ABSTRACT
Background:
COVID-19 is known to affect the alveolar-capillary membrane and interstitial tissue. Cardiopulmonary bypass (CPB) is proven to cause “pump-lung” syndrome. Little is known about the subgroup of COVID-19-recovered children undergoing cardiac surgeries under CPB.
Aim:
To compare the lung ultrasound score (LUSS) and morbidity of COVID-19-recovered children to those without COVID-19 after congenital cardiac surgery.
Setting and Design:
Prospective observational pilot study at a tertiary care institution.
Materials and Methods:
The study was carried out on 15 COVID-recovered children and 15 matched controls (Group B) posted for congenital cardiac surgery. COVID-recovered children were further divided into those who received in-hospital care for COVID (Group C) and those who did not (Group A). LUSS measured immediately after cardiac surgery was compared between the groups. PaO2/FiO2, ratio, incidence of pulmonary infection, re-intubation rate, duration of ventilation, in-hospital mortality, and 30-day mortality were also compared between the groups.
Results:
LUSS was comparable between Groups A and B (mean difference = 1.467, P = 0.721). Compared to the control group, Group C showed higher LUSS (mean difference = 11.67, P < 0.001), lower PaO2/FiO2 ratio (207.8 ± 95.49 Vs 357.6 ± 63.82, P = 0.003), and one in-hospital mortality. A significant negative correlation was seen between LUSS and PaO2/FiO2 ratio (rs = - 0.75, P < 0.001).
Conclusion:
LUSS was not higher in COVID-recovered children. Children with a history of severe COVID-19 recorded higher LUSS, in-hospital mortality, duration of ICU stay, and duration of ventilation.
Keywords: Congenital heart surgery, COVID-19, lung ultrasound score, morbidity, mortality
INTRODUCTION
COVID-19 infection in the pediatric age group is rare, constituting only 1.7% of the confirmed cases.[1] With the successful development of vaccines and effective vaccination campaigns, a new subset of patients that cardiac anesthesiologists routinely see now is “COVID-recovered” with patients having recovered from varying severities of the illness.[2] The disease is often mild with complete and uneventful recovery.[3,4] However, COVID-19 alters the immune system, activating a hyper-immune response in some patients, who often develop severe manifestations of the disease. How this category of patients responds to endothelial activation and immunological response to CPB is not known.[5,6] Increased response in the past can be compared to the outcome parameters after CPB for better understanding. There are no studies that specifically address this topic, to the best of the authors’ knowledge.
Perioperative respiratory complications can increase morbidity and mortality. Information about the susceptibility to the same can have prognostic implications and can potentially change treatment algorithms. The perioperative use of lung ultrasound in pediatric cardiac surgery to detect pulmonary complications is time-tested.[1,3] Lung ultrasound examination is easy, reproducible, and has high sensitivity and specificity. The use of lung ultrasound to detect COVID-19-related pulmonary complications is also common.[7] The authors could not find any study evaluating pulmonary parenchymal changes in COVID-recovered pediatric patients undergoing cardiac surgery using lung ultrasonography.
This study aimed to test the hypothesis that COVID-19-recovered children will have significantly more pulmonary changes detected by ultrasonography after congenital heart surgery compared to children without a history of COVID-19 infection. Thus, the primary objective was to compare the lung ultrasound score (LUSS) after pediatric cardiac surgery in COVID-19-recovered children to that of children without a history of COVID-19. The secondary objectives were to compare the duration of ventilation, incidence of re-intubation, incidence of pulmonary infection, duration of ICU stay, in-hospital mortality, and 30-day mortality between the groups. Furthermore, the impact of the severity of past COVID-19 infection on the LUSS was also studied.
MATERIALS AND METHODS
This was a prospective, observational, non-randomized, non-blinded pilot study performed in a tertiary-level referral center doing 400–500 congenital cardiac surgeries per year. This study was approved by the Institute Ethics Committee (SCT/IEC/1888/MAY/2022) and registered with CTRI (CTRI/2022/07/043846). Children up to the age of 12 years who tested positive for COVID-19 by RT-PCR or rapid antigen test within a period of 1 year were recruited, and the duration of study was between May and October 2022. Children who gave a history of possible COVID-19 but have no laboratory confirmation, or emergency surgeries and those with active pre-operative pulmonary infection were excluded. Children included in the control group gave no history of a COVID infection and tested consistently negative for COVID-19 during the pre-operative visits, most of which were six months apart, by RT-PCR. Immunoglobulin G detection was not part of our study due to unclear immunoglobulin response of the delta variant, which predominantly affected children.[8-10] Written informed consent was taken from the parents during the pre-anesthetic check-up. The two groups of allotment were children who were once positive for SARS-COVID-19 by RT PCR or antigen tests and Group B (children who have never been COVID-positive in RT-PCR test control). The first group was divided further into children who were in domiciliary care (Group A) and those who received in-hospital care for COVID-19 (Group C).
A complete lung ultrasound examination was performed after intubation in the operation theater by the principal investigator, who had more than 5 years of experience in performing pulmonary ultrasound examinations in pediatric patients. The examination was performed in the supine position, and posterior lung fields were scanned by turning the patient to the lateral decubitus position. A 7 to 15 MHz linear probe was used to examine the lung fields by placing the probe perpendicular to the ribs. Twelve regions were examined, which included the upper and lower parts of the anterior, lateral, and posterior chest wall, bilaterally. A score of zero to three was assigned for each lung region.
Points assigned during the lung ultrasound are as follows[11] [Figure 1].
Figure 1.
Ultrasound images showing lung ultrasound scores-LUSS 0, 1, 2, and 3
Zero points—lung sliding present with A lines.
One point—scattered/multiple B lines.
Two points—confluent B lines appearing as white lung/glass rockets.
Three points—consolidation with or without air bronchogram.
The final LUSS is a sum of scores in all 12 regions and ranged between zero and thirty-six, which was documented as the baseline LUSS (LUSS-Baseline).
After surgery, before resuming ventilation, lungs were recruited to avoid the confounding effect of atelectasis. The endpoint of recruitment was visual inflation of both lungs in the surgical field, at a peak inspiratory pressure of less than 30 cm H2O. In the ICU, pulmonary ultrasound was repeated for both Group A and Group B patients and LUSS was documented. This score was used for further analysis signifying the pulmonary parenchymal changes after CPB in all children. In case of any positive findings, lung ultrasound was repeated daily till resolution. All children in the immediate postoperative period in the pediatric cardiac surgery ICU, irrespective of being part of the study group, were evaluated by daily chest radiograms as per the ICU protocol. Children were followed up for assessment of the duration of ventilation, the incidence of re-intubation, incidence of pulmonary infection (documented by clinical signs, radiological signs, and laboratory criteria of pneumonia), duration of ICU stay, in-hospital mortality, and 30-day mortality. Arterial blood gas analysis was performed as part of routine management, and partial pressure of oxygen and partial pressure of carbon dioxide were also documented.
For this pilot study, we had a sample size of fifteen per group. The distribution of data was tested using visual inspection of histograms, normality Q-Q plots, and the Shapiro–Wilk test. Categorical data were expressed as frequency and percentages and were compared by using the Chi-square test. Normally distributed quantitative data were expressed as mean with standard deviation and were compared between the study groups using an independent t-test (two groups) or one-way ANOVA (more than two groups). Non-normally distributed quantitative data were expressed as median with interquartile range (IQR) and compared between study groups using the Mann–Whitney U test (two groups) or using the Kruskal–Wallis test (more than two groups). The association between quantitative and outcome variables was assessed by calculating the Spearman correlation coefficient. P value <0.05 was considered statistically significant. Data analysis was performed using SPSS software.
RESULTS
The average age and gender distribution of patients in Group A, Group B, and Group C were comparable [Table 1]. The diagnoses for which the children were operated on are given in Table 2. All patients with cyanotic heart disease (TOF) underwent intracardiac repair to restore biventricular physiology. The mean baseline LUSS score significantly differed between Groups A and C (p < 0.001) as well as between Groups B and C (p = 0.001). However, there was no significant difference between Groups A and B. The mean LUSS immediately after shifting the patient to ICU after the surgery (LUSS) in Group A, Group B, and Group C were 2.4 ± 4.19, 0.93 ± 1.98, and 12.60 ± 9.58, respectively, which were significantly different (p < 0.01). Post hoc analysis revealed that the difference was significant between Groups A and C (p = 0.001) as well as between Groups B and C (<0.001). There was no significant difference between Groups A and B (p = 0.721) [Table 3, Figure 2].
Table 1.
Demographics of study groups (n=30)
| Parameter | Study Groups | P | ||
|---|---|---|---|---|
|
| ||||
| Group A (n=10) | Group B (n=15) | Group C (n=5) | ||
| Age (Years) | 6.07±3.71 | 3.91±2.64 | 0.97±1.14 | 0.087 |
| Gender | ||||
| Male | 5 (50%) | 5 (33.33%) | 2 (40.00%) | 0.487 |
| Female | 5 (50%) | 10 (66.67%) | 3 (60.00%) | |
Table 2.
Distribution of diagnoses between the study groups (n=30)
| Diagnosis | Study Groups | ||
|---|---|---|---|
|
| |||
| Group A (n=10) | Group B (n=15) | Group C (n=5) | |
| ASD | 6 (60.00%) | 5 (33.33%) | 1 (20%) |
| VSD | 4 (40.00%) | 7 (46.67%) | 3 (60%) |
| TOF | 3 (20%) | 1 (20%) | |
Table 3.
Comparison of lung ultrasound scores between the groups (n=30)
| Groups Compared | Mean Difference | Standard Error | Confidence Interval | P | |
|---|---|---|---|---|---|
|
| |||||
| Lower Limit | Upper Limit | ||||
|
| |||||
| LUSS-Baseline | |||||
| Group A vs Group B | 0.2 | 0.89 | -2.02 | 2.42 | 0.973 |
| Group C vs Group B | 5.4 | 1.13 | 2.59 | 8.2 | <0.001 |
| Group A vs Group C | -5.2 | 1.2 | -8.17 | -2.22 | 0.001 |
| Groups (A + C) vs Group B | 1.93 | 1.02* | -0.16 | 4.03 | 0.069 |
|
| |||||
| LUSS-ICU | |||||
|
| |||||
| Group A vs Group B | 1.467 | 1.89 | -3.22 | 6.16 | 0.721 |
| Group C vs Group B | 11.667 | 2.39 | 5.7 | 17.6 | <0.001 |
| Group A vs Group C | -10.2 | 2.53 | -16.49 | -3.9 | 0.001 |
| Groups (A + C) vs Group B | 4.86 | 2.1* | -0.56 | 9.17 | 0.028 |
*Standard error difference
Figure 2.
Bar diagram comparing the past severity of COVID infection to LUSS
LUSS at all time points showed a strong negative correlation to the PaO2/FiO2 ratio, that is, as the LUSS increased, PaO2/FiO2 ratio decreased (rs = -0.75, P < 0.001). The duration of ventilation, incidence of pulmonary infection, duration of stay in the ICU, in-hospital mortality, and 30-day mortality showed a significantly strong correlation to the LUSS [Table 4].
Table 4.
Comparison of LUSS to in-hospital mortality, duration of ventilation, duration of stay in ICU, and incidence of pulmonary infection
| LUSS | ||
|---|---|---|
|
| ||
| Parameter | Correlation Coefficient | P |
| In-hospital mortality | 0.723 | <0.043 |
| Incidence of pulmonary infection | 0.8 | <0.001 |
| Duration of stay in ICU (Days) | 0.938 | <0.001 |
| Days of ventilation | 0.802 | <0.001 |
| 30-day mortality | 0.723 | <0.043 |
The duration of ventilation and the duration of ICU stay were significantly different between Groups A and C as well as Groups B and C [Table 5]. One child in Group A (10%) and three children in Group C (60%) developed pulmonary infection. One child in Group C eventually had a fatal outcome. None of the patients were re-intubated. Owing to low event frequency, these parameters could not be statistically analyzed.
Table 5.
Comparison of duration of ventilation, incidence of pulmonary infection, duration of stay in ICU, in-hospital mortality, and 30-day mortality between the groups
| Parameter | Study Groups | P | P | ||||
|---|---|---|---|---|---|---|---|
|
|
|
||||||
| Group A (n=10) | Group B (n=15) | Group C (n=5) | A vs C | B Vs C | A vs B | ||
| Duration of ventilation (Days) | 0.1±0.316 | 0.13±0.35 | 3.6±6.38 | <0.05 | 0.04 | 0.03 | 0.99 |
| Incidence of pulmonary infection | 1 (10%) | 0 | 3 (60%) | Statistical analysis is not possible due to low event frequency | |||
| Duration of stay in ICU (Days) | 1.6±1.26 | 2±1.36 | 6.4±5.17 | 0.011 | 0.002 | 0.003 | 0.908 |
| In-hospital mortality | 0 | 0 | 1 (20%) | Statistical analysis is not possible due to low event frequency | |||
| 30-day mortality | 0 | 0 | 1 (20%) | Statistical analysis is not possible due to low event frequency | |||
Group C had a significantly lower PaO2/FiO2 ratio before and after cardiac surgery when compared to the control group (Group B). However, there was no significant difference between the PaO2/FiO2 ratio in Group A and B as well as Group A and Group C at both time points [Table 6]. Before surgery, only patients with non-cyanotic heart disease were included in the analysis.
Table 6.
Comparison of PaO2/FiO2 between groups before (pre-CPB) and after cardiac surgery in the ICU (POD-0)
| Parameter | Study Groups | P | P | ||||
|---|---|---|---|---|---|---|---|
|
|
|
||||||
| Group A (n=10) | Group B (n=12) | Group C (n=4) | A vs C | B Vs C | A vs B | ||
| PaO2/FiO2-Pre CPB | 340.90±58.82 | 391.33±43.46 | 288.00±48.69 | 0.004 | 0.204 | 0.005 | 0.072 |
|
| |||||||
| Parameter | Group A (n=10) | Group B (n=15) | Group C (n=5) | P | P | ||
|
| |||||||
| A vs C | B Vs C | A vs B | |||||
|
| |||||||
| PaO2/FiO2- POD 0 | 312.8±90.18 | 357.6±63.82 | 207.8±95.49 | 0.004 | 0.054 | 0.003 | 0.357 |
DISCUSSION
After effective vaccination campaigns and successful control of the COVID-19 pandemic, we are at a phase where we learn to live with the COVID-19 virus.[12] As elective congenital cardiac surgery programs are restarting, we are encountering a new subset of children that are COVID-recovered in our operating rooms. Data on this subset are lacking.
CPB is known to affect the pulmonary parenchymal function due to endothelial activation, neutrophil sequestration, and inflammatory response.[13] COVID-19 is known to affect the alveolar-capillary membrane and interstitial tissue. Depending on the immune response mounted against the virus, the severity of COVID-19 infection varies. The more heightened the immune response involving the activation of macrophages, the more extensive the lung damage.[14] Though statistics vary between continents, most of the studies report a maximum of 10% incidence in children.[3,15] Patients with more severe disease that affects their oxygenation or hemodynamic parameters receive in-hospital care as opposed to most children who mount a brisk T cell response and clear the virus effectively and hence remain asymptomatic or mildly symptomatic, receiving domiciliary care.[16] That was our rationale for further subdividing the COVID-recovered children into those who received in-hospital care and who received domiciliary care for their past infection. All the patients in Group C had an oxygen saturation lower than 90% without supplementary oxygen, during the infection. One patient who eventually had a fatal outcome received non-invasive ventilation and tested positive for D-dimer and ferritin during the infection.
LUSS is used successfully in adults to predict the need for intubation, ICU admission, or even the risk of mortality.[11,17] Lung ultrasound examination is an easy, safe, reproducible tool used routinely in pediatric cardiac surgery intensive care units.[18] In COVID-19-infected adults, LUSS is well validated though data are lacking on the LUSS in pediatric cardiac surgery units. Our study agrees with the available literature, and we demonstrated a strong correlation of LUSS to patient morbidity as well as an inverse relation to the PaO2/FiO2 ratio. This observation agreed with the study by de Alencar et al.[17] that had demonstrated that the LUSS used in the emergency department in COVID-19 adult patients was a good predictor of death, ICU admission, and endotracheal intubation. This is one of the first original research using LUSS in children undergoing heart surgeries. After further studies, LUSS has the potential to become an integral part of pediatric cardiac surgery ICUs.
From our study, for all practical purposes, we can expect COVID-recovered children, who had an uneventful infection, to behave like the general population who present for pediatric cardiac surgery as far as the respiratory system is concerned. This finding agrees with the study by Joshi et al.[19] which has reported no unfavorable outcomes in COVID-19-recovered children when compared to controls. But this study did not use LUSS in evaluation. Our study is the first study to identify patients with a history of severe COVID-19 infection as a high-risk group, to the best of our knowledge.
Children with a history of severe COVID-19 documented a longer duration of ventilation, higher incidence of pulmonary infection, increased duration of ICU stays, and one mortality. Though statistical analysis was not possible in most of these outcome parameters due to low event frequency and small sample size, the clinical implications were profound. PaO2/FiO2 ratio was consistently low in this group, in comparison with the control group, which is a novel finding. The child who had a fatal course was a case of a recent severe COVID-19 infection. The child was admitted to the hospital with oxygen supplementation by nasal prongs after testing positive for COVID-19. C reactive protein, ferritin, and D-dimer were positive during the infection, signifying a multisystem inflammation and coagulopathy. Due to the semi-emergency nature of the surgery owing to dropping arterial saturation, the child had to be taken up for intracardiac repair of Tetralogy of Fallot, one month after recovery from the COVID-19 infection. Inflammatory markers and D-dimer were negative when the child was taken for surgery. The patient had severe third space loss after CPB and never improved despite optimal care. COVID-19 is known to cause an inflammatory response in multiple organ systems. The inflammation and endothelialitis can damage the epithelial and endothelial barrier integrity.[17] How long the damaged endothelium takes to regenerate and how long we need to wait before CPB can be safely instituted for the patient is not known. Despite multiple recommendations by various cardiovascular societies, we need to investigate this subset with an open mind and further studies are indicated to draw any potent conclusions.
Limitations of the study
Being a pilot study, the sample size is inadequate to conclude.
Increased pulmonary blood flow can affect the lung ultrasound scores in left to right cardiac shunts. However, the distribution of diagnoses for which the children underwent surgery was matched in both groups.
CONCLUSION
Lung ultrasound score (LUSS) in COVID-19-recovered children was not significantly different from those without a history of COVID-19 after congenital heart surgery. COVID-19-recovered children who previously had severe COVID-19 had significantly higher LUSS, duration of ventilation, and duration of ICU stay after cardiac surgery compared to those without a history of COVID-19 infection or who received only domiciliary care. COVID-19-recovered children who previously received domiciliary care had comparable LUSS, duration of ventilation, and duration of ICU stay to those without a history of COVID-19 infection.
Children with a history of COVID-19 requiring hospital admission need further extensive studies to identify the frequency of adverse events like mortality, duration of ventilation and ICU stays, and incidence of pulmonary infection since a 20% mortality and 60% incidence of pulmonary infection was noted in our study, which cannot be generalized due to limited sample size.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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