In emergency trauma situations of patients who have sustained severe trauma injuries, there is an increased risk of dislocation of unstable cervical spinal columns . In emergency airway management of such patients, the protection of the respiratory tract is of essential importance; the main goal is to secure rapidly the respiratory tract without resulting in an impairment of the neurological status of the patients . Cervical spinal column injuries account for 2-4% of all injuries and are frequently associated with increased morbidity and mortality [1,3]. Sometimes an injury of the cervical spine is unexpected; in which case protective measures do not seem necessary. In such a case anaesthesia is induced, oral endotracheal intubation using direct laryngoscopy for airway protection and controlled ventilation under application of cricoid pressure is performed. There is much controversy about the methods for tracheal intubation in patients with unstable or potentially unstable cervical spine injuries.
To date, no real-time data have been published about the comparison of the in vivo range of motion during well-established laryngeal intubation under the conditions of manual in-line stabilization with the Macintosh laryngoscope, with intubating laryngeal mask airway, fibre-endoscopic nasal intubation and fibre-endoscopic oral intubation. In cervical spine-injured patients in a trauma situation, an investigation like this is not possible for ethical reasons, as there is an increased risk of causing further damage to the cervical spinal cord; therefore, we decided to investigate manual in-line stabilization during intubation under anaesthesia. The main goal of the current investigation was to detect the amount of real-time cervical spine three-dimensional motion under manual in-line stabilization during intubation with the Macintosh laryngoscope, with intubating laryngeal mask airway, fibre-endoscopic nasal and fibre-endoscopic oral intubation. The extent of the reduction of cervical spine motion under manual in-line stabilization during intubation and the time required for intubation was previously unknown. The use of in vivo real-time ultraound-based motion analysis in this study has been successful in determining the actual three-dimensional movements occurring in real time.
After obtaining approval from the Local Ethics Committee for the study design and consent forms for this prospective randomized non-invasive in vivo investigation, all subjects gave written informed.
Fifty-six subjects were evaluated preoperatively. Eight subjects were excluded as a result of one or more of the following mentioned exclusion criteria. Twenty-four men and 24 women, averaging 40.8 yr of age (range 20-65 yr), participated in the investigation. Forty-eight male and female adult subjects (ASA I or II), who were scheduled for various elective surgical procedures under general anaesthesia, were enrolled in this study. Their physical characteristics are shown in Table 1. The subjects were randomly divided into four intubation groups based on a computer-generated selection. One day after extubation, all subjects' complaints were noted.
Included were adult subjects undergoing elective surgery with no significant co-morbidity in whom difficult intubation was not anticipated. No subject had a Mallampati score  of 3 or 4, a sternomental distance less than 13 cm, a thyromental distance less than 6 cm or an inter-incisor gap less than 3 cm. Subjects with any history of trauma, bone pathology, arthritic or inflammatory disorders of the cervical spine, full stomach, gastroesophageal reflux disease, hiatus hernia, chronic headache, neurological, oropharyngeal or vocal cord problems, any neck pain during the evaluation and any limitation in the normal cervical motion range during pre-evaluation were excluded from the study.
Anaesthetic management was standardized. Monitoring was established before induction and included an electrocardiograph, pulse oximeter, capnograph, non-invasive blood pressure monitor and the ultrasound-guided device used for analysis. The subjects' heads and necks were placed in a neutral supine position. Subjects were pre-oxygenated and anaesthesia was induced with fentanyl and thiopental in weight-based dosages. During the induction of anaesthesia, subjects were ventilated with 100% oxygen. Muscular relaxation was facilitated with atracrurium and total relaxation was controlled by a relaxometer (TOF-Guard®; Organon Teknika, The Netherlands). The subjects were intubated using standardized techniques according to the randomized schedule. All subjects were intubated by the same experienced staff anaesthesiologist who was very familiar with the use of all intubation techniques. The tubes were inserted when the jaw was relaxed, the eyelash reflex absent and the subjects were apneic. Optimal tube position was assumed by symmetric chest wall movement, bilateral chest auscultation, auscultation over the epigastrium for sounds suggestive of stomach inflation, expired tidal volume of greater than 7 mL kg-1 and CO2 exchange on capnograph during gentle, manually assisted ventilation.
To perform intubation with Macintosh laryngoscope, fibre-endoscopic nasal and oral intubation, conventional tracheal tubes (Lo-Contour™; Murphy Mallinckrodt Medical, Athlone, Ireland) were used. In fibre-endoscopic nasal and fibre-endoscopic oral procedures, a fibroscope (Storz, Tuttlingen, Germany) with a xenon light source was inserted transorally or transnasally above the carina. In intubating laryngeal mask airway LMA-Fastrach™ (LMA Deutschland GmbH, Bonn, Germany) was used. After insertion, using a handheld cuff inflator-manometer, the intubating laryngeal mask airway was inflated to an intracuff pressure of 60-70 cm H2O and a conventional tracheal tube was inserted and passed into the trachea through the intubating laryngeal mask airway. Following successful tracheal intubation, the intubating laryngeal mask airway was removed and the tracheal tube was left in situ.
The same investigator performed each manual in-line stabilization manoeuvre for all intubations. For cervical manual in-line immobilization, the investigator manually grabbed hold of the head bilaterally in neutral position without applying axial traction and without compromising the triple markers attached to the head. The degree of intubation difficulty for all subjects was determined based on the classification described by Mallampati and colleagues . Total intubation time was measured as the time from insertion to removal of the intubating device. The use of the four-grade Cormack-Lehane score of laryngoscopic views was investigated during laryngoscopy .
Data acquisition during the intubation procedure was performed on subjects in the supine position; head and chest were immobilized by a rigid board. The measuring stand sensors were placed laterally next to the patient's head and cervical spine. The triple markers were routinely attached to the subject's head by a non-slipping tape. The chest was immobilized at shoulder height by a bandage to suppress motion of the thoracic spine. The system was calibrated in the resting position. The motion of the head out of the start position was measured and described the motion of the whole cervical column. The intubation procedures were investigated continuously in the real-time mode and indicators were set at the beginning and end of intubation. Each subject was tested at the same time of day.
The ultrasound-guided CMS 70P system (Zebris Medizintechnik GmbH, Isny, Germany) is a non-invasive device, which comprises a stand sensor, a basic unit, a triple marker with three ultrasonic transmitters and application aids. The system is based on the determination of spatial co-ordinates of ultrasound transmitters. The basic unit was connected to a mobile, battery-powered laptop. The dynamic data were converted to analogue data in the basic unit. The measuring stand sensor was connected to the stand by means of a ball-and-socket joint and could be adjusted to any desired position. The triple marker was routinely attached to the subject head in a fixed supine position (Fig. 1). A frequency of 35 kHz for the ultrasound triple marker signal was used. The system allows a three-dimensional, real-time kinematic analysis with millimetre-accurate tracking of the measuring system. The basic unit of the system generates curves for flexion/extension, lateral bending and rotation.
Statistical analyses were performed using the SPSS 11.0 (SPSS, Chicago, IL, USA) program. Sample size calculation of the one-way variance analysis is based on the significance level α = 0.05, the power of 80% and the effect size of Δ2 = 0.25. Four groups were analysed. The resulting sample size per group is n = 12 and the total sample size is n = 48. The median was determined for intubation times and cervical spine movements. To analyse the median intubation times between the different intubation procedures, closed test procedures were used. Statistical analysis with simultaneous comparison between the different intubation groups was performed using the non-parametric Kruskal-Wallis test for multiple unassociated samples. The evaluation was carried out for the maximal deflection in each direction. A P-value of less than 0.05 was considered statistically significant.
Forty-two subjects were classified as Type I using the Mallampati score, and six subjects as Mallampati Type II. In the pre-evaluation exercises within the randomly selected groups, there was no significant difference in any values for the range of motion (Table 2). Just before the intubation procedure, all subjects were asleep and fully relaxed. The quality of the laryngeal view depended on the laryngoscope. The laryngeal views were classified according to the Cormack and Lehane score . In the Macintosh laryngoscopic intubation investigations, the distribution of the laryngoscopy scores was 58.3% (Grade I, full view of the vocal cords) and 41.7% (Grade II, partial view of the vocal cords). External laryngeal cricoid pressure was necessary in 92% of the Macintosh laryngoscopic intubation cases in order to optimize laryngoscopic views. In all fibre-endoscopic investigations, Grade I optimal view (full view of the vocal cords) was achieved. In subjects who were intubated using the intubating laryngeal mask airway, a laryngeal view was unimportant. All subjects were intubated at the first attempt. There were no measuring or intubating-related complaints noted for all the investigated subjects.
Under manual in-line stabilization, the cervical spine motion in the sagittal plane, expressed by the flexion/extension motion, was significantly reduced with the fibre-endoscopic techniques and the intubating laryngeal mask airway in comparison to the Macintosh laryngoscopic intubation. The median of cervical spine motion during intubating laryngeal mask airway lay in between the motion of fibreoptic oral intubation and fibreoptic nasal intubation. The intubating laryngeal mask airway, in contrast to the Macintosh laryngoscope intubation, resulted in less extension, less flexion, less bending and less rotation of the cervical spine. Macintosh laryngoscopic intubation and fibreoptic nasal intubation showed more flexion than extension, whereas for intubating laryngeal mask airway and fibreoptic oral intubation, no differences were detected between the single flexion and single extension amplitude (Table 4). Lateral bending (frontal plane) and rotational (axial plane) coupled movements were also listed in Table 4. Greatest variations under manual in-line stabilization for coupled rotations and coupled lateral bending were seen in Macintosh laryngoscopic intubation; the intubating laryngeal mask airway showed a lower extent of coupled rotations and lateral bending movements. Statistical analyses with the closed test procedure showed significant differences between all tested procedures (P < 0.001).
The total time of intubation for the different devices is shown in Table 3. The shortest intubation time was detected in the intubating laryngeal mask airway, followed by times of intubation with the Macintosh laryngoscope. Fibre-endoscopic techniques showed significantly higher intubation times, in which the nasal technique had particularly longer times. In both fibreoptic techniques a wide range was exposed.
For patients suffering from injuries to the head, face, neck or upper thorax, an unstable cervical spine injury should be suspected . Airway management of trauma patients with a suspected cervical spine injury requires a lot of care for the cervical spine. The main attention is thereby on the well-established intubation techniques. To facilitate laryngoscopy and tracheal intubation, rigid laryngoscopes such as the Macintosh  have become the standard tool for practicing anaesthesiologists despite certain disadvantages such as the limitation of entry via the mouth opening, anterior larynx, sternal space restriction, small intra-oral cavity and immobile or unstable cervical spines. The intubating laryngeal mask airway is an important supraglottic ventilatory airway device. The laryngeal mask airway was originally developed for airway management of routine cases with spontaneous ventilation, but through modification it can now be used as a ventilatory device for endotracheal intubation . Contraindications are non-fasted patients, pregnancy, abdominal and thoracic trauma, any condition known to delay gastric emptying and patients with low pulmonary compliance needing positive pressure ventilation . Despite these limitations, the intubating laryngeal mask airway concerns a widespread procedure in difficult airway management that is also propagated in cervical spine trauma [10,11]. Flexible fibreoptic intubation is a very reliable approach to difficult airway management and airway assessment. It has more universal applications than any other technique and can be used orally or nasally. Each airway device has unique properties that may be advantageous in certain situations, but are limiting in others. However, the overall risk of neurological deterioration following intubation has been estimated to be low .
Normally, analyses of the cervical range of motion focus on conscious subjects with or without chronic diseases of the cervical spine. Motion measurements of the cervical spine have been published by different authors with different techniques. Physical examination and visual evaluation depend on the examiner's subjective assessment . Radiographic investigations only represent a static two-dimensional situation and have the disadvantage of exposure to radiation. Many authors consider radiology to be the most accurate method to assess static positioning using bony landmarks .
In a clinical context such as this, with passive and precise real-time motion measurements, studies are rarely found [14,15]. Some cine- and videofluoroscopic studies described cervical spine motion under intubation conditions, but had the disadvantage of investigating the motion in only one plane or in cadavers [10,16-19]. Several devices for non-invasive measurements of the cervical range of motion were described [20-23]. Of the real-time computer-aided devices discussed, an ultrasound-based system produced precise and reproducible measurements [24,25]. Furthermore, these techniques do not expose individuals to X-ray radiation. For assessing cervical spinal positioning and movement, non-invasive techniques such as ultrasound-guided analysis have the advantage of being less expensive and are technically less difficult than radiographic procedures.
In the emergency airway management, besides the different intubation devices, methods for stabilization of potentially injured cervical spines are required during orolaryngeal intubation. Since 1980, direct laryngoscopy and orotracheal intubation with manual in-line stabilization became the standard of care in cervical spine-injured patients . Today, manual in-line stabilization remains standard, and there is a 25-yr-experience history of direct laryngoscopy and orotracheal intubation with manual in-line stabilization , and only a few credible publications of neurologic deterioration . In the literature, no data have been published about the comparison of real-time in vivo range of motion during well-established different intubation techniques under the conditions of manual in-line stabilization. Therefore, the present study was undertaken to compare the range of motion of the cervical spine during laryngeal intubation under manual in-line stabilization with the well-established and in emergency airway management propagated Macintosh laryngoscope and with different other above-mentioned intubating devices using an ultrasound-guided measuring device.
Orolaryngeal intubation with direct laryngoscopy is the most accepted way of performing endotracheal intubation. However, this also requires under manual in-line stabilization flexion and also extension of the cervical spine to expose the larynx. The total range of motion of the cervical spine was determined in this investigation in all three planaes. Other studies focused on the sagittal plane, because a three-dimensional in vitro study of the normal and injured lower cervical spine showed that the movement in the flexion/extension direction is the most sensitive load direction for discoligamentous instabilities .
Lennarson and colleagues published results from a cervical range of motion investigation, in which they evaluated the sagittal range of motion of the cervical spine under intact and C4-5 posterior ligamentous injury conditions. They investigated not the global cervical spine motion but the segmental motions of the levels C0/C1, C1/2, C2/3, C3/4 and C4/5. During direct orolaryngeal intubation in intact spines without manual in-line cervical immobilization, using a video fluoroscopic device, they saw a median extension of 6.6° at the C0-C1 junction, 4.8° at C1/2, 3.2° at C2/3, 2.8° at C3/4 and 2.9° at C4/5. Summation of the medians therefore results in a global motion of 20.3° at the C0/C5 level. Further on, no significant reduction of these results were reported through manual in-line cervical immobilization at any measured level . The same authors published an additional study to evaluate the efficacy of immobilization techniques; therefore, they produced a complete segmental instability C4/5. Under these conditions of complete segmental instability, authors represented that oral tracheal intubation with manual in-line stabilization produced some subluxation, but however did not led to an excess of the physiological segmental cervical spine motion limits. Traction results in unacceptable amounts of distraction and should be avoided . Sawins and colleagues  found the greatest motion of the cervical spine during Macintosh laryngoscopic intubation; they used continuous lateral fluoroscopy while lifting the epiglottis forward to expose the glottis. In comparison to Lennarsons' results, our in vivo results for the total cervical spine range of motion in the sagittal plane showed a comparable extent.
Manual in-line stabilization manoeuvre is recommended to reduce head extension during exposure of the larynx  and has been shown to reduce cervical spine movement during intubation in radiographic investigation [33,34]. Kihara and colleagues  quantified the extent and distribution of segmental cervical movement produced by the intubating laryngeal mask under manual in-line stabilization in 20 anaesthetized patients with cervical pathology undergoing cervical spine surgery and concluded that the intubating laryngeal mask airway produces segmental movement of the cervical spine despite manual in-line stabilization. In comparison to extension motion data from Watts and colleagues , who described orolaryngeal Macintosh intubation with and without manual in-line stabilization, we detected similar extension results (11.01° own data to 13.1° Watts data) under the condition of manual in-line stabilization
In the current study, we evaluated, in comparison to an earlier study, a reduced extent of cervical spine motion with the Macintosh laryngoscope, we detected a global cervical range of motion of 17.57° during direct orolaryngeal intubation with Macintosh under manual in-line cervical stabilization, compared to results from an earlier study of a 22.5° flexion/extension range without manual in-line cervical stabilization . But overall, the extent of cervical spine motion during Macintosh laryngoscopic intubation was rather high in comparison to the other tested intubating techniques and devices, whereas the range of motion during intubating laryngeal mask airway under manual in-line stabilization showed only a slight reduction.
Intubation using the fibre-endoscopic devices showed clear advantages for the laryngeal view and resulted in less movement of the cervical spine in flexion/extension, rotation as well as lateral bending when compared to the direct laryngoscopy with Macintosh. The intubating laryngeal mask airway, in contrast to the Macintosh laryngoscopic intubation under manual in-line stabilization, resulted in less extension, less flexion and less rotation of the cervical spine. The difference between intubating laryngeal mask airway and the fibreoptic techniques in the sagittal plane was statistically significant, but the median value of the intubating laryngeal mask airway lay in between the median result of oral and nasal fibreoptic intubation.
The times required for laryngeal intubation with a Macintosh laryngoscope were significantly longer in comparison to times to intubation with the intubating laryngeal mask airway. Other authors detected that the median time to intubation was 20 s in patients with a simulated cervical spine injury under in-line stabilization . In an earlier study, we found times to orolaryngeal intubation without manual in-line stabilization of 18.9 s. , Sawin and colleagues  demonstrated intubation times of less than 15 s without manual in-line stabilization. However, times required to intubate the respiratory tract under manual in-line stabilization in our investigation were significantly increased when orolaryngeal intubation with the Macintosh laryngoscope was performed (27.25 s mean) in comparison to intubating laryngeal mask airway (16.5 s).Despite the fact that under manual in-line stabilization the use of fibreoptic oral intubation and fibreoptic nasal intubation resulted in reduced motion of the cervical spine during intubation, time to secure the airway was significantly longer than with the use of the Macintosh laryngoscopic intubation or intubating laryngeal mask airway. These findings in the current study indicate that intubating laryngeal mask airway could be a useful device for the intubation of patients in critical situations, where the time for intubation is limited. Our results may present a growing challenge of orolaryngeal intubation under the condition of manual in-line stabilization.
This study was developed as a prediction model for an asymptomatic population; the scope of this paper is limited to generalizations regarding subjects with potential cervical spine injuries. The current investigations were performed under ideal conditions and could be resulted in underestimated extent for the range of cervical spine motion and underestimated time to intubation compared to real emergency situations. All intubation procedures were conducted by one investigator, which could be affected times to intubation as well as cervical spine range of motion. Through this study design, a randomized blinding of the different intubation procedures was impossible. However, our results were in accordance with results reported in other studies.
In conclusion, the present study demonstrated that manual in-line stabilization reduces the cervical spine range of motion during different intubation procedures to a limited extent. However, the results of this study support the use of intubating laryngeal mask airway in airway management of suspected cervical spine patients, if there are no contraindications to these methods. Fibre-endoscopic techniques reduce the cervical movement reliable, but have the disadvantage of prolonged times to intubation; therefore, these techniques are unsuitable in preclinical and emergency situations.
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