Hussain and Younes BMC Pediatrics(2024) 24:499
https://doi.org/10.1186/s12887-024-04976-9

BMC Pediatrics

RESEARCH

Open Access

Early outcomes of experience warm surgery
in children undergoing complete repairof tetralogy of Fallot in developing countries
Alaa Mohamad Hussain1* and Mohammad Ali Younes1*
Abstract
Objectives While significant evidence supports the benefits of normothermic cardiopulmonary bypass (NCPB) overhypothermic techniques, many institutions in developing countries, including ours, continue to employ hypothermic
methods. This study aimed to assess the early postoperative outcomes of normothermic cardiopulmonary bypass(NCPB) for complete surgical repair via the Tetralogy of Fallot (TOF) within our national context.
Methods We conducted this study in the Pediatric Cardiac Intensive Care Unit (PCICU) at the University Children’s
Hospital. One hundred patients who underwent complete TOF repair were enrolled and categorized into two groups:
the normothermic group (n = 50, temperature 35–37 °C) and the moderate hypothermic group (n = 50, temperature
28–32 °C). We evaluated mortality, morbidity, and postoperative complications in the PCICU as outcome measures.
Results The demographic characteristics were similar between the two groups. However, the cardiopulmonary
bypass (CPB) time and aortic cross-clamp (ACC) time were notably longer in the hypothermic group. The study
recorded seven deaths, yielding an overall mortality rate of 7%. No significant differences were observed between thetwo groups concerning mortality, morbidity, or postoperative complications in the PCICU.
Conclusions Our findings suggest that normothermic procedures, while not demonstrably effective, are safe forpediatric cardiac surgery. Further research is warranted to substantiate and endorse the adoption of this technique.
Keywords Warm surgery, Hypothermia, Cardiopulmonary bypass, Tetralogy of Fallot, Early outcomes, Developing
country*Correspondence:
Alaa Mohamad Hussain
alaahussain.sy@gmail.com; alaa.hussain@damascusuniversity.edu.sy
Mohammad Ali Younes
mohammad.younes@damascusuniversity.edu.sy
1
University Children’s Hospital, Damascus University, Damascus, Syrian
Arab Republic

Introduction
The optimal temperature for cardiopulmonary bypass(CPB) during pediatric cardiac surgeries has historically
been a subject of debate [1]. Traditionally, hypothermic perfusion was widely used based on the premisethat lowering the body temperature would attenuate
the inflammatory response triggered by CPB, offering
protection to vital organs such as the brain, heart, andkidneys, particularly in scenarios involving unexpected
technical failures during the CPB process [2]. However,recent studies have cast doubt on the long-held beliefs
about hypothermic perfusion. Some research indicates© The Author(s) 2024. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use,sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) andthe source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in thisarticle are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not includedin the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you willneed to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Hussain and Younes BMC Pediatrics(2024) 24:499

that hypothermia may delay the inflammatory response
rather than mitigate it [3–5]. This raises questions about
the actual clinical benefits of using hypothermic perfusion. Additionally, the rarity of technical failures that
could lead to circulatory arrest limits the justification of
hypothermic perfusion.
In contrast, in the last two decades, there has been asurge in interest in normothermic cardiopulmonary
bypass (NCPB), both in adult and pediatric cardiac surgeries [6–9].
The main potential concern toward using NCPB is
the absence of a safe margin when an incident requiring
circulatory arrest lasts more than a few minutes [9, 10].
Even though this disadvantage is known, NCPB is associated with lower oxidative stress, myocardial reperfusion
injury, renal injury, and inflammatory response than ishypothermic cardiopulmonary bypass (HCPB) [5, 11].
Many studies have confirmed the benefits of warm perfusion on immediate outcomes through a low requirement for inotropic support, a short time to extubation,
low lactate production, adequate urine output, minimal
drainage from the chest drain, a short intensive care unit
(ICU) stay, and a short length of hospital stay [7, 9, 12].
This has led several European centers to make the transition from hypothermic to normothermic procedures,with none opting to revert to the older method [13, 14].
Tetralogy of Fallot (TOF) is the most common formof cyanotic congenital heart disease in children. Despiteadvancements and the shift toward normothermic procedures in many developed countries, hypothermic perfusion remains the standard practice for the surgical repair
of TOF in our national context. This study, therefore,
aimed to fill this knowledge gap by comparing the outcomes of using normothermic and moderate hypothermic techniques during CPB. Specifically, we will focus on
key metrics such as mortality rates, duration of patient
intubation, length of stay in the pediatric cardiac intensive care unit (PCICU), postoperative hospital stays, andincidence of postoperative complications in children
undergoing complete repair of TOF.

Materials and methods
This comparison study was conducted in the PCICU at
the University Children’s Hospital, Damascus. We evaluated 100 pediatric patients who underwent complete
repair of TOF at the Cardiothoracic Unit of the Children’s Hospital from November 2018 to February 2023.
Ethical Considerations: Prior to the study, approval was
secured from the hospital’s institutional ethics committee. Additionally, informed consent was obtained fromthe parents or guardians of the participating children.

Page 2 of 6

Study criteria
Inclusion criteria

Patients aged 13 years or younger who had undergone
complete repair of TOF.
Exclusion criteria

Patients who required emergency surgery or surgeries
conducted at temperatures ranging from 32 to 35 °C or
below 28 °C or during periods of circulatory arrest.
Excluding patients within the 32–35 °C range was
essential to clearly differentiate between the two main
approaches and to avoid potential confusion from overlapping results.
Temperature Definitions and Grouping: Ambiguities
in the definitions of normothermic perfusion and hypothermia led us to define normothermia as ≥ 35 °C, as referenced in [15]. Consequently, patients were categorized
into two groups:
1. NCPB Group (50 patients): Surgeries were
performed at temperatures between 35 and 37 °C.
2. Patients in the moderate HCPB Group (50 patients):
Surgeries were conducted at temperatures between
28 and 32 °C.
Temperature monitoring was achieved using nasopharyngeal and rectal probes.
Surgical Procedure: All surgeries during the study period
were performed by a consistent surgeon employing analogous techniques. Standard CPB conditions with intermittent warm blood cardioplegia were maintained. For
every patient, ventricular septal defect (VSD) closure
via a transatrial approach was performed. Patients with
valvular-PS underwent either commissurotomy or valvulotomy. Complete infundibular muscle resection was
conducted, followed by enlargement of the outflow pathway using a bovine pericardial patch. If the right ventricular outflow tract obstruction persisted after pulmonary
valvotomy and muscle resection, a transannular patch(TAP) was applied using a bovine pericardial patch.
Data collection

Medical records were meticulously reviewed to extract
pertinent clinical variables, encompassing demographic
information such as age, body weight, body surface area,
incidence of cyanotic spells, and sex. Parents were admitted to the cardiac intensive care unit postoperatively for
informed consent and verification of their past medical
history. Data acquisition was facilitated by the Drager–
Infinity Delta kappa, which enables event recording.
Preoperative data collection commenced at the timeof surgery, during which the patient was a daily activity. The key metrics recorded included CPB and aorticHussain and Younes BMC Pediatrics(2024) 24:499

cross-clamp (ACC) times, the lowest CPB temperatureduring surgery, and the necessity for a TAP. Postoperative data included intubation duration, intensive care unit
(ICU) stay duration, total hospital stay, mortality incidence, and postoperative complications such as acuterenal injury, neurological complications, arrhythmias,
pulmonary complications, sepsis, bleeding, high inotropic support dosage, low cardiac output syndrome, andheart block. Continuous ECG monitoring was facilitatedby Drager monitors, with standard 12-lead ECGs taken
preoperatively and upon ICU admission.
Definitions

High inotropic agent doses in the ICU were defined as
doses exceeding 0.5 mcg/kg/min for epinephrine andnorepinephrine and 10 mcg/kg/min for dopamine anddobutamine.
Pulmonary complications were defined as the presence of pneumonia, pleural effusion, pulmonary
edema, pulmonary hemorrhage, pneumothorax, or
pneumomediastinum.
Neurological Complications Assessment: This assessment was confined to clinical examinations, excluding
electroencephalogram (EEG) or magnetic resonanceimaging (MRI) evaluations. Medical personnel documented any transient or permanent neurological deficits,
seizures, irritability, or aberrant behavior.
Acute Renal Injury: Either an absolute creatinine value
increase of more than 0.3 mg/dL within 48 h or a urinary
output of less than 0.5 ml/kg/hour for 6 h.
Postoperative low cardiac output syndrome: The presence of two or more of the following criteria:
1. The serum lactate concentration was more than 3
mmol/L.
2. Urinary output was less than 0.5 ml/kg/hour.
3. The difference between the skin temperature andcentral temperature was more than 5 degrees.
4. A drop in blood pressure below the 5% line, a weakpulse, or a prolonged capillary refill time.
5. Tachycardia above normal rates for age.

Page 3 of 6

Outcomes

This study focused on assessing the influence of cardiopulmonary bypass (CPB) temperature on key clinicalmetrics, including mortality rates, duration of intensive
care unit (ICU) stay, overall hospital stay, and intubation
time. These metrics were chosen to determine the overall effectiveness and safety of using normothermic versus
hypothermic CPB techniques in pediatric patients undergoing complete repair of Tetralogy of Fallot (TOF).
Statistical analysis

Descriptive statistics were calculated as frequency counts
and percentages for categorical variables and medianswith interquartile ranges (IQRs) for continuous variables.
We used the Mann‒Whitney test to compare continuous variables, and the chi-square test was used to compare categorical variables between the NCPB and the
HCPB groups. We used univariate logistic regression toassess the associations between mortality and postoperative complications and between mortality and the CPB
temperature. We also used univariate Cox regression toassess the associations between the length of hospital stay
and CPB temperature. P < 0.05 was considered to indicate
statistical significance. All analyses were performed using
SPSS 26 software (IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp.).

Results
Baseline characteristics

During this study, 100 patients who underwent complete
repair of TOF were included, and they were divided into
two groups: normothermic (50 patients) and moderate
hypothermic (50 patients). Our findings indicate thatboth groups were demographically homogeneous, withno statistically significant differences in variables suchas age, body weight, body mass index, sex distribution,or incidence of cyanotic spells, as delineated in Table 1.
In addition, the median age at the time of operation was
2 years, with an IQR of 1–3 years. Statistical analysis
revealed no significant difference between the two groups(p value = 0.76).

Table 1 Comparison of the baseline characteristics between the two groups
variableTotal(n = 100)

Age, median (IQR) years
Sex, Male (%)
Weight, median (IQR) kg
BSA, median (IQR) m2
Cyanotic spells (%)
Right aortic arch (%)

2 (1–3)63%
10 (8.5–13)
0.48 (0.42–0.56)
55%
18%

BSA: body surface area, IQR: Interquartile range

Normothermia(n = 50) 50%
2 (1–3)56%
10 (8.8–13)
0.48 (0.43–0.57)
54%
16%

Hypothermia(n = 50) 50%
2 (0.9–3.3)
70%
10 (8.4–12)
0.47 (0.41–0.54)
56%
20%

P value
0.76
0.14
0.8
0.63
0.84
-

Hussain and Younes BMC Pediatrics(2024) 24:499

Intraoperative data

To assess the impact of temperature on surgical duration, we compared the CPB and ACC times between the
hypothermic and normothermic groups. Our findings
revealed that the hypothermic group had a longer CPB
duration by an average of 10 min, with a median timeof 115 min (IQR 77.5–97.75), in contrast to the normothermic group’s median of 104 min (IQR 89–118.5). Thisdifference was statistically significant, as indicated by a pvalue of 0.008.
Similarly, the ACC time was notably different between
the two groups. The median ACC time in the hypothermic group was 88 min (IQR 5.9–25.3), approximately
10 min longer than that in the normothermic group,
which had a median of 76 min (IQR 66.5–92). This difference was also statistically significant, with a p value of
0.009.
In summary, both the CPB and ACC durations weresignificantly longer in the hypothermic group than in
the normothermic group. These differences are further
detailed in Table 2.
Outcomes

To evaluate the impact of temperature modulation on
patient outcomes, we analyzed various metrics including mortality, hospitalization duration, mechanicalventilation time, and duration of ICU stay, as well as
postoperative complications between the hypothermicand normothermic groups. Our findings indicated thatout of the total participants, seven died, for an overallmortality rate of 7%. The specific causes of mortality in
our study were as follows: heart failure led to the death of
4 patients, septic shock was responsible for the deaths of
2 patients, and pulmonary hemorrhage led to the deathof 1 patient.
After a greater delay, the hypothermic group exhibiteda greater mortality rate—5 deaths (10%)—than did thenormothermic group (4%). However, this difference was
not statistically significant (P value = 0.25).
In terms of hospitalization duration, the hypothermic
group had a slightly shorter median hospital stay (6 days;
IQR 5–9) than did the normothermic group (median
7 days; IQR 5.75-10). However, this difference did notreach statistical significance (p value = 0.75). Similarly,both groups had comparable median mechanical ventilation times (20 h) and ICU stay durations (3 days), but

Page 4 of 6neither difference was statistically significant (P values of
0.84 and 0.75, respectively).
When assessing the requirement for high doses of inotropic support, 34% of the patients in the normothermic
group had this condition compared to 44% of those in the
hypothermic group. This difference, however, was notstatistically significant (p value = 0.3).
Finally, regarding other postoperative complicationsin the ICU, such as acute renal injury, neurologicalcomplications, pulmonary complications, and bleeding, no significant differences were observed between
the two groups (with p values of 0.56, 0.2, 0.59, and 0.65,
respectively).
In summary, while there were observable differencesin outcomes between the hypothermic and normothermic groups, they did not reach statistical significance. A
detailed comparison of the postoperative data for bothgroups can be found in Table 3.

Discussion
NCPB in pediatric cardiac surgery has garnered
increased attention due to its demonstrated safety andefficacy and has become a prevalent practice in numerous European cardiac centers. Despite its popularity
elsewhere, this technique remains underutilized in ourcountry, prompting us to conduct this study. We aimed
to evaluate the early outcomes of performing normothermic CPB in children who underwent complete surgicalrepair of TOF, with a particular focus on its safety andfeasibility in our local context.
In this study, descriptive statistics showed that themedian age of the children was 2 years (IQR 1–3), which
was greater than the age mentioned in the study of Mercer-Rosa, L. et al. conducted at Philadelphia Hospital in
2018 [16], where the median age was 3.6 months (interquartile range 2.1, 5.2). We can explain the older ages inthis study by the delay in diagnosis and the delay in surgery for patients due to the large number of patients relative to the center’s ability to reach admission and due tothe insufficient availability of centers specializing in pediatric heart surgery in other regions of our country.
The overall mortality rate in the current study was
7%, which was higher than that reported in other studies (less than 2%) [16–18]. This increase can be linked tothe challenging economic and health conditions in ourcountry stemming from ongoing conflict, which leads toTable 2 Comparison of the intraoperative data between the two groups
variableTotal(n = 100)

ACC time, median (IQR) min
CPB time, median (IQR) min
TAP (%)

84 (70–94)
109 (95–122)
7%

Normothermia(n = 50) 50%
76 (66.5–92)
104 (89-118.5)
4%

ACC: aortic cross-clamp, CPB: cardiopulmonary bypass, TAP: transannular patch, IQR: Interquartile range

Hypothermia(n = 50) 50%
88 (77.5–98)
115 (103–126)
10%

P value
0.009
0.008
0.24

Hussain and Younes BMC Pediatrics(2024) 24:499

Page 5 of 6

Table 3 Comparison of the postoperative data between the two groups
variableTotal(n = 100)

Mortality (%)
Length of hospital stay, median (IQR) days
Length of PCICU stay, median (IQR) days
Intubation time, median (IQR) hours
Acute renal injury (%)
Pulmonary complications (%)
Neurological complications (%)
Bleeding (%)
Sepsis (%)
Heart Block (%)
Arrhythmias (%)
LCOS (%)
High Dose of Inotropic Support (%)

7%
6.5 (5-9.75)
3 (2-4.75)
20 (8–37)
3%
26%
5%
5%
29%
1%
20%
26%
39%

Normothermia(n = 50) 50%
4%7 (5.75-10)
3 (2–5)20 (8-43.25)
2%
26%
2%
4%
34%
2%
16%
20%
34%

Hypothermia(n = 50) 50%
10%
6 (5-9.25)
3 (2-4.25)
20 (7-32.5)
4%
26%
8%
6%
24%
0%
24%
32%
44%

Exp B (95% CI)

P value

0.37 (0.07–2.03)
1.07 (0.71–1.61)
2 (0.18–23.26)
1 (0.4–2.44)
4.2 (0.46–39.54)
1.5 (0.24–9.59)
0.61 (0.25–1.47)
1.66 (0.61–4.49)
1.9 (0.75–4.69)
1.52 (0.68–3.42)

0.25
0.75
0.75
0.84
0.56
0.59
0.2
0.65
0.27
0.99
0.32
0.17
0.3

Lcos: low cardiac output syndrome, PCICU: pediatric cardiac intensive care unit, IQR: Interquartile range

shortages of essential medical supplies and equipment,
particularly in operating rooms and ICUs. The mortality rate was greater in the HCPB group (10%) than in thenormothermic group (4%), although these differences did
not reach statistical significance (P = 0.25). These findings align with previous studies that also reported nosignificant difference in mortality rates between the twotemperature groups [7, 11]. Our results revealed no significant differences between the hypothermic and normothermic groups in terms of hospital stay, ICU stay, or
mechanical ventilation time (P values of 0.75, 0.75, and0.84, respectively). These findings are consistent withthose reported by Xiong et al. and Caputo et al. [7, 19],
although they contrast with the findings of other studies[8]. Postoperative complications in the ICU were generally more prevalent in the HCPB group, but this difference was not statistically significant, in agreement withprior research [7, 19].
A critical observation from our study was the longer
CPB duration in the HCPB group, which was attributed
to the additional time required for cooling at the startand rewarming at the end of CPB. The NCPB group also
exhibited a shorter ACC duration, likely because the aortic cross-clamp was used solely for intracardiac defectrepairs, while right ventricular outflow tract reconstruction was performed on a beating heart. In contrast, the
HCPB group underwent the entire procedure with theaortic cross-clamp in place, with heart reperfusion occurring only after the required rewarming period. Thesefindings are in line with those of several previous studies[9, 11], though two other studies reported no significant
differences in CPB or ACC times between the two groups[12, 20].
Notably, the difference between the two groups concerning the CPB and ACC times was small, approximately

10 min, which likely explains the lack of impact on surgical repair outcomes observed in our study.
Study limitations

Despite these insights, our study is not without limitations. The relatively small sample size and the challenging
conditions of the health system in our country introduced variables that could have influenced the outcomes,
and the unstable availability of laboratory materials prevented a comprehensive laboratory variable analysis.
We acknowledge that utilizing the area under the curve(AUC) method to analyze temperature and flow rate data
could provide valuable insights into the detailed physiological dynamics during surgery. However, due to limited resources and technical capabilities at the time ofdesigning this study, we were unable to implement thisapproach. Future studies should incorporate AUC analysis to provide a more nuanced understanding of temperature management and its impact on patient outcomes.
This will help in offering a comprehensive evaluation of
the different CPB techniques.
Study strengths

This study has several strengths, including the consistency of surgical experience and technique, the fact that
all the operations were performed by the same surgeon,
and the homogeneity of the patient sample, as all theparticipants had classical TOF disease. Additionally, theelective nature of the surgeries eliminated the potential
influence of surgical repair complexity on the results.

Conclusion
This study found that although the duration of aortic
cross-clamp (ACC) and cardiopulmonary bypass (CPB)
was shorter in the normothermic cardiopulmonary
bypass (NCPB) group compared to the hypothermic

Hussain and Younes BMC Pediatrics(2024) 24:499

cardiopulmonary bypass (HCPB) group, the early postoperative outcomes did not significantly differ between
the two groups of patients undergoing surgical repair of
Tetralogy of Fallot (TOF). This suggests that employing
a warm surgical approach, even if not more effective, issafe in children with TOF. However, to further substantiate the applicability and benefits of this technique, it isimperative to expand the research to include other congenital heart diseases. Future studies in this direction
could provide a more comprehensive understanding andvalidation of the technique’s potential benefits across a
broader spectrum of pediatric cardiac conditions.
By focusing on enhancing surgical training, resource
allocation, policy advocacy, and early diagnosis, we aim
to reduce mortality rates and improve overall outcomesin pediatric cardiac surgery. We believe these measures will significantly contribute to the advancementof pediatric cardiac care in our region, ensuring ourpatients receive the best possible care under challenging
circumstances.
Abbreviations
NCPB	Normothermic cardiopulmonary bypass
TOF	Tetralogy of Fallot
PCICU	Pediatric Cardiac Intensive Care Unit
CPB	Cardiopulmonary bypass
ACC	Aortic cross-clamp
HCPB	Hypothermic cardiopulmonary bypass
ICU	Intensive care unit
VSD	Ventricular septal defect
TAP	Transannular patch
EEG	Electroencephalogram
MRI	Magnetic resonance imaging
IQR	Interquartile ranges
Acknowledgements
We want to extend our gratitude to the University Children’s Hospital,
Damascus University, and to the doctors, nurses, and researchers for theirsupport of my research through the hospital’s PhD research program.
Author contributions
Equal Contributions: Alaa Hussain and Mohammad Younes contributed
equally to this work by writing the main manuscript, editing it, analyzing data,and preparing tables. All authors reviewed and approved the final manuscript.
Funding
Not applicable.
Data availability
The datasets used and analysed during the current study available from thecorresponding author on reasonable request.

Declarations
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Ethical approval
Ethics approval and consent to participate: Ethics approval was obtained
from the Research Ethics Committee of University Children’s Hospital, Facultyof Medicine, Damascus University. Informed consent was obtained from all

Page 6 of 6participants’ parents for their children’s participation in this study and for the
publication of the data. All methods were conducted in accordance with
relevant guidelines and regulations.
Informed consent
Written informed consent was obtained from the parents of the participating
children.
Received: 14 March 2024 / Accepted: 26 July 2024

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