right
heart failure, life-threatening ventricular
arrhytmia, and sudden death. Numerous
studies have shown a close relationship
between the degree of PR and RV
dimensions and RV ejection fraction.
Varying degrees of pulmonary
regurgitation and/or pulmonary stenosis
remain in the majority of patients after right
ventricular outflow tract (RVOT)
reconstruction, and severe PS and free PR
are both ends of the spectrum in residual
hemodynamic impairment (Yoo & Park,
2013). In addition left ventricular (LV)
function deteriorates with progressive RV
dysfunction through interventricular
interaction, that called “reversed Berheim
effect”. The reverse Bernheim effect occurs
when there is right ventricular pressure and
volume overload that results in the
interventricular septum bulging toward the
LV causing LV diastolic impairment
14
. In
situations where a part of the RV is akinetic,
due to scarring post myocardial infarction
or after replacement with a noncontractile
material (synthetic patch), the septum is
able to maintain circulatory stability as long
as the RV is not dilated. In acute RV
pressure- or volume-overload states,
dilatation of the RV increases
intrapericardial pressure and shifts the
interventricular septum to the left, altering
LV geometry. As a consequence,
distensibility of LV decreases, leading to a
decreased LV preload, increased LV end-
diastolic pressure, and consequently a low
cardiac output state. This can cause
symptoms of LV failure or dysfunction
(Magoon et al., 2020); (Kanter et al., 2010);
(Saran et al., 2019). Its similar in our study
terdapat asosiasi pulmonary regurgitation
terhadap frothy sputum (p-value 0.049).
Although the TOF repair procedure has
a mortality rate of <5% and the results of
the procedure are satisfactory6. The
postoperative morbidity and mortality rate
is quite high17. About 75% are due to RV
Suprayitno Wardoyo, Dhama Shinta Susanti, Aflah Dhea Bariz Yasta
Rendy Agustian,
| 1740
Laksana Paduan Wilangsoka
and/or LV dysfunction18. This study
supports our finding that frothy sputum
has a significant relationship with mortality
(p-value 0.033).
There are certain limitation to this
study. The sample of this study is the
comparison of the number of genders in
the sample is not evenly distributed, not all
patients have documented LV/RV function
evaluation, but PS/PR is well documented,
so other factors cannot be ruled out.
CONCLUSIONS
Our finding showed frothy sputum was
associated with pulmonary regurgitation
and mortality. However, the unmeasured
factors with confounding and effect
modifying potentials affecting frothy
sputum cannot excluded. Based on our
study frothy sputum not only associated
with mortality but also morbidity. Although
any result of the study and weakness
described previously, the study can be as
basis for futher research so that an
appropiate guideline can be established to
deal frothy sputum in patients TOF
repaired.
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