Anesthesiology 2006; 104:680 5

2006 American Society of Anesthesiologists, Inc. Lippincott Williams & Wilkins, Inc.

Preoperative Evaluation of Extension Capacity of the Occipitoatlantoaxial Complex in Patients with Rheumatoid Arthritis
Comparison between the Bellhouse Test and a New Method, Hyomental Distance Ratio
Ichiro Takenaka, M.D.,* Tamao Iwagaki, M.D., Kazuyoshi Aoyama, M.D., Hiroshi Ishimura, M.D., Tatsuo Kadoya, M.D.

Background: The authors devised a new method, the hyomental distance ratio (HMDR), for preoperatively identifying patients with a reduced occipitoatlantoaxial extension capacity, which was dened as the ratio of the hyomental distance in head extension position to that in the neutral position. They compared the accuracy of the HMDR with that of the Bellhouse test in 40 patients with rheumatoid arthritis. Methods: Each patient wearing goggles on which a goniometer was mounted sat upright with the head in the neutral position and then extended the head maximally. The angle of the goggles and the hyomental distance were measured in the two head positions, and a lateral cervical radiograph was taken simultaneously. The Bellhouse angle was dened as a difference in the angles of the goggles between these positions. Results: Median values of the radiologic occipitoatlantoaxial extension angle and the Bellhouse angle were 11.2 and 24.9, respectively. In 21 of 40 patients, the radiologic occipitoatlantoaxial extension angle was less than 12 (reduced occipitoatlantoaxial extension capacity). In these patients, extension of the median angle of 16.4 occurred at the subaxial regions and was greater than that of 8.5 in patients with a radiologic occipitoatlantoaxial extension angle of 12 or more (P < 0.01). As a result, a strong relation between the Bellhouse angle and radiologic occipitoatlantoaxial extension angle was not established (P < 0.01, r 0.48). In contrast, the HMDR correlated well with the radiologic occipitoatlantoaxial extension angle (P < 0.0001, r 0.88). The areas under the receiver operating characteristic curve of the Bellhouse test and the HMDR were 0.72 and 0.95, respectively. Conclusions: The HMDR was a good predictor of a reduced occipitoatlantoaxial extension capacity in patients with rheumatoid arthritis, but the Bellhouse test was not a clinically reliable method.

AMONG the cervical spine segments, the occipitoatlantoaxial complex plays a pivotal role for visualizing the glottis during direct laryngoscopy.1 6 Therefore, identifying patients with reduced mobility of the occipitoatlantoaxial complex is an important component of preoperative airway evaluation tests.1,5 A simple bedside test described by Bellhouse and Dore1 (the Bellhouse
* Director of Surgical Center, Staff Anesthetist, Chief Anesthetist, Department of Anesthesia, Nippon Steel Yawata Memorial Hospital. Received from the Department of Anesthesia, Nippon Steel Yawata Memorial Hospital, Kitakyushu, Japan. Submitted for publication April 25, 2005. Accepted for publication January 5, 2006. Support was provided solely from institutional and/or departmental sources. Address correspondence to Dr. Takenaka: Department of Anesthesia, Nippon Steel Yawata Memorial Hospital, 1-1-1 Harunomachi, Yahatahigashi-ku, Kitakyushu 805-8508, Japan. takenaka.i@ns.yawata-mhp.or.jp. Individual article reprints may be purchased through the Journal Web site, www.anesthesiology.org.

test) has been commonly used for this purpose and is performed by measuring the angle traversed by the occlusal surface of the maxillary teeth when only the occipitoatlantoaxial complex is fully extended. We have demonstrated that while the test is being performed, the occipitoatlantoaxial extension capacity is overestimated by the degree of the subaxial extension in volunteers with normal cervical spines because not only the occipitoatlantoaxial complex but also the subaxial regions are extended.6 Moreover, occurrence of the subaxial extension cannot be found by observing skin surface contours.6,7 These indicate that even if the occipitoatlantoaxial extension is limited and if the subaxial regions are normal, the angle measured using the Bellhouse test becomes large. Therefore, we have considered that the test may not detect the pathologic condition at the occipitoatlantoaxial complex, leading to missing a prediction of a difcult airway.6 Calder et al.4 have also pointed out that identifying a reduced occipitoatlantoaxial extension capacity clinically is not always easy despite considerable practice. Involvement of the cervical spine is often found in patients with rheumatoid arthritis and tends to be located in the occipitoatlantoaxial complex. We examined this issue regarding the Bellhouse test in these patients. The mandibular space is an airway element contributing to difculty in laryngoscopy other than the occipitoatlantoaxial extension capacity.5,8,9 The hyomental distance (HMD) has been used to estimate the space.5,8,9 The hyoid bone is attached to the styloid process of the basiocciput by stylohyoid ligament. Penning10 demonstrated that because the distance between the hyoid bone and the basiocciput is invariable during movements of the head and neck, the hyoid bone moves parallel to the cervical spine. When the occipitoatlantoaxial complex is extended, the mandible goes away from the hyoid bone as a result of rotation of the head around the basiocciput, and thus the HMD should increase. In contrast, when the head is extended at the subaxial regions without the occipitoatlantoaxial extension, the position of the mandible relative to the hyoid bone remains the same because head rotation does not occur. Therefore, the HMD should not change. We hypothesized that there may be a relation between the occipi680

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Fig. 1. Method for the Bellhouse test and measuring the hyomental distance (HMD).

toatlantoaxial extension capacity and the ratio of the HMD in different head positions. We dened the ratio of the HMDs in the neutral position and in head extension position as the hyomental distance ratio (HMDR). Our second aim was to test the accuracy of the HMDR in assessing the occipitoatlantoaxial extension capacity in patients with rheumatoid arthritis. In addition, we examined radiologically the position of the hyoid bone relative to the basiocciput and the cervical spine during extension of the head and neck.

Fig. 2. Diagram of lateral cervical radiograph displaying reference lines and points. B the center of the external acoustic meatus; C0 reference line for the occiput (McGregor line); C2 reference line for the axis; CL common line; H anteroinferior border of the hyoid body; M the most anterior part of the mentum; V the line drawing tangential to anterior border of the vertebral body adjacent to the hyoid bone.

Materials and Methods

Patients Forty patients with rheumatoid arthritis who were scheduled to undergo total hip or knee arthroplasty requiring general anesthesia were studied. The study was approved by the institutional ethical committee (Nippon Steel Yawata Memorial Hospital, Kitakyushu, Japan), and written informed consent to participate in the study was obtained from all patients. Patients with severely symptomatic instability were excluded from the study. We did not always choose general anesthesia with a conventional laryngoscopy when airway difculty was predicted. Experimental Protocol All testing was performed by two observers (I. T. and T. I.), who had the appropriate training in accordance with the original method,1 in the following manner (g. 1). The goggles on which a goniometer was mounted were secured snugly on the patients head. The patient sat upright adjacent to the lm cassette, looking straight ahead and with the head in the neutral position. The observer (I. T.) supported the patients shoulders to minimize leaning. Another observer (T. I.) measured the angle of the goggles and the HMD using a specially made ruler. The ruler was made out of a metal stylet with a diameter of 2 mm for a pediatric-sized endotracheal tube. A rounded tip of the thin stylet was pressed on the
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skin surface just above the hyoid bone, and the distance from the tip to the most anterior part of the mentum was measured using a Vernier micrometer, which was dened as the HMD (g. 1).8,9 The patient 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. The angle of the goggles and the HMD were again measured in this position. Lateral cervical radiographs were taken at the same time that the angle of the goggles and the HMD were measured in the two head positions. The HMDR was dened as the ratio of the HMD at the extreme of head extension to that in the neutral position. The Bellhouse angle was dened as a difference in the angle of the goggles between the two head positions. Radiologic Measurement The radiographs were analyzed by two experienced radiologists who were blinded to the purpose of the study and who did not know the Bellhouse angle, the HMD, or the HMDR. As a reference for the position of the occiput relative 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 (g. 2). The reference line for the axis was drawn through the basal plate of the vertebral body (g. 2). Because reference lines did not intersect on the radiograph in some patients, the occiput or axis angle was dened as a difference in angle between the occiput or axis reference line and the common line that was the ventral vertical edge on each radiograph, respectively. The occipitoatlantoaxial angle was calculated by the difference between the occiput and axis angles. The occipitoatlantoaxial extension angle was dened as the difference between the occipitoatlantoaxial angle in the neutral position and that at the extreme of head extension. The subaxial extension was assessed by the difference between the axis angles in these positions. The HMD on the radiograph was measured in each

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head and neck position using the same denition stated above, and the HMDR was calculated (g. 2). In addition, the distances from anteroinferior border of the hyoid body to the center of the external acoustic meatus and to the line drawing tangential to anterior border of the vertebral body adjacent to the hyoid bone were measured on the radiograph in each head and neck position (g. 2). Denition of a Reduced Occipitoatlantoaxial Extension Capacity The occipitoatlantoaxial extension angle required to expose the glottis during conventional laryngoscopy has been reported as varying from 12 to 23.3,11 Because there seemed no doubt that at least 12 was needed for laryngoscopy,3 the occipitoatlantoaxial extension capacity of less than 12 was dened as reduced. We compared the degree of the subaxial extension between patients with and without a reduced occipitoatlantoaxial extension capacity. Statistical Analysis The difference was determined using the Wilcoxon signed rank test or the MannWhitney U test and was considered signicant when a P value was less than 0.05. The relation between paired measurements was analyzed by linear regression analysis. A high correlation had an r value of greater than 0.85, a poor correlation had an r value of less than 0.5, and a moderate correlation lay between these two values. Sensitivity was the ratio of the true-positive number to the sum of truepositive plus false-negative numbers. Specicity was the ratio of the true-negative number to the sum of truenegative plus false-positive numbers. Positive and negative likelihood ratios were calculated as sensitivity/(1 specicity) and (1 sensitivity)/specicity, respectively. Likelihood ratios above 10 and below 0.1 were considered to provide strong evidence for ruling in or out diagnoses, respectively.12 The accuracy of the Bellhouse test and the HMDR in identifying a reduced occipitoatlantoaxial extension capacity was assessed by building the receiver operating characteristic (ROC) curve.13 The ROC curve was constructed from a set of (x,y) points, where x the proportion of false positive results (1 specicity) and y the proportion of true positive results (sensitivity). The area under the ROC curve equals the probability of correctly identifying a reduced occipitoatlantoaxial extension capacity. An area under the ROC curve ranges from 0.5 to 1.0. An area of 1.0 indicates perfectly accuracy, whereas an area of 0.5 means a completely uninformative test. Statistical comparison of areas under the ROC curves was based on the method described by Delong et al.14
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Table 1. Measurements of Hyomental Distance and Hyomental Distance Ratio

Median (Interquartile Range)

HMD measured externally with the ruler Neutral position, cm Head extension position, cm External HMDR HMD measured radiologically Neutral position, cm Head extension position, cm Radiologic HMDR
*P HMD 0.01 vs. each radiologic measurement. hyomental distance; HMDR

3.7 (3.44.0)* 4.7 (4.35.0)* 1.24 (1.151.35)* 4.3 (4.04.6) 5.1 (4.75.6) 1.19 (1.121.28)

hyomental distance ratio.

Results
Demographics A total of 40 patients were enrolled in the study. There were 3 men and 37 women. Mean ( SD) age, weight, and height were 62 7 yr (range, 5178 yr), 51 9 kg (3773 kg), and 153 6 cm (142172 cm), respectively. Position of Hyoid Bone Relative to Basiocciput and Cervical Spine Median distances between the hyoid bone and the basiocciput (external acoustic meatus) in the neutral position and in head extension position were 8.8 cm (lower and upper quartiles: 8.3, 9.6 cm) and 8.9 cm (8.3, 9.5 cm), respectively. There was no statistically signicant difference between them. The median value of the distance between the hyoid bone and the adjacent cervical vertebra was 3.3 cm (3.1, 3.6 cm) in the neutral position, signicantly increased to 3.4 cm (3.1, 3.7 cm; P 0.05) in head extension position. But the median difference in the distance between the two positions was only 0.0 cm ( 0.05, 0.2 cm). Accuracy of HMD/HMDR Measured Externally with the Ruler Median hyomental distances measured externally in the neutral position and in head extension position were

Fig. 3. Relation between the hyomental distance ratios measured externally with the ruler and radiologically in 40 rheumatoid patients. External hyomental distance ratio (HMDR) correlates well with radiologic HMDR (P < 0.0001, r 0.92). The solid and dashed lines represent the regression line and the line of identity, respectively.

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Table 2. Actual Occipitoatlantoaxial Extension Angle and Bellhouse Angle

Median (Interquartile Range),

Actual occipitoatlantoaxial extension angle Bellhouse angle Subaxial extension angle

11.2 (7.516.7) 24.9 (2227.6) 12.5 (717.1)

3.7 and 4.7 cm, respectively, which were approximately 0.5 cm smaller than those measured radiologically (P 0.01; table 1). There was a high correlation between hyomental distances measured externally and radiologically (P 0.0001, r 0.89 and 0.91 in the neutral and head extension positions, respectively). Median hyomental distance ratios measured externally and radiologically were 1.24 and 1.19, respectively (table 1). External HMDR correlated well with radiologic HMDR (P 0.0001, r 0.92; g. 3). Accuracy of Bellhouse Test and HMDR for Estimating Occipitoatlantoaxial Extension Capacity The median occipitoatlantoaxial extension angle measured radiologically (actual occipitoatlantoaxial extension angle) was 11.2 in the 40 patients (table 2). In 21 of them (53%), the occipitoatlantoaxial extension angle was less than 12 (reduced occipitoatlantoaxial extension capacity). Lateral radiographs at the extreme of head extension showed that near-maximal extension of the occipitoatlantoaxial complex occurred in all patients. Obvious atlantoaxial subluxation was not found on the radiographs. Discrepancies in radiologic angle measurement between two radiologists averaged 1.3. The median value of the Bellhouse angle was 24.9 (table 2). When the test was performed in patients with rheumatoid arthritis, extension of 12.5 occurred at the subaxial regions despite attempts to move the neck as little as possible, which could not be found by inspecting surface contours of the neck. The extent of the subaxial extension was consistent with a difference between the Bellhouse angle and the actual occipitoatlantoaxial ex-

Fig. 5. Relation between the hyomental distance ratio (HMDR) and the occipitoatlantoaxial extension angle measured radiologically (actual occipitoatlantoaxial extension angle) in 40 rheumatoid patients. There is a high correlation between the two (P < 0.0001, r 0.88).

tension angle. Among 40 patients, in patients with an actual occipitoatlantoaxial extension angle of less than 12, a subaxial extension of median angle of 16.4 (13.0, 19.5) occurred, which was greater than that of 8.5 (5.8, 12.5) in patients with an actual occipitoatlantoaxial extension angle of 12 or more (P 0.01). Because a greater degree of subaxial extension occurred when the occipitoatlantoaxial complex was impaired, there was a poor correlation between the Bellhouse angle and the actual occipitoatlantoaxial extension angle (P 0.01, r 0.48; g. 4). In contrast, because the HMDR was not inuenced by occurrence of the subaxial extension, the HMDR was highly correlated with the actual occipitoatlantoaxial extension angle (P 0.0001, r 0.88; g. 5). The ROC plots for the Bellhouse test and the HMDR in identifying a reduced occipitoatlantoaxial extension capacity are shown in gures 6 and 7, respectively. The areas under the ROC curves of the test and the HMDR were 0.72 and 0.95, respectively. The area in the latter was greater than that in the former (P 0.01). Sensitivity, specicity, and likelihood ratios at different cutoff HMDR values for identifying a reduced occipitoatlantoaxial extension capacity are shown in table 3. The cutoff HMDR value of 1.25 was considered to be appropriate.

Fig. 4. Relation between the Bellhouse angle and the occipitoatlantoaxial extension angle measured radiologically (actual occipitoatlantoaxial extension angle) in 40 rheumatoid patients. There is a poor correlation between the two angles (P < 0.01, r 0.48). The solid and dashed lines represent the regression line and the line of identity, respectively. Anesthesiology, V 104, No 4, Apr 2006

Fig. 6. Receiver operating characteristic curve of the Bellhouse test for identifying patients with a reduced occipitoatlantoaxial extension capacity (occipitoatlantoaxial extension angle < 12). The area under the curve (AUC) is 0.72.

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Fig. 7. Receiver operating characteristic curve of the hyomental distance ratio for identifying patients with a reduced occipitoatlantoaxial extension capacity (occipitoatlantoaxial extension angle < 12). The area under the curve (AUC) is 0.95, which is greater than that of the Bellhouse test in gure 6 (P < 0.01).

Discussion
There was a high prevalence of a reduced occipitoatlantoaxial extension capacity (occipitoatlantoaxial extension angle 12) in patients with rheumatoid arthritis requiring total hip or knee arthroplasty. But the subaxial cervical regions were relatively intact in most of them. In this study, when performing the Bellhouse test in patients with an occipitoatlantoaxial extension capacity of 12 or more, the degree of the subaxial extension was similar to that in volunteers with normal cervical spines in our previous study.6 In contrast, in patients with a reduced occipitoatlantoaxial extension capacity, a greater degree of compensatory extension occurred at the subaxial regions because most of them had intact regions. Occurrence of even a great degree of the subaxial extension was difcult to nd by observing appearance because movement of skin overlying a cervical spinous process did not dependably follow the underlying spinal segment.7 Moreover, rheumatoid patients with an impaired occipitoatlantoaxial complex had moved the head using intact subaxial regions for a long time, which made detection of the subaxial extension all the more difcult. Because the degree of the subaxial extension was an error when performing the Bellhouse test, unavoidable and unbalanced occurrence of it caused a poor correlation between the Bellhouse angle and the actual occipitoatlantoaxial extension angle. Therefore, the Bellhouse test did not identify a substanTable 3. Diagnostic Value of Hyomental Distance Ratio at Different Cut Points for Identifying Patients with Reduced Occipitoatlantoaxial Extension Capacity*
Likelihood Ratio Cut Point of HMDR Sensitivity Specicity Positive Negative

1.20 1.25 1.30 1.35

0.67 0.90 0.95 1.0

1.0 0.84 0.74 0.52

67 5.6 3.7 2.1

0.33 0.12 0.07 0

* Occipitoatlantoaxial extension angle less than 12. HMDR hyomental distance ratio.

tial proportion of patients with a reduced occipitoatlantoaxial extension capacity and was not clinically reliable. This problem can present a potential for missing a prediction of difcult airway in patients with rheumatoid arthritis. We found a median HMD of 4.7 cm in the head extension position in patients with rheumatoid arthritis. Turkan et al.9 demonstrated that mean hyomental distances in the same head and neck position were 5.9 cm in men and 5.6 cm in women. A reason for this difference may be related to slightly built rheumatoid patients having a small mandibular space associated with severe rheumatoid arthritis that was long-standing. Radiography revealed that when the occipitoatlantoaxial complex was extended and the head rotated around the basiocciput, the hyoid bone hardly moved anteriorly together with the mandible and was pulled cranially parallel to the cervical vertebra by the basiocciput, which was in accord with the ndings of Penning.10 As the mandible went away from the hyoid bone by the degree of the head rotation, the HMD increased in proportion to the degree of the occipitoatlantoaxial extension. Therefore, the HMDR was highly correlated with the occipitoatlantoaxial extension capacity and could correctly assess it in rheumatoid patients. We considered that an HMDR of less than 1.25 was a good predictor of a reduced occipitoatlantoaxial extension capacity. To calculate the HMDR, the HMD is measured in the head extension position for evaluating the mandibular space and then is merely measured in the neutral position again. Therefore, the HMDR can serve as a simple and effective method for preoperatively identifying rheumatoid patients with a reduced occipitoatlantoaxial extension capacity. There are some potential study limitations of our experimental design. First, we did not investigate the relation between the HMDR and difculty in laryngoscopy. Moreover, only with the HMDR, it may be difcult to predict difcult laryngoscopy completely because several anatomical factors other than a reduced occipitoatlantoaxial extension capacity inuence visualization of the glottis during laryngoscopy.5,8,9 However, because capacity is one of these factors, we believe that the HMDR may be a useful predictor of difcult laryngoscopy. Second, there was the variation of the skin thickness on the hyoid bone among the patients and between different head and neck positions, which could affect accuracy of the HMD and HMDR measurements. In this study, there were some differences between the hyomental distances measured externally and radiologically. We measured the HMD by pressing the tip of the thin stylet (ruler) on the skin surface just above the hyoid bone. Moreover, because most of patients were considerably thin, the hyoid bone was easily palpable from the skin surface. As a result, a high correlation was established between hyomental distance ratios measured externally and radiologically. Therefore, we believe that the variability was of minor importance in this study.

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When the hyoid bone is not palpable, such as in morbidly obese patients, the occipitoatlantoaxial extension capacity should be evaluated by other methods, e.g., radiologic examinations. Although the notch of the thyroid cartilage is more easily identied from the skin surface than the hyoid bone, it should be cautioned that the ratio of the thyromental distances in different head and neck positions is a poorer predictor of a reduced occipitoatlantoaxial extension capacity than the HMDR (our preliminary study). Third, the intrapatient variability of the Bellhouse angle was also possible because the end point for extending the head maximally depended on the voluntary participation of each patient. We did not examine it because of using a radiologic method for measuring the occipitoatlantoaxial extension capacity. However, we do not consider that the variability was important because the observer had the appropriate training in accordance with the original method,1 and near-maximal extension at the occipitoatlantoaxial complex without the inclination of the body was conrmed on lateral radiographs at the extreme of head extension. Fourth, despite severe cases of rheumatoid arthritis, we did not nd obvious atlantoaxial subluxation. In this study, lateral radiographs were taken in the neutral and head extension positions in which the subluxation was commonly corrected. Finally, we found a 53% prevalence of reduced occipitoatlantoaxial extension capacities because of severe rheumatoid arthritis that was longstanding. It should be cautioned that this is not applicable to all rheumatoid cases. In summary, in rheumatoid patients requiring total hip or knee arthroplasty, the Bellhouse test did not reect well the occipitoatlantoaxial extension capacity because of the occurrence of compensatory extension at the subaxial regions when the occipitoatlantoaxial complex was impaired. Therefore, the test missed identifying

many pathologic conditions at the occipitoatlantoaxial complex, which can lead to missing a prediction of a difcult airway. However, the HMDR could accurately identify patients with a reduced occipitoatlantoaxial extension capacity despite occurrence of the subaxial extension in this study. Additional studies are indicated to validate this result.

References
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