Abstract
Background: In this study, we estimated the predictive factors of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) transmission in anesthesiologists performing endotracheal intubation in patients with confirmed SARS-CoV-2. Method: We analyzed data from a survey conducted by the Chinese Society of Anesthesiology Task Force on Airway Management on endotracheal intubation in 98 patients with SARS-CoV-2 confirmed through nucleic acid testing and chest computed tomography. The multivariate logistic model with stepwise selection was used for selecting the predictive factors significantly associated with SARS-CoV-2 infection in the corresponding anesthesiologists. Results: SARS-CoV-2 prevalence in the corresponding anesthesiologists was 20.41% after intubation in patients with SARS-CoV-2. Univariate analysis indicated that intubation for elective treatment, intubation in an operating room or isolation ward, and routine rapid induction with continuous positive-pressure ventilation (PPV) for intubation were associated with a lower SARS-CoV-2 risk in the anesthesiologists. Multivariate analysis revealed that intubation for elective treatment was associated with a significantly decreased SARS-CoV-2 risk (adjusted odds ratio [aOR] = 0.28, 95% confidence interval [CI]: 0.14-0.68, P < 0.0001), and coughing by patients during endotracheal intubation was associated with a significantly increased SARS-CoV-2 risk (aOR = 1.70, 95% CI: 1.39-2.97, P = 0.0404) in the anesthesiologists. Conclusion: Endotracheal intubation for elective treatments, intubation in an operating room or isolation ward, and routine rapid induction with continuous PPV for patients with confirmed SARS-CoV-2 are associated with a lower risk of SARS-CoV-2 transmission in practicing anesthesiologists, and coughing by patients during intubation increases the risk.
Keywords: SARS-CoV-2, anesthesiologists, intubation, predictive factors, risk
Introduction
In late 2019, a novel coronavirus was identified as the cause of an outbreak of an acute respiratory illness in Wuhan, China [1-4]. In February 2020, the World Health Organization (WHO) labeled this disease as coronavirus disease 2019 (COVID-19) and named as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) by the International Committee on Taxonomy of Viruses [5]. On March 11 WHO declared the pandemic [6]. In suspected SARS-CoV-2 cases, infection control measures should be implemented and public health officials notified [6,7]. The US Centers for Disease Control and Prevention (CDC) recommends standard, contact, and airborne precautions in health care settings [7]. The CDC suggests that all health care workers who enter the room of a patient with suspected or confirmed SARS-CoV-2 should wear personal protective equipment (PPE), including a gown, gloves, a respirator or medical mask, and eye or face protection, to reduce the risk of exposure [7].
Shortages in first-line health care staff may be the primary challenge of implementing surge-capacity medical plans during an epidemic [8]. Health care staff may be furloughed or isolated on accidental exposure to or contamination by SARS-CoV-2 [9-11]. SARS-CoV-2 poses a direct threat to an already overburdened medical care system and to the supporting supply chains for medications and materials [10]. Studies have analyzed the characteristics, clinical presentation, and outcomes of patients hospitalized with SARS-CoV-2 and the number of infected health care workers [12,13]. The most common comorbidities in patients with SARS-CoV-2 are hypertension, obesity, and diabetes [13]. Among patients with SARS-CoV-2 who were discharged or died (n = 2634), 14.2% were treated in the intensive care unit, 12.2% received invasive mechanical ventilation, 3.2% were treated with kidney replacement therapy, and 21% died. Only through planning, training, and teamwork will clinicians and health care systems be best placed to deal with the many complex implications of this pandemic [12].
Health care facilities should develop tiered, proactive strategies using the best available clinical information and build on their existing surge-capacity plans to optimize resource use in the event that the current outbreak spreads and creates severe resource demands [10]. Health care systems and providers must be prepared to obtain maximal benefits from limited resources while mitigating harm to individuals, the health care system, and society [10]. Therefore, understanding the factors affecting SARS-CoV-2 transmission in first-line health care workers, such as anesthesiologists performing endotracheal intubation for patients with SARS-CoV-2, is crucial to reducing the burden on or collapse of first-line health care workers and health care facilities because of exposure to SARS-CoV-2 during aerosol-generating procedures (ie, intubation and nebulization of medication) [14]. Therefore, the current study describes the results of the survey conducted by the Chinese Society of Anesthesiology Task Force on Airway Management (CSATF-AM) to clarify the predictive factors of the infection of first-line anesthesiologists performing endotracheal intubation in patients with SARS-CoV-2.
Patients and methods
Database
In February 2020, CSATF-AM administered questionnaires to anesthesiologists on endotracheal intubation in patients with SARS-CoV-2 each time they performed the intubation in patients with confirmed SARS-CoV-2. The questionnaires were designed to collect the basic information of every eligible patient-including age, sex, physical characteristics (eg, incisor distance and thyromental distance), medical tests (eg, chest computed tomography [CT] and nucleic acid test results), and medical services received-and that of the corresponding anesthesiologist-including contamination status as well as routine blood test, chest CT, and nucleic acid test results. To protect privacy, the personal information of patients and anesthesiologists was encrypted in the database and anonymous identification numbers were provided. The study protocols were approved by the Institutional Review Board, Clinical Committee of Henan Provincial People’s Hospital, Zhengzhou University (IRB No. 57, 2020).
Patients and anesthesiologists
All patients with suspected SARS-CoV-2 underwent three nucleic acid tests and chest CT. At least one positive nucleic acid test result along with chest CT abnormality was used to confirm the diagnosis of SARS-CoV-2. The survey was sent before the procedure and prepared for each patient contemporarily with the procedure. Therefore, this was a prospective survey study. CSATF-AM distributed the questionnaires in the associated anesthesiology departments in hospitals that had patients with SARS-CoV-2. Anesthesiologists received the questionnaires before performing endotracheal intubation and completed them after the procedure. All CSATF-AM-registered anesthesiologists have performed ≥ 500 intubations or worked for ≥ 5 years after specialization; thus, they were all similarly skilled in performing intubation. Of 118 suspected patients, 98 were confirmed to have SARS-CoV-2. Similarly, of the 98 corresponding anesthesiologists, 20 who had positive results in at least one nucleic acid test and demonstrated chest CT abnormality after they performed endotracheal intubation, were included in the infected anesthesiologist group, whereas the remaining 78 tested negative in all tests and had no chest CT abnormality and were included in the noninfected anesthesiologist group.
Questionnaire
Information on patients with confirmed SARS-CoV-2 was collected using 10 questions (Table 1A), and the medical information during intubation was collected using 11 questions (Table 1B).
Table 1A.
Questionnaire for anesthesiologists performing endotracheal intubation in patients with SARS-CoV-2: information related to the patient
| Q1: Patient sex and age |
| Q2: Does the patient have a fever? (Response: Yes or No) |
| Q3: Does the patient have a history of exposure to patients with SARS-CoV-2? (Response: (a) Direct contact with patients with SARS-CoV-2, (b) Direct contact with a person who was in a highly affected area, (c) Indirect contact with a person who was in a highly affected area, or (d) No history of contact) |
| Q4: Does the patient have a history of difficult airway intubation? (Response: Yes, No, or Not evaluated) |
| Q5: Patient incisor distance (Response: < 3 cm, ≥ 3 cm, and Not evaluated) |
| Q6: Patient thyromental distance (Response: < 6 cm, ≥ 6 cm, and Not evaluated) |
| Q7: Patient head and neck mobility (Response: Normal, Limited, and Not evaluated) |
| Q8: Patient neck thickness (Response: Normal, Stubby, and Not evaluated) |
| Q9: Patient Mallampati score (Response: I, II, III, IV, and Not evaluated) |
| Q10: Summary of negative results on any of the three nucleic acid tests |
Table 1B.
Questionnaire for anesthesiologists performing endotracheal intubation patients with SARS-CoV-2: information related to the procedure
| M1: Reason for performing endotracheal intubation (Response: (a) General anesthesia, (b) Elective treatment, or (c) Emergency) |
| M2: Location of performing endotracheal intubation (Response: (a) Operating room, (b) Isolation ward, (c) Emergency department, (d) Intensive care unit, or (e) Respiratory care ward) |
| M3: Protective measures taken (Response: (a) Tertiary protection, (b) Secondary protection, or (c) Primary protection) |
| M4: Preparation before performing endotracheal intubation (choose one or more answers). (Response: (a) Difficult airway cart, (b) Difficult airway box, (c) Simple respirator, (d) Respirator or anesthesia machine, and/or (e) Filter or artificial nose) |
| M5: Endotracheal intubation method (Response: (a) Routine rapid induction with continuous positive-pressure ventilation, (b) Rapid sequence induction, (c) Retention of spontaneous breathing, or (d) Other) |
| M6: Was positive-pressure mask ventilation employed before intubation? (Response: Yes or No) |
| M7: Was disposable intubation equipment used? (Response: Yes or No) |
| M8: Intubation equipment used (Response: (a) Video laryngoscopy intubation, (b) Ordinary laryngoscopy intubation, (c) Video tube intubation, (d) Visual intubation soft scope, or (e) Other) |
| M9: Number of operators (Response: (a) One anesthetist, (b) Two anesthesiologists, (c) One anesthetist and one doctor, or (d) Other) |
| M10: Did the patient cough during intubation? (Response: Yes or No) |
| M11: Number of attempts at intubation (Response: (a) Success the first time, (b) Success the second time, (c) Success the third time, or (d) failure) |
Statistical analysis
All analyses were performed using R® for Windows. Statistical significance was set at P < 0.05. Fisher’s exact test of independence (for a total sample size of < 1000) was performed to compare patients’ basic characteristics and endotracheal intubation information between the noninfected and infected anesthesiologist groups. A multivariate logistic model with stepwise selection was used to select all variables with significant effects on SARS-CoV-2 in anesthesiologists. Univariate and multivariate logistic regression analyses were performed to calculate the odds ratio (OR) and corresponding 95% confidence interval (CI) for SARS-CoV-2 risk in the anesthesiologists.
Results
SARS-CoV-2 prevalence in the anesthesiologists who performed intubation in patients with confirmed SARS-CoV-2 was 20.41% (Table 2). Moreover, the distribution of patient and anesthesiologist baseline characteristics and Q1-Q10 responses did not significantly differ between the noninfected and infected anesthesiologist groups (Table 2). Table 3 presents the differences in procedures used during endotracheal intubation between noninfected and infected anesthesiologist groups. Reason for performing endotracheal intubation, M1 (P = 0.0276), location of performing endotracheal intubation, M2 (P = 0.0193), endotracheal intubation method, M5 (P = 0.0092), and the patient cough during intubation, M10 (P = 0.0161) were significantly associated with infection in the participating anesthesiologists. Table 4 presents the estimated coefficients of multivariate logistic regression for all variables in Table 2 (M1-M11). Because of the collinearity between these variables, only a few variables were significant in this model (Supplementary Tables 1 and 2). Therefore, we used a stepwise selection method for variable selection and found intubation for elective treatment and coughing by the patient during intubation to be significant variables (Table 4).
Table 2.
Baseline characteristics of patients with SARS-CoV-2 receiving endotracheal intubation described by the anesthesiologists performing intubation
| Characteristics | Noninfected anesthesiologists N = 78 (%) | Infected anesthesiologists N = 20 (%) | P Value |
|---|---|---|---|
| Age, mean (SD) | 59.26 (15.14) | 61.46 (8.81) | 0.4000 |
| Sex | 0.5545 | ||
| Male | 61 (78.21) | 14 (70) | |
| Female | 17 (21.79) | 6 (30) | |
| Patients with fever | 0.7673 | ||
| Yes | 68 (87.18) | 17 (85) | |
| No | 9 (11.54) | 3 (15) | |
| Unclear | 1 (1.28) | 0 (0) | |
| Patient exposure to SARS-CoV-2 | 0.5882 | ||
| Direct with SARS-CoV-2 | 36 (46.15) | 8 (40) | |
| Direct with affected areas | 31 (39.74) | 7 (35) | |
| Indirect with affected areas | 8 (10.26) | 4 (20) | |
| No | 3 (3.85) | 1 (5) | |
| Patients with a history of difficult airway for intubation | 0.4902 | ||
| Yes | 7 (8.97) | 0 (0) | |
| No | 58 (74.36) | 17 (85) | |
| Not evaluated | 13 (16.67) | 3 (15) | |
| Incisors distance in patients | 0.3015 | ||
| < 3 cm | 5 (6.41) | 3 (15) | |
| ≥ 3 cm | 64 (82.05) | 14 (70) | |
| Not evaluated | 9 (11.54) | 3 (15) | |
| Thyromental distance in patients | 0.4052 | ||
| < 6 cm | 21 (26.92) | 3 (15) | |
| > 6 cm | 44 (56.41) | 15 (75) | |
| Not evaluated | 13 (16.67) | 2 (10) | |
| Head and neck mobility in patients | 0.5252 | ||
| Normal | 63 (80.77) | 15 (75) | |
| Limited | 6 (7.69) | 3 (15) | |
| Not evaluated | 9 (11.54) | 2 (10) | |
| Thickness of neck in patients | 1.000 | ||
| Normal | 55 (70.51) | 14 (70) | |
| Stubby | 22 (28.21) | 6 (30) | |
| Not evaluated | 1 (1.28) | 0 (0) | |
| Mallampati Scoring in patients | 0.8321 | ||
| I | 9 (11.54) | 2 (10) | |
| II | 32 (41.03) | 11 (55) | |
| III | 4 (5.13) | 1 (5) | |
| IV | 1 (1.28) | 0 (0) | |
| Not evaluated | 32 (41.03) | 6 (30) | |
| False negative of SARS-CoV-2 test in patients | 0.5169 | ||
| Yes | 13 (16.67) | 5 (25) | |
| No | 65 (83.33) | 15 (75) |
SARS-CoV-2, Severe Acute Respiratory Syndrome Coronavirus 2; SD, standard deviation.
Table 3.
Procedures performed by anesthesiologist during endotracheal intubation in patients with confirmed SARS-CoV-2
| Procedures | Noninfected anesthesiologists N = 78 (%) | Infected anesthesiologists N = 20 (%) | P Value |
|---|---|---|---|
| Reasons for performing endotracheal intubation | 0.0276 | ||
| Intubation for general anesthesia | 12 (15.38) | 4 (20) | |
| Intubation for elective treatment | 39 (50) | 6 (30) | |
| Intubation for emergency | 27 (34.62) | 10 (50) | |
| Intubation location | 0.0193 | ||
| Operating room | 10 (12.82) | 1 (5) | |
| Isolation ward | 39 (50) | 7 (35) | |
| Emergency department | 0 (0) | 2 (10) | |
| ICU | 29 (37.18) | 9 (45) | |
| Respiratory care ward | 0 (0) | 1 (5) | |
| Protective measures | 1.0000 | ||
| Tertiary protection | 61 (78.21) | 16 (80) | |
| Secondary protection | 14 (17.95) | 4 (20) | |
| Primary protection | 3 (3.85) | 0 (0) | |
| Prepare before performing endotracheal intubation | |||
| Difficult airway cart | 0.4997 | ||
| Yes | 11 (14.1) | 4 (20) | |
| No | 67 (85.9) | 16 (80) | |
| Difficult airway box | 0.4227 | ||
| Yes | 55 (70.51) | 12 (60) | |
| No | 23 (29.49) | 8 (40) | |
| Simple respirator | 0.3166 | ||
| Yes | 49 (62.82) | 10 (50) | |
| No | 29 (37.18) | 10 (50) | |
| Respirator or anesthesia machine | 0.3295 | ||
| Yes | 66 (84.62) | 15 (75) | |
| No | 12 (15.38) | 5 (25) | |
| Filter or artificial nose | 0.8066 | ||
| Yes | 38 (48.72) | 9 (45) | |
| No | 40 (51.28) | 11 (55) | |
| Endotracheal intubation methods | 0.0092 | ||
| Routine rapid induction with continuous PPV | 56 (71.79) | 11 (55) | |
| Rapid sequence induction without PPV | 21 (26.92) | 5 (25) | |
| Retain spontaneous breathing | 0 (0) | 3 (15) | |
| Other | 1 (1.28) | 1 (5) | |
| Positive-pressure ventilation | 0.7842 | ||
| Yes | 57 (73.08) | 14 (70) | |
| No | 21 (26.92) | 6 (30) | |
| Disposable intubation tools | 1 | ||
| Yes | 68 (87.18) | 18 (90) | |
| No | 10 (12.82) | 2 (10) | |
| Tools used in intubation | 0.2254 | ||
| Video laryngoscopy intubation | 75 (96.15) | 18 (90) | |
| Ordinary laryngoscopy intubation | 3 (3.85) | 1 (5) | |
| Video tube intubation | 0 (0) | 0 (0) | |
| Visual intubation soft scope | 0 (0) | 0 (0) | |
| Other | 0 (0) | 1 (5) | |
| Numbers of operators | 0.4416 | ||
| One anesthesiologist | 17 (21.79) | 4 (20) | |
| Multiple anesthesiologists (≥ 2) | 23 (29.49) | 9 (45) | |
| One anesthesiologist and other doctors (≥ 2) | 37 (47.44) | 7 (35) | |
| Other | 1 (1.28) | 0 (0) | |
| Patients with cough during intubation | 0.0160 | ||
| Yes | 11 (11.22) | 7 (35) | |
| No | 67 (88.78) | 14 (65) | |
| How many intubation attempts | 0.3682 | ||
| Success the first time | 77 (98.72) | 19 (95) | |
| Success the second time | 1 (1.28) | 1 (5) | |
| Success the third time | 0 (0) | 0 (0) | |
| Failure | 0 (0) | 0 (0) |
PPV, positive-pressure ventilation; ICU, intensive care unit.
Table 4.
Multivariate logistic model with stepwise selection for SARS-CoV-2 risk in the anesthesiologists performing endotracheal intubation in patients with confirmed SARS-CoV-2
| Coefficient | SE | Z | P | |
|---|---|---|---|---|
| Endotracheal intubation for elective treatment | -1.41 | 0.68 | -2.06 | 0.0390 |
| Coughing by patients during intubation | 3.39 | 1.29 | 2.62 | 0.0088 |
SE, standard error; Z, Z-test.
The results of univariate and multivariate logistic regression for assessing SARS-CoV-2 risk in anesthesiologists are presented in Table 5. Univariate logistic regression demonstrated that endotracheal intubation for elective treatment, in the operating room, in isolation wards, and by using routine rapid induction with continuous positive-pressure ventilation (PPV) were associated with a relatively low SARS-CoV-2 risk (crude ORs = 0.13 [P < 0.0001], 0.10 [P = 0.0281], 0.19 [P = 0.0001], and 0.20 [P < 0.0001], respectively). By contrast, presence of multiple anesthesiologists and coughing by the patient during intubation were associated with a relatively high SARS-CoV-2 risk (crude ORs = 1.39 [P = 0.0170] and 3.00 [P = 0.0227], respectively). After multivariate analysis, only endotracheal intubation for elective treatment remained associated with a relatively low SARS-CoV-2 risk (adjusted OR = 0.28, 95% CI: 0.14-0.68) and only coughing by the patient during intubation associated with a relatively high SARS-CoV-2 risk (adjusted OR = 1.70, 95% CI = 1.39-2.97).
Table 5.
Univariate and multivariate logistic regression for SARS-CoV-2 risk in anesthesiologists performing endotracheal intubation in patients with confirmed SARS-CoV-2
| Value | 95% CI | P | ||
|---|---|---|---|---|
| Intubation for elective treatment | Crude OR | 0.13 | 0.05-0.30 | < 0.0001 |
| Adjusted OR* | 0.28 | 0.14-0.68 | 0.0194 | |
| Endotracheal intubation in operating room | Crude OR | 0.10 | 0.01-0.52 | 0.0281 |
| Adjusted OR* | 0.12 | 0.01-0.95 | 0.0787 | |
| Endotracheal intubation in isolation ward | Crude OR | 0.19 | 0.08-0.40 | 0.0001 |
| Adjusted OR* | 0.58 | 0.15-2.09 | 0.4048 | |
| Routine rapid induction for intubation | Crude OR | 0.20 | 0.10-0.37 | < 0.0001 |
| Adjusted OR* | 0.36 | 0.08-1.51 | 0.1577 | |
| Number of operators: Multiple anesthesiologists | Crude OR | 1.39 | 1.07-1.82 | 0.0170 |
| Adjusted OR* | 3.04 | 0.74-4.12 | 0.2297 | |
| Patients with cough during intubation | Crude OR | 3.00 | 1.79-4.90 | 0.0227 |
| Adjusted OR* | 1.70 | 1.39-2.97 | 0.0404 |
All the aforementioned variables were used in the multivariate analysis.
OR, odds ratio; CI, confidence interval.
Discussion
Limiting transmission is an essential component of care in patients with suspected or confirmed SARS-CoV-2. In a report on 138 patients with SARS-CoV-2 in China, 43% were estimated to have acquired the infection in a hospital setting [15]. Airborne precautions are necessary during aerosol-generating procedures, such as tracheal intubation [6]. Because airborne infections are possible, the use of isolation room (ie, a single-patient negative-pressure room) is recommended. Patients should at least be asked to wear masks and be placed in a private room with the door closed, and any personnel entering this room should wear the appropriate PPE [6,7]. Patients with suspected or confirmed SARS-CoV-2 who require hospitalization should be cared for in a facility that can provide an isolation room. However, no study has investigated risk factors for SARS-CoV-2 infection and its transmission rate in anesthesiologists performing endotracheal intubation in patients with SARS-CoV-2 or indicated the intubation equipment and location, protective measures, and procedures that can provide sufficient safety to them. Whether patients with SARS-CoV-2 with fever have a higher transmission rate to anesthesiologists performing intubation in them remains unclear. All SARS-CoV-2 guidelines have been designed on the basis of experiences with other airborne transmission diseases, such as tuberculosis, varicella, measles, smallpox, Middle East respiratory syndrome, SARS, and Ebola. Therefore, the current survey estimated the SARS-CoV-2 transmission risk factors associated with various endotracheal intubation equipment, protective measures, and methods to identify the optimal protective measures when performing intubation in patients with SARS-CoV-2.
Full-genome sequencing and phylogenic analysis indicated that SARS-CoV-2 is a betacoronavirus in the same subgenus as SARS-CoV but in a different clade. Nevertheless, the structure of its receptor-binding gene region is very similar to that of SARS-CoV; thus, SARS-CoV-2 uses the same receptor as SARS-CoV, that is, the angiotensin-converting enzyme 2 (ACE2), for cell entry [16]. For health care workers with potential exposure to SARS-CoV-2, the US CDC and WHO have provided guidelines for work restriction and monitoring [6,7]. These guidelines are based on experiences of health care workers with SARS, given that SARS demonstrated airborne transmission [17] and transmission to health care workers was a common feature of most SARS outbreaks [18,19]. The approach depends on exposure duration, patient symptoms, and facemask use (for anesthesiologists), PPE type used by the health care workers, and the aerosol-generating procedure used [6,7]. However, SARS and SARS-CoV-2 have differences in transmissibility, infectious period, infectious situation, community spread, and clinical spectrum [20]. Therefore, the prevention policies for SARS-CoV-2 cannot be identical to those used for SARS, particularly in health care workers; the SARS-CoV-2 pandemic has required the use of more health facilities than SARS. Moreover, transmissibility appears to be higher for SARS-CoV-2 than for SARS [20], and health care workers must be protected so that they can care for more patients with SARS-CoV-2 [20].
In our study, SARS-CoV-2 transmissibility in the anesthesiologists was 20.41% after performing intubation in patients with confirmed SARS-CoV-2. However, this rate was only 4.16%-13.04% for SARS [21,22]. Therefore, understanding the significant predictive factors of high SARS-CoV-2 transmissibility in first-line health care workers, such as anesthesiologists who perform intubation in patients with SARS-CoV-2, is vital for public health and policy development.
Table 1 demonstrates that no significant factors were associated with patients with confirmed SARS-CoV-2 and the infected anesthesiologists performing intubation in them. No association was noted between patient symptoms and signs, such as fever and other clinical characteristics, and SARS-CoV-2 transmissibility in the anesthesiologists. Confirmed SARS-CoV-2 with fever, false-negative nuclear acid test results, history of exposure to other patients with SARS-CoV-2, difficult airway for intubation, narrow incisor distance, narrow thyromental distance, limited head and neck mobility, and stubby neck were not associated with the transmissibility of SARS-CoV-2 infection in the anesthesiologists. Patients with SARS-CoV-2 typically first experience a viral-type illness with symptoms ranging from a mild upper respiratory tract infection (eg, pharyngitis and rhinorrhea) to a lower respiratory tract infection (eg, cough and fever), influenza-like symptoms (eg, fever, chills, headache, and myalgias), or gastroenteritis (eg, nausea, vomiting, and diarrhea) [7,23]. Nevertheless, older adults with infection may lack fever or localized infection-specific symptoms or signs [24]. For example, rather than high fever, productive cough, and pleuritic chest pain, pneumonia in older adults may present as a low-grade fever (37.22°C) and increased oxygen requirement like dyspnea [24]. Pneumonia in some patients may also be associated with nonspecific symptoms such as increased confusion, falls, and anorexia. These nonspecific symptoms are common in older adults and do not have high positive predictive value for infection [24]. Therefore, the endpoint of our study (transmission risk of intubation for patients with SARS-CoV-2) was different from that of Wang Y et al., who demonstrated that symptomatic febrile patients are exposed to higher viral loads. Moreover, higher viral load was not proportional to high risk of transmission during intubation [25].
The incidence of SARS-CoV-2 was lower with elective intubation than with intubation for emergency procedures probably because during the emergency situations, the anesthesiologists might not have been able to adequately follow the standard protective measures [26,27]. Furthermore, oxygen saturation is relatively low in patients with SARS-CoV-2 with unplanned intubation; these patients may present with conditions such as pressure-assisted ventilation-induced cough reflex during intubation, leading to droplet diffusion and aerosol formation and thus increasing airborne SARS-CoV-2 transmission [26-28]. Performing intubation in an isolation ward or operating room is safer and reduces SARS-CoV-2 prevalence compared with that in an emergency room, intensive care unit, and respiratory care ward [26], because isolation wards or operating rooms in China are equipped with anesthesiologists and medical personnel with training in standard protection and sufficient preparation for protection against airborne transmission [26]. Anesthesiologists have a better understanding of patient condition when intubating in an isolation ward or operating room; moreover, in these areas, elective rather than emergency intubation is performed, and before intubation, adequate anesthesia is administered [26]. In these areas, enhanced PPE for droplet or airborne infection and a sufficient amount of muscle relaxant are used before intubation, particularly in patients with SARS-CoV-2. All these measures are generally effective in preventing patients from coughing, droplet spread, and other infectious events [26]. Moreover, for sputum removal, a closed sputum suction device is used, which is difficult to use during emergency intubation [26]. In the current study, on univariate logistic regression, routine rapid induction with continuous PPV for intubation in patients with SARS-CoV-2 was found to reduce SARS-CoV-2 transmission to anesthesiologists (Table 4). Routine rapid induction with continuous PPV for anesthesia-induced tracheal intubation is routinely used for patients with SARS-CoV-2 [26]. After patients are anesthetized, they are given muscle relaxants and maintained under continuous PPV, which reduces hypoxia and the resultant coughing, thereby allowing anesthesiologists to perform intubation safely. Our results (Table 5) indicated that reduction in coughing by patients during intubation was essential. Another risk factor for SARS-CoV-2 transmission on univariate analysis was the presence of two or more anesthesiologists during intubation (Table 4), probably because the presence of more than one anesthesiologist indicates difficult or emergency intubation. However, because this factor corresponded with emergency and difficult intubation and other clinical factors, it became nonsignificant on multivariate analysis (Table 4). Multivariate analysis revealed that only two factors were associated with risk of SARS-CoV-2 infection in anesthesiologists performing intubation: elective intubation as a protective factor and patient coughing during intubation as a high-risk factor.
Endotracheal intubation in patients with SARS-CoV-2 entails a risk to both the physiologically compromised patient and the attending health care providers [29]. On the basis of a two-center retrospective observational case series from Wuhan, China, a panel of international airway management experts formulated recommendations for the management of tracheal intubation in patients with SARS-CoV-2 [29]. PPE was recommended to be worn by all intubating health care workers. Rapid sequence induction (RSI) or modified RSI was used with an intubation success rate of 89.1% on the first attempt and 100% overall. However, these clinical recommendations were not based on a multivariate logistic model with stepwise selection considering all the variables with significant effects on the SARS-CoV-2 in anesthesiologists. Sorbello et al. also presented recommendations based on clinical experiences of managing patients throughout Italy and described key elements of clinical management, including safe oxygen therapy; airway management; PPE; and nontechnical aspects of caring for patients diagnosed with SARS-CoV-2 [12]. Only through planning, training, and team work will clinicians and health care systems be best placed to deal with the many complex implications of this new pandemic [12]. These recommendations and key elements from the United Kingdom consensus [30] and the study by Sorbello et al. were similar to our finding that elective intubation was associated with a relatively low SARS-CoV-2 transmission risk (Table 5). Other single-center Italian study supported Sorbello et al.’s findings [31]. Most recommendations support the need to minimize the team size and administer full-dose RSI [12,29-31]. Our results based on a multivariate logistic model with stepwise selection were consistent with these recommendations. However, 19 patients experienced coughing during intubation in our study, possibly indicating inadequate dose of neuromuscular blocking agents. The full dose RSI is strongly recommended. The China consensus should be improved as soon as possible and decrease the human error and highlight the importance of checklists.
We noted that anesthesiologists performing intubation in patients with SARS-CoV-2 had a significantly increased SARS-CoV-2 risk when patients coughed during intubation (Table 5). On the basis of the SARS-related experiences, the health care procedures with high potential of generating droplets and aerosols thereby increasing SARS risk were manipulation of the airway (ie, performing endotracheal intubation or suctioning) and administration of aerosolized medications [32,33]. Therefore, CSATF-AM recommended administration of muscle relaxants to patients with SARS-CoV-2 before intubation [26]. In airways that are difficult to intubate, muscle relaxant use minimizes choking or coughing [34,35]. Performing intubation without muscle relaxants typically causes patients to cough [26]. Moreover, anesthesiologists should begin the intubation only after the onset of the effect of the muscle relaxant to minimize coughing by patients [26]. Muscle relaxants such as succinylcholine and rocuronium bromide that have a rapid onset of action are recommended by CSATF-AM for patients with SARS-CoV-2 [26]. CSATF-AM strongly recommends using positive-pressure headgear when intubating patients with SARS-CoV-2 to prevent the airborne transmission through patients coughing during intubation [26]. Our finding that coughing by patients with SARS-CoV-2 during intubation is a risk factor for SARS-CoV-2 infection in the anesthesiologists validates the recommendations of CSATF-AM [26].
This is the first study demonstrating the factors predicting the risk of SARS-CoV-2 transmission to anesthesiologists performing intubation in patients with SARS-CoV-2. Moreover, all CSATF-AM-registered anesthesiologists have performed ≥ 500 intubations or worked for ≥ 5 years after specialization; thus, they were all similarly skilled in performing intubation. However, the SARS-CoV-2 prevalence was found to be high (20.41%)-higher than that reported for patients with SARS [21,22]. Our results could provide valuable information regarding SARS-CoV-2 transmission during intubation. Moreover, the high SARS-CoV-2 transmissibility during intubation in patients with SARS-CoV-2 demonstrates the importance of implementing protective procedures during intubation for SARS-CoV-2 cases. Performing elective rather than emergency intubation, intubation in isolation ward or operating room, and routine rapid induction for intubation with continuous PPV are strongly recommended. Moreover, using an adequate dose of muscle relaxants and performing intubation after drug effect onset could minimize or prevent patient coughing during intubation. We hope that these measures will reduce SARS-CoV-2 risk in anesthesiologists and thus prevent increasing the burden on the health care systems. These findings may serve a valuable reference to anesthesiologists performing intubation in patients with any airborne transmission diseases in the future.
The limitations of our study are as follows: First, the major limitations of using questionnaires could not be avoided. Nevertheless, only CSATF-AM-registered experienced anesthesiologists answered the questionnaires. Moreover, the interval between SARS-CoV-2 outbreak and the survey was very close (< 1 month). Thus, the recall bias, understanding, interpretation bias, or unconscientious responses in the questionnaires might be low. Second, SARS-CoV-2 severity in the anesthesiologists after performing intubation in patients with SARS-CoV-2 was unclear. In several cases, anesthesiologists with severe SARS-CoV-2 symptoms could not respond to the questionnaires. Therefore, underestimation of the prevalence and loss of some crucial events may have occurred. Third, SARS-CoV-2 prevalence in the participating anesthesiologists after the intubation of patients with confirmed SARS-CoV-2 was 20.41%. These findings might be because inadequate protective measures or endotracheal intubation methods in anesthesiologists meeting the initial outbreak of SARS-CoV-2 in February 2020 (Table 3). Moreover, the anesthesiologists might have a history of exposure to other SARS-CoV-2 cases outside the health care systems, which could not be evaluated in this survey, indicating a potential for overestimation of SARS-CoV-2 prevalence. Fourth, the sample size was too small to analyze all variables in the regression model. Fifth, a mixed formula (records for patients and survey for anesthesiologists) would have been more precise and less at risk of bias. However, the some of the patients with SARS-CoV-2 receiving intubation might be too severely ill to answer the questionnaires. Moreover, patients who could answer the questionnaires might be associated with recovery from SARS-CoV-2 or other severe underlying diseases, leading to a risk of selection bias from relatively healthy SARS-CoV-2 patients. Thus, we did not access the patients’ records. Sixth, PPE was not standardized for all anesthesiologists in February in China. No official records exist on which standard PPE should be worn by anesthesiologists performing endotracheal intubation for patients with SARS-CoV-2. Therefore, we wished to determine the predictors of the risk SARS-CoV-2 transmission for anesthesiologists performing endotracheal intubation in patients with SARS-CoV-2. Sometimes, for emergency intubation, protective measures taken need to be categorized into tertiary, secondary, or primary protection (Table 1). Tertiary protection might be difficult for anesthesiologists performing unplanned intubations. Therefore, three levels of PPE were considered for the multivariate logistic model with stepwise selection by selecting all the variables with significant effects on the SARS-CoV-2 in anesthesiologists.
Conclusions
SARS-CoV-2 transmissibility in anesthesiologists during intubation in patients with confirmed SARS-CoV-2 was 20.41%. Performing intubation for elective treatment rather than emergency treatment and preventing coughing by patients during intubation are the most crucial factors to reduce SARS-CoV-2 transmission.
Acknowledgements
Szu-Yuan Wu’s received funding from Lo-Hsu Medical Foundation, Lotung Poh-Ai Hospital (Funding Number: 10908, 10909, 11001, 11002, 11003, 11006, and 11013). Lei Qin’s work is supported by University of International Business and Economics Huiyuan outstanding young scholars research funding (17YQ15), “the Fundamental Research Funds for the central Universities” in UIBE (CXTD10-10). Lo-Hsu Medical Foundation, Lotung Poh-Ai Hospital, supports Szu-Yuan Wu’s work (Funding Number: 10908 and 10909). Lei Qin’s work is supported by University of International Business and Economics Huiyuan outstanding young scholars research funding (17YQ15), “the Fundamental Research Funds for the central Universities” in UIBE (CXTD10-10).
Disclosure of conflict of interest
None.
Abbreviations
- SARS-CoV-2
severe acute respiratory syndrome coronavirus 2
- PPV
positive-pressure ventilation
- OR
odds ratio
- CI
confidence intervals
- WHO
World Health Organization
- CDC
Centers for Disease Control and Prevention
- CSATF-AM
Chinese Society of Anesthesiology Task Force on Airway Management
- CT
computed tomography
- MERS
Middle East Respiratory Syndrome
- SARS
Severe Acute Respiratory Syndrome
- ACE2
angiotensin-converting enzyme 2
- AIC
Akaike’s Information Criteria
- ICU
intensive care unit
- PPE
personal protective equipment
Supporting Information
References
- 1.Van Cuong L, Giang HTN, Linh LK, Shah J, Van Sy L, Hung TH, Reda A, Truong LN, Tien DX, Huy NT. The first Vietnamese case of COVID-19 acquired from China. Lancet Infect Dis. 2020;20:408–409. doi: 10.1016/S1473-3099(20)30111-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Chen X, Tian J, Li G, Li G. Initiation of a new infection control system for the COVID-19 outbreak. Lancet Infect Dis. 2020;20:397–398. doi: 10.1016/S1473-3099(20)30110-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Xiang YT, Li W, Zhang Q, Jin Y, Rao WW, Zeng LN, Lok GKI, Chow IHI, Cheung T, Hall BJ. Timely research papers about COVID-19 in China. Lancet. 2020;395:684–685. doi: 10.1016/S0140-6736(20)30375-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Heymann DL, Shindo N WHO Scientific and Technical Advisory Group for Infectious Hazards. COVID-19: what is next for public health? Lancet. 2020;395:542–545. doi: 10.1016/S0140-6736(20)30374-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Coronaviridae Study Group of the International Committee on Taxonomy of Viruses. The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. Nat Microbiol. 2020;5:536–544. doi: 10.1038/s41564-020-0695-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.World Health Organization. Infection prevention and control during health care when novel coronavirus (nCoV) infection is suspected 2020 [January 25, 2020] Available from: https://www.who.int/publications-detail/infection-prevention-and-control-during-health-care-when-novel-coronavirus-(ncov)-infection-is-suspected-20200125.
- 7.Centers for Disease Control and Prevention. Interim U.S. Guidance for Risk Assessment and Public Health Management of Healthcare Personnel with Potential Exposure in a Healthcare Setting to Patients with Coronavirus Disease (COVID-19) 2020. [Available from: https://www.cdc.gov/coronavirus/2019-ncov/hcp/guidance-risk-assesment-hcp.html]
- 8.Crisis standards of care: a systems framework for catastrophic disaster response. Mil Med. 2016;181:719–721. doi: 10.7205/MILMED-D-16-00226. [DOI] [PubMed] [Google Scholar]
- 9.Yasin J, Fisseha R, Mekonnen F, Yirdaw K. Occupational exposure to blood and body fluids and associated factors among health care workers at the University of Gondar Hospital, Northwest Ethiopia. Environ Health Prev Med. 2019;24:18. doi: 10.1186/s12199-019-0769-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Hick JL, Hanfling D, Wynia MK, Pavia AT. Duty to plan: health care, crisis standards of care, and novel coronavirus SARS-CoV-2. National Academy of Medicine. Washington, DC.: National Academy of Medicine. Washington, DC.; 2020. [Available from: https://doi.org/10.31478/202003b.] [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Mossburg S, Agore A, Nkimbeng M, Commodore-Mensah Y. Occupational hazards among healthcare workers in africa: a systematic review. Ann Glob Health. 2019;85:1–13. doi: 10.5334/aogh.2434. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Sorbello M, El-Boghdadly K, Di Giacinto I, Cataldo R, Esposito C, Falcetta S, Merli G, Cortese G, Corso RM, Bressan F, Pintaudi S, Greif R, Donati A, Petrini F Società Italiana di Anestesia Analgesia Rianimazione e Terapia Intensiva (SIAARTI) Airway Research Group, and The European Airway Management Society. The Italian coronavirus disease 2019 outbreak: recommendations from clinical practice. Anaesthesia. 2020;75:724–732. doi: 10.1111/anae.15049. [DOI] [PubMed] [Google Scholar]
- 13.Richardson S, Hirsch JS, Narasimhan M, Crawford JM, McGinn T, Davidson KW the Northwell COVID-19 Research Consortium. Barnaby DP, Becker LB, Chelico JD, Cohen SL, Cookingham J, Coppa K, Diefenbach MA, Dominello AJ, Duer-Hefele J, Falzon L, Gitlin J, Hajizadeh N, Harvin TG, Hirschwerk DA, Kim EJ, Kozel ZM, Marrast LM, Mogavero JN, Osorio GA, Qiu M, Zanos TP. Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the New York city area. JAMA. 2020;323:2052–2059. doi: 10.1001/jama.2020.6775. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.McDonald LC, Simor AE, Su IJ, Maloney S, Ofner M, Chen KT, Lando JF, McGeer A, Lee ML, Jernigan DB. SARS in healthcare facilities, Toronto and Taiwan. Emerg Infect Dis. 2004;10:777–781. doi: 10.3201/eid1005.030791. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, Wang B, Xiang H, Cheng Z, Xiong Y, Zhao Y, Li Y, Wang X, Peng Z. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA. 2020;323:1061–1069. doi: 10.1001/jama.2020.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Zhou P, Yang XL, Wang XG, Hu B, Zhang L, Zhang W, Si HR, Zhu Y, Li B, Huang CL, Chen HD, Chen J, Luo Y, Guo H, Jiang RD, Liu MQ, Chen Y, Shen XR, Wang X, Zheng XS, Zhao K, Chen QJ, Deng F, Liu LL, Yan B, Zhan FX, Wang YY, Xiao GF, Shi ZL. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020;579:270–273. doi: 10.1038/s41586-020-2012-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Olsen SJ, Chang HL, Cheung TY, Tang AF, Fisk TL, Ooi SP, Kuo HW, Jiang DD, Chen KT, Lando J, Hsu KH, Chen TJ, Dowell SF. Transmission of the severe acute respiratory syndrome on aircraft. N Engl J Med. 2003;349:2416–2422. doi: 10.1056/NEJMoa031349. [DOI] [PubMed] [Google Scholar]
- 18.Cheng PK, Wong DA, Tong LK, Ip SM, Lo AC, Lau CS, Yeung EY, Lim WW. Viral shedding patterns of coronavirus in patients with probable severe acute respiratory syndrome. Lancet. 2004;363:1699–1700. doi: 10.1016/S0140-6736(04)16255-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Peiris JS, Chu CM, Cheng VC, Chan KS, Hung IF, Poon LL, Law KI, Tang BS, Hon TY, Chan CS, Chan KH, Ng JS, Zheng BJ, Ng WL, Lai RW, Guan Y, Yuen KY HKU/UCH SARS Study Group. Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet. 2003;361:1767–1772. doi: 10.1016/S0140-6736(03)13412-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Wilder-Smith A, Chiew CJ, Lee VJ. Can we contain the COVID-19 outbreak with the same measures as for SARS? Lancet Infect Dis. 2020;20:e102–e107. doi: 10.1016/S1473-3099(20)30129-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Raboud J, Shigayeva A, McGeer A, Bontovics E, Chapman M, Gravel D, Henry B, Lapinsky S, Loeb M, McDonald LC, Ofner M, Paton S, Reynolds D, Scales D, Shen S, Simor A, Stewart T, Vearncombe M, Zoutman D, Green K. Risk factors for SARS transmission from patients requiring intubation: a multicentre investigation in Toronto, Canada. PLoS One. 2010;5:e10717. doi: 10.1371/journal.pone.0010717. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Caputo KM, Byrick R, Chapman MG, Orser BJ, Orser BA. Intubation of SARS patients: infection and perspectives of healthcare workers. Can J Anaesth. 2006;53:122–129. doi: 10.1007/BF03021815. [DOI] [PubMed] [Google Scholar]
- 23.Cohen PA, Hall LE, John JN, Rapoport AB. The early natural history of SARS-CoV-2 Infection: clinical observations from an urban, ambulatory COVID-19 clinic. Mayo Clin Proc. 2020;95:1124–1126. doi: 10.1016/j.mayocp.2020.04.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Caterino JM, Kline DM, Leininger R, Southerland LT, Carpenter CR, Baugh CW, Pallin DJ, Hunold KM, Stevenson KB. Nonspecific symptoms lack diagnostic accuracy for infection in older patients in the emergency department. J Am Geriatr Soc. 2019;67:484–492. doi: 10.1111/jgs.15679. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Wang Y, Wang Y, Chen Y, Qin Q. Unique epidemiological and clinical features of the emerging 2019 novel coronavirus pneumonia (COVID-19) implicate special control measures. J Med Virol. 2020;92:568–576. doi: 10.1002/jmv.25748. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Zuo MZ, Huang YG, Ma WH, Xue ZG, Zhang JQ, Gong YH, Che L Chinese Society of Anesthesiology Task Force on Airway Management, Airway Management Chinese Society of Anesthesiology Task Force on. Expert recommendations for tracheal intubation in critically ill patients with noval coronavirus disease 2019. Chin Med Sci J. 2020;2:105–109. doi: 10.24920/003724. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Cheung JC, Ho LT, Cheng JV, Cham EYK, Lam KN. Staff safety during emergency airway management for COVID-19 in Hong Kong. Lancet Respir Med. 2020;4:19. doi: 10.1016/S2213-2600(20)30084-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Aliabadi AA, Rogak SN, Bartlett KH, Green SI. Preventing airborne disease transmission: review of methods for ventilation design in health care facilities. Adv Prev Med. 2011;2011:124064. doi: 10.4061/2011/124064. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Yao W, Wang T, Jiang B, Gao F, Wang L, Zheng H, Xiao W, Yao S, Mei W, Chen X, Luo A, Sun L, Cook T, Behringer E, Huitink JM, Wong DT, Lane-Fall M, McNarry AF, McGuire B, Higgs A, Shah A, Patel A, Zuo M, Ma W, Xue Z, Zhang LM, Li W, Wang Y, Hagberg C, O’Sullivan EP, Fleisher LA, Wei H collaborators. Emergency tracheal intubation in 202 patients with COVID-19 in Wuhan, China: lessons learnt and international expert recommendations. Br J Anaesth. 2020;125:e28–e37. doi: 10.1016/j.bja.2020.03.026. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Cook TM, El-Boghdadly K, McGuire B, McNarry AF, Patel A, Higgs A. Consensus guidelines for managing the airway in patients with covid-19: guidelines from the difficult airway society, the association of anaesthetists the intensive care society, the faculty of intensive care medicine and the royal college of anaesthetists. Anaesthesia. 2020;75:785–799. doi: 10.1111/anae.15054. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Sorbello M, Morello G, Pintaudi S, Cataldo R. COVID-19: intubation kit, intubation team, or intubation spots? Anesth Analg. 2020;131:e128–e130. doi: 10.1213/ANE.0000000000004970. [DOI] [PubMed] [Google Scholar]
- 32.Chen YC, Chen PJ, Chang SC, Kao CL, Wang SH, Wang LH, Yang PC SARS Research Group of National Taiwan University College of Medicine and National Taiwan University Hospital. Infection control and SARS transmission among healthcare workers, Taiwan. Emerg Infect Dis. 2004;10:895–898. doi: 10.3201/eid1005.030777. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Peck AJ, Newbern EC, Feikin DR, Issakbaeva ET, Park BJ, Fehr J, LaMonte AC, Le TP, Burger TL, Rhodes LV 3rd, Weltman A, Erdman D, Ksiazek TG, Lingappa JR SARS Pennsylvania Case Investigation Team. Lack of SARS transmission and U.S. SARS case-patient. Emerg Infect Dis. 2004;10:217–224. doi: 10.3201/eid1002.030746. [DOI] [PubMed] [Google Scholar]
- 34.Moon HY, Baek CW, Kim JS, Koo GH, Kim JY, Woo YC, Jung YH, Kang H, Shin HY, Yang SY. The causes of difficult tracheal intubation and preoperative assessments in different age groups. Korean J Anesthesiol. 2013;64:308–314. doi: 10.4097/kjae.2013.64.4.308. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Wong P, Wong J, Mok MU. Anaesthetic management of acute airway obstruction. Singapore Med J. 2016;57:110–117. doi: 10.11622/smedj.2016050. [DOI] [PMC free article] [PubMed] [Google Scholar]
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