Abstract
Croup is a common respiratory illness in children with a substantial variation in the severity of symptoms. Most of the patients present with mild symptoms, but patients with severe croup require intensive care unit (ICU) management. The aim of this study was to investigate the airway management of patients with severe croup who required intubation and determine the risk factors for prolonged intubation. We performed an 18-year retrospective observational cohort study at the pediatric ICU of a tertiary children's hospital in Japan. A total of 16 patients with croup who were intubated for upper airway obstruction were included in the study. Most patients (13of 16, 81%) were intubated with an endotracheal tube (ETT) smaller than their age-appropriate size. The median difference in the internal diameter (ID) between the selected ETT and the age-appropriate size was 1.0 mm (interquartile range: 0.5–1.0). Multivariate analysis performed on factors affecting the cumulative incidence of extubation revealed that the difference in ID between the selected ETT and age-appropriate size (mm) significantly reduced the duration of intubation (hazard ratio: 0.092, p = 0.03). A downsized ETT without a cuff may be recommended for intubation of patients with croup.
Keywords: severe croup, airway management, endotracheal tube size
Introduction
Croup is a common pediatric respiratory disease with substantial range in the severity of symptoms. Although most of the patients present with only mild symptoms and can be managed in the outpatient setting, extreme cases present with life-threatening airway obstruction and require prompt endotracheal intubation. 1 Pediatric intensivists should have expertise in the airway management of these patients. Practical skills and proper determination of the mode of anesthetic induction, choice of endotracheal tube (ETT) size, timing, and site of intubation are warranted.
Several publications regarding management of croup patients have described patient management in the emergency department, steroid and antibiotic therapy, causative organisms, and intensive care unit (ICU) management of intubated patients, 1 2 3 but detailed studies on specific airway management of children needing intubation for croup are scarce. 3 Therefore, we aimed to examine the management of patients intubated for croup in our hospital and determine the risk factors for prolonged intubation in these patients.
Patients and Methods
This study is a retrospective observational cohort study at the pediatric ICU (PICU) of the National Center for Child Health and Development (NCCHD) in Tokyo, Japan. The unit is a medical and surgical PICU composed of 20 beds. This study was approved by the ethics committee of our institution.
Patients
All patients younger than 2 years who were intubated for upper airway obstruction due to croup and admitted to the PICU at NCCHD between January 2001 and March 2019 were included. Patients with tracheostomy or airway anomalies (including trisomy 21) were excluded. Patients older than 2 years were also excluded for their atypical age for croup syndrome. Medical records were reviewed and the following data were extracted: age, weight, sex, underlying disease, pediatric index of mortality 2 (PIM2) score, croup score on admission, site of intubation (in referral hospital, emergency department, operating room, or PICU), presence of difficulty in mask ventilation or intubation, internal diameter (ID) and type (cuffed or uncuffed) of ETT, use of inhalation anesthesia, use of neuromuscular blocking (NMB) agents before intubation, presence of ETT leakage immediately after intubation, steroid use after intubation, presence of stridor after extubation, extubation failure, and number of days of intubation, PICU stay, and hospital stay.
In this study, the Westley croup score was used to define the severity of the symptoms; it consists of the following five factors: level of consciousness, cyanosis, stridor, air entry, and retractions. 4 The points given for each factor are listed in Table 1 , and the final score ranges from 0 to 17. The scores were calculated and recorded at the first physician contact in the emergency department. In some cases, the scores were re-evaluated multiple times to assess treatment response while in the emergency department, and the highest score was adopted in such cases. We compared the selected ETT size for each patient with age-appropriate size. Age-appropriate ETT ID for the patients older than 2 years was calculated by the following formula: age/4 plus 4 (in millimeters) for uncuffed ETTs and age/4 plus 3.5 for cuffed ETTs. Age-appropriate ETT sizes are shown in Table 2 .
Table 1. Westley score: classification of croup severity.
| Number of points assigned for this feature | ||||||
|---|---|---|---|---|---|---|
| 0 | 1 | 2 | 3 | 4 | 5 | |
| Chest wall retraction | None | Mild | Moderate | Severe | ||
| Stridor | None | With agitation | At rest | |||
| Cyanosis | None | With agitation | At rest | |||
| Level of consciousness | Normal | Disoriented | ||||
| Air entry | Normal | Decreased | Markedly decreased | |||
Notes: A total score of ≤ 2 indicates mild croup. The characteristic barking cough and hoarseness may be present, but there is no stridor at rest. A total score of 3 to 5 is classified as moderate croup. It presents with easily heard stridor but with few other signs. A total score of 6 to 11 is severe croup. It also presents with obvious stridor but also features marked chest wall indrawing. A total score of ≥ 12 indicates impending respiratory failure. The barking cough and stridor may no longer be prominent at this stage.
Table 2. Age-appropriate endotracheal tube size.
| Age group | Uncuffed ETT size (mm) | Cuffed ETT size (mm) |
|---|---|---|
| Term infant to 1 mo | 3.0 | – |
| 1 to 9 mo | 3.5 | 3.0 |
| 9 mo to 2 y | 4.0 | 3.5 |
| 2 y and older | Age/4 + 4 | Age/4 + 3.5 |
Abbreviation: ETT, endotracheal tube.
Methods
The cumulative incidence of events (extubation or tracheostomy) was analyzed and graphed from the day of intubation. Multivariate analysis was performed on five factors affecting the cumulative incidence of extubation: patient's age (months), Westley croup score at the emergency department, difference in ID between the selected tube and age-appropriate size (mm), presence of ETT leakage immediately after intubation, and PIM2 on PICU admission. Data other than these five factors were excluded from the multivariate analysis due to insufficient data number, unclear clinical implications, or collinearity.
Statistical Analyses
Descriptive statistics were expressed as medians and interquartile ranges (IQRs) or mean and standard deviation for continuous data, and absolute frequencies and percentage for categorical data. Cumulative incidence of extubation or tracheostomy was demonstrated by the Gray method. Multivariate analysis on the cumulative incidence of extubation was performed using the Fine and Gray subdistribution hazard model. Two-sided p -values less than 0.05 were considered statistically significant. All analyses were performed with EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphical user interface for R (The R Foundation for Statistical Computing, Vienna, Austria).
Results
During the observation period, a total of 16 patients were included. Patient data are summarized in Table 3 . The study sample consisted of mostly male patients (10of 16, 63%) with a median age of 12.0 months (IQR: 7.0–13.3). Underlying diseases were seen in 3 of 16 (19%) of patients. The three cases consisted of premature birth, Pfeiffer's syndrome, and cholestatic liver disease. The mean PIM2 was 0.93 ± 0.38 and median croup score was 9.0 (8.0–10.0). Intubations were performed in referral hospitals in 1 of 16 (6%) case and the remaining 15 of 16 (94%) in the operating room. There was no patient intubated in the emergency department. Most patients (13 of 16, 81%) were intubated with ETTs smaller than their age-appropriate size. The median difference in ID between the selected tube and the age-appropriate-size tube was 1.0 mm (0.5–1.0).
Table 3. Patient demographics, airway management, and clinical course ( n = 16) .
| Demographics | |
| Age (mo), median (IQR) | 12.0 (7.0–13.3) |
| Weight (kg), median (IQR) | 8.7 (7.8–9.3) |
| Male, n (%) | 10 (63) |
| Pediatric index of mortality 2 on PICU admission (%), mean (±SD) | 0.93 ± 0.38 |
| Westley croup score at emergency department, median (IQR) | 9.0 (8.0–10.0) |
| Underlying disease, n (%) | 3 (19) |
| Airway management | |
| Difficulty in face mask ventilation, n (%) | 1 (7) |
| Difficulty in tracheal intubation, n (%) | 4 (29) |
| Cuffed endotracheal tube, n (%) | 2 (13) |
| Use of inhalation anesthesia, n (%) | 9 (69) |
| Use of neuromuscular blocking agents, n (%) | 11 (73) |
| Difference in internal diameter between the selected tube and age-appropriate size (mm), median (IQR) | 1.0 (0.5–1.0) |
| Presence of endotracheal tube leakage immediately after intubation, n (%) | 8 (50) |
| Clinical course | |
| Extubation failure, n (%) | 2 (13) |
| Steroid use after intubation, n (%) | 15 (94) |
| Presence of stridor after extubation, n (%) | 7 (54) |
| Duration of intubation (d), median (IQR) | 5.5 (3.0–9.3) |
| Duration of PICU stay (d), median (IQR) | 5.5 (4.0–10.0) |
| Duration of hospital stay (d), median (IQR) | 11.5 (9.0–15.0) |
| Received tracheostomy, n (%) | 1 (6) |
| In-hospital death, n (%) | 0 (0) |
Abbreviations: IQR, interquartile range; PICU, pediatric intensive care unit; SD, standard deviation.
Notes: The Fisher's exact test and Mann–Whitney's U test were used to compare between the two groups. Values are n (%) or as otherwise indicated.
Cumulative incidence of events (extubation or tracheostomy) from the day of intubation is demonstrated in Fig. 1 . All patients were extubated in the PICU, except for one who was transferred while intubated and one who underwent tracheostomy. Median duration of intubation was 5.5 days (IQR: 3.0–9.3). The patient who underwent tracheostomy had no underlying disease and was intubated with a smaller ETT than age-appropriate size for croup associated with influenza A infection. The patient had difficulty in extubation due to tracheal granulation formation, and tracheostomy was performed. After surgical resection of the tracheal granuloma and tracheoplasty, the cannula was removed from the patient 19 months later. Except for the case of tracheostomy, there were no cases requiring treatment for subglottic stenosis or granulation tissue.
Fig. 1.
Cumulative incidence of events (extubation or tracheostomy) from the day of intubation.
Results of multivariate analysis performed on five factors affecting the cumulative incidence of extubation are shown in Table 4 . Of the five factors, the difference in ID between the selected tube and age-appropriate size (mm) significantly reduced the duration of intubation (hazard ratio: 0.092, p = 0.03).
Table 4. Multivariate analysis performed on five factors affecting the cumulative incidence of extubation.
| Hazard ratio | 95% confidence interval | p -Value | |
|---|---|---|---|
| Age (mo) | 0.993 | 0.762–1.293 | 0.96 |
| Westley croup score at emergency department | 1.589 | 0.796–3.172 | 0.19 |
| Difference in internal diameter between the selected tube and age-appropriate size (mm) | 0.092 | 0.011–0.798 | 0.03 |
| Presence of endotracheal tube leakage immediately after intubation | 0.359 | 0.025–5.159 | 0.45 |
| Pediatric index of mortality 2 on PICU admission | 2.593 | 0.153–44.050 | 0.51 |
Abbreviation: PICU, pediatric intensive care unit.
Discussion
In this study, a total of 16 patients with a median age of 12.0 months were included. Most of them were intubated with ETTs smaller than their age-appropriate size. We demonstrated that the difference in ID between the selected tube and age-appropriate size (mm) significantly reduced the duration of intubation.
Croup is a common pediatric illness that can range in severity from rhinorrhea and a barky cough to stridor, respiratory distress, and, in extreme cases, airway obstruction. 1 3 Although the majority of the patients with croup receive outpatient care, croup can be a life-threatening disease. 1 3 The rate of hospitalization was reported to be 1.3 to 6% in pediatric practice and 31% in the pediatric emergency department. 1 5 In another study, 64 (9%) of 710 patients hospitalized for croup were admitted to the PICU, of which 13 (1.8%) required intubation. 6 It was also reported that 23 to 35% of croup patients who were admitted to the PICU required intubation. 3
When a croup patient with impending airway obstruction is brought to the emergency department, strategies for airway management should be determined prudently. In our series, most patients (15 of 16, 94%) were intubated by anesthesiologists in the operating room. The reports from the Royal Children's Hospital (RCH) and Alberta Children's Hospital (ACH) state the following: of the RCH cases, intubations were performed in referral hospitals or by the emergency transfer services in 31 of 65 (48%) cases, 27 of 65 (41%) in the ICU, 5 of 65 (8%) in the operating room, and 2 of 65 (3%) in the emergency department; at ACH, 10 of 12 (83%) cases were intubated in the operating room, 1 was intubated in the referring hospital, and 1 by a transport physician. 3 The advantage of intubation in the operating room is the availability of inhalation anesthesia, which enables maintenance of spontaneous breathing and upper airway muscle tone during induction. In our cases, sevoflurane was used in 9 of 13 (69%) of patients. A survey conducted in Canada reported that pediatric anesthesiologists prefer inhaled anesthetics for patients with difficult airway. 7 NMB agents were used before intubation in 11 of 15 (73%) of patients in our study. In general, the use of NMB agents facilitates tracheal intubation, 8 9 but carries a potential risk of “can't-intubate-can't-oxygenate” (CICO) in patients with upper airway stenosis due to loss of skeletal muscle tone. Rocuronium is the drug of choice and its antagonist sugammadex is available for immediate use in our institution. However, it should be noted that the CICO scenario is often multifactorial and reversing NMB agents may not always be a solution. 10 In these cases, emergent tracheostomy may be required, and, therefore, the operating room would be an ideal environment. In our hospital, an otolaryngologist is not always present in cases when difficult intubation is anticipated. However, an otolaryngologist is available at the discretion of the anesthesiologist as necessary. Some other institutions have a policy that patients with difficult intubation should be attended by an otolaryngologist. In summary, we believe that intubation in the operating room is the best option if the facility has adequate equipment and manpower, and if the patient can be transported safely in a timely manner.
In croup patients who require intubation, ETTs of ID 0.5 mm smaller than the age-appropriate size are traditionally recommended, 3 11 but there have apparently been no studies that have examined the relationship between selected tube size and duration of intubation. In this study, ETTs smaller than age-appropriate size were chosen in most of the patients (13 of 16, 81%), ranging from 0.5 to 1.0 mm smaller in ID. No association was observed between the selected size of ETT and the presence of leakage. On the contrary, multivariate analysis revealed that the difference in ID between the selected tube and age-appropriate size (mm) significantly reduced the duration of intubation. The rationale for selecting an ETT smaller than the age-appropriate size is the assumed reduction in the direct pressure applied to the larynx, although this has not been demonstrated. However, a smaller-than-age-appropriate-size ETT has the disadvantage of increased airway resistance that may further increase the work of breathing, 12 and this should be considered upon tube selection. Whether to select a cuffed or uncuffed tube is another common question regarding tube selection. The disadvantage of a smaller-than-age-appropriate-size ETT also needs to be considered when using a cuffed tube. Gelbart et al reported that 4% of their study population with severe croup (3 out of 77) were intubated with a cuffed ETT. 3 Cuffed tubes were selected in only 2 of 16 of cases (13%) in our study. In two patients intubated with cuffed tubes in our study, the selected ETT size was not reduced from the age-appropriate tube size. The absence of leakage right after intubation implies laryngeal edema and is generally thought to be a risk factor for prolonged intubation. However, there was no association between the duration of intubation and the presence of leakage immediately after intubation in the present study. In summary, a downsized ETT without cuff may be recommended to be selected for intubation of patients with croup. This might be the first report concluding that selecting smaller tubes than the age-appropriate size for intubation in patients with croup may reduce the duration of intubation.
Limitations
This study has several limitations. First, it was a small retrospective observational study in a single institution, and there was a lack of data for some patients. Second, selection of the ETT, mode of anesthetic induction, and whether to use NMB agents before intubation was at the discretion of the attending physician. Third, the presence of concurrent lower respiratory tract infections could not be defined, as microbiological assays were not performed. Despite these limitations, literature regarding this topic is scarce, and the current report adds significant insight into the airway management of patients with severe croup.
Conclusion
Among intubated patients with croup, the difference in ID between the selected tube and age-appropriate size (mm) significantly reduced the duration of intubation. A downsized ETT without a cuff may be recommended for intubation of patients with croup.
Footnotes
Conflict of Interest None declared.
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