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Anesth Analg 2002;95:1437-1441
© 2002 International Anesthesia Research Society


GENERAL ARTICLES

The Reliability of the Bellhouse Test for Evaluating Extension Capacity of the Occipitoatlantoaxial Complex

Yasunari Urakami, MD*, Ichiro Takenaka, MD*, Motohiro Nakamura, MD*, Hiroshi Fukuyama, MD*, Kazuyoshi Aoyama, MD{dagger}, and Tatsuo Kadoya, MD*

*Department of Anesthesia, Nippon Steel Yawata Memorial Hospital; and {dagger}Department of Anesthesia, Moji Rosai Hospital, Kitakyushu, Japan

Address correspondence and reprint requests to Ichiro Takenaka, MD, Department of Anesthesia, Nippon Steel Yawata Memorial Hospital, 1–1-1 Harunomachi, Yahatahigashi-ku, Kitakyushu 805–8508, Japan. Address e-mail to takenaka.i{at}ns.yawata-mhp.or.jp


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
We examined the reliability of an airway evaluation test to assess the occipitoatlantoaxial (OAA) extension capacity described by Bellhouse et al. (Bellhouse test) in 20 adult volunteers with normal cervical spines. Each subject sat upright with the head in the neutral position and was then asked to extend the head maximally while attempting to move the neck as little as possible. The angle from the neutral position to the extreme extension was measured using the goggle-goniometer. Lateral cervical radiographs were taken in these positions, and the OAA extension angle was radiographically measured. Median values for OAA extension measured radiographically and extension of the head measured with the Bellhouse test were 21.5° and 30°, respectively. Extension of 9.5° occurred at the subaxial regions, which could not be detected by inspecting surface contours of the neck. The extent of the subaxial extension was almost consistent with the degree of overestimation of the OAA extension capacity by the Bellhouse test. Because the subaxial extension occurred independent of the degree of the OAA extension, a strong relationship between the angle measured with the goggle-goniometer and the OAA extension angle measured radiographically was not established (P < 0.01, r2 = 0.44). These findings mean that the test is not always accurate to evaluate the OAA extension capacity and will fail to detect a reduction of the OAA extension capacity if the subaxial regions are normal. Therefore, these problems derived from the Bellhouse test offer a potential for missing a prediction of difficult tracheal intubations because reduced OAA extension is one of the important factors that make intubation difficult.

IMPLICATIONS. The Bellhouse test was not always accurate to evaluate the actual occipitoatlantoaxial extension capacity because of the inevitable occurrence of the subaxial extension. This may mean that some difficult endotracheal intubations will be unpredictable.


    Introduction
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
The ability to fully extend the head is one of the main determinants for whether an optimal view of the glottis can be achieved during direct laryngoscopy. Thus, assessment of head mobility is an important component of preoperative tests for predicting a difficult airway (1,2). Among the cervical spine segments related to extension of the head, extension at the occipitoatlantoaxial (OAA) complex is pivotal for obtaining a good laryngoscopic view for several reasons. First, to consider the occipitoatlantal and atlantoaxial motions as separate is inappropriate. They act as one unit, and essential movement of the upper cervical spine takes place between the occiput and the axis (3,4). Second, most extension created by direct laryngoscopy occurs at the OAA complex, and the subaxial cervical segments are only minimally displaced during laryngoscopy (4,5). Third, Calder et al. (6) have demonstrated that, in 253 patients with cervical spine disease, patients with disease that includes the OAA complex have an increased prevalence of difficult laryngoscopy than those with disease below the axis vertebra. Finally, bringing the pharyngeal axis close to the oral axis, which is the main factor for improving a laryngoscopic view, depends entirely on the degree of the OAA extension (Fig. 1). Thus, assessment of the OAA extension capacity is essential for accurate prediction of difficulty in tracheal intubation.



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Figure 1. Lateral radiograph displaying the oral axis (OA), the pharyngeal axis (PA), and reference lines for the occiput (C0) and the axis (C2). According to the definition described by Adnet et al. (7), the OA and PA are drawn the line parallel to the hard palate and the line passing through the anterior portion of the atlas (C1) and of C2, respectively. Reference lines for C0 and C2 are defined as the McGregor line, which connects the dorsal edge of the hard palate and the most dorsal and caudal portion of C0 and the line passing through anterior and posterior basal plate of the C2 vertebral body, respectively. The angle between the OA and C0 (a) is constant despite any head position because both are fixed lines on the skull base. The angle between the PA and C2 (b) is also constant despite any head position because the transverse atlantal ligament holds the odontoid process of C2 to the posterior surface of the anterior arch of C1. Therefore, the angle between the OA and PA ({delta}) depends entirely upon the angle between C0 and C2 ({theta}), indicating the degree of the occipitoatlantoaxial (OAA) extension capacity as follows: {delta} = {theta} + b - a.

 
A simple bedside test described by Bellhouse and Dore (1) (Bellhouse test) has often been used for assessing OAA extension capacity because of its ease of performance. The test is performed by estimating the angle transversed by the occlusal surface of the maxillary teeth when the OAA complex is fully extended, attempting to extend the subaxial intervertebral regions as little as possible (1). Thus, accuracy of the test is based on the assumption that separate movements of the OAA complex and the subaxial regions are possible. If extension at the subaxial regions occurs during head extension, the Bellhouse test may not accurately estimate the OAA extension capacity because the test evaluates an overall extension of the cervical spine. This can cause missing a prediction of difficult intubation. However, there are few reports about the reliability of the Bellhouse test. Therefore, the aim of this study was to determine the reliability of the test for evaluating the OAA extension capacity in human subjects without head and neck abnormality using radiological measurement.


    Methods
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Twenty healthy male volunteers without cervical spine pathology were studied. The study was ap- proved by the institutional ethical committee, and written informed consent to participate in the study was obtained from all subjects.

All testing was performed by a single observer (IT), who was an experienced anesthesiologist and had the appropriate training in accordance with the original method (1), in the following manner (Fig. 2). The goggle mounted on a goniometer was secured snugly on the subject’s head with a strap. The subject sat upright adjacent to the film cassette, looking straight ahead, and with the head in the neutral position. The observer supported the subject’s shoulders to minimize leaning and measured the angle with the goggle-goniometer in the neutral position. The subject was then asked to extend the head maximally while attempting to move the neck as little as possible. The observer was careful not to move the neck by inspecting surface contours and measured the angle with the goggle-goniometer at the extreme of extension. The extension angle measured with the Bellhouse test was defined as the difference in angles measured with the goggle-goniometer between these positions. Lateral cervical radiographs were taken at the same time that the angles were measured in the neutral position and at the extreme of extension.



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Figure 2. Method for measuring the extension angle with the Bellhouse test. The goggle mounted on a goniometer is secured snugly on the subject’s head with a strap. The subject sits upright looking straight ahead and with the head in the neutral position. The observer supports the subject’s shoulders to minimize leaning and measures the angle with the goggle-goniometer in the neutral position. The subject is then asked to extend the head maximally while attempting to move the neck as little as possible. The observer is careful not to move the neck by inspecting surface contours and measures the angle with the goggle-goniometer at the extreme of extension. The extension angle measured with the Bellhouse test ({theta}) is defined as the difference in angles measured with the goggle-goniometer between these positions.

 
The radiographs were analyzed by two experienced radiologists who were blinded to the purpose of the study and who did not know the angle measured with the goggle-goniometer. As a reference for the position of the occiput (C0) in relation to the cervical spine, the McGregor line was used. This line connected the most dorsal edge of and caudal portion of the occiput and the dorsal edge of the hard palate (Fig. 3). The reference line for the axis (C2) was drawn through the basal plate of the vertebral body (Fig. 3). Because reference lines did not intersect on the radiograph in some subjects, the C0 or C2 angle was defined as the difference in angles between the C0 or C2 reference line and the common line, which was the ventral vertical edge on each radiograph, respectively. The C0-2 angle was calculated by the difference between C0 and C2 angles. The OAA extension angle was defined as the difference between the C0-2 angle in the neutral position and that at the extreme of extension. The subaxial extension was assessed by the difference between C2 angles in these positions.



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Figure 3. Sample lateral neck radiograph at the extreme of extension displaying reference lines for the occiput (C0) and axis (C2). The McGregor line, which connects the most dorsal edge of and caudal portion of the occiput and the dorsal edge of the hard palate, is used as a reference for C0. The reference line for C2 is drawn through the basal plate of the vertebral body. The angle between each reference line and a common line, which is the ventral vertical edge on each radiograph, is measured. C0-2 angle is calculated by the difference between C0 and C2 angles.

 
Wilcoxon’s matched pairs signed rank sum test was used to compare between extension angle measured with the Bellhouse test and that of the OAA complex measured radiographically. A P value of <0.05 was considered significantly different. The relationship between paired measurements was analyzed by linear regression analysis.


    Results
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
The subjects’ ages ranged from 26 to 48 yr (mean ± SD, 32 ± 8 yr), and their weights ranged from 50 to 90 kg (69 ± 12 kg). The median OAA extension angle measured radiographically for the 20 subjects was 21.5° (17.5° and 26° were the lower and upper quartiles). Lateral radiographs at the extreme of extension showed that near maximal extension of the OAA complex occurred in all subjects. The median extension angle measured with the Bellhouse test was 30° (27° and 35°) and was significantly larger than the OAA extension angle measured radiographically (Fig. 4; P < 0.001). The test overestimated the actual OAA extension capacity. The median subaxial extension angle was 9.5° (5° and 12.5°), and more than 10° subaxial extension occurred in 10 of the 20 subjects despite attempts to move the neck as little as possible. The extent of the subaxial extension was almost consistent with the degree of the overestimation of the actual OAA extension capacity by the Bellhouse test. Occurrence of the subaxial extension could not be found by inspecting surface contours of the neck. Because the extent of the subaxial extension did not correlate with the degree of the OAA extension angle (P = 0.14, r2 = 0.12), a strong relationship between the angle measured with the Bellhouse test and the OAA extension angle measured radiographically was not established (P < 0.01, r2 = 0.44). Measurement discrepancies in radiographic measurement between two radiologists averaged 1.2°.



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Figure 4. Comparison between the extension angle measured with the Bellhouse test and the occipitoatlantoaxial (OAA) (C0-2) extension angle measured radiographically. *P < 0.001 with Wilcoxon’s signed rank test.

 

    Discussion
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Direct laryngoscopy requires an extension of the upper cervical spine for optimal visualization of the glottis, especially in a functional unit of the OAA complex (4,5,8). Sawin et al. (5) and Hastings et al. (8) have demonstrated that the OAA extension angles required to expose the glottis during direct laryngoscopy are 12° and 23°, respectively. In contrast, it has been thought that 35° of extension is possible in the normal OAA complex from the neutral position to the maximum extension, which is much larger than the angle for a good laryngoscopic view (1,2). However, Johnson et al. (9) showed a mean maximum extension of 24.1° at the OAA complex in normal volunteers. Our finding of the median extension angle of 21.5° at normal OAA complex was similar to the measurement of Johnson et al. (9). Thus, the difference between normal OAA extension capacity and extension angle for laryngoscopy is smaller than expected. When the OAA extension angle required to obtain an optimal laryngoscopic view is 23°, as described by Hastings et al. (8), in approximately two thirds of the 20 subjects, extension capacity could not exceed 23°. There are some cases where the angle for laryngoscopy exceeds extension capacity, even in an intact cervical spine. These findings mean that whether there is sufficient OAA extension capacity to obtain an optimal laryngoscopic view cannot be decided unless the capacity is precisely assessed. Therefore, a precise method is required.

It is believed that the OAA complex can be extended without the subaxial extension because the structure of the OAA complex differs from that of the subaxial intervertebral joints. However, in half of the 20 subjects, a more than 10° subaxial extension occurred despite attempts to move the neck as little as possible. Subaxial extension could not be detected by observing the surface contours of the neck. Refshauge et al. (10) showed that cervical spinal posture could not be predicted by observing surface contours because movement of the skin overlying a cervical spinous process did not dependably follow the underlying spinal segment. Thus, extension at the subaxial regions was inevitable while performing the Bellhouse test. The degree of the subaxial extension was consistent with the degree of the overestimation of the actual OAA extension capacity by the Bellhouse test. Moreover, because the subaxial extension occurred independently of the degree of the OAA extension, the relationship between the extension angle measured with the Bellhouse test and that of the OAA complex measured radiographically was not a degree-for-degree match.

These findings pose two problems associated with the Bellhouse test that are not preventable. First, the Bellhouse test does not always accurately evaluate the OAA extension capacity despite the need of a precise method for assessing it. In addition, overestimation from the test cannot be bypassed because there is little difference between normal OAA extension capacity and the extension angle for a glottic exposure during direct laryngoscopy, as stated above. Second, the test may fail to detect the pathological condition at the OAA complex because the test predicts the OAA extension capacity to be normal if the subaxial regions are normal, even when the OAA extension capacity is reduced, such as in some patients with rheumatoid arthritis. Therefore, these problems present a potential for missing a prediction of difficult tracheal intubation because reduced OAA extension capacity is one of the important factors that make intubation difficult. To overcome these problems, radiographic examination is the only method, although it is seldom used. Lateral neck radiographs in the neutral position and at the extreme of head extension are useful as one of the preoperative airway evaluation tests. These also help in determining alternative techniques for airway management when tracheal intubation with a conventional laryngoscope fails (11).

There are some potential study limitations of our experimental design. First, the angle measured with the Bellhouse test reflects not only cervical spine motion, but also the inclination of the body. However, we are confident that the bias introduced by the inclination of the body is minimal because care was taken to ensure that the subjects did not lean while extending their heads. Second, intra-subject variability was possible because the end-point for extending the head maximally depended on the voluntary participation of each subject. We did not examine intra-subject variability because of using the radiological method in healthy volunteers. However, we believe that variability was of minor importance because the observer had the appropriate training in accordance with the original method (1), and near maximal extension at the OAA complex without the inclination of the body was confirmed on lateral radiographs at the extreme of extension. Third, we did not determine the reliability of the Bellhouse test for predicting difficult tracheal intubation. Fourth, assessment of the OAA extension capacity alone cannot predict difficult tracheal intubation because several anatomical factors affect visualization of the larynx during direct laryngoscopy. Finally, regarding radiographic biases, the variation in the radiographic angle measurement was <1.2°, demonstrating a small interobserver variability.

In summary, while performing the Bellhouse test, the subaxial extension occurred independently of the degree of the OAA extension, which could not be detected by observing appearance. Thus, with the test, the actual OAA extension capacity was overestimated by the degree of the subaxial extension and was not always accurately evaluated. Thus, the Bellhouse test may miss a prediction of a difficult endotracheal intubation.


    References
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

  1. Bellhouse CP, Dore C. Criteria for estimating likelihood of difficulty of endotracheal intubation with the Macintosh laryngoscope. Anaesth Intensive Care 1988; 16: 329–37.[Web of Science][Medline]
  2. Benumof JL. Management of the difficult adult airway: with special emphasis on awake tracheal intubation. Anesthesiology 1991; 75: 1087–110.[Web of Science][Medline]
  3. Penning L. Normal movements of the cervical spine. AJR Am J Roentgenol 1978; 130: 317–26.[Abstract]
  4. Horton WA, Fahy L, Charters P. Disposition of cervical vertebrae, atlanto-axial joint, hyoid and mandible during radiograph laryngoscopy. Br J Anaesth 1989; 63: 435–8.[Abstract/Free Full Text]
  5. Sawin PD, Todd MM, Traynelis VC, et al. Cervical spine motion with direct laryngoscopy and orotracheal intubation: an in vivo cinefluoroscopic study of subjects without cervical abnormality. Anesthesiology 1996; 85: 26–36.[Web of Science][Medline]
  6. Calder I, Calder J, Crockard HA. Difficult direct laryngoscopy in patients with cervical spine disease. Anaesthesia 1995; 50: 756–63.[Web of Science][Medline]
  7. Adnet F, Borron SW, Dumas JL, et al. Study of the "sniffing position" by magnetic resonance imaging. Anesthesiology 2001; 94: 83–6.[Web of Science][Medline]
  8. Hastings RH, Vigil AC, Hanna R, et al. Cervical spine movement during laryngoscopy with the Bullard, Macintosh, and Miller laryngoscopes. Anesthesiology 1995; 82: 859–69.[Web of Science][Medline]
  9. Johnson RM, Owen JR, Hart DL, Callahan RA. Cervical orthoses: a guide to their selection and use. Clin Orthop 1981; 154: 34–45.
  10. Refshauge KM, Goodsell M, Lee M. The relationship between surface contour and vertebral body measures of upper spine curvature. Spine 1994; 19: 2180–5.[Web of Science][Medline]
  11. Takenaka I, Aoyama K, Kadoya T. Is awake intubation necessary when the laryngeal mask airway is feasible? Anesth Analg 2000; 91: 246–7.[Free Full Text]
Accepted for publication June 17, 2002.




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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins and Stanford University Libraries' HighWire Press®. Copyright 2002 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press