Background Severe obesity causes respiratory morbidity and mortality. The impact of obesity on the mechanics of breathing is not fully understood.
Patients and methods We undertook a comprehensive observational study of lung volumes and elasticity in nine obese and nine normal weight subjects, seated and supine, during spontaneous breathing. Seated and supine total lung capacity (TLC) and subdivisions were measured by multibreath helium dilution method. Using balloon catheters, oesophageal (Poes) and gastric (Pgas) pressures were recorded. Transpulmonary pressure (PL) was calculated as mouth pressure (Pmouth)-Poes, and complete expiratory PL volume curves were measured.
Results The obese group had a body mass index (BMI) of 46.8 (17.2) kg/m2, and the normal group had a BMI of 23.2 (1.6) kg/m2 (p=0.001). Obese and normals were matched for age (p=0.233), gender (p=0.637) and height (p=0.094). The obese were more restricted than the normals (TLC 88.6 (16.9) vs 104.4 (12.3) %predicted, p=0.033; FEV1/FVC 79.6 (7.3) vs 82.5 (4.2) %, p=0.325), had dramatically reduced expiratory reserve volume (ERV 0.4 (0.4) vs 1.7 (0.6) L, p<0.001) and end-tidal functional residual capacity (FRC) was smaller (37.5 (6.9) vs 46.9 (4.6) %TLC, p=0.004) when seated, but was similar when supine (39.4 (7.7) vs 41.5 (4.3) %TLC, p=0.477). Gastric pressures at FRC were significantly elevated in the obese (seated 19.1 (4.7) vs 12.1 (6.2) cm H2O, p=0.015; supine 14.3 (5.7) vs 7.1 (2.6) cm H2O, p=0.003), as were end-expiratory oesophageal pressures at FRC (seated 5.2 (6.9) vs −2.0 (3.5) cm H2O, p=0.013; supine 14.0 (8.0) vs 5.4 (3.1) cm H2O, p=0.008). BMI correlated with end-expiratory gastric (seated R2=0.43, supine R2=0.66, p<0.01) and oesophageal pressures (seated R2=0.51, supine R2=0.62, p<0.01).
Conclusions Obese subjects have markedly increased gastric and oesophageal pressures, both when upright and supine, causing dramatically reduced FRC and ERV, which increases work of breathing.
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What is the key question?
Obesity is associated with changes of lung volumes, but the physiological origin of this is unknown.
What is the bottom line?
The main abnormalities in obesity are the transmission of the high pressures in the intra-abdominal compartment to the thorax that dramatically reduce functional residual capacity and expiratory reserve volume and oblige patients to breathe on a flatter, less efficient, part of their pressure–volume curve, increasing the work of breathing.
Why read on?
This comprehensive study, for the first time, measures the entire expiratory pressure–volume curve in spontaneously breathing and non-sedated obese subjects, explaining the increased work of breathing and analysing the relationship between intra-abdominal pressures and altered lung volumes.
The huge increase in obesity in recent decades requires urgent public health strategies for adults1–3 and children4 and a better understanding of the abnormalities of breathing by those caring for obese patients. From a respiratory perspective, it is accepted that compared with subjects with normal weight, obese subjects can have a reduced total lung capacity (TLC)5 ,6 and breathe at a lower functional residual capacity (FRC).7–10 Obesity increases work of breathing, neural respiratory drive,11 ,12 breathlessness,13 causes sleep-disordered breathing and eventually hypercapnic respiratory failure.7 ,14 ,15 However, the details of the abnormal underlying pulmonary mechanics remain to be elucidated.
Changes in lung volumes with posture are important.16–19 In normal subjects, FRC falls when changing from the seated to the supine posture. In contrast, obese subjects,8 who breathe closer to residual volume (RV) when seated, may reach closing volume of the airways, and FRC may not decrease further with recumbency.20 ,21 Obese subjects can develop intrinsic positive end-expiratory pressure (PEEPi),22 ,23 and some have a higher threshold inflation airway pressure.23 A study by Pelosi et al24 in sedated and paralysed morbidly obese subjects suggested that high intra-abdominal pressures may have an important effect on mechanical properties of the respiratory system, but the methodology used did not allow their findings on operating lung volumes to be extrapolated to spontaneously breathing subjects.
Therefore, the aim of the present study was to undertake a comprehensive study to determine the factors contributing to impaired lung mechanics in obese but otherwise healthy people in both seated and supine postures.
Patients and methods
The study was approved by King’s College Hospital local research ethics committee. We approached obese but otherwise healthy patients, usually attending for consideration of bariatric surgery, and normal subjects at King’s College Hospital to participate. Each participant gave written informed consent. None of the participants was an active smoker, three of the obese and two of the normal subjects were ex-smokers, each one of them with a smoking history of less than 10 pack-years.
The methods used in this study have been established in clinical practice;25–28 for a more detailed report on measurements of anthropometric data, lung function, dynamic compliance, pressures and electromyogram (EMG), please refer to the online supplement.
The ratio of oesophageal to mouth pressure measured during efforts against an occlusion (Poes:Pmouth) was used to verify correct placement of the oesophageal balloon catheter. It was 1.05 (0.06) seated in normal vs 1.01 (0.08) in obese subjects (p=0.299) and 0.98 (0.05) in the normal vs 0.93 (0.04) in the obese when supine (p=0.039).
Resting breathing and recording of pressure volume curves
Resting breathing was recorded for 2 min while relaxed, seated in an arm chair and for 2 min lying supine on a bed, the head resting on a pillow, wearing a noseclip, breathing through a flanged mouthpiece connected to a pneumotachograph. The subjects then performed three TLC manoeuvres through a spirometer (Morgan, Massachusetts, USA), followed by brief and stepwise occlusions and openings of the mouthpiece at different lung volumes, to obtain pressure–volume (PV) curves over the complete expiratory vital capacity (figure 1). The measurements were repeated 3–5 times when seated and 3–5 times when supine. In addition, as the spirometer provided a closed system, we were able, as the subjects moved from the seated to the supine posture, to determine changes in FRC and TLC. For this purpose, subjects performed an inspiratory capacity (IC) manoeuvre seated and, allowing several tidal breaths to adjust for the new posture, another IC manoeuvre when reclined in a chair, tilted backwards with the body horizontal. They were then made to sit upright again to perform a third IC manoeuvre. Subjects stayed connected to the mouthpiece while undergoing this manoeuvre, and this enabled the measurement of differences in IC and TLC (figure 2). The manoeuvre was repeated 2–3 times.
We analysed data from all recorded PV curves. Mean and SD are reported for normally distributed data. Correlations are reported between variables using the R2-value. Group differences were compared using an unpaired t test, and changes in parameters when changing posture from the seated to the supine were analysed with paired t tests. Fisher’s exact test was used to analyse categorical data (gender). Differences were considered to be of significance with a p<0.05.29 For a more detailed report on the sample size calculation, please refer to the online supplement.
We studied nine obese subjects (mean (SD) body mass index (BMI) 46.8 (17.2) kg/m2) and nine normal weight controls (mean (SD) BMI 23.2 (1.6) kg/m2). Three of the obese subjects and two of the control subjects were ex-smokers (<10 pack-years), but all had a normal FEV1/FVC ratio. The two groups were matched for gender, age and were similar in height. The obese group were more breathless than normals. Waist circumference correlated with the amount of fat tissue deposited in the abdominal wall (abdominal skin fold double layer vs waist circumference; R2=0.69, p<0.001; table 1).
Spirometry and lung volumes
FEV1 and FVC (L) were reduced in the obese subjects. Obese subjects had a smaller TLC, expressed as per cent predicted, and a smaller vital capacity. IC (defined as TLC minus FRC) was not different between the groups when seated. Seated FRC was reduced in the obese, both measured in litres and expressed as FRC/TLC. Although FRC was larger in the supine posture when expressed as volume (in litres) in normals, it was similar between the groups when expressed as per cent of TLC. RV in absolute volume (litres) was similar in both groups, but RV/TLC in the obese subjects was higher. Expiratory reserve volume (ERV) was significantly reduced in the obese (table 2; figure 2). Waist circumference correlated negatively with FRC (R2=0.47, p<0.01) and with TLC, expressed as per cent predicted (R2=0.41, p<0.01; figures 3 and 4).
Reduction in TLC when supine was small and similar in normal and obese groups (−0.24 (0.08) L in normal vs −0.25 (0.08) L in obese subjects, p=0.70). When supine, IC decreased only in the obese subjects and FRC remained constant in both postures in obese subjects. In normal subjects, IC increased when changing to the supine posture, despite a decrease in TLC, with a fall of approximately 500 mL in FRC with change in posture (table 2, figure 2). In contrast, IC did not change in the obese group and five obese subjects had no measurable ERV when supine.
Dynamic and static lung compliance
Tidal volume (Vt) was similar between the groups and did not change significantly with posture. Seated dynamic lung compliance, when expressed as %predicted TLC in order to correct for differing height and gender, was not different between groups. With change in posture to the supine position, dynamic compliance decreased in both groups (table 3; figures 3 and 4). A calculated mid-range slope of the static expiratory PV curves revealed no significant difference between the groups within the range of 50–60% predicted TLC, but there was reduced compliance between 60 and 70% of predicted TLC in the obese subjects, seated and supine (table 4; for individual PV curves, please review the online supplement).
End-expiratory pressures at FRC during tidal breathing
At FRC, end-expiratory oesophageal pressures were higher in the obese group when seated and supine. Both groups revealed a similar increase (mean change of 7.4 vs 8.8 cm H2O) in the mean oesophageal pressure when changing to the supine posture. End-expiratory gastric pressures were higher in the obese group, seated and supine. However, intra-abdominal pressures fell when changing from the seated posture to the supine in both groups by around 5 cm H2O. End-expiratory transdiaphragmatic pressure was not different between the two groups, sitting and supine, and was consistent with pressure equilibration between the abdominal and thoracic compartment in supine posture. Transpulmonary pressures were significantly lower at end-expiration in obese subjects, but fell with recumbency by a similar amount in both groups (table 3).
Pressures during maximal inspiratory effort
Pressure changes associated with full lung inflation (IC manoeuvre) revealed no significant differences between the two groups in intrathoracic (Poes), intra-abdominal (Pgas) or transdiaphragmatic (Pdi) pressures. However, the transpulmonary pressure gradient was reduced in the obese group at TLC when seated and supine (table 4).
Respiratory muscle tests
There was a moderate positive correlation between end-expiratory gastric pressure and waist circumference (R2=0.52 seated, R2=0.60 supine, p<0.01). Similarly, the BMI was positively correlated to end-expiratory gastric pressure, seated (R2=0.43, p<0.01) and supine (R2=0.66, p<0.01). End-expiratory gastric pressure was negatively correlated with FRC (R2=0.59 seated, R2=0.67 supine, p<0.01) and ERV (R2=0.47 seated, R2=0.28 supine, p<0.01; both in percent of TLC), and therefore the more obese patients had higher gastric pressures and lower FRC and ERV.
End-expiratory oesophageal pressures were related to end-expiratory gastric pressures (R2=0.48 seated; R2=0.68 supine, p<0.01) and, therefore, also correlated to waist circumference (R2=0.48 seated; R2=0.61 supine, p<0.01) and BMI (R2=0.51 seated; R2=0.62 supine, p<0.01).
The main findings of the current study are that obese people, particularly when supine, have raised gastric and oesophageal pressures and associated dramatic reductions of FRC and ERV. The high oesophageal pressure imposes a threshold load on inspiration. The obese individual has the option of breathing at low lung volumes, with limited tidal volume, or increasing Vt by adopting a breathing position on a higher part of the PV curve. The reduced compliance when breathing at lower volumes, as well as the inspiratory threshold load, increase the work of breathing, reflected in elevated levels of neural respiratory drive.12
Increased intra-abdominal pressures cause a threshold load on the diaphragm at end-expiration that needs to be overcome prior to any diaphragmatic movement. This leads to higher than normal intrathoracic pressures in obese subjects, particular at end-expiration when transdiaphragmatic pressures indicate a relaxed diaphragm, and it increases further with supine posture. High oesophageal pressures are associated with low FRC and reduced ERV in obesity as they diminish transpulmonary pressures during tidal breathing.
Postural changes in intra-abdominal and intrathoracic pressures become more important in obesity due to reduced ERV and the higher threshold load on the diaphragm. Work of breathing in obesity, which is already high when seated, further increases with recumbency, caused by a disadvantageous impact of gravity. There is equilibration of the high intra-abdominal with intrathoracic pressures because the diaphragm is relatively inactive (table 3).
Significance of the findings
Previously, our group studied neural respiratory drive in obesity and found it to be raised.12 In that study, we also measured oesophageal and gastric pressures, seated and supine, confirming increased levels of gastric and oesophageal pressures in wakeful breathing subjects, but the study did not measure lung volumes or transpulmonary pressures.
Data on oesophageal pressures and spirometry in wakeful spontaneously breathing overweight and obese subjects have been published by Owens et al.31 Although their subjects were less obese (BMI 33.3 (5.7) kg/m2), they concluded that oesophageal pressure can be reliably measured in the seated and supine posture. However, they did not measure PV curves, abdominal pressures and lung compartments. In this context, it is of interest that Washko et al19 also assessed the change in transpulmonary pressure in healthy normal subjects that was associated with change in posture from the seated to the supine. They found that PL decreases by 7.0 cm H2O, in agreement with our finding that PL decreases by 7.4 cm H2O with change in posture in the normal group and by 8.8 cm H2O in the obese subjects.
Behazin et al23 studied obese and normal subjects supine, anaesthetised and paralysed perioperatively. They measured Poes at relaxation volume (Poes, rel) and found it to be above atmospheric pressure, 12.5 (3.9) cm H2O in the obese and 6.9 (3.1) in the normal (p<0.0001) groups, comparable pressure levels to our findings in wakeful subjects breathing at FRC, supine (table 4). Similarly, the gastric pressures of the obese group in their study were within the range of our observations considering that our obese group had a slightly higher BMI (11.5 (2.8) cm H2O in their data compared with 14.3 (5.7) cm H2O in obese subjects supine at FRC in our study).
Intra-abdominal hypertension has been identified as an important issue in obesity that potentially impacts on ventilation in the perioperative setting.32 ,33 Pelosi et al24 investigated the respiratory system in sedated and paralysed morbidly obese subjects. They included eight subjects (BMI 48.7 (7.8) kg/m2) with a similar age (38 (12) years) to our groups and compared respiratory mechanics in supine posture with a historic normal control group. FRC was remarkably reduced in obesity. Changes in mechanical properties secondary to reduced lung volumes were found to be caused by an excessive and unopposed intra-abdominal pressure (24.0 (2.2) cm H2O), as measured with a transurethral bladder catheter and the bladder being filled with 100 mL of saline solution. However, the study design24 did not allow them to measure lung volumes simultaneously during wakeful breathing nor did it consider the upright posture. Our study analysed spontaneous respiratory muscle function opposing the high intra-abdominal pressure in non-sedated and non-paralysed spontaneously breathing obese subjects, seated and supine.
Our data confirm differences in compliance related to posture23 ,34 and differences in lung volumes associated with obesity and posture.8 ,12 ,19 The mid-range compliance at 50–60% of TLC was not different between the groups, but tended to fall with recumbency. At a higher lung volume of 60–70% TLC, the compliance was reduced in obese subjects, seated and supine, and tended to fall in this group with recumbency. The difference between the groups was explained, to some extent, by the plateau of the PV curve in the restricted obese subjects when approaching TLC. However, a reduced compliance with change in posture to the supine might be caused by multiple factors, including a drop in lung volumes, the increased impact of abdominal pressures on the thoracic cavity, a change in the chest configuration and an increased venous return. These results provide a likely explanation why patients with obesity benefit from CPAP when supine12 ,35; CPAP counterbalances the high intrathoracic and intra-abdominal pressures and elevates the FRC levels. However, questions regarding the proposed model of lung ‘hypoinflation’ in obesity remain,16 ,18 and further larger studies distinguishing between obese subjects with and without restriction may provide additional insight into the pathophysiological origin of intra-abdominal hypertension and its impact on respiratory function and symptoms in obesity. The variability of the relationship between static and dynamic compliance in obese subjects requires further investigations, including whether or not it could be caused by chronic changes to the small airways or lung parenchyma.
The impact of obesity, particularly morbid obesity, on the respiratory system has long been observed in the clinical setting. Obese subjects are more breathless and at risk of developing respiratory failure by day and sleep-disordered breathing by night compared with their matched peer group. Our findings set out the importance of obesity in the clinical setting in the fields of respiratory, sleep and critical care medicine. In particular, the negative effect of the supine posture should be considered when assessing the bed-bound patient or deciding ventilator settings.
Hypothetically, it could be speculated that interventions that reduce intra-abdominal pressures would improve respiratory function in the obese, with an impact on sleep-disordered breathing, breathlessness and respiratory failure, as well as reducing perioperative risks.
Our findings may also provide an explanation for an observation that occurs with increasing frequency in our clinical practice. Specifically the authors have seen overweight patients with seated hypoxia and restrictive defects where the a-A gradient narrows with exercise. We speculate that such patients are moved, as the minute ventilation increases, to a steeper part of the PV curve, thus improving ventilation–perfusion matching. This is consistent with the findings by O'Donnell et al that the exercise capacity of severely obese patients is less impaired than expected.9 Such findings are important in the context of exercise rehabilitation programmes for patients with severe obesity.
Critique of the method
Careful matching is essential in studies with small groups. We sought to compare similar groups with regard to age, gender and height. There were small differences in lung volumes, and it could be argued that expressing all lung volumes as per cent predicted could be more helpful for data presentation. However, this is difficult because there are no standard reference volumes for supine posture that could have been used. We have therefore chosen to describe volumes in absolute units (L) and, where appropriate, in per cent predicted. Nonetheless, we appreciate that the gender difference in lung volumes, with lower expected TLC in females, may have led to the assumption that there is no gender difference in dynamic compliance between our groups. To address this limitation for which our study was not powered, we have presented the PV slopes for each individual male and female subject (see online supplementary figures E1 and E2). We accept that larger studies may be required to fully address the relationship between obesity and dynamic compliance. In addition, extreme or morbid obesity has not been explicitly considered when generating reference equations for lung volumes and the current obesity rates in the UK would impact on what is considered ‘normal lung function’; approximately 25% of adults in the UK are obese. This explains why existing reference equations might need to be interpreted with caution if they have not been updated; the respective cohort (eg, ECCS) might have evolved, an effect called the ‘cohort effect’.
This study focused on pressure gradients as the driving force for lung inflation. To our knowledge, absolute pressures and pressure gradients do not require correction or normalisation in a different way than has been achieved by matching our groups and, therefore, the impact of small differences between the groups in height and lung volumes may be less important.
The measurement of PImax is a volitional manoeuvre and the results, indicating that obese subjects may have been weaker, have to be interpreted with caution, particularly because previous studies failed to show a difference.12 In the current dataset, although obese subjects were weaker than expected, they were not weak compared with published data.25 ,30 The PV curves indicated available pressure generation capacity when TLC was reached in the obese, which makes it unlikely that restriction is caused by weakness. Therefore, the specific cause for the restriction in TLC observed in the obese remains unclear.
Increased intra-abdominal pressure and the consequent increased intrathoracic pressure in obese subjects reduce FRC and ERV. In consequence, patients must either limit Vt or breathe on a less compliant part of the PV curve, thereby increasing their work of breathing, which is already elevated due to the inspiratory threshold load caused by high intrathoracic pressures. The reduced FRC and ERV is an important abnormality of pulmonary mechanics in obesity.
The clinical management of severely obese patients is helped by our increased understanding of intra-abdominal hypertension and the associated reduced lung volumes.
We gratefully acknowledge the support and help of Mr Simon Ward and Mark Unstead, Lung Function Laboratory, Royal Brompton Hospital.
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.
Files in this Data Supplement:
- Data supplement 1 - Online supplement
Contributors Involvement in the conception, hypotheses delineation and design of the study: JS, MIP and JM. Acquisition of the data or the analysis and interpretation of such information: JS, AL, MIP and JM. Writing the article or substantial involvement in its revision prior to submission: JS, NH, MIP and JM.
Funding The research was supported by the National Institute for Health Research (NIHR) Biomedical Research Centre based at Guy’s and St Thomas’ NHS Foundation Trust and King’s College London. MIP's salary is part funded by the NIHR Respiratory Biomedical Research Unit at the Royal Brompton and Harefield NHS trust and Imperial College.
Competing interests None.
Ethics approval King's College Hospital, London Local Research Ethics Committee.
Provenance and peer review Not commissioned; externally peer reviewed.
Data sharing statement The raw data recordings are stored at King's College Hospital and have been accessed by all coauthors for analysis.