Do Patients with Obstructive Sleep Apnea Have Thick Necks?1,2
I. KATZ, 3 J. STRADLING, A. S. SWTSKY, N. ZAMEL, and V. HOFFSTEIN
Introduction
Patients with obstructive sleep apnea (OSA) have been shown to have abnormal upper airways as assessed by objective techniques, such as CT scans (1, 2), X-ray cephalometry (3), and acoustic reflections (4). These techniques have shown that patients with OSA have decreased cross-sectional area and increased compliance of their upper airways. In addition, based on a subjective observation, it appears that these patients have short and fat necks (5), that are out of proportion to their obesity. These clinical observations suggest that the neck circumference and length of the upper airway may be important in the pathogenesis of repetitive airway obstructions during sleep observed in such patients. These latter two aspects of upper airway anatomy have never been assessed objectively in a formal study. In the present report, we examined the size of the neck as a predictor of sleep apnea. Neck circumference was used as a surrogate measure of how "fat" the patients' necks were, and airway acoustic measurements were used to determine the inner dimensions of the airway. Methods We studied 123 patients referred to the sleep clinic at St. Michael's Hospital because of a history of snoring and suspected sleep apnea. They all underwent nocturnal polysomnography, which included the measurements of the chest wall and abdominal movements using a Respitrace'" (Ambulatory Monitoring, Inc., Ardsley, NY), oxygen saturation using an ear oximeter (Biox 3700, Ohmeda Corp., Boulder, CO), heart rate, and combined oronasal flow using a thermistor inside an oronasal mask. Measurements of EEG, submental EMG, and EOG, were all performed according to standard techniques using a Grass polygraph (Model 78D, Grass Instruments, Quincy, MA). In all patients we measured the external neck circumference at the superior border of the cricothyroid membrane, with the patients awake and in the upright position. This measurement was performed and recorded by a sleep technologist prior to the sleep study. All measurements were performed by two sleep 1228
SUMMARY During physical examination of patients with suspected obstructive sleep apnea (OSA), a comment is frequently made that they appear to have a short and fat neck. Toconfirm this sublective impression by oblective measurements, we studied a group of 123 patients referred to us because of snoring and suspected OSA, all of whom had nocturnal polysomnography and measurements of external and internal neck circumference. The external neck circumference was measured at the level of the superior border of the cricothyroid cartilage. Internal neck circumferences were calculated from the measurements of pharyngeal, glottic, and tracheal areas obtained by the acoustic reflection technique. Internal pharyngeal circumference was further subdivided into the proximal, middle, and distal thirds. The acoustic technique also permitted us to measure the distance between the teeth and the glottic minimum, which reflects the length of the upper airway. Stepwise multiple linear regression analysis revealed that the apnea/hypopnea index (AHI) correlated only with the external neck circumference, the body mass index, and the internal circumference of the distal pharynx; these three variables accounted for 39% of the variability in AHI. We conclude that the external and internal neck circumferences and the degree of obesity are important predictors of sleep apnea; it is possible that obesity produces its effect via fat in the neck. We speculate that the static pharyngeal size modulated by the dynamic loading of the airway due to the weight of fatty tissue of the neck may contribute to the pathogenesis of OSA. AM REV RESPIR DIS 1990; 141:1228-1231
technologists trained in identifying the cricothyroid notch. To reduce the variability in the inter- and intra-observer measurement error, the neck circumference was reported only to the nearest 0.5 ern; this reduced the accuracy of our measurement to within 5 mm. Pharyngeal, glottic, and tracheal areas were measured using the acoustic reflection technique (6). These measurements were performed by the technologists who were unaware of the sleep study findings. The details of the acoustic technique have been extensively described before and will not be repeated here (6-12). It permits us to measure the crosssectional area of the upper airway as a function of distance from the microphone, located at the teeth. All acoustic measurements were performed with the subjects awake, sitting, and breathing quietly at functional residual capacity (FRC). In each subject 64 measurements of airway area as a function of distance (airway echograms) were performed. The average airway echogram was then constructed. The pharynx was defined as the airway segment contained between the teeth and the glottic minimum (figure 1). The glottis was defined as a 4-cm segment centered on the glottic minimum. The proximal tracheal segments were taken to be a 3-cm segment of the airway located 2 cm distal to the glottic minimum. We computed the average pharyngeal, glottic, and tracheal areas by integrating the area function over the appropriate segments and dividing the result by the length of the segment. From these mean areas, we computed
the circumferences of the airway segments assuming circular geometry, so that circumference = 2 X (n x area)" .•. Since the pharynx as defined above spans a rather large distance (from the teeth to the glottis), we subdivided it into three equal parts: a proximal third, middle third, and the distal third. The areas and the circumferences of the three pharyngeal segments were computed as described above. Acoustic measurements also permitted us to measure the distance between the teeth and the glottis, which reflects the length of the upper airway. All sleep tracings were analyzed to separate apneic from nonapneic patients. Obstructive apneas were identified as episodes of the cessation of airflow lasting more than 10 s, accompanied by the paradoxical movements of the rib cage and the abdomen, and accompanied by the reduction of oxygen saturation by more than 40/0 from the baseline value. Central apneas were identified in a similar
(Received in original form June 21, 1989 and in revised form November 9, 1989) 1 From the University of Toronto, Toronto, Canada and from Oxford University, Oxford, England. 2 Correspondence and requests for reprints should be addressed to Dr. V. Hoffstein, St. Michael's Hospital, 30 Bond Street, Toronto, Ontario, Canada M5B lW8. 3 Supported by a fellowship from the Canadian Thoracic Society
1229
NECK SIZE IN OSA
0
Fig. 1. Average (± SD) airway echogram obtained during quiet tidal breathing at functional residual capacity with anatomical landmarks identified.
I
8
Pharynx
6
r~
,'-'r
f If 2
I IJ II
~
o
~
centr9 Glottis I--- I--~irways ~
~.
I
"'
? 10
20
-
t
Trachea ....
... =
30
40
50
Distance (ern)
TABLE 1 ANTHROPOMETRIC AND SLEEP DATA, UPPER AIRWAY LENGTH, AND NECK CIRCUMFERENCE Non-OSA
Sex (M:F) Age Weight BMI AHI Lowest 0, sat External neck circumference Mouth-to-glottis distance Pharyngeal circumference Proximal Middle Distal Glottic circumference Tracheal circumference
OSA
Mean
SD
Mean
SD
27:16 44 83 29 5 87 39.6 17.2
10 20 6 3 6 4.5 1.5
71:9 49 98 32 45 75 43.7 17.5
11 24 7 31 14 4.5 1.8
6.9 8.5 5.7 4.8 5.8
0.4 1.3 0.9 0.7 1.2
6.8 8.2 5.5 4.6 5.6
0.5 1.2 1.0 0.8 1.1
p
0.001 0.007 0.0003 0.005 0.0001 0.0001 NS NS NS NS NS NS
TABLE 2 CORRELATION BETWEEN INDIVIDUAL VARIABLES
AHI AGE BMI EXT LEN
AHI
AGE
BMI
EXT
1.0
0.20
0.51
0.53
1.0
LEN
0.12
PRO
MID
DIS
GLO
TRA
-0.11
-0.22
-0.28
-0.27
-0.06
0.04
0.04
0.04
0.08
NS
NS
NS
0.04
0.07
0.06
-0.05
NS
NS
NS
NS
NS
NS
NS
NS
0.68
-0.02
-0.02
-0.17
-0.23
-0.27
-0.11
NS
NS
NS
-0.11
-0.24
-0.18
-0.17
-0.01
NS
NS
0.36
0.10
-0.05
-0.08
1.0
1.0
0.10 NS
NS
1.0
0.11 NS
PRO MID
1.0
0.51 1.0
NS
NS
NS
0.13
0.02
NS
NS
0.67
0.29
NS
-0.07 NS
0.05 NS
DIS GLO TRA
1.0
0.76
0.54
1.0
0.80 1.0
Definition of abbreviations: AHI = apnealhypopnea index; 8MI = body mass index; EXT = external neck circumference; LEN = mouth-to-glottis distance; PRO, MID, DIS = internal circumferences of the proximal, middle, and distal pharyngeal segments, respectively; GLO, TRA = internal circumferences of the glottic and tracheal segments, respectively. For each variable the first line shows Pearson correlation coefficient and the second line indicates whether this coefficient is significant (0) at the 0.05 level or not (NS).
60
fashion, except that movements of the rib cage and the abdomen were absent. Hypopneas were defined similarly to the obstructive apneas as far as the duration and oxygen desaturation are concerned, but instead of complete cessation of airflow, they were accompanied by more than a 50070 reduction in tidal volume as compared to the previous unobstructed breathing. The number of apneas and hypopneas per hour of sleep was defined as the apnea/hypopnea index (AHI). Statistical analysis was performed using the SAS statistical package (SAS Institute, Inc., Cary, NC). We first performed a correlation analysis between the AHI (dependent variable) and age, BMI, external neck circumference, and internal neck circumferences (pharynx, glottis, and trachea). We then took only those variables that had a significant (p < 0.05) correlation with AHI and used these variables in the stepwise, forward multiple regression analysis. We used Student's t test to examine the differences in all variables between the apneic and nonapneic groups. Results
In our group of 123 patients, 80 had obstructive apnea defined as the apnea/ hypopnea index> 10,and 43 werenonapneic snorers. As expected, there was a significant male predominance among the apneic patients (chi square = 12, p < 0.001).
The anthropometric data, sleep data, external and internal neck circumferences, and upper airway lengths are given in table 1 for the apneic and nonapneic groups. Patients with OSA were slightly, but significantly, older and more obese, whether assessed by weight or the body mass index [BMI = weight (kg)/ height (m)"], The external neck circumference was significantly larger in the apneic than nonapneic snorers (43.7 ± 4.5 em versus 39.6 ± 4.5 em, p < 0.0001), but the upper airway length and pharyngeal, glottic, and tracheal circumferences were similar in both groups (table 1). To identify the variables that significantly influence the apnea/hypopnea index, we first performed simple correlation between all individual variables. This is shown in table 2; AHI correlated significantly only with age, BMI, external neck circumference, and the circumferences of the middle and distal pharynx and glottis. Weentered all these variables into a stepwise, forward, multiple linear regression analysis, whose results showed (table 3) that only the external neck circumference, BMI, age, and the internal circumference of the distal pharynx were independent and significant predictors of the apnea/hypopnea index, accounting for 39% of the variability in AHI (total
1230
KATZ, STRADLING, SWTSKY, ZAMEL, AND HOFFSTEIN
TABLE 3 SUMMARY OF STEPWISE FORWARD MULTIPLE LINEAR REGRESSION ANALYSIS FOR THE DEPENDENT VARIABLE AHI Independent Variables
Partial R2
Model R2
P
0.29 0.04 0.03 0.03
0.29 0.33 0.36 0.39
0.0001 0.0078 0.0267 0.0200
EXTNECK BMI AGE DIST PHAR CIRC
Definition of abbreviations: EXTNECK = axternal neck circumference; DIST PHAR CIRC = internal circumference of the distal pharynx.
r = 0.62). External neck circumference was a more important determinant of AHI than BMI, accounting for 29070 of the variability in AHI, as opposed to only 4% variability in AHI contributed by BMI (table 3). Figure 2 shows that none of the patients with severe sleep apnea (AHI > 50) had a small external neck circumference. Discussion
In this study, we found that the external neck circumference, degree of obesity, age, and internal circumference of the distal pharynx are significant predictors of sleep apnea, accounting in total for 39% of the variability in the apnea/hypopnea index. Furthermore, we have also demonstrated that patients with OSA are more
obese and have thicker, but not shorter, necks than patients without OSA. This corroborates a clinical impression that patients with obstructive sleep apnea have fat necks. To measure upper airway length and internal dimensions, we utilized the acoustic reflection technique. The accuracy, reproducibility, and resolution of this technique, as well as its applicability to studying upper airway areas, have been described previously (4, 6-12). The length of the upper airway has not been previously measured using this technique. However, this measurement is quite simple, since both the anatomical landmarks, the teeth and the glottis, are easily identifiable from the area-distance plots. We took this distance to represent the length of the upper airway. The length measured in this fashion may be subject to errors due to the longitudinal glottic movements during breathing. These movements are relatively small, ranging between 1 and 2.5 em during VC maneuvers, and most likely appreciably smaller than that during quiet tidal breathing at FRC (13). In view of the spatial resolution of the technique (1 to 2 em), it is unlikely that these glottic movements significantly affected our distance measurements. Another potential error in the measurements of upper airway length is head position, i.e., flexion or extension
160
o
..-..
140
l-
I. KATZ, 3 J. STRADLING, A. S. SWTSKY, N. ZAMEL, and V. HOFFSTEIN
Introduction
Patients with obstructive sleep apnea (OSA) have been shown to have abnormal upper airways as assessed by objective techniques, such as CT scans (1, 2), X-ray cephalometry (3), and acoustic reflections (4). These techniques have shown that patients with OSA have decreased cross-sectional area and increased compliance of their upper airways. In addition, based on a subjective observation, it appears that these patients have short and fat necks (5), that are out of proportion to their obesity. These clinical observations suggest that the neck circumference and length of the upper airway may be important in the pathogenesis of repetitive airway obstructions during sleep observed in such patients. These latter two aspects of upper airway anatomy have never been assessed objectively in a formal study. In the present report, we examined the size of the neck as a predictor of sleep apnea. Neck circumference was used as a surrogate measure of how "fat" the patients' necks were, and airway acoustic measurements were used to determine the inner dimensions of the airway. Methods We studied 123 patients referred to the sleep clinic at St. Michael's Hospital because of a history of snoring and suspected sleep apnea. They all underwent nocturnal polysomnography, which included the measurements of the chest wall and abdominal movements using a Respitrace'" (Ambulatory Monitoring, Inc., Ardsley, NY), oxygen saturation using an ear oximeter (Biox 3700, Ohmeda Corp., Boulder, CO), heart rate, and combined oronasal flow using a thermistor inside an oronasal mask. Measurements of EEG, submental EMG, and EOG, were all performed according to standard techniques using a Grass polygraph (Model 78D, Grass Instruments, Quincy, MA). In all patients we measured the external neck circumference at the superior border of the cricothyroid membrane, with the patients awake and in the upright position. This measurement was performed and recorded by a sleep technologist prior to the sleep study. All measurements were performed by two sleep 1228
SUMMARY During physical examination of patients with suspected obstructive sleep apnea (OSA), a comment is frequently made that they appear to have a short and fat neck. Toconfirm this sublective impression by oblective measurements, we studied a group of 123 patients referred to us because of snoring and suspected OSA, all of whom had nocturnal polysomnography and measurements of external and internal neck circumference. The external neck circumference was measured at the level of the superior border of the cricothyroid cartilage. Internal neck circumferences were calculated from the measurements of pharyngeal, glottic, and tracheal areas obtained by the acoustic reflection technique. Internal pharyngeal circumference was further subdivided into the proximal, middle, and distal thirds. The acoustic technique also permitted us to measure the distance between the teeth and the glottic minimum, which reflects the length of the upper airway. Stepwise multiple linear regression analysis revealed that the apnea/hypopnea index (AHI) correlated only with the external neck circumference, the body mass index, and the internal circumference of the distal pharynx; these three variables accounted for 39% of the variability in AHI. We conclude that the external and internal neck circumferences and the degree of obesity are important predictors of sleep apnea; it is possible that obesity produces its effect via fat in the neck. We speculate that the static pharyngeal size modulated by the dynamic loading of the airway due to the weight of fatty tissue of the neck may contribute to the pathogenesis of OSA. AM REV RESPIR DIS 1990; 141:1228-1231
technologists trained in identifying the cricothyroid notch. To reduce the variability in the inter- and intra-observer measurement error, the neck circumference was reported only to the nearest 0.5 ern; this reduced the accuracy of our measurement to within 5 mm. Pharyngeal, glottic, and tracheal areas were measured using the acoustic reflection technique (6). These measurements were performed by the technologists who were unaware of the sleep study findings. The details of the acoustic technique have been extensively described before and will not be repeated here (6-12). It permits us to measure the crosssectional area of the upper airway as a function of distance from the microphone, located at the teeth. All acoustic measurements were performed with the subjects awake, sitting, and breathing quietly at functional residual capacity (FRC). In each subject 64 measurements of airway area as a function of distance (airway echograms) were performed. The average airway echogram was then constructed. The pharynx was defined as the airway segment contained between the teeth and the glottic minimum (figure 1). The glottis was defined as a 4-cm segment centered on the glottic minimum. The proximal tracheal segments were taken to be a 3-cm segment of the airway located 2 cm distal to the glottic minimum. We computed the average pharyngeal, glottic, and tracheal areas by integrating the area function over the appropriate segments and dividing the result by the length of the segment. From these mean areas, we computed
the circumferences of the airway segments assuming circular geometry, so that circumference = 2 X (n x area)" .•. Since the pharynx as defined above spans a rather large distance (from the teeth to the glottis), we subdivided it into three equal parts: a proximal third, middle third, and the distal third. The areas and the circumferences of the three pharyngeal segments were computed as described above. Acoustic measurements also permitted us to measure the distance between the teeth and the glottis, which reflects the length of the upper airway. All sleep tracings were analyzed to separate apneic from nonapneic patients. Obstructive apneas were identified as episodes of the cessation of airflow lasting more than 10 s, accompanied by the paradoxical movements of the rib cage and the abdomen, and accompanied by the reduction of oxygen saturation by more than 40/0 from the baseline value. Central apneas were identified in a similar
(Received in original form June 21, 1989 and in revised form November 9, 1989) 1 From the University of Toronto, Toronto, Canada and from Oxford University, Oxford, England. 2 Correspondence and requests for reprints should be addressed to Dr. V. Hoffstein, St. Michael's Hospital, 30 Bond Street, Toronto, Ontario, Canada M5B lW8. 3 Supported by a fellowship from the Canadian Thoracic Society
1229
NECK SIZE IN OSA
0
Fig. 1. Average (± SD) airway echogram obtained during quiet tidal breathing at functional residual capacity with anatomical landmarks identified.
I
8
Pharynx
6
r~
,'-'r
f If 2
I IJ II
~
o
~
centr9 Glottis I--- I--~irways ~
~.
I
"'
? 10
20
-
t
Trachea ....
... =
30
40
50
Distance (ern)
TABLE 1 ANTHROPOMETRIC AND SLEEP DATA, UPPER AIRWAY LENGTH, AND NECK CIRCUMFERENCE Non-OSA
Sex (M:F) Age Weight BMI AHI Lowest 0, sat External neck circumference Mouth-to-glottis distance Pharyngeal circumference Proximal Middle Distal Glottic circumference Tracheal circumference
OSA
Mean
SD
Mean
SD
27:16 44 83 29 5 87 39.6 17.2
10 20 6 3 6 4.5 1.5
71:9 49 98 32 45 75 43.7 17.5
11 24 7 31 14 4.5 1.8
6.9 8.5 5.7 4.8 5.8
0.4 1.3 0.9 0.7 1.2
6.8 8.2 5.5 4.6 5.6
0.5 1.2 1.0 0.8 1.1
p
0.001 0.007 0.0003 0.005 0.0001 0.0001 NS NS NS NS NS NS
TABLE 2 CORRELATION BETWEEN INDIVIDUAL VARIABLES
AHI AGE BMI EXT LEN
AHI
AGE
BMI
EXT
1.0
0.20
0.51
0.53
1.0
LEN
0.12
PRO
MID
DIS
GLO
TRA
-0.11
-0.22
-0.28
-0.27
-0.06
0.04
0.04
0.04
0.08
NS
NS
NS
0.04
0.07
0.06
-0.05
NS
NS
NS
NS
NS
NS
NS
NS
0.68
-0.02
-0.02
-0.17
-0.23
-0.27
-0.11
NS
NS
NS
-0.11
-0.24
-0.18
-0.17
-0.01
NS
NS
0.36
0.10
-0.05
-0.08
1.0
1.0
0.10 NS
NS
1.0
0.11 NS
PRO MID
1.0
0.51 1.0
NS
NS
NS
0.13
0.02
NS
NS
0.67
0.29
NS
-0.07 NS
0.05 NS
DIS GLO TRA
1.0
0.76
0.54
1.0
0.80 1.0
Definition of abbreviations: AHI = apnealhypopnea index; 8MI = body mass index; EXT = external neck circumference; LEN = mouth-to-glottis distance; PRO, MID, DIS = internal circumferences of the proximal, middle, and distal pharyngeal segments, respectively; GLO, TRA = internal circumferences of the glottic and tracheal segments, respectively. For each variable the first line shows Pearson correlation coefficient and the second line indicates whether this coefficient is significant (0) at the 0.05 level or not (NS).
60
fashion, except that movements of the rib cage and the abdomen were absent. Hypopneas were defined similarly to the obstructive apneas as far as the duration and oxygen desaturation are concerned, but instead of complete cessation of airflow, they were accompanied by more than a 50070 reduction in tidal volume as compared to the previous unobstructed breathing. The number of apneas and hypopneas per hour of sleep was defined as the apnea/hypopnea index (AHI). Statistical analysis was performed using the SAS statistical package (SAS Institute, Inc., Cary, NC). We first performed a correlation analysis between the AHI (dependent variable) and age, BMI, external neck circumference, and internal neck circumferences (pharynx, glottis, and trachea). We then took only those variables that had a significant (p < 0.05) correlation with AHI and used these variables in the stepwise, forward multiple regression analysis. We used Student's t test to examine the differences in all variables between the apneic and nonapneic groups. Results
In our group of 123 patients, 80 had obstructive apnea defined as the apnea/ hypopnea index> 10,and 43 werenonapneic snorers. As expected, there was a significant male predominance among the apneic patients (chi square = 12, p < 0.001).
The anthropometric data, sleep data, external and internal neck circumferences, and upper airway lengths are given in table 1 for the apneic and nonapneic groups. Patients with OSA were slightly, but significantly, older and more obese, whether assessed by weight or the body mass index [BMI = weight (kg)/ height (m)"], The external neck circumference was significantly larger in the apneic than nonapneic snorers (43.7 ± 4.5 em versus 39.6 ± 4.5 em, p < 0.0001), but the upper airway length and pharyngeal, glottic, and tracheal circumferences were similar in both groups (table 1). To identify the variables that significantly influence the apnea/hypopnea index, we first performed simple correlation between all individual variables. This is shown in table 2; AHI correlated significantly only with age, BMI, external neck circumference, and the circumferences of the middle and distal pharynx and glottis. Weentered all these variables into a stepwise, forward, multiple linear regression analysis, whose results showed (table 3) that only the external neck circumference, BMI, age, and the internal circumference of the distal pharynx were independent and significant predictors of the apnea/hypopnea index, accounting for 39% of the variability in AHI (total
1230
KATZ, STRADLING, SWTSKY, ZAMEL, AND HOFFSTEIN
TABLE 3 SUMMARY OF STEPWISE FORWARD MULTIPLE LINEAR REGRESSION ANALYSIS FOR THE DEPENDENT VARIABLE AHI Independent Variables
Partial R2
Model R2
P
0.29 0.04 0.03 0.03
0.29 0.33 0.36 0.39
0.0001 0.0078 0.0267 0.0200
EXTNECK BMI AGE DIST PHAR CIRC
Definition of abbreviations: EXTNECK = axternal neck circumference; DIST PHAR CIRC = internal circumference of the distal pharynx.
r = 0.62). External neck circumference was a more important determinant of AHI than BMI, accounting for 29070 of the variability in AHI, as opposed to only 4% variability in AHI contributed by BMI (table 3). Figure 2 shows that none of the patients with severe sleep apnea (AHI > 50) had a small external neck circumference. Discussion
In this study, we found that the external neck circumference, degree of obesity, age, and internal circumference of the distal pharynx are significant predictors of sleep apnea, accounting in total for 39% of the variability in the apnea/hypopnea index. Furthermore, we have also demonstrated that patients with OSA are more
obese and have thicker, but not shorter, necks than patients without OSA. This corroborates a clinical impression that patients with obstructive sleep apnea have fat necks. To measure upper airway length and internal dimensions, we utilized the acoustic reflection technique. The accuracy, reproducibility, and resolution of this technique, as well as its applicability to studying upper airway areas, have been described previously (4, 6-12). The length of the upper airway has not been previously measured using this technique. However, this measurement is quite simple, since both the anatomical landmarks, the teeth and the glottis, are easily identifiable from the area-distance plots. We took this distance to represent the length of the upper airway. The length measured in this fashion may be subject to errors due to the longitudinal glottic movements during breathing. These movements are relatively small, ranging between 1 and 2.5 em during VC maneuvers, and most likely appreciably smaller than that during quiet tidal breathing at FRC (13). In view of the spatial resolution of the technique (1 to 2 em), it is unlikely that these glottic movements significantly affected our distance measurements. Another potential error in the measurements of upper airway length is head position, i.e., flexion or extension
160
o
..-..
140
l-
