Abdominal Compression Increases Upper Airway Collapsibility During Sleep in Obese Male Obstructive Sleep Apnea Patients

Abstract

Study Objectives:

Abdominal obesity, particularly common in centrally obese males, may have a negative impact on upper airway (UA) function during sleep. For example, cranial displacement of the diaphragm with raised intra-abdominal pressure may reduce axial tension exerted on the UA by intrathoracic structures and increase UA collapsibility during sleep.

Design:

This study aimed to examine the effect of abdominal compression on UA function during sleep in obese male obstructive sleep apnea patients.

Setting:

Participants slept in a sound-insulated room with physiologic measurements controlled from an adjacent room.

Participants:

Fifteen obese (body mass index: 34.5 ± 1.1 kg/m²) male obstructive sleep apnea patients (apnea-hypopnea index: 58.1 ± 6.8 events/h) aged 50 ± 2.6 years participated.

Interventions:

Gastric (P_GA) and transdiaphragmatic pressures (P_DI), UA closing pressure (UACP), UA airflow resistance (R_UA), and changes in end-expiratory lung volume (EELV) were determined during stable stage 2 sleep with and without abdominal compression, achieved via inflation of a pneumatic cuff placed around the abdomen. UACP was assessed during brief mask occlusions.

Measurements and Results:

Abdominal compression significantly decreased EELV by 0.53 ± 0.24 L (P = 0.045) and increased P_GA (16.2 ± 0.8 versus 10.8 ± 0.7 cm H₂O, P < 0.001), P_DI (11.7 ± 0.9 versus 7.6 ± 1.2 cm H₂O, P < 0.001) and UACP (1.4 ± 0.8 versus 0.9 ± 0.9 cm H₂O, P = 0.039) but not R_UA (6.5 ± 1.4 versus 6.9 ± 1.4 cm H₂O·L/s, P = 0.585).

Conclusions:

Abdominal compression negatively impacts on UA collapsibility during sleep and this effect may help explain strong associations between central obesity and obstructive sleep apnea.

Citation:

Stadler DL; McEvoy RD; Sprecher KE; Thomson KJ; Ryan MK; Thompson CC; Catcheside PG. Abdominal compression increases upper airway collapsibility during sleep in obese male obstructive sleep apnea patients. SLEEP 2009;32(12):1579-1587.

OBSTRUCTIVE SLEEP APNEA (OSA) IS A COMMON SLEEP DISORDER CHARACTERIZED BY REPETITIVE PERIODS OF UPPER AIRWAY (UA) COLLAPSE DURING sleep. Male gender and obesity are 2 key predictors of OSA,^1,2 but the mechanisms via which these factors contribute to OSA remain unclear. Central obesity, particularly common in obese male OSA patients, leads to increased intra-abdominal pressure (IAP). This pressure may have an important influence on diaphragm position, which may affect the degree of axial tension (caudal traction) exerted on the UA, and therefore the propensity for UA collapse. Such effects are likely to be most evident in the supine posture and during sleep, when other compensatory mechanisms are diminished and may at least partly explain gender and obesity influences in OSA.

While airway patency is importantly modulated by respiratory drive and negative airway pressure reflex activation of UA dilator muscles during inspiration, caudal traction is also likely to influence UA patency throughout the respiratory cycle. Studies in anesthetized animals^3,4 show that decreased UA tension via cranial tracheal movement promotes UA collapse, which emphasizes the potential importance of tracheal traction for maintaining airway patency.

Investigating the influence of tracheal traction on UA function in humans is inevitably difficult. Changes in lung volume are well known to affect UA function and may reflect predominantly tracheal traction effects. Several studies have shown UA patency to decrease with compression of the abdominal and thoracic compartments via positive extrathoracic pressure.^5–7 While data concerning the magnitude of lung volume changes during sleep with obesity are currently lacking, end-expiratory lung volume (EELV), which normally falls ~15% during sleep in healthy weight individuals,^8,9 is profoundly reduced in obese patients during general anesthesia¹⁰ and likely during sleep. EELV reductions, at least in anesthesia, appear to be largely explained by cranial movement of the diaphragm.¹¹ Consequently, changes in lung volume with obesity alone may substantially underpin the increased propensity for UA collapse in OSA.

Extrathoracic pressure induced changes in lung volume may have different effects on transdiaphragmatic forces, lung volume and tracheal traction than the thoracoabdominal compressive effects of obesity. While closely related to lung volume changes, intra-abdominal and transdiaphragmatic pressure changes are potentially stronger determinants of UA function than lung volume change per se. IAP, a key determinant of transdiaphragmatic force is approximately doubled in obese compared to healthy-weight individuals.¹² Consequently, abdominal mass loading effects of obesity appear likely to influence UA function during sleep via influences on tracheal traction. However, direct evidence that abdominal compression has any impact on UA function during sleep is currently lacking.

The aim of this study was to examine the effect of experimental abdominal compression on UA function during sleep in obese male OSA patients, to test the hypothesis that acute abdominal compression would increase UA collapsibility and UA resistance (R_UA) during sleep.

METHODS

Patient selection

Twenty-five obese (body mass index [BMI] 30-40 kg/m²) male OSA patients with moderate-to-severe OSA (apnea-hypopnea index [AHI] > 30 events/h) and between the ages of 18-65 years participated. Apart from OSA, patients were void of any other respiratory diseases and all demonstrated normal lung function (forced expiratory volume in 1 sec [FEV₁] and forced vital capacity [FVC] > 80% predicted, JLab software version 4.53; Compactlab, Jaeger, Wuerzburg, Germany). Patients were asked to refrain from consuming caffeine and alcohol for 12 and 24 hours prior to the experiment respectively. This study was approved by the Daw Park Repatriation General Hospital and Adelaide University Human Research and Ethics Committees. Each patient gave informed written consent to participate in the study.

Measurements and Equipment

Sleep was monitored by 2 channels of EEG (C₄/A₁, C₃/A₂), left and right electro-oculograms, submental EMG, and ECG. Sleep recordings were classified according to standard sleep staging¹³ and arousal scoring criteria¹⁴ by a single experienced polysomnographer who was blinded to the experimental conditions. The nostrils were decongested with xylometazoline hydrochloride nasal spray (Otrivin, Novartis Australasia, Rowville, Victoria, Australia) and anesthetized (2% lignocaine spray). Esophageal (P_ES) and gastric (P_GA) pressures were recorded via 2 separate latex balloon catheters consisting of a 5-cm balloon (Viasys Healthcare, Hoechberg, Germany) attached to the distal end of polyethylene tubing (2.08 mm OD, 1.57 mm ID; Microtube Extrusions, North Rocks, NSW, Australia). P_GA and P_ES catheters were advanced approximately 60 cm and 45 cm respectively through the most patent nostril. The balloons were then filled with ~0.5 mL air, and each catheter connected to solid-state pressure transducers (Spectramed DTX, Oxnard, USA). Catheter positions were adjusted until positive P_GA and negative P_ES swings were detected during and in phase with inspiration. Epiglottic (P_EPI) pressure was assessed by a thin air-perfused nasal catheter (see Hilditch et al.¹⁵ for further detail). This catheter was advanced 1–2 cm below the base of the tongue under direct visualization and connected to another pressure transducer (MP45; Validyne Engineering, Northridge, CA). All catheters were taped at the nose. Patients were fitted with a nasal mask (Series 2600, Hans Rudolph, Kansas City, MO, USA). Nasal flow and volume were measured by a pneumotachograph (PT16, Jaeger, Germany). Arterial oxyhemoglobin saturation was recorded by finger pulse oximetry (POET II model 602-3; Criticare Systems, Waukesha, WI) while end-tidal CO₂ was measured at the mask (Capstar-100, CWE Inc, PA). Mask pressure (P_MASK) was measured by a differential pressure transducer (MP45; Validyne Engineering, Northridge, CA) referenced to atmospheric pressure. Transdiaphragmatic pressure (P_DI) was determined as P_GA-P_ES at end-expiration. Abdominal and thoracic excursions were measured continuously using 2 pairs of magnetometer coils (Polhemus Liberty, Colchester, USA) placed in the anterior-posterior (AP) axis of the chest and abdomen. Abdominal compression was achieved by 2 large inflatable pneumatic cuffs (5082-88-1, Welch Allyn Inc, Arden, USA) with a width of 21 cm connected in series and placed externally around the abdomen. Care was taken to ensure abdominal compression did not directly restrict lower rib cage movement. This was achieved by positioning the cranial edge of the pressure cuff below the anterior lower ribs. The cuff was inflated and rapidly deflated remotely via delivery of compressed air, and via suction respectively. Cuff pressure (P_CUFF) was recorded throughout each study using a solid-state pressure transducer (Spectramed DTX, Oxnard, USA) connected via a T-piece at the cuff inlet.

All conventional sleep-related signals were recorded on a Compumedics data acquisition system (E-series, Compumedics Inc., Melbourne, Australia). X, Y, and Z coordinates for each of the 4 magnetometer sensors were acquired on a second computer at a sample rate of 120 Hz. The remaining signals were recorded on a 32-channel Windaq (DI-720 DATAQ Instruments Inc, OH, USA) data acquisition system at 200 Hz. To allow accurate time-matching among the 3 recording systems, a computer activated event mark signal was simultaneously placed on all 3 acquisition systems coincident with the onset of each mask occlusion.

Nasal Continuous Positive Airway Pressure (CPAP) Apparatus and Assessment of UA Collapsibility

A custom designed breathing circuit (Figure 1) similar to that described by Issa and Sullivan¹⁶ was constructed to allow delivery of nasal CPAP as well as rapid external occlusion of the airway. External mask occlusion was achieved via a computer-controlled solenoid valve that delivered compressed air to rapidly inflate a balloon occlusion valve near the inspiratory port of the mask (Figure 1). Occlusions were commenced near end-expiration and were sustained until UA closure had developed or until there was clear evidence of EEG arousal. During occlusions (Figure 2), inspiratory efforts produce parallel increases in P_MASK, P_EPI, and P_ES throughout inspiration when the airway is patent. Subsequent inspiratory efforts produce progressively larger pressure deflections with increasing respiratory drive until a critical pressure is reached where P_MASK ceases to change despite progressively more negative P_EPI and P_ES. This critical pressure is indicative of UA collapse and was defined as UA closing pressure (UACP).^16,17

Figure 1.

A schematic diagram of the breathing circuit used to deliver continuous positive airway pressure (CPAP) and the undertaking of external mask occlusions. CPAP was delivered to the patient via the inspiratory limb and air was expired via the plateau valve. During an external mask occlusion, a balloon located upstream of the mask was rapidly inflated near end-expiration. Occlusion termination was achieved by rapid balloon deflation.

Figure 2.

A 30-sec trace showing the events during a brief external mask occlusion in an OSA patient. Note the parallel increase in mask (P_MASK), epiglottic (P_EPI) and esophageal (P_ES) pressures during the first inspiratory effort followed by a return back to baseline. During subsequent efforts, P_MASK again initially tracks P_EPI and P_ES until a point at which it deflects away from P_EPI and P_ES. This deflection point is indicative of UA collapse and is classified as the UACP.

Protocol

Following equipment setup and with patients supine, a trial of abdominal compression was performed during wakefulness to find a cuff inflation pressure that the patient believed was tolerable during sleep. This pressure was designated as the “inflated” cuff pressure for the remainder of the study. Patients were asked to relax and breathe nasally during 5 min of quite wakefulness for baseline ventilatory recordings prior to lights out. The patient's mouth was then taped (Sleek; Smith and Nephew, London, UK) to ensure nasal breathing and prevent mouth leaks. CPAP was commenced at the therapeutic level and the patient was allowed to fall asleep while remaining in the supine position. All subsequent experimental manipulations conducted by the researchers were undertaken from an adjacent room. Patients were monitored continuously by a video camera and polysomnograph recordings. Once asleep, the minimum level of CPAP required to abolish flow limitation was determined and then maintained throughout the remainder of the night unless adjustments became necessary (see below). Cuff state (deflated or inflated), initially chosen at random, was then initiated. Following at least one full 30-sec epoch of stable stage 2 sleep, a brief external mask occlusion was performed to assess UA collapsibility. An occlusion was terminated if the patient aroused during the occlusion or following 2-3 inspiratory efforts showing UA closure (Figure 2). At least 30 sec of stable stage 2 sleep without arousal was subsequently required before the next occlusion. Approximately 3-5 occlusions were conducted under the initial cuff condition before cuff state was alternated. This process continued throughout the remainder of the night to record as many multiple replicate measures of UACP as was possible under both cuff conditions during stage 2 sleep. In 4 patients, flow limitation recurred later in the night requiring a 1-2 cm H₂O increase in CPAP. In addition, 6 patients briefly moved from the supine posture due to discomfort and allowed to return to sleep. Following ~10 min of sleep, patients were awoken and asked to shift back to the supine position. CPAP was monitored and adjusted if required before mask occlusions were again undertaken once stage 2 sleep was re-established. To control for CPAP, postural and other potential sleep stage effects, all cuff deflated vs inflated comparisons were restricted to supine stage 2 sleep, where CPAP was at the same level between cuff conditions.

Data Analysis

Chest and abdominal anterior-posterior excursions (ΔAP_CHEST and ΔAP_ABDO) and pneumotachograph derived tidal volume (V_T) during the baseline wake period were calculated breath-by-breath via custom software.¹⁸ A statistical calibration method¹⁹ was employed to solve the regression constants achieving the best fit of V_T (change in lung volume from EELV to end-inspiration) versus magnetometer excursion in the following equation;

V_T (mL) = ΔEELV (mL) = M*[(K*ΔAP_CHEST (cm))+ΔAP_ABDO (cm)]

Where: K = the relative contribution of chest versus abdominal excursions and M = a scaling factor

Changes in EELV induced by external abdominal compression were calculated using the best fit regression constants K and M and the appropriate measurements of chest and abdominal displacements. ΔAP_CHEST and ΔAP_ABDO were defined as the difference between the minimum AP_CHEST and AP_ABDO dimensions (in cm) at end-expiration, for each breath in the preceding 30 sec prior to occlusions between periods with and without abdominal compression.

Respiratory data including V_T, inspiratory, expiratory and total breath time (T_I, T_E, T_TOT), breathing frequency (F_B), minute ventilation (V_I), peak inspiratory flow (PIF), end-expiratory P_GA, P_ES and P_DI, and R_UA were calculated on a breath-by-breath basis using custom analysis software used previously.^18,20 Baseline ventilatory parameters were determined by averaging breath-by-breath measures in the 30 sec prior to each occlusion. A single observer, blinded to cuff condition and P_CUFF, as well as patient and occlusion number, determined UACP. The first breath clearly exhibiting P_MASK flattening was identified for each trial. The pressure at which P_MASK flattening began was defined as the UACP (Figure 2). Trials were excluded from data analysis if UACP was not reached (e.g., due to arousal), if the occlusion occurred other than in stage 2 sleep or if the patient was not in the supine position (confirmed by video camera) during the mask occlusion.

Statistical Analysis

Data from replicate trials were averaged within each condition in each subject and the effect of cuff state (deflated and inflated) on UACP, lung volume change and respiratory parameters analyzed using Student's paired t-tests. Relationships between single variables were examined by Pearson correlation. Multivariate linear regression analyses using backwards linear regression with P values < 0.05 to enter and P values > 0.1 to remove were undertaken to determine independent predictors of UACP. Variables entered were P_GA, P_DI, BMI, waist circumference, hip circumference, waist-to-hip ratio, and AHI. All data are expressed as means ± SEM. Statistical significance was inferred when P < 0.05. Statistical analyses were performed using SPSS for Windows software version 16.0 (SPSS, Inc., Chicago, IL.).

RESULTS

Anthropometric Data

Twenty-five patients were recruited, with 15 successfully completing the study. Data from the remaining 10 patients were excluded due to inability to sleep (5 patients) or mask leak and/or oral breathing despite all efforts to prevent leaks (5 patients). Of the 15 successful studies, one patient was unable to tolerate the gastric and esophageal catheters and R_UA data from 2 patients were unavailable because of catheter blockage. Anthropometric measurements are displayed in Table 1. Patients were middle-aged, obese with severe OSA. Lung function was in the normal range for this group.

Table 1.

Anthropometric Data for 15 OSA Patients

	Mean ± SEM	Range
Age (years)	50.0 ± 2.6	33–65
BMI (kg/m2)	34.5 ± 1.1	29.7–41.6
AHI (events/h)	58.1 ± 6.8	30–114
WC (cm)	119.3 ± 3.3	104–136
HC (cm)	119.0 ± 2.8	103–130
WHR	1.0 ± 0.1	0.89–1.06
FEV1 (% predicted)	98.3 ± 3.1	82–122
FVC (% predicted)	93.7 ± 3.0	79–110

BMI = body mass index; AHI = apnea-hypopnea index; WC = waist circumference; HC = hip circumference; WHR = waist-to-hip ratio; FEV₁ = forced expiratory volume in 1 second; FVC = forced vital capacity

Effect of Abdominal Compression

Parameters recorded in the 30-sec period preceding each cuff deflation and inflation occlusion trial are presented in Table 2. CPAP was not different between cuff conditions. Abdominal cuff inflation produced a significant increase in F_B via T_E shortening. However, a concomitant V_T reduction was evident such that V_I remained unchanged with abdominal compression. There was a non-significant trend for a decrease in PIF with abdominal compression (P = 0.07).

Table 2.

Parameters Recorded in the 30-sec Baseline Period Preceding Airway Occlusion Trials with and without Abdominal Compression

	Cuff Deflated	Cuff Inflated	P value
PCUFF (cm H2O)	0	26.5 ± 1.3	< 0.001
CPAP (cm H2O)	13.2 ± 1.1	13.3 ± 1.1	0.304
TI (sec)	1.9 ± 0.1	2.0 ± 0.1	0.233
TE (sec)	2.4 ± 0.2	2.2 ± 0.2	0.023
TTOT (sec)	4.3 ± 0.2	4.2 ± 0.2	0.318
FB (breaths/min)	14.5 ± 0.6	14.8 ± 0.6	0.039
VT(L)	0.54 ± 0.02	0.52 ± 0.02	0.011
VI (L/min)	7.7 ± 0.3	7.6 ± 0.2	0.343
PIF (L/min)	43.4 ± 1.7	41.7 ± 1.7	0.070
RUA (cm H2O L/s)#	6.8 ± 1.4	6.5 ± 1.4	0.585

P_CUFF = cuff pressure; CPAP = continuous positive airway pressure; T_I, T_E, T_TOT = inspiratory, expiratory and total breath time respectively; F_B = breathing frequency; V_T = tidal volume; V_I, = minute ventilation; PIF = peak inspiratory flow; R_UA = upper airway airflow resistance.

Values are mean ± SEM. (N = 15,).

^#N = 13

An average of 16.2 ± 3.8 (range 4–62) and 15.7 ± 4.0 (range 2–64) occlusion trials with and without cuff inflation, respectively, were successfully completed during stage 2 sleep. Abdominal compression significantly increased P_GA and P_DI in the order of 50% (Figure 3A, P < 0.001 for both), while there was a trend for increased end-expiratory P_ES (4.6 ± 0.8 vs 3.2 ± 0.8 cm H₂O, P = 0.07). UACP also increased following abdominal compression (Figure 3B, 1.4 ± 0.8 vs 0.9 ± 0.9 cm H₂O, P = 0.04), but R_UA remained unchanged (Table 2, P = 0.59). Abdominal compression was accompanied by an abdominal volume shift of 1.1 ± 0.2 L (P < 0.001) and an increase in thoracic volume of 0.5 ± 0.1 L (P = 0.001), leading to an overall decrease in EELV by 0.5 ± 0.2 L (P = 0.045).

Figure 3.

The effect of external abdominal compression on (A) gastric pressure (P_GA) and transdiaphragmatic pressure (P_DI) and (B) upper airway closing pressure (UACP) Means ± SEM. (N = 14 for P_GA and P_DI and N = 15 for UACP).

Regression Analyses

Baseline (cuff deflated) P_GA was found to significantly correlate with waist circumference (r² = 0.30, P = 0.049). No variables correlated with AHI. However, baseline UACP was strongly correlated with baseline P_DI (Figure 4A) and baseline P_GA (Figure 4B), r² = 0.645 and r² = 0.572 respectively (both P < 0.001), and there was a trend for a correlation between P_GA and UACP following abdominal compression (r² = 0.24, P = 0.08). There was no correlation between the ΔUACP with either the ΔP_DI or ΔP_GA. In multivariate analyses, baseline P_DI was found to be the only independent predictor of baseline UACP (P < 0.001), accounting for 73% (r² = 0.731) of the variance in UACP.

Figure 4.

Relationship between (A) upper airway closing pressure (UACP) with transdiaphragmatic pressure (P_DI) and (B) with gastric pressure (P_GA) without abdominal compression (N = 14).

DISCUSSION

The major finding of this study was that abdominal compression significantly increased UA collapsibility during sleep in obese OSA patients. This is the first study to demonstrate a direct effect of abdominal loading on UA collapsibility in sleep, and implicates mechanical effects of abdominal obesity as a potentially important mechanism causing increased UA collapsibility in OSA.

Effect of Abdominal Compression on UA Function and Respiratory Variables

It is not possible to determine the precise mechanisms underpinning changes in UACP with abdominal compression in this study. Potential mechanisms include (a) direct mechanical effects of increased IAP and/or lung volume mediated influences on UA compliance, and/or (b) hemodynamic effects or increased edema surrounding the UA.

There are likely to be complex interactions between variables potentially mediating increased UA collapsibility following abdominal compression, because of the nature of anatomical connections between the UA and surrounding/distal tissues, the geometry of diaphragm insertion to the rib cage and variable effects of obesity and abdominal compressive forces on chest and abdominal compartment volumes and compliances. A smaller EELV seen in obese individuals in the supine position compared to healthy-weight controls²¹ is likely dominated by cranial ascent of the diaphragm as a consequence of increased IAP, with further rises in IAP promoting additional cranial displacement limited by diaphragm stretch and opposing inspiratory effects of rib cage expansion.²² In the current study, abdominal compression increased P_GA and P_DI in the order of ~50%, produced a marginal increase in P_ES and decreased the abdominal AP dimension by ~1.8 cm, with slight AP chest expansion. Given that the abdominal compartment is relatively incompressible, the reduced abdominal AP dimension with abdominal compression indicates abdominal volume redistribution, equating to a volume shift of ~1 L, of which ~0.5 L was exhaled and ~0.5 L translated to an increase in rib cage AP dimensions and volume, resulting in a net fall in EELV of ~0.5 L. Increased IAP, via external loading or CO₂ insufflation into the peritoneal cavity, leads to a rightward shift and a decrease in the slope of the pressure-volume curve of the total respiratory system, primarily via a fall in chest wall compliance.^23–25 The expansion of the rib cage following abdominal compression has been documented by others²⁶ and likely reflects lateral lower rib displacement at the zone of apposition of the diaphragm and rib cage (appositional effect) while passive tension generated by the diaphragm elevates the rib cage by its insertions at the costal margin (insertional effects)^22,26 leading to an inspiratory effect on the rib cage.

A change in EELV is known to have profound effects on UA function. Lung inflation above resting EELV increases UA cross-sectional area,^27,28 reduces airway collapsibility²⁹ and airflow resistance.⁶ Conversely, lung deflation below EELV reduces UA size^27,28 and produces marked increases in pharyngeal resistance.⁶ A study by Stanchina and colleagues²⁹ showed greater airway collapsibility (~1.1 cm H₂O increase in UA critical closing pressure, [P_CRIT]) in healthy-weight individuals following a decrease in lung volume of ~0.6 L via positive extrathoracic pressure. Using an iron lung to manipulate lung volume in a group of obese OSA patients, the level of CPAP required to abolish flow limitation increased from ~12 to ~17 cm H₂O following a ~0.6 L reduction in lung volume, and was reduced from ~12 to ~4 cm H₂O with ~0.4 L lung inflation.⁷ With similar lung inflation via negative extrathoracic pressure (~0.7 L), Tagaito and colleagues³⁰ found a reduced P_CRIT in the order of ~1.2 cm H₂O in anesthetized and paralyzed obese OSA patients. In the absence of neuromuscular influences, these latter findings strongly support mechanical effects of lung volume change on passive UA properties.

Lung volume effects on UA function may be mediated primarily by changes in caudal tracheal traction. This “tracheal tug” is an axial force pulling on the airway via negative intrathoracic pressure and movements of the trachea and interconnected mediastinal structures that move along with the diaphragm.³¹ While end-expiratory diaphragm position was not directly assessed in the present study, the observed changes in chest/abdominal AP dimensions and volumes, P_DI and P_ES are consistent with cranial diaphragm displacement and would be expected to reduce axial tension transmitted to the UA via intrathoracic structures. Classic studies in anesthetized dogs,⁴ clearly show tracheal tug is a major factor promoting UA patency. Severing the esophagus and trachea caused marked pharyngeal airway narrowing or collapse. Axial tension exerted on the caudal end of the severed trachea was very strongly related to negative intrathoracic pressure and diaphragm descent. Similar findings have subsequently been reported in cats³ and most recently in pigs.³² Caudal tracheal traction has also been shown to decrease UA collapsibility and extraluminal tissue pressure in anesthetized and tracheostomized rabbits.³³ These animal studies suggest mechanical interdependence between the diaphragm and intrathoracic and UA structures is critically important for maintaining pharyngeal patency.

While the mechanisms of lung volume influence on UA size and function remain unclear, thoracoabdominal distortion, through interventions specifically designed to alter lung volume or through abdominal compression performed in this study, appear likely to operate via similar mechanisms; predominantly via mechanical coupling between the upper and lower airway structures. Nevertheless, abdominal compression/mass loading and extrathoracic pressure induced changes in lung volume may have somewhat different effects on diaphragm position and UA function. Since the abdominal compartment is less compressible than the chest, extrathoracic pressure changes in an iron lung will tend to influence thoracic more than abdominal compartment volume and may have variable effects on diaphragm position, pleural pressure and tracheal traction. In contrast, raised IAP with abdominal compression or mass loading will likely produce predominantly diaphragm ascent, either with or without (i.e., counterbalanced by mass loading of the chest) concomitant chest expansion.

While abdominal compression led to a significant increase in UACP, there was no change in R_UA. Diaphragm ascent and UA shortening, while potentially reducing UA wall tension and increasing UA collapsibility, may have relatively little net impact on overall UA size and consequently R_UA. In support of this view, Rowley and colleagues³⁴ found no change in R_UA despite a ~2 cm H₂O decrease in UA collapsibility with 1 cm tracheal stretch in anesthetized cats.

Increased central venous volume and/or edema surrounding the airway may also contribute to increased UA collapsibility. Chui and colleagues³⁵ found an increase in neck circumference and a 102% rise in pharyngeal resistance following expulsion of leg fluid volume via lower body positive pressure (~55 cm H₂O). Two subsequent studies by the same group showed similar levels of lower body positive pressure produced a decrease in UA area by ~10%,³⁶ while UA collapsibility increased by ~20% during wakefulness.³⁷ Reduced lung volume did not appear to explain these findings suggesting that fluid displacement into the neck was the primary cause of these effects. In addition, a recent study³⁸ found that AHI was strongly correlated with changes in overnight leg fluid volume. Increased IAP (maximum of ~27 cm H₂O) via CO₂ insufflation into the peritoneal cavity has also been shown to displace blood from the abdominal compartment into the chest³⁹ and to result in enlargement of left end-diastolic ventricular volumes⁴⁰ indicative of venous congestion. Consequently, while the IAP achieved in this study was lower than in these previous studies, displacement of blood into the chest and neck cannot be discounted as a potential mechanism contributing to increased UA collapsibility with abdominal compression.

Abdominal compression significantly altered breathing patterns in these patients indicating respiratory compensatory mechanisms with abdominal loading. Both V_T and T_E significantly decreased whilst F_B increased. On the other hand, T_I and V_I were unchanged, while PIF tended to be lower following cuff inflation. Similar changes in breathing pattern have been observed in obese compared to healthy weight individuals,⁴¹ and with externally applied elastic loads during wakefulness.^42,43 Given abdominal compression impairs diaphragm descent, it may have similar effects to externally applied inspiratory elastic loads. While there is limited data available in sleep, ventilation has been shown to fall acutely with an elastic load, followed by partial ventilatory recovery in NREM sleep in three healthy-weight individuals.⁴⁴ The changes in breathing pattern following prolonged abdominal compression during sleep in this study likely reflect similar compensatory responses.

Methodological Limitations

There are several methodological limitations that warrant brief discussion. Firstly, diaphragm/trachea displacement following abdominal compression could not be directly measured and inferences regarding diaphragm and tracheal ascent are somewhat speculative, based on changes in other interrelated measures. Imaging methods such as radiography, CT scanning, and ultrasonography, potentially useful for more direct measurements of intrathoracic changes with abdominal compression are difficult during sleep. Based on a ~3 cm decrease in abdominal AP dimension and an increase in P_GA of ~23 cm H₂O, Reid et al.²⁶ inferred a 3.5-cm rise in end-expiratory diaphragm position following upright water immersion to the neck. Tokics and colleagues⁴⁵ observed ~1.2 cm cranial diaphragm displacement following thoracoabdominal restriction. Following CO₂ insufflation of the abdomen, 1.9 cm cephalad movements of the diaphragm⁴⁶ and 1.4 cm migration of the carina towards the tip of an endotracheal tube⁴⁷ have been observed. Consequently, abdominal compression almost certainly produced ascent of the diaphragm and intrathoracic structures.

The current study utilized a mask occlusion protocol^16,48 rather than the more widely used P_CRIT technique to assess UA collapsibility. This was chosen for two reasons: (1) it allows for more rapid and repeated measurements over a shorter time, and (2) pressure drops during P_CRIT determination inevitably produce systematic reductions in lung volume that may further impact on UA collapsibility that the technique is designed to measure. With inspiratory mask occlusion, lung volume is effectively maintained at the same initial pressure. Our circuit did not occlude expiration such that some expiratory lung volume loss was possible if UA patency returned with increasing expiratory drive. However, UA closure tended to occur within 1-3 breaths following mask occlusions, before any substantial increase in ventilatory drive necessary to overcome the majority of obstructive events and therefore produce expiratory volume loss.

Magnetometer coils allow measurement of lung volume change such that further studies using body plethysmography or helium dilution measurements would be useful to assess absolute lung volume with and without abdominal loading in obese and non-obese individuals. In addition, the calibration constant K used to estimate lung volume change is likely influenced by posture.⁴⁹ However, all measurements were restricted to the supine position and cuff inflated versus deflated conditions continued throughout the study such that overnight changes in K are unlikely to have importantly influenced lung volume comparisons between conditions.

The effects of acute abdominal compression may well differ from chronic mechanical effects of abdominal obesity on UA function. Increasing IAP with abdominal obesity occurs over a long time frame, potentially has different mechanical effects depending on visceral versus subcutaneous fat deposition and may be associated with other effects that may independently influence UA function, such as UA and thoracic adiposity, hormonal, metabolic and hemodynamic effects and potentially progressive respiratory compensatory changes. Nevertheless, our findings of increased airway collapsibility following acute abdominal compression demonstrate the existence of compressive effects that may well still operate with chronic natural abdominal compression with obesity.

Clinical Significance

The effect of a ~0.5 cm H₂O increase in UACP on OSA severity remains unclear. However, studies investigating the relationship between P_CRIT and AHI^50,51 suggest that changes of this order may well be important. Sforza et al.⁵⁰ found a low (r = 0.23) but significant correlation, with small differences in P_CRIT associated with substantial increases in AHI in 106 patients. In 25 OSA patients, Wellman and colleagues⁵¹ demonstrated a tighter relationship (r = 0.66), with an increase in AHI of ~10 events/h with a ~0.5 cm H₂O increase in P_CRIT. In a study by Gold et al.,⁵² the average P_CRIT in mild/moderate OSA patients (AHI ≥ 10 and < 40 events/h) and moderate/severe OSA patients (AHI ≥ 40 events/h) was approximately −1.6 and 2.4 cm H₂O respectively, although there was considerable overlap in P_CRIT between the two groups. Given the importance of UA collapsibility in OSA and relatively steep relationships between P_CRIT and AHI across patients, a ~0.5 cm H₂O within-patient increase in UACP appears likely to significantly impact OSA severity. Further studies are needed to establish if this is the case and the magnitude of the effect.

Obesity and male gender are well known major risk factors for OSA.^1,2 However, the mechanisms via which obesity and male gender influence UA in sleep remain poorly defined. While experimental abdominal compression in the current study may not directly simulate the effects of obesity per se, increased IAP appears the most likely dominant factor underpinning increased UA collapsibility in this study. Of all available variables influenced by obesity, including BMI, waist-hip ratio, and waist and hip circumference, only P_DI emerged as a significant predictor of UA collapsibility, accounting for an impressive ~73% of the variance in UACP. Consequently, compressive effects of obesity and the male propensity to an abdominal pattern of fat distribution could therefore largely underpin strong associations between obesity/male gender and OSA.

While increased neck circumference/fat deposition are known predictors of OSA severity^53,54 and could directly affect UA function, they may also co-vary with other potentially more important measures of central obesity. In the Wisconsin Sleep Cohort,² men were three times as likely as women to have OSA and six times as likely after adjusting for BMI. However, male gender was no longer predictive of OSA following adjustment for waist-hip ratio. These data are consistent with a primary underlying role of central adiposity as a cause of OSA in most patients and the gender difference in OSA prevalence. In smaller samples, observations that measures of central adiposity including waist circumference and visceral fat consistently emerge as stronger predictors of OSA severity than BMI are consistent with this view.^55,56 Reports of increased snoring and OSA in the third trimester of pregnancy, despite increased ventilatory drive from hyperprogesteronemia, are also consistent with abdominal compressive forces importantly influencing UA function in sleep.⁵⁷

Summary

This is the first study to show a direct effect of abdominal compression on UA collapsibility during sleep. The results support and extend previous work showing detrimental effects of reduced lung volume on UA patency and suggest that increased IAP with obesity may negatively impact on UA function. While IAP appears the most likely dominant factor underpinning these effects, further studies are needed to better elucidate the mechanisms behind these findings.

DISCLOSURE STATEMENT

This was not an industry supported study. Dr. McEvoy has received research support from Philips Respironics, ResMed, Fisher – Paykel, and Apnex and the use of equipment from Respironics, ResMed, and SomnoMed. Dr. Catcheside has received research support from Apnex and the use of equipment from Respironics. The other authors have indicated no financial conflicts of interest.

ABBREVIATIONS

OSA

obstructive sleep apnea

UA

upper airway

IAP

intra-abdominal pressure

EELV

end-expiratory lung volume

R_UA

upper airway airflow resistance

BMI

body mass index

AHI

apnea-hypopnea index

FEV₁

forced expiratory volume in one second

FVC

forced vital capacity

WC

waist circumference

HC

hip circumference

WHR

waist-to-hip ratio

P_ES

esophageal pressure

P_GA

gastric pressure

P_EPI

epiglottic pressure

P_MASK

mask pressure

P_DI

transdiaphragmatic pressure

AP

anterior-posterior

P_CUFF

cuff pressure

UACP

upper airway closing pressure

ΔAP_CHEST

chest excursion

ΔAP_ABDO

abdominal excursion

V_T

tidal volume

T_I

inspiratory time

T_E

expiratory time

T_TOT

total breath time

F_B

breathing frequency

V_I

minute ventilation

PIF

peak inspiratory flow

P_CRIT

upper airway critical closing pressure

CPAP

continuous positive airway pressure