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Anesthesiology 2006; 104:6805 2006 American Society of Anesthesiologists, Inc. Lippincott Williams & Wilkins, Inc.

Preoperative Evaluation of Extension Capacity of theOccipitoatlantoaxial Complex in Patients with RheumatoidArthritis

Comparison between the Bellhouse Test and a New Method, Hyomental

Distance RatioIchiro 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 hyo-

mental distance ratio (HMDR), for preoperatively identifying

patients with a reduced occipitoatlantoaxial extension capacity,

which was defined 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 goniome-

ter was mounted sat upright with the head in the neutral posi-

tion 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 defined 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 occipitoatlan-

toaxial extension angle was less than 12 (reduced occipitoat-

lantoaxial 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 oc-

cipitoatlantoaxial 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 estab-lished (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 rheu-

matoid arthritis, but the Bellhouse test was not a clinically

reliable method.

AMONG the cervical spine segments, the occipitoatlan-toaxial complex plays a pivotal role for visualizing theglottis during direct laryngoscopy.16 Therefore, identi-

fying patients with reduced mobility of the occipitoat-lantoaxial complex is an important component of pre-operative airway evaluation tests.1,5 A simple bedsidetest described by Bellhouse and Dore1 (the Bellhouse

test) has been commonly used for this purpose and is

performed by measuring the angle traversed by the oc-

clusal surface of the maxillary teeth when only the oc-

cipitoatlantoaxial 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 occipi-toatlantoaxial complex but also the subaxial regions are

extended.6 Moreover, occurrence of the subaxial exten-

sion cannot be found by observing skin surface con-

tours.6,7 These indicate that even if the occipitoatlanto-

axial 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 pre-

diction of a difficult airway.6 Calder et al.4 have also

pointed out that identifying a reduced occipitoatlanto-

axial extension capacity clinically is not always easydespite considerable practice. Involvement of the cervi-

cal spine is often found in patients with rheumatoid

arthritis and tends to be located in the occipitoatlanto-

axial complex. We examined this issue regarding the

Bellhouse test in these patients.

The mandibular space is an airway element contribut-

ing to difficulty in laryngoscopy other than the occipi-

toatlantoaxial extension capacity.5,8,9 The hyomental dis-

tance (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 demon-

strated that because the distance between the hyoidbone and the basiocciput is invariable during move-

ments of the head and neck, the hyoid bone moves

parallel to the cervical spine. When the occipitoatlanto-

axial 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 hypothe-

sized that there may be a relation between the occipi-

* Director of Surgical Center, Staff Anesthetist, Chief Anesthetist, Depart-ment of Anesthesia, Nippon Steel Yawata Memorial Hospital.

Received from the Department of Anesthesia, Nippon Steel Yawata MemorialHospital, Kitakyushu, Japan. Submitted for publication April 25, 2005. Acceptedfor publication January 5, 2006. Support was provided solely from institutionaland/or departmental sources.

Address correspondence to Dr. Takenaka: Department of An esthesia, Nip ponSteel Yawata Memorial Hospital, 1-1-1 Harunomachi, Yahatahigashi-ku, Kitaky-ushu 805-8508, Japan. [email protected]. Individual article re-prints may be purchased through the Journal Web site, www.anesthesiology.org.

Anesthesiology, V 104, No 4, Apr 2006 680


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toatlantoaxial extension capacity and the ratio of theHMD in different head positions. We defined the ratio ofthe HMDs in the neutral position and in head extension

position as the hyomental distance ratio (HMDR). Oursecond aim was to test the accuracy of the HMDR inassessing the occipitoatlantoaxial extension capacity inpatients with rheumatoid arthritis. In addition, we exam-ined radiologically the position of the hyoid bone rela-tive to the basiocciput and the cervical spine duringextension of the head and neck.

Materials and Methods

Patients

Forty patients with rheumatoid arthritis who werescheduled to undergo total hip or knee arthroplastyrequiring 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 inthe study was obtained from all patients. Patients withseverely symptomatic instability were excluded from thestudy. We did not always choose general anesthesia witha conventional laryngoscopy when airway difficulty waspredicted.

Experimental Protocol

All testing was performed by two observers (I. T. andT. I.), who had the appropriate training in accordance

with the original method,1 in the following manner (fig.1). The goggles on which a goniometer was mounted

were secured snugly on the patients head. The patientsat upright adjacent to the film cassette, looking straightahead and with the head in the neutral position. Theobserver (I. T.) supported the patients shoulders tominimize leaning. Another observer (T. I.) measured theangle of the goggles and the HMD using a specially maderuler. The ruler was made out of a metal stylet with adiameter of 2 mm for a pediatric-sized endotracheal

tube. A rounded tip of the thin stylet was pressed on the

skin surface just above the hyoid bone, and the distance

from the tip to the most anterior part of the mentum wasmeasured using a Vernier micrometer, which was de-fined as the HMD (fig. 1).8,9 The patient was then askedto extend the head maximally while attempting to movethe neck as little as possible. The observer was carefulnot to move the neck by inspecting surface contours.The angle of the goggles and the HMD were again mea-sured in this position. Lateral cervical radiographs weretaken at the same time that the angle of the goggles andthe HMD were measured in the two head positions. TheHMDR was defined as the ratio of the HMD at theextreme of head extension to that in the neutral posi-

tion. The Bellhouse angle was defined as a difference inthe angle of the goggles between the two head positions.

Radiologic Measurement

The radiographs were analyzed by two experiencedradiologists who were blinded to the purpose of thestudy and who did not know the Bellhouse angle, theHMD, or the HMDR. As a reference for the position ofthe occiput relative to the cervical spine, the McGregorline was used. This line connected the most dorsal edgeof and caudal portion of the occiput and the dorsal edgeof the hard palate (fig. 2). The reference line for the axis

was drawn through the basal plate of the vertebral body(fig. 2). Because reference lines did not intersect on theradiograph in some patients, the occiput or axis angle

was defined as a difference in angle between the occiputor axis reference line and the common line that was the

ventral vertical edge on each radiograph, respectively. Theoccipitoatlantoaxial angle was calculated by the differencebetween the occiput and axis angles. The occipitoatlanto-axial extension angle was defined as the difference be-tween the occipitoatlantoaxial angle in the neutral positionand that at the extreme of head extension. The subaxialextension was assessed by the difference between the axisangles in these positions.

The HMD on the radiograph was measured in each

Fig. 1. Method for the Bellhouse test and measuring the hyo-mental distance (HMD).

Fig. 2. Diagram of lateral cervical radiograph displaying refer-ence lines and points. B the center of the external acousticmeatus; 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 anteriorpart of the mentum; V the line drawing tangential to anteriorborder of the vertebral body adjacent to the hyoid bone.

681OAA MOBILITY ASSESSMENT: BELLHOUSE TEST VS. HMDR

Anesthesiology, V 104, No 4, Apr 2006


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head and neck position using the same definition stated

above, and the HMDR was calculated (fig. 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 mea-

sured on the radiograph in each head and neck position(fig. 2).

Definition 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 capac-

ity of less than 12 was defined as reduced. We com-

pared the degree of the subaxial extension betweenpatients 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 significant when a Pvalue was less than 0.05.

The relation between paired measurements was ana-

lyzed 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 correla-tion lay between these two values. Sensitivity was the

ratio of the true-positive number to the sum of true-

positive plus false-negative numbers. Specificity was the

ratio of the true-negative number to the sum of true-

negative plus false-positive numbers. Positive and nega-

tive likelihood ratios were calculated as sensitivity/(1

specificity) and (1 sensitivity)/specificity, respec-

tively. 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 Bell-

house test and the HMDR in identifying a reduced oc-

cipitoatlantoaxial extension capacity was assessed bybuilding 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 specificity) 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 com-

parison of areas under the ROC curves was based on the

method described by Delong et al.14

Results

Demographics

A total of 40 patients were enrolled in the study. Therewere 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 thebasiocciput (external acoustic meatus) in the neutralposition 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 signifi-cant difference between them. The median value of thedistance between the hyoid bone and the adjacent cer-

vical vertebra was 3.3 cm (3.1, 3.6 cm) in the neutralposition, significantly increased to 3.4 cm (3.1, 3.7 cm;

P 0.05) in head extension position. But the mediandifference 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 inthe neutral position and in head extension position were

Fig. 3. Relation between the hyomental distance ratios mea-sured externally with the ruler and radiologically in 40 rheu-matoid patients. External hyomental distance ratio (HMDR) cor-relates well with radiologic HMDR (P < 0.0001, r 0.92). Thesolid and dashed lines represent the regression line and theline of identity, respectively.

Table 1. Measurements of Hyomental Distance and Hyomental

Distance Ratio

Median (Interquartile Range)

HMD measured externally with the ruler

Neutral position, cm 3.7 (3.44.0)*

Head extension position, cm 4.7 (4.35.0)*

External HMDR 1.24 (1.151.35)*HMD measured radiologically

Neutral position, cm 4.3 (4.04.6)

Head extension position, cm 5.1 (4.75.6)

Radiologic HMDR 1.19 (1.121.28)

* P 0.01 vs. each radiologic measurement.

HMD hyomental distance; HMDR hyomental distance ratio.

682 TAKENAKA ET AL.



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3.7 and 4.7 cm, respectively, which were approximately0.5 cm smaller than those measured radiologically (P

0.01; table 1). There was a high correlation betweenhyomental distances measured externally and radiologi-cally (P 0.0001, r 0.89 and 0.91 in the neutral andhead extension positions, respectively). Median hyomen-tal distance ratios measured externally and radiologically

were 1.24 and 1.19, respectively (table 1). ExternalHMDR correlated well with radiologic HMDR (P

0.0001, r

0.92; fig. 3).

Accuracy of Bellhouse Test and HMDR for

Estimating Occipitoatlantoaxial Extension Capacity

The median occipitoatlantoaxial extension angle mea-sured radiologically (actual occipitoatlantoaxial exten-sion angle) was 11.2 in the 40 patients (table 2). In 21of them (53%), the occipitoatlantoaxial extension angle

was less than 12 (reduced occipitoatlantoaxial exten-sion capacity). Lateral radiographs at the extreme ofhead extension showed that near-maximal extension ofthe occipitoatlantoaxial complex occurred in all pa-tients. Obvious atlantoaxial subluxation was not foundon the radiographs. Discrepancies in radiologic anglemeasurement between two radiologists averaged 1.3.The median value of the Bellhouse angle was 24.9 (table2). When the test was performed in patients with rheu-matoid arthritis, extension of 12.5 occurred at the sub-axial regions despite attempts to move the neck as littleas possible, which could not be found by inspectingsurface contours of the neck. The extent of the subaxialextension was consistent with a difference between theBellhouse angle and the actual occipitoatlantoaxial ex-

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 of8.5 (5.8, 12.5) in patients with an actual occipitoat-

lantoaxial 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; fig. 4). In contrast, because the

HMDR was not influenced by occurrence of the subaxial

extension, the HMDR was highly correlated with the

actual occipitoatlantoaxial extension angle (P 0.0001,

r 0.88; fig. 5). The ROC plots for the Bellhouse test

and the HMDR in identifying a reduced occipitoatlanto-axial extension capacity are shown in figures 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, specificity, and likelihood ratios

at different cutoff HMDR values for identifying a reduced

occipitoatlantoaxial extension capacity are shown in ta-

ble 3. The cutoff HMDR value of 1.25 was considered to

be appropriate.

Fig. 4. Relation between the Bellhouse angle and the occipitoat-lantoaxial extension angle measured radiologically (actual oc-cipitoatlantoaxial 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 regressionline and the line of identity, respectively.

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

Table 2. Actual Occipitoatlantoaxial Extension Angle and

Bellhouse Angle

Median(Interquartile Range),

Actual occipitoatlantoaxial extension angle 11.2 (7.516.7)

Bellhouse angle 24.9 (2227.6)

Subaxial extension angle 12.5 (717.1)

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




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Discussion

There was a high prevalence of a reduced occipitoat-lantoaxial extension capacity (occipitoatlantoaxial ex-

tension angle

12) in patients with rheumatoid arthri-tis requiring total hip or knee arthroplasty. But thesubaxial cervical regions were relatively intact in most ofthem. In this study, when performing the Bellhouse testin patients with an occipitoatlantoaxial extension capac-ity of 12 or more, the degree of the subaxial extension

was similar to that in volunteers with normal cervicalspines in our previous study.6 In contrast, in patients

with a reduced occipitoatlantoaxial extension capacity,a greater degree of compensatory extension occurred atthe subaxial regions because most of them had intactregions. Occurrence of even a great degree of the sub-axial extension was difficult to find by observing appear-ance because movement of skin overlying a cervicalspinous process did not dependably follow the underly-ing spinal segment.7 Moreover, rheumatoid patients

with an impaired occipitoatlantoaxial complex hadmoved the head using intact subaxial regions for a longtime, which made detection of the subaxial extension allthe more difficult. Because the degree of the subaxialextension was an error when performing the Bellhousetest, unavoidable and unbalanced occurrence of itcaused a poor correlation between the Bellhouse angleand the actual occipitoatlantoaxial extension angle.Therefore, the Bellhouse test did not identify a substan-

tial proportion of patients with a reduced occipitoatlan-toaxial extension capacity and was not clinically reliable.This problem can present a potential for missing a pre-diction of difficult airway in patients with rheumatoidarthritis.

We found a median HMD of 4.7 cm in the head exten-

sion position in patients with rheumatoid arthritis. Tur-kan et al.9 demonstrated that mean hyomental distancesin the same head and neck position were 5.9 cm in menand 5.6 cm in women. A reason for this difference maybe related to slightly built rheumatoid patients having asmall mandibular space associated with severe rheumatoidarthritis that was long-standing. Radiography revealed that

when the occipitoatlantoaxial complex was extended andthe head rotated around the basiocciput, the hyoid bonehardly moved anteriorly together with the mandible and

was pulled cranially parallel to the cervical vertebra by thebasiocciput, which was in accord with the findings of

Penning.10

As the mandible went away from the hyoidbone by the degree of the head rotation, the HMD in-creased in proportion to the degree of the occipitoatlanto-axial extension. Therefore, the HMDR was highly corre-lated with the occipitoatlantoaxial extension capacity andcould correctly assess it in rheumatoid patients. We con-sidered that an HMDR of less than 1.25 was a good predic-tor of a reduced occipitoatlantoaxial extension capacity. Tocalculate the HMDR, the HMD is measured in the headextension position for evaluating the mandibular space andthen is merely measured in the neutral position again.Therefore, the HMDR can serve as a simple and effective

method for preoperatively identifying rheumatoid patientswith a reduced occipitoatlantoaxial extension capacity.There are some potential study limitations of our ex-

perimental design. First, we did not investigate the rela-tion between the HMDR and difficulty in laryngoscopy.Moreover, only with the HMDR, it may be difficult topredict difficult laryngoscopy completely because sev-eral anatomical factors other than a reduced occipitoat-lantoaxial extension capacity influence visualization ofthe glottis during laryngoscopy.5,8,9 However, becausecapacity is one of these factors, we believe that theHMDR may be a useful predictor of difficult laryngos-copy. Second, there was the variation of the skin thick-ness on the hyoid bone among the patients and betweendifferent head and neck positions, which could affectaccuracy of the HMD and HMDR measurements. In thisstudy, there were some differences between the hyo-mental distances measured externally and radiologically.

We measured the HMD by pressing the tip of the thinstylet (ruler) on the skin surface just above the hyoidbone. Moreover, because most of patients were consid-erably thin, the hyoid bone was easily palpable from theskin surface. As a result, a high correlation was estab-lished between hyomental distance ratios measured ex-ternally and radiologically. Therefore, we believe that

the variability was of minor importance in this study.

Fig. 7. Receiver operating characteristic curve of the hyomentaldistance ratio for identifying patients with a reduced occipitoat-lantoaxial extension capacity (occipitoatlantoaxial extensionangle < 12). The area under the curve (AUC) is 0.95, which isgreater than that of the Bellhouse test in figure 6 (P < 0.01).

Table 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 Specificity Posit ive Negative

1.20 0.67 1.0 67 0.33

1.25 0.90 0.84 5.6 0.12

1.30 0.95 0.74 3.7 0.07

1.35 1.0 0.52 2.1 0

* Occipitoatlantoaxial extension angle less than 12.

HMDR hyomental distance ratio.

684 TAKENAKA ET AL.



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When the hyoid bone is not palpable, such as in mor-bidly obese patients, the occipitoatlantoaxial extensioncapacity should be evaluated by other methods, e.g.,radiologic examinations. Although the notch of the thy-roid cartilage is more easily identified from the skinsurface than the hyoid bone, it should be cautioned that

the ratio of the thyromental distances in different headand neck positions is a poorer predictor of a reducedoccipitoatlantoaxial extension capacity than the HMDR(our preliminary study). Third, the intrapatient variabil-ity of the Bellhouse angle was also possible because theend point for extending the head maximally dependedon the voluntary participation of each patient. We didnot examine it because of using a radiologic method formeasuring the occipitoatlantoaxial extension capacity.However, we do not consider that the variability wasimportant because the observer had the appropriatetraining in accordance with the original method,1 and

near-maximal extension at the occipitoatlantoaxial com-plex without the inclination of the body was confirmedon lateral radiographs at the extreme of head extension.Fourth, despite severe cases of rheumatoid arthritis, wedid not find obvious atlantoaxial subluxation. In thisstudy, lateral radiographs were taken in the neutral andhead extension positions in which the subluxation wascommonly corrected. Finally, we found a 53% preva-lence of reduced occipitoatlantoaxial extension capaci-ties because of severe rheumatoid arthritis that was long-standing. It should be cautioned that this is notapplicable to all rheumatoid cases.

In summary, in rheumatoid patients requiring total hipor knee arthroplasty, the Bellhouse test did not reflectwell the occipitoatlantoaxial extension capacity becauseof the occurrence of compensatory extension at thesubaxial regions when the occipitoatlantoaxial complex

was impaired. Therefore, the test missed identifying

many pathologic conditions at the occipitoatlantoaxialcomplex, which can lead to missing a prediction of adifficult airway. However, the HMDR could accuratelyidentify patients with a reduced occipitoatlantoaxial ex-tension capacity despite occurrence of the subaxial ex-tension in this study. Additional studies are indicated to

validate this result.

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