Lung volume and pharyngeal stability in sleeping humans: the knee bone is connected to the thigh bone

Abstract

INVITED EDITORIALLung volume and pharyngeal stability in sleeping humans: the knee bone is connected to the thigh bonePeter R. EastwoodPeter R. EastwoodWest Australian Sleep Disorders Research Institute, Department of Pulmonary Physiology, Sir Charles Gairdner Hospital and School of Anatomy & Human Biology, University of Western Australia, Nedlands, AustraliaPublished Online:01 Oct 2010https://doi.org/10.1152/japplphysiol.00838.2010This is the final version - click for previous versionMoreSectionsPDF (36 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations in 1988 the Journal of Applied Physiology published a seminal article by William Van de Graaff (13) demonstrating that inflation of the thorax in anesthetized dogs decreased upper airway resistance independently of upper airway muscle activity. The mechanism underlying this effect was shown to be caudal inspiratory traction on the upper airway transmitted from the thorax via ventrolateral cervical soft tissue structures including the trachea. Van de Graaff recognized that although an increase in lung volume might favor upper airway stability, the converse would also apply. That is, upper airway patency could be impaired via decreased caudal traction in individuals breathing at low lung volumes, such as those with obesity, particularly when recumbent and asleep.Many studies have since examined the effect of lung volume on collapsibility of the human upper airway. In general, they show a similar pattern of response: an increase in lung volume is accompanied by decreased pharyngeal collapsibility, increased pharyngeal area, and decreased pharyngeal resistance (1, 3, 6, 7, 12). These changes appear to translate into therapeutic benefits in individuals with obstructive sleep apnea as elevation of end-expiratory lung volume (EELV) using negative chest wall pressure decreases the severity of sleep-disordered breathing and the magnitude of positive airway pressure required to eliminate upper airway flow limitation (4, 5). However, although these studies point to a positive effect of increasing EELV on pharyngeal mechanics, it has proven challenging to clearly separate neuromuscular and other influences on the upper airway from any direct mechanical effects related to changes in lung volume. Furthermore, between-study differences in methods of assessing collapsibility and conditions of measurement (e.g., awake, asleep, anesthetized) have meant that it is difficult to determine the importance of lung volume on pharyngeal collapsibility relative to these other influences.The current gold-standard method for measuring collapsibility of the passive upper airway in sleeping humans was originally described by Schwartz et al. (10) in 1988. The technique requires application and maintenance of continuous positive airway pressure, usually via a nasal mask, at a level sufficient to abolish inspiratory airflow obstruction and thereby induce a state of relative muscle hypotonia (9). Intermittently, mask pressure is abruptly reduced over a range of positive and, where necessary, negative pressures to produce variable degrees of upper airway obstruction for three to five breaths before being returned to the “maintenance” pressure level. Because muscle hypotonia persists for several breaths after reduction of mask pressure, any resultant flow limitation reflects the mechanical changes in upper airway behavior independently of neuromuscular influences (i.e., its “passive” behavior). By performing multiple pressure drops and examining the relationship between inspiratory flow and pressure, the “critical” pressure at which flow is abolished can be identified (Pcrit). Despite this technique becoming widely used for measuring upper airway collapsibility in sleeping humans, the use of Pcrit to assess the effect of lung volume change is confounded by changes in lung volume that accompany each pressure drop. Indeed, the magnitude of decrease in EELV can be substantial, being related to the magnitude of the pressure drop (8).In this issue of the Journal of Applied Physiology, Squier et al. (11) report a novel method of measuring Pcrit under conditions where EELV does not change during pressure drops. By having volunteers sleep supine in a head-out rigid shell, albeit with some pharmacological assistance, the investigators were able to adjust extrathoracic pressure to match nasal mask pressure and maintain a fixed pressure difference across the respiratory system, thereby ensuring that, regardless of magnitude of a pressure drop, all measurements of inspiratory flow were obtained at each subject's sleeping functional residual capacity (FRC). Comparison of the Pcrit derived under these conditions to the Pcrit derived using the conventional technique (in which lung volume varies with mask pressure) revealed differences between the two methods that could be largely attributed to differences in lung volume. Specifically, those individuals requiring application of a negative mask pressure to elicit flow limitation (i.e., those with a negative conventional Pcrit) had a more negative Pcrit under isovolume conditions, reflecting a stiffer, less collapsible pharynx. This was attributed to the relatively higher lung volume at which Pcrit was measured in the isovolume versus the conventional method. The subjects in this study, being a group of healthy, lean volunteers, all had a negative conventional Pcrit. The authors argue, in contrast, that individuals with a positive conventional Pcrit would have an increased isovolume Pcrit, due to the conventional Pcrit being measured at a higher lung volume than the isovolume method. Although this is a reasonable speculation, it requires validation in obese patients with obstructive sleep apnea, who would be expected to have a positive Pcrit.Having established a technique by which to control lung volume during Pcrit measurements, Squier et al. (11) then used this methodology to systematically assess the effect of change in absolute lung volume on Pcrit during sleep. In each of their 18 subjects, isovolume Pcrit was measured when EELV was held at FRC (by matching extrathoracic and mask pressure), elevated (by maintaining extrathoracic pressure systematically more negative than mask pressure), or reduced (by maintaining extrathoracic pressure systematically less negative than mask pressure). For the group, overall Pcrit decreased by 2.0 ± 0.2 cmH2O for each 1.0-liter increase in EELV. The magnitude of this response was independent of sex, intrinsic collapsibility (conventional Pcrit), body mass index, and neck, waist, or hip circumference. However, the investigators noted a relatively strong relationship between the magnitude of the response and respiratory system compliance such that individuals with a less compliant respiratory system had greater Pcrit responses to changes in lung volume. It is possible that a less compliant respiratory system produces greater changes in axial airway tension and Pcrit when the lungs inflate.This is a technically challenging study, and Squier et al. (11) should be congratulated for successfully undertaking it. Their findings provide clear evidence that the collapsibility of the passive upper airway varies inversely with EELV during sleep. They provide a robust measure of the magnitude of this effect and explain the variability in magnitude of response between individuals by examining differences in respiratory system compliance. It is tempting to speculate that obese individuals, who might be expected to breathe at low lung volumes and have decreased respiratory system compliance (2), could experience substantial improvements in pharyngeal stability by increasing EELV.DISCLOSURESNo conflicts of interest, financial or otherwise, are declared by the author(s).REFERENCES1. Begle RL , Badr S , Skatrud JB , Dempsey JA. 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J Appl Physiol 65: 2124–2131, 1988.Link | ISI | Google ScholarAUTHOR NOTESAddress for reprint requests and other correspondence: P. R. Eastwood, West Australian Sleep Disorders Research Institute, Dept. of Pulmonary Physiology, Sir Charles Gairdner Hospital, Nedlands, Western Australia 6009 (e-mail: Peter.[email protected]wa.gov.au). Download PDF Previous Back to Top Next FiguresReferencesRelatedInformation More from this issue > Volume 109Issue 4October 2010Pages 949-950 Copyright & PermissionsCopyright © 2010 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.00838.2010PubMed20671037History Received 25 July 2010 Accepted 26 July 2010 Published online 1 October 2010 Published in print 1 October 2010 Metrics