Abstract
Background:
Postoperative pulmonary complications including atelectasis are common complications after surgery. However, the incidence of postoperative atelectasis in pediatric surgical population is not yet well delineated.
Methods:
Using electronic medical record, we identified pediatric patients who underwent gastrointestinal surgery from January 2016 to September 2019 and determined the presence or absence of postoperative atelectasis by postoperative X-ray read. Risk factor analysis of postoperative atelectasis was performed using logistic regression analysis.
Results:
We found that 25.6 % of patients had radiographic evidence of postoperative atelectasis. Univariate and multivariate analyses demonstrated that the risk factors included lower weight, higher ASA class, emergency surgery, the use of higher peak airway pressure, lower lung compliance, and the lack of neuromuscular relaxant reversal agent use. In patients who received muscle relaxants, the lack of neuromuscular relaxant reversal agent use was associated with an increased risk of postoperative atelectasis (odds ratio 0.421, 95 % confidence interval 0.235–0.723, p < 0.001).
Discussion:
Postoperative atelectasis was frequently observed in pediatric patients undergoing gastrointestinal surgery. For cases where neuromuscular blockade is used, adequate reversal is critical.
Keywords: Postoperative, Atelectasis, Neuromuscular blockade, Reversal
1. Introduction
Postoperative pulmonary complications (PPCs) are common complications after surgery.1 They are often associated with longer hospital stays2 and higher in-hospital postoperative mortality.3 The European Perioperative Clinical Outcome (EPCO) task force defined PPCs as a composite outcome measure of respiratory infection, respiratory failure, pleural effusion, atelectasis, pneumothorax, bronchospasm, aspiration pneumonitis, and pneumonia in 2015.4 Based on this definition, the estimated incidences of PPCs are 5.8–7.9 % in general surgery in patients ≥18 years old.5,6 PPCs are particularly common after major abdominal surgery, with the estimated incidence of 9 ~ 40 %.7 Their incidences are much higher in cardiothoracic surgery (up to 69 %).8 Among PPCs, postoperative atelectasis is one of the most frequently encountered complications.9
In pediatric populations, an initiative comparable to the EPCO has not yet been launched.10 Overall, the data on PPCs in pediatric populations is less robust. Absorption atelectasis and compression of lung tissues due to the loss of tone under anesthesia are largely responsible for the development of atelectasis.11 The latter may also be affected by the development aspect in pediatric populations. The rib cage is pliable at birth and undergoes stiffness over the first few years of lung. Thus, pediatric patients undergo a dynamic change of respiratory mechanics. Taking this into account, we expect that the incidence of postoperative atelectasis differs in pediatrics depending on age. In this study, we examined the incidence of postoperative atelectasis and its risk factors in pediatric patients undergoing gastrointestinal surgery.
2. Methods
2.1. Study cohort and data collection
The Institutional Review Board at Boston Children’s Hospital (BCH) approved the study protocol. Informed consent was waived by the Institutional Review Board (IRB). The study referred to the SQUIRE 2.0 (Standards for Quality Improvement Reporting Excellence) guidelines of the Enhancing the Quality and Transparency of Health Research (EQUATOR) network. Postoperative atelectasis can be suspected with the presence of an increased breathing rate, fever, and desaturation, but the gold standard of its diagnosis is by imaging study such as Chest X-ray.12 Pediatric patients who underwent gastrointestinal surgery at BCH from January 2017 to September 2019 and had postoperative X-ray were considered eligible. The majority of patients underwent routine postoperative X-ray on day 1. Postoperative X-ray results officially read by radiology staff physicians were used to determine the presence or absence of atelectasis. We excluded patients who underwent endoscopic procedures or who did not have postoperative X-ray. We used the electronic medical record to obtain patients’ demographics, intraoperative information such as medications, blood transfusion, respiratory parameters, and the duration of anesthesia care, and the American Society of Anesthesiology (ASA) physical status classification.
2.2. Statistical analysis
Categorical data was expressed as numbers and percentages. Continuous variables were expressed as median and interquartile range when not normally distributed. Normality was measured using the Shapiro-Wilk test. Univariate analysis and multivariate analysis were performed using logistic regression analysis. The results were expressed as the odds ratio (O.R.) as a measure of risk, the 95 % confidence interval (C.I.), and p values from the Wald test. P < 0.05 was considered as statistically significant. The statistical analyses were performed using Stata 13 software (College Station, Texas).
3. Results
3.1. The incidence of postoperative atelectasis and its risk factors in pediatric patients undergoing gastrointestinal surgery
We identified 636 patients who met the inclusion criteria from January 2016 to September 2019. In this cohort, we found radiographic evidence of postoperative atelectasis in 163 out of 636 patients (25.6 %) on postoperative day 1 (Table 1). We performed univariate analysis to identify risk factors associated with postoperative atelectasis. We found lower age, weight, higher ASA class, emergency surgery, the use of higher peak airway pressure, lower lung compliance, higher transfusion requirement, the use of bronchodilator, muscle relaxant, and no use of neuromuscular relaxant reversal agent as risk factors. Then, we performed multivariate analysis of those risk factors. Lower weight, higher ASA class, emergency surgery, the use of higher peak airway pressure, lower lung compliance, and no use of neuromuscular relaxant reversal agent were considered significant risk factors (Table 2).
Table 1.
Univariate analysis of risk factors for postoperative atelectasis.
| Atelectasis | P value | ||
|---|---|---|---|
| No (n = 473) | Yes (n = 163) | ||
| Age (month) | 107.5 (9.5, 203.5) | 26.7 (3.6, 159.4) | <0.001 |
| Gender | Male 275 (58.4 %) | Male 87 (53.4 %) | 0.27 |
| Female 196 (41.6 %) | Female 76 (46.6 %) | ||
| Weight (Kg) | 30.7 (8.5, 57.1) | 7.6 (3.5, 25.6) | <0.001 |
| ASA class | ASA I 14 (3.0 %) | ASA I 0 (0 %) | <0.001 |
| ASA II 239 (50.9 %) | ASA II 24 (15.0 %) | ||
| ASA III 201 (42.8 %) | ASA III 76 (47.5 %) | ||
| ASA IV 13 (2.8 %) | ASA IV 52 (32.5 %) | ||
| ASA V 3 (0.6 %) | ASA V 8 (5.0 %) | ||
| ASA category | ASA I & II 253 (53.5 %) | ASA I & II 24 (14.7 %) | <0.001 |
| ASA III, IV & V 220 (46.5 %) | ASA III, IV & V 139 (85.3 %) | ||
| Emergency | 66 cases (14.0 %) | 69 cases (42.3 %) | <0.001 |
| Laparoscopy | 8 cases (1.7 %) | 2 cases (1.2 %) | 0.68 |
| Anesthesia duration (min) | 266 (191, 371) | 266.5 (177.5, 426) | 0.51 |
| Inhaler tx | 7 (1.5 %) | 9 (5.5 %) | 0.005 |
| Use of muscle relaxant | 431 (91.5 %) | 140 (85.9 %) | 0.039 |
| Use of reversal | 363 (77.1 %) | 61 (37.4 %) | <0.001 |
| PRBC (mL/kg) | 0 (0, 0) | 0 (0, 9.3) | <0.001 |
| FFP (mL/kg) | 0 (0,)) | 0 (0, 0) | <0.001 |
| Platelet (mL/kg) | 0 (0, 0) | 0 (0, 0) | 0.003 |
| Cryoprecipitate (mL/kg) | 0 (0, 0) | 0 (0, 0) | 0.27 |
| PIP (cmH2O) | 15.1 (13.2, 17.6) | 19.6 (16.0, 24.7) | <0.001 |
| PEEP (cmH2O) | 3.9 (3.0, 4.9) | 4.1 (2.6, 5.1) | 0.16 |
| TV (mL/kg) | 7.9 (6.7, 9.0) | 8.0 (6.8, 9.2) | 0.37 |
| Lung compliance (mL/cmH2O) | 21.7 (6.7, 37.8) | 4.8 (1.8, 13.3) | <0.001 |
Tx, treatment; PRBC, packed red blood cell; FFP, fresh frozen plasma; PIP, peak inspiratory pressure; PEEP, positive end-expiratory pressure; TV, tidal volume.
Table 2.
Multivariate analysis of risk factors for postoperative atelectasis.
| Odd ratio | 95 % C.I. | p value | |
|---|---|---|---|
| Age | 1.0008 | 0.998–1.004 | 0.597 |
| Weight | 1.021 | 1.003–1.039 | 0.021 |
| ASA category | 2.725 | 1.557–4.771 | < 0.001 |
| Emergency | 1.831 | 1.079–3.107 | 0.025 |
| Bronchodilator tx | 2.838 | 0.884–9.116 | 0.08 |
| Use of muscle relaxant | 1.332 | 0.601–2.953 | 0.48 |
| Use of reversal | 0.465 | 0.276–0.782 | 0.004 |
| PRBC | 0.99 | 0.960–1.021 | 0.529 |
| FFP | 1.076 | 0.998–1.160 | 0.057 |
| Platelet | 0.912 | 0.821–1.014 | 0.089 |
| PIP | 1.052 | 1.031–1.074 | < 0.001 |
| Lung compliance | 0.927 | 0.899–0.955 | < 0.001 |
tx, treatment; PRBC, packed red blood cell; FFP, fresh frozen plasma; PIP, peak inspiratory pressure.
3.2. No use of neuromuscular relaxant reversal agent was associated with higher incidence of postoperative atelectasis
Although patient’s weight, ASA class, and respiratory mechanics may not be intervenable, the role of neuromuscular relaxant reversal agent in postoperative atelectasis would be a critical issue to be dissected. We found 571 patients who received neuromuscular blockade during surgery. 411 patients out of 571 patients (71.9 %) received neuromuscular reversal agents (Table 3), but the rest did not. In this analysis, we also found that no use of neuromuscular relaxant reversal agent was associated with higher incidence of postoperative atelectasis in both univariate and multivariate analyses (Table 3 and Table 4).
Table 3.
Univariate analysis of risk factors for postoperative atelectasis in the setting of muscle relaxant use.
| Atelectasis | Pvalue | ||
|---|---|---|---|
| No (n = 431) | Yes (n = 140) | ||
| Age (month) | 113.7 (9.5, 203.5) | 35.7 (3.6, 159.5) | <0.001 |
| Gender | Male 249 (57.8 %) | Male 72 (51.4 %) | 0.19 |
| Female 182 (42.2 %) | Female 68 (48.6 %) | ||
| Weight (Kg) | 31.4 (8.9, 58.8) | 7.6 (3.5, 24.9) | <0.001 |
| ASA class | ASA I 13 (3.0 %) | ASA I 0 (0 %) | <0.001 |
| ASA II 218 (50.6 %) | ASA II 20 (14.3 %) | ||
| ASA III 187 (43.4 %) | ASA III 69 (49.3 %) | ||
| ASA IV 10 (2.3 %) | ASA IV 44 (31.4 %) | ||
| ASA V 3 (0.7 %) | ASA V 7 (5.0 %) | ||
| ASA category | ASA I & II 231 (53.6 %) | ASA I & II 20 (14.3 %) | <0.001 |
| ASA III, IV & V 200 (46.4 %) | ASA III, IV & V 120 (85.7 %) | ||
| Emergency | 57 cases (13.2 %) | 55 cases (39.3 %) | <0.001 |
| Laparoscopy | 7 cases (1.6 %) | 1 case (0.7 %) | 0.43 |
| Anesthesia duration (min) | 276 (196, 377) | 272.5 (191.5, 451) | 0.39 |
| Bronchodilator tx | 7 (1.6 %) | 5 (3.6 %) | 0.16 |
| Use of reversal | 353 (81.9 %) | 58 (41.4 %) | <0.001 |
| PRBC (mL/kg) | 0 (0, 0) | 0 (0, 9.5) | <0.001 |
| FFP (mL/kg) | 0 (0,)) | 0 (0, 0) | <0.001 |
| Platelet (mL/kg) | 0 (0, 0) | 0 (0, 0) | 0.003 |
| Cryoprecipitate (mL/kg) | 0 (0, 0) | 0 (0, 0) | 0.73 |
| PIP (cmH2O) | 15.2 (13.4, 17.6) | 19.6 (16.0, 25.0) | <0.001 |
| PEEP (cmH2O) | 4.0 (3.0, 4.9) | 4.1 (2.7, 5.1) | 0.29 |
| TV (mL/kg) | 7.9 (6.7, 9.0) | 8.0 (6.9, 9.2) | 0.31 |
| Lung compliance (mL/cmH2O) | 21.9 (7.2, 37.5) | 4.8 (1.8, 12.6) | <0.001 |
tx, treatment; PRBC, packed red blood cell; FFP, fresh frozen plasma; PIP, peak inspiratory pressure; PEEP, positive end-expiratory pressure; TV, tidal volume.
Table 4.
Multivariate analysis of risk factors for postoperative atelectasis in the setting of muscle relaxant use.
| Odd ratio | 95 % C.I. | p value | |
|---|---|---|---|
| Age | 1.0003 | 0.998–1.003 | 0.849 |
| Weight | 1.02 | 1.002–1.038 | 0.031 |
| ASA category | 2.774 | 1.537–5.005 | 0.001 |
| Emergency | 1.707 | 0.974–2.991 | 0.062 |
| Use of reversal | 0.421 | 0.245–0.723 | < 0.001 |
| PRBC | 0.99 | 0.958–1.019 | 0.435 |
| FFP | 1.067 | 0.992–1.148 | 0.08 |
| Platelet | 0.923 | 0.833–1.023 | 0.129 |
| PIP | 1.05 | 1.028–1.073 | < 0.001 |
| Lung compliance | 0.929 | 0.899–0.959 | < 0.001 |
PRBC, packed red blood cell; FFP, fresh frozen plasma; PIP, peak inspiratory pressure.
4. Discussion
We observed about 25 % incidence of radiographically identified, postoperative atelectasis in pediatric patients undergoing gastrointestinal surgery. Furthermore, our multivariate analysis showed that the risk factors of postoperative atelectasis included lower weight, the use of higher peak inspiratory pressure, lower lung compliance, emergency surgery, higher ASA class, and no use of neuromuscular relaxant reversal agents.
The majority of risk factors for postoperative atelectasis we identified here are intuitive. Lower weight can be reflective of lower age, and/or poor overall health. Patients of younger age may have a pliable rib cage, which leads to propensity of lung decruitment under anesthesia. Non-anesthetized neonates and infants breathe with very high respiratory rates to maintain functional residual capacity (laryngeal braking) due to the presence of pliable rib cage. Under anesthesia, their respiratory drive is taken over, making them susceptible to lung decruitment. Emergency surgery and higher ASA class indicate worse health status. Those patients could have an already tenuous respiratory status. Lower lung compliance with the use of high peak inspiratory pressure could indicate the presence of lung pathology. Therefore, the lungs of patients with lower lung compliance requiring the use of high peak inspiratory pressure can be easily de-recruited, leading to atelectasis.
Neuromuscular relaxants have been advantageous to safely anesthetize patients with significant cardiopulmonary diseases and also to provide relaxed surgical field.13 Relaxation of the upper abdominal muscles, the larynx and the diaphragm require deep neuromuscular blockade (Train of four (TOF) count =0) .14 However, complications from the use of neuromuscular blockade agents have also been reported. Kirmerier et al. reported that the use of neuromuscular blockade agents in general anesthesia was associated with an increased risk of PPCs in adult patients.15 Similarly, the use of neuromuscular blockade posed a higher risk of developing postoperative pneumonia in adults in the study by Bulka et al.16 Furthermore, the lack of neuromuscular blockade reversal using neostigmine increased the incidence of pneumonia by 2.26 times in the study. A study by Sasaki et al. also showed an increased incidence of postoperative atelectasis without neostigmine reversal.17 Sugammadex is a newer neuromuscular blockade reversal agent. In adult patients, the effectiveness of sugammadex vs neostigmine reversal was compared by Kheterpal et al.18 They found that the use of sugammadex was associated with less PPCs compared to neostigmine. The use of neuromuscular blockade monitoring is highly advocated during general anesthesia when muscle relaxant is administered. TOF ratio > 0.9 is often considered adequate, but even when TOF ratio of 1.0, most postsynaptic receptors are still occupied by the neuromuscular blockade agent, when forced vital capacity is only partially recovered, and the acute ventilatory response to hypoxia is still depressed from the baseline.19 Thus, the administration of reversal agents may be considered in the case of TOF ratio of >0.9.
PPCs have been studied less in pediatric populations. As we found that about 25 % of pediatric patients had postoperative atelectasis, pediatric patients may have higher incidence of PPCs compared to adult patients. To our surprise, around 28 % of patients did not receive neuromuscular blockade reversals following muscle relaxant use. While the presence of TOF ratio of > 0.9 was not consistently documented in the cases without reversal agents, some residual muscle relaxation might have been present.14 Thus, the incidence of postoperative atelectasis might have been lower if all patients were fully reversed. The effectiveness of sugammadex vs neostigmine reversal was compared in pediatric cohort by Beltran et al. They examined children undergoing inpatient noncardiac surgery using the Pediatric Health Information System (PHIS) dataset from 2016 to 2020.20 PHIS is an administrative health database by the Children’s Hospital Corporation of America. PPCs were defined as pneumonia and/or respiratory failure in the study. Both neostigmine and sugammadex groups showed 3.1 % of postoperative pneumonia and/or respiratory failure. However, they did not compare postoperative atelectasis as Kheterpal et al. did in adult cohort. Thus, further study needs to be done. We should also note that just giving reversal agents might not be enough. Scheffenbichler et al. reported that the use of high dose neuromuscular blockade was associated with an increased incidence of PPCs in pediatric population.21 It is unclear if the use of high dose blockade was reflective of the presence of residual neuromuscular blockade. However, it is safe to say that an adequate reversal of neuromuscular blockade would be important in our clinical practice.
Our study has limitations. Our study is retrospective in nature, and we are aware of the presence of many confounding factors that might have been detected. It is also possible that anesthesia providers did not record neuromuscular reversal agents in the record even when they were given. Nonetheless, we found that about 28 % of patients did not have recorded use of reversal agents following neuromuscular use. A second limitation is the detection of postoperative atelectasis. We used postoperative X ray as a modality to determine postoperative atelectasis. While CT scans would be more sensitive, it is not practical to detect postoperative atelectasis using it. Third, we did not determine the correlation between postoperative atelectasis and postoperative clinical outcomes such as oxygen requirement and saturation. In our hospital, it is routine to have oxygen saturation measured continuously, but actual recording is required only every four hours. Thus, it would be difficult to accurately determine oxygen saturation status. Similarly, it would be hard to know how much oxygen patients are actually receiving, given oxygen may not be applied to pediatric patients reliably. Nonetheless, we presented objective evidence of postoperative atelectasis in our cohort.
In summary, we reported the incidence of postoperative atelectasis in pediatric patients undergoing gastrointestinal surgery. Our data also supports that adequate reversal of neuromuscular blockade is important.
Acknowledgement
We thank Ms. Jennifer Ormsby (Boston Children’s Hospital) for technical assistance.
Footnotes
CRediT authorship contribution statement
Emi Yuki: Writing – original draft, Investigation, Formal analysis, Data curation. Sulpicio G. Soriano: Writing – review & editing, Supervision. Miho Shibamura-Fujiogi: Writing – review & editing, Supervision, Investigation, Formal analysis. Koichi Yuki: Writing – review & editing, Supervision, Investigation, Conceptualization.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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