The value of a method to reduce the exposure of the upper respiratory tract for predicting dicult laryngoscopy

Background: The current global situation of COVID-19 epidemic is serious. Routine preoperative methods to assess airway such as the interincisor distance(IID), Mallampati classication, and the upper lip bite test(ULBT) have a certain risk of upper respiratory tract exposure and virus spread. The condyle-tragus maximal distance(C-TMD) can be used to assess the airway, and the assessment method does not require the patient to expose the upper respiratory tract, but its value in predicting dicult laryngoscopy compared to other indicators (Mallampati classication, IID, and ULBT) remains unknown. The purpose of this study was to observe the value of C-TMD to predict dicult laryngoscopy and the inuence on intubation time and intubation attempts, and provide a new idea for preoperative airway assessment during epidemic. Methods: We enrolled adult patients who underwent general anesthesia and tracheal intubation. The IID, Mallampati test result, ULBT result, and the C-TMD of each patient were evaluated prior to the initiation of anesthesia. The primary outcome were dicult laryngoscopy dened as the Cormack-Lehane Level > grade 2 , the number of intubation attempts and intubation time. Results: A total of 304 patients were successfully included in the study, 39 patients were identied as dicult laryngoscopy. The intubation time was shorter with the C-TMD (cid:0) 1 nger group 46.8±7.3s, compared with the C-TMD (cid:0) 1 nger group 50.8±8.6s (p (cid:0) 0.01).First attempt success rate was higher in the C-TMD (cid:0) 1 nger group than in the C-TMD (cid:0) 1 nger group (P (cid:0) 0.01).The correlation between the C-TMD and Cormack-Lehane Level was 0.317(Spearman correlation coecient, P (cid:0) 0.001), and the area under the ROC curve was 0.699(P laryngoscopy in classifying laryngoscopy and predicting dicult laryngoscopy, and to calculate the predictive value of C-TMD. The number of intubation attempts and the time of intubation were also be recorded and calculated. It may provide a new idea for preoperative airway assessment and dicult laryngoscopy prediction during the epidemic of COVID-19.


Background
With the development of surgery and the increasing number of operations, it is very important for anesthesiologists to evaluate the airway accurately and simply before surgery [1] . To control the pandemic and prevent novel coronavirus pneumonia nowadays, admitted patients are all required to wear masks to prevent the spread of epidemic disease. It undoubtedly brings certain di culties and risks to our anesthesiologists to perform preoperative airway evaluation and predict di cult laryngoscopy. The routine physical examination indicators, such as the interincisor distance (IID), Mallampati classi cation, and the upper lip bite test (ULBT), require the patient to remove his/her mask and open the mouth while the anesthesiologist conduct a close-up observation of the anatomical structure of the pharyngeal cavity and incisors. The process of evaluation will undoubtedly greatly increase the risk of nosocomial infection during the special period. Therefore, it is necessary to explore a method to reduce the exposure of the upper respiratory tract for predicting di cult laryngoscopy accuracy and simplicity.
It is temporomandibular joint (TMJ) mobility that plays a signi cant role in the grading of laryngoscopic exposure and the prediction of di cult laryngoscopy [2] . TMJ mobility is usually indirectly re ected by some routine physical examination indicators such as the interincisor distance (IID), Mallampati classi cation, and the upper lip bite test (ULBT). The above indicators have certain predictive value for di cult airways, but the accuracy and reliability of this prediction are still relatively limited [3] . Ultrasound measurement of the maximum movement distance of the condyle is thought to directly re ect the degree of TMJ mobility. It can be effectively used for preoperative airway assessment [4] . However, this method, which need the help of ultrosound, is slightly complicated.
The condyle-tragus maximal distance (C-TMD) can be used for preoperative airway assessment. The evaluation method is as follows: The patient sits, and the examiner uses his/her ngers to locate the mandibular condyle of the patient, instructs the patient to open the mouth as wide as possible, and then evaluates whether the distance between the condyle and the tragus can accommodate the width of one nger [5] . This method of assessing the airway can re ect the degree of TMJ mobility directly. Besides, it can be completed relatively simple while the patient wears a mask. However, compared with other indicators,such as Mallampati classi cation, IID, and ULBT, the value of the C-TMD remains unknown.
The purpose of this study was to observe the correlation and agreement between C-TMD and other valuable predictive indicators of di cult laryngoscopy in classifying laryngoscopy and predicting di cult laryngoscopy, and to calculate the predictive value of C-TMD. The number of intubation attempts and the time of intubation were also be recorded and calculated. It may provide a new idea for preoperative airway assessment and di cult laryngoscopy prediction during the epidemic of COVID-19. In this trial, we enrolled patients who underwent elective surgeries with endotracheal intubation under general anesthesia and were of ASA status I-III and 18-90 years of age. We excluded patients with no teeth, with maxillofacial injuries, inability to cooperate, a thyromental distance less than three ngers wide, or limited head and neck movement (less than 80 degrees).

Methods
For all the patients enrolled in this study, during the preoperative examination one day before the operation or after the patient entered the preparation room on the day of the operation, an anesthesiologist who was skilled in the operative procedures used in this study examined whether the C-TMD could accommodate one nger width. The speci c measurement procedure was as follows: the patient sat upright, and the examiner used the index ngers of both hands to locate the mandibular condyle of the mandible, instructed the patient to open the mouth as wide as possible, and felt that the condyle moved with the mouth opening movement. When the mouth opened as far as possible, the examiner then evaluated whether the distance between the condyle and the tragus could accommodate the width of one nger. The above measurement was repeated three times, and the maximum distance between the condyle and the tragus was taken See Figure 1 for details .
Later, another anesthesiologist, who was not aware of the evaluation results of C-TMD, measured other relevant indicators for airway evaluation. These indicators all indirectly re ected the degree of TMJ mobility: Mallampati classi cation: The patient sat upright, opened the mouth wide, and extended the tongue to the maximum (no sound is made). The patient was then scored according to the pharyngeal structure that could be observed. Mallampati class > 2 was considered to be a predictive risk factor for di cult airways [6] .
Interincisor distance (IID): The patient sat and opened the mouth as wide as possible, and then the doctor estimated IID with ngers. IID less than the width of three ngers was a predictive risk factor for di cult airways [7] .
Upper lip bite test (ULBT) classi cation: The patient sat with the chin extending forward. The patient was asked to try his/her best to bite the upper lip with the lower incisors. According to the ability of the lower incisors to bite the upper lip, the test result was divided into three classes: Class 1: the lower incisors completely bit the upper lip above the vermilion border and completely covered the upper lip membrane; class 2: the lower incisors only bit half of the upper lip membrane and failed to reach the vermilion border; class 3: the lower incisor could not bite the upper lip. Classes 2 and 3 were the predictive risk factors for di cult airways [8] .
All patients underwent routine electrocardiographic monitoring and induction of general anesthesia that started after the venous access was opened. The induction protocol utilized the following standardized recipe: midazolam 0.05 mg/kg, sufentanil 0.6 µg/kg, rocuronium 0.6 mg/kg and etomidate 0.3 mg/kg. An anesthesiologist with more than 3 years of experience, who was not aware of any preoperative airway evaluation results, conducted tracheal intubation with laryngoscopic exposure 3 min after bolus injection of rocuronium. According to the speci c situation, either No. 3 or No. 4 laryngoscopy blades were used, and all patients took the head-up sni ng position. After intubation, the grading of all patients' laryngoscopic exposure, the number of intubation attempts and the time of intubation were recorded. The time of intubation de ned when the laryngoscope blade tip passed the incisors until con rmation of the rst wave of CO2 of the capnometer [9] . The Cormack-Lehane classi cation was used to grade laryngoscopic exposure, and observations of the structure of the larynx and the glottis were divided into four classes. Class 1: the glottis structure was fully exposed, and the front and back joint structure could be seen; class 2: the glottis was partially revealed, and the rear glottal joint structure could be seen; class 3: only the epiglottis was seen; class 4: neither the glottis nor epiglottis was visible, Classes >2 were de ned as di cult laryngoscopy [10] . In our institution, no more than 3 intubation attempts via the application of conventional laryngoscope blades were permitted to ensure patient safety, and the operating time for each attempt was no longer than 1 minute. Before next intubation attempts, mask ventilation was used to ensure that the Spo2 was 98% or higher. If di cult airway appeared in the process, we followed the di cult airway treatment guidelines for the treatment and we also prepared conventional treatment tools such as a beroptic bronchoscope, laryngeal mask, and video laryngoscope.

Reliability test
To verify whether C-TMD accommodating the width of one nger can directly re ect the TMJ mobility and whether the method can accurately evaluate the condition when the patient wore protective equipment such as masks, we added two sets of reliability tests. We recruited 20 volunteers. All volunteers wore masks, and an anesthesiologist skilled in the experimental operation method evaluated whether the C-TMD of the volunteers could accommodate the width of a nger See Figure 2 for details).
After the evaluation was completed, all volunteers took off their masks, and then another anesthesiologist skilled in the operation of this experiment, who was not aware of the previous measurement results, assessed whether the C-TMD of the volunteers could accommodate the width of a nger. The difference between the two evaluation results was compared. In addition, an anesthesiologist used ultrasound to measure the maximum condylar movement distance of all volunteers, that is, the degree of condylar mobility. We then analyzed the correlation between C-TMD and the degree of condyle mobility measured by ultrasound.

Sample size
Sample size calculation was performed based on a pilot study. In this study, the incidence of C-TMD 1 nger was 39%, using α = 0.05 and β = 0.1 and we found that a minimum of 176 participants were required in order to detect at least a 4 s difference in means in intubation times.

Statistical analysis
The SPSS 19.0 and MedCalc 19.2.0 statistical software packages were used. Measurement data were expressed as mean ± standard deviation (χ̅ ± s), and ranked or categorical variables were expressed as frequency/ratio (n/%). For univariate comparison, the independent-sample t test, rank sum test, and chisquared test were selected, according to speci c circumstances. Spearman correlation analysis was used to analyze the correlation of variables, and the results of each predictor and laryngoscopic exposure were compared with the paired chi-squared test and internal agreement tests and kappa values were calculated. The receiver operating characteristic curve (ROC curve) was used to analyze the predictive value of each observed parameter to predict di cult laryngoscopy, expressed as the area under the curve (AUC) with its 95% con dence interval (95% CI), and the odds ratio (OR), speci city, and sensitivity of each index for predicting di cult laryngoscopy were calculated. A P<0.05 indicated statistical signi cance.

Results
General information of patients and airway assessment results 373 patients were selected to be intubated under general anesthesia. Laryngeal mask airway management was performed in 58 patients, and surgery was temporarily canceled in 11 patients. Therefore, a total of 304 patients were successfully included in this study, including 137 male patients and 39 patients with di cult laryngoscopy. All patients were successfully intubated within 3 attempts.
After group analysis of all patients according to whether they had di cult laryngoscopy, the differences of Mallampati classi cation, ULBT classi cation, IID, and the C-TMD between the two groups were statistically signi cant, while the differences of body mass index were not. Descriptive data of the patients and the airway assessment results are shown in Table 1.

The time of intubation and the number of intubation attempts of all predictors
The intubation time was shorter with the C-TMD 1 nger group 46.8±7.3s, compared to the C-TMD 1 nger group 50.8±8.6s (P 0.01). The intubation time differences of IID and Mallampati classi cation were statistically signi cant, while the ULBT were not. First attempt success rate was higher in the C-TMD 1 nger group than in the C-TMD 1 nger group (P 0.01). The intubation attempts differences of ULBT and Mallampati classi cation group were not statistically signi cant (see Table 2 and Table 3).

Correlation of all predictors with intubation time and intubation attempts
The  Table 4).

Comparison of preoperative predictors and the Cormack-Lehane Levels
The r values of correlation between C-TMD, IID, ULBT, Mallampati classi cation and Cormack-Lehane Levels was 0.317,0.261,0.266 and 0.213 respectively (all P values were less than 0.01). Paired chi-square and agreement test showed that the C-TMD < 1 nger width had a signi cant k value (0.485) (see Table 4 and Table 5 for details).
The predictive value of each predictor to predict di cult laryngoscopy The receiver operating characteristic (ROC) curve analysis showed that the AUC of the C-TMD, IID, Mallampati classi cation and ULBT classi cation for predicting di cult laryngoscopy were 0.699, 0.637, 0.613 and 0.648 respectively (all P values were less than 0.001,See Figure 3 for details).

Results of reliability test
Twenty volunteers (14 males and 6 females) were successfully enrolled in the trial. There was no difference between the incidence rates of C-TMD <1 nger width estimated by the two anesthesiologists (both were 5%). The maximum movement distance of the condyle measured by ultrasound was 12.6 ± 2.3 mm. Analysis of the correlation between whether the C-TMD <1 nger width and the maximum movement distance of the condyle measured by ultrasound showed r = 0.91, and P<0.001 (Spearman correlation analysis).

Discussion
This study con rms that evaluating whether the C-TMD can accommodate the width of one nger can relatively effectively predict di cult laryngoscopy, and it has signi cant correlation with intubation time and intubation attempts.
The differences in the Mallampati classi cation, ULBT, IID and C-TMD were signi cant between the di cult laryngoscopy group and the nondi cult laryngoscopy group, which shows that they are all indicators predicting di cult laryngoscopy. The difference in age between the two groups was also signi cant. The most common age range of patients in the di cult laryngoscopy group was 44-70 years.
This result is consistent with the recent study of Schnittker R et al [11] .The intubation attempts and time signi cant differences of whether the C-TMD can accommodate the width of one nger reveal that C-TMD < 1 nger width indicates prolonged intubation time and increased number of intubation attempts compared with C-TMD > 1 nger width. The reason is because a patient presenting grade of 3 or 4 in the Cormack-Lehane grade is known to be in high risk of several intubation attempts or intubation failure [12] .
The airway is evaluated before anesthesia mainly by two methods: accurate measurement and nger width estimation. Finger-width estimation is more commonly used because of its simplicity and speed, and it is more advantageous in large-scale top-tiered hospitals with a high surgery volume and fast pace.
Yao et al. [4] used ultrasound to measure the distance moved by the condyle before and after the opening of the mouth to evaluate the degree of condyle mobility and applied it to the prediction of di cult laryngoscopy. The resulting AUC value of the ROC curve was 0.934, which is higher than those of the accurate measurement methods IID, ULBT grading, and Mallampati classi cation. The current method used the tragus as a reference line and used the width of the nger to estimate the maximum distance between the condyle and the tragus. This method can avoid the constraints of objective conditions, such as the availability of ultrasound, and is more convenient. Its AUC value was 0.699, which was higher than the AUCS from the nger-width estimation of IID, ULBT grading, and Mallampati classi cation. These results are basically consistent with those of Yao et al.
C-TMD had the highest agreement with the laryngoscope classi cation. This may have been because C-TMD can directly re ect the degree of TMJ movement. Reliability testing results showed that C-TMD was highly correlated with the maximum movement distance of the condyle measured by ultrasound. The maximum movement distance of the condyle measured by ultrasound can directly re ect TMJ mobility. Thus C-TMD can directly re ect the degree of TMJ mobility as well. The process of laryngoscopic exposure is actually the process of mandibular opening and forward movement, in which the condyle is the pivot point of the entire movement [13] . The wider the range of motion of the condyle, the greater the potential for mandibular movement. Sójka A et al. [14] also showed that the degree of TMJ mobility was closely correlated with the range of motion of the condyle at the maximum mouth opening. Taking the tragus as a reference, C-TMD can re ect the maximum mobility of the condyles. Therefore, C-TMD <1 nger width may be an independent risk factor for di cult laryngoscopy.
The results of this study showed that the speci city of this predictive index of C-TMD <1 nger width was 0.929, and the positive predictive value was 0.676, higher than those of other indices, indicating that the misdiagnosis rate and missed diagnosis rate of this index were lower than those of other related indicators. In predicting di cult laryngoscopy, the indicator of IID<3 nger width, which is used most frequently in our clinical practice, only had a positive predictive value of 0.467, in line with the ndings of China AK et al. [15] . These data further support the advantage of C-TMD <1 nger width in predicting di cult laryngoscopy.
From the perspective of intubation time, intubation attempts, correlation and predictive value, the main reasons for the unsatisfactory performance of ULBT may be its misdiagnosis rate is high. Many patients who do not have di cult laryngoscopy are misdiagnosed because of higher ULBT classes [16] . Our results are consistent with this observation and showed that the sensitivity of high ULBT class was 0.796, while its positive predictive value was only 0.295. We believe that the reason why many patients can not bite the upper lip above the vermilion border with the lower incisors could be due to thick lips rather than reduced TMJ mobility. Whether the factor of lip thickness is one of the reasons for the low positive predictive value of ULBT classi cation needs to be further investigated.
At present, COVID-19 has broken out all over the world, the situation is still very grim, and we can not lower our guard. While adopting protection for ourselves and our patients, we can improve the traditional diagnosis and treatment methods to reduce the cross-infection rate between medical staff and patients [17] . For patients undergoing elective surgery in the new environment, preoperative airway assessment is essential. But the examination may bring anesthesiologists plenty of unknown risks. It is meaningful to nd a way to balance the effectiveness and safety of airway assessment. The assessment of C-TMD can be completed even if the patient wears personal protective equipment such as a mask, and it has high predictive value. During this pandemic, it can be used as a simple method to reduce the exposure of the upper respiratory tract for predicting di cult laryngoscopy instead of IID, Mallampati classi cation, and ULBT. In addition, preoperative evaluation of C-TMD may bene t airway management by anesthesiologist during COVID-19, because when C -TMD < 1 nger width, it may indicate a prolonged intubation and increased number of intubation attempts, thus we can possibly decreased the exposure time of the anesthesiologist to the open mouth of the patient by using more advanced equipment such as a video laryngoscope.
This study still has some limitations. First, in the perspective of methodology, the method of evaluating the condyle mobility depends on the estimation using nger width. Whether it will have lower predictive value than accurate measurement still needs to be con rmed. Secondly, the sample size of this study was not big enough that we cannot analyse di cult intubation due to its low incidence. Thirdly, in some patients, the condyles can not be accurately identi ed by touching due to obesity, which may affect the test results.
The width of the index nger of a normal adult is approximately 1.2 cm. Whether this means that C-TMD less than 1.2 cm is a high-risk factor for di cult laryngoscopic exposure still needs to be explored through visualization techniques such as ultrasound. In the next study, we will enlarge sample size to research its value to predict di cult intubation and use ultrasound to locate the condyle to measure C-TMD, in order to calculate the error rate of nger positioning, eliminate the impact of individual ngerwidth differences on the prediction results, and compare the advantages and disadvantages of ultrasound positioning and nger positioning.

Conclusions
In summary, compared with IID, Mallampati classi cation, and ULBT test, C-TMD is better at predicting di cult laryngoscopy, and it can be a more favorable airway assessment method during the epidemic of COVID-19.    Abbreviations: ULBT, Upper lip bite test; IID, interincisor distance; C-TMD, condyle-tragus maximal distance; C-L, Cormack-Lehane.    Figure 1 When opening the mouth as wide as possible, the condyle will move forward and down, the condyletragus maximal distance of this patient could accommodate one nger width without mask on.

Figure 2
The condyle-tragus maximal distance of this patient could accommodate one nger width with mask on.