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Original Research: LUNG FUNCTION TESTING |

Waist-to-Hip Ratio Is Associated With Pulmonary Gas Exchange in the Morbidly Obese* FREE TO VIEW

Gerald S. Zavorsky, PhD; Juan M. Murias, MSc; Do Jun Kim, MSc; Jennifer Gow, MSc; Jean-Loup Sylvestre, MSc; Nicolas V. Christou, MD, PhD
Author and Funding Information

*From the Departments of Anesthesia (Dr. Zavorsky, Mr. Murias Mr. Kim, and Ms. Gow) and Surgery (Mr. Sylvestre and Dr. Christou), Bariatric Clinic, McGill University Health Center, Royal Victoria Hospital, Montreal, QC, Canada.

Correspondence to: Gerald S. Zavorsky, PhD, Assistant Professor, Department of Anesthesia, McGill University Health Center, Montreal General Hospital, 1650 Cedar Ave, Room D10–144, Montreal, QC, Canada H3G 1A4; e-mail: gerald.zavorsky@mcgill.ca



Chest. 2007;131(2):362-367. doi:10.1378/chest.06-1513
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Published online

Backround: Morbidly obese individuals (ie, body mass index [BMI], ≥ 40 kg/m2) may have a pulmonary gas exchange impairment due to the large fat mass surrounding their abdomen.

Purpose: To examine the effect of the waist-to-hip (W/H) ratio on pulmonary gas exchange in the morbidly obese.

Methods: Twenty-five morbidly obese individuals (mean [± SD] age, 39 ± 10 years; mean BMI, 49 ± 7 kg/m2; mean body fat, 50 ± 6%; mean waist circumference, 135 ± 15 cm; mean W/H ratio, 0.97 ± 0.11) scheduled for bariatric surgery were recruited. Arterial blood was sampled in duplicate after 5 min of rest sitting upright.

Results: The mean Pao2 at rest was 88 ± 7 mm Hg (range, 72 to 108 mm Hg), the alveolar-arterial oxygen pressure difference (P[A-a]O2) was 19 ± 9 mm Hg (range, 1 to 37 mm Hg), and the Paco2 was 38 ± 3 mm Hg (range, 32 to 44 mm Hg). Linear regression showed that 32% and 36%, respectively, of the variance in the P(A-a)O2 and Pao2 were explained by the W/H ratio (p < 0.004 for both). As well, 20% of the variance in Paco2 was explained by the W/H ratio (p = 0.02). Men had larger W/H ratios (p < 0.01) and poorer gas exchange (p = 0.06) compared to women (mean difference: Pao2, −7 mm Hg; P[A-a]O2, 6 mm Hg).

Conclusion: Morbidly obese men showed a trend to have poorer pulmonary gas exchange compared to morbidly obese women, and a significant part of the blood gas status in these patients is associated with the W/H ratio.

Figures in this Article

Pulmonary gas exchange may be affected by morbid obesity. Morbidly obese individuals (ie, body mass index [BMI], ≥ 40 kg/m2) have poorer exercise capacity and may also have poorer pulmonary gas exchange compared to healthy, nonobese counterparts because of the added energy needed to move fat mass.1The increase in mechanical ventilatory constraints and lower lung volumes from large amounts of abdominal fat causes poor lung function and is thus one exercise-limiting factor in morbidly obese individuals.2The decrease in lung volumes, specifically expiratory reserve volume (as an index of decreased functional residual capacity) is a cause for poor gas exchange in the lung.3

A pulmonary gas exchange impairment at rest may be a prognostic marker for postoperative pulmonary complications. Very few studies have examined pulmonary gas exchange in morbidly obese persons, and those studies have had varied results. Some4 have shown that Pao2 and Paco2 remain normal at rest in the morbidly obese, while others,3,56 have shown mild hypoxemia (Pao2, approximately 78 to 83 mm Hg) with normal Paco2 values at rest. However, those studies have provided mean arterial blood gas values and did not provide the individual responses of pulmonary gas exchange in the obese. Indexes of obesity, such as BMI, total body weight, body fat percentage, and waist-to-hip (W/H) ratios, may be related to gas exchange impairments in the morbidly obese, and knowing the individual data in these studies would allow a dissection of the relationship between the magnitude of obesity and the gas exchange impairment.

An attempt has been made to investigate the effect of W/H ratio on pulmonary gas exchange in the morbidly obese. A large W/H ratio indicates that a substantial portion of fat mass is surrounding the thorax, which could lead to ventilation-perfusion abnormalities and an increase in the alveolar-arterial oxygen pressure difference (P[A-a]O2) while lowering the Pao2. Consequently, the purpose of this study was to examine the effect of obesity, as depicted by W/H ratios, on P(A-a)O2 and Pao2. Our hypothesis was that, as a group, morbidly obese men would have a larger W/H ratio compared to morbidly obese women, and that those with a higher W/H ratio at rest would show poorer pulmonary gas exchange at rest compared to those with a lower W/H ratio.

Each subject was required to participate in one testing session

Subjects

Twenty-five morbidly obese individuals (mean [± SD] age, 39 ± 10 years; mean BMI, 49 ± 7 kg/m2; mean body fat proportion, 50 ± 6%; mean waist circumference, 135 ± 15 cm; and mean W/H ratio, 0.97 ± 0.11) who were scheduled for bariatric surgery were recruited. These individuals were community-dwelling, ambulatory persons who were scheduled for laparoscopic weight reduction surgery. Twenty individuals also had normal lung function, as determined by spirometry (ie, FEV1, > 80% predicted,7 and normal FEV1/FVC ratio or FVC of > 0.70). Five subjects did not meet the criteria for normal spirometry (FEV1, 67 to 79% predicted; and FEV1/FVC ratio, 58 to 65% predicted). Also, five subjects were below the lower limit of normal (LLN) for FEV1,,7 and two of those five subjects also had FVC values below the LLN. Therefore, seven subjects in total did not have an FEV1 of > 80% predicted,7 or an FEV1/FVC ratio of > 0.70, or were below the LLN for either FEV1 or FVC. Excluded from the population of the morbidly obese were individuals with (1) BMI ≥ 70 kg/m2; (2) respiratory, renal, or hepatic failure; (3) metastatic disease; (4) senility, Alzheimer disease, or other dementias; and (5) the inability to comprehend the instructions during tests. All subjects signed an informed consent form. This study was approved by the Research Ethics Board of the McGill University Health Centre.

The cardiopulmonary variables oxygen consumption (V̇o2), minute ventilation, carbon dioxide production, respiratory exchange ratio, and the concentration of mixed expired CO2 were assessed at rest with a metabolic cart (model VMax 229LV; SensorsMedics; Yorba Linda, CA) using the breath-by-breath option. The mean of the 5-min values (averaged over 20-s intervals) was used in the calculations. Heart rate was recorded using a three lead ECG (Cardiocap/5; Datex Ohmeda; Louisville, CO).

Body Composition, Venous Blood Samples, and Arterial Cannulation

Before measuring the resting V̇o2, height, weight, and body composition were assessed. Lean and fat mass were measured from an 8 polar bioelectrical impedance device that has been validated for the morbidly obese.8 Venous blood hematocrit, progesterone and hemoglobin levels, WBC count, RBC count, fasting blood glucose level, and glycosylated hemoglobin concentration, along with a complete lipid profile were measured in each subject. Then, after performing an Allen test, arterial cannulation of the radial artery was performed by an anesthesiologist under local anesthesia (2% lidocaine) using a 20-gauge 1.25-inch length needle (Cathlon Clear Needle; Johnson & Johnson; Arlington, TX).

Arterial blood gases were measured after the patient had rested for 5 min, sitting upright on a chair. The average of the duplicate samples was recorded. All blood gas samples were corrected for changes in arterial blood temperature. A rapid-response, polytetrafluoroethylene (Teflon; Dupont; Wilmington, DE)-coated thermocouple (IT-18; Physitemp Instruments; Clifton, NJ) passed through the rubber part of the extension set (Interlink, Y type, model number JC6613; Baxter Healthcare Corp; Deerfield, IL) and was positioned in the hub of the radial artery catheter. A three-way stopcock was connected to a rubber extension set (Interlink; Baxter Healthcare Corp), and the other end was connected to an IV extension line and saline solution flush fluid transducer (Transpac IV Monitoring Kit; Abbott Laboratories; North Chicago, IL). The catheter, extension set, and stopcock were routinely flushed with heparinized saline solution. Prior to obtaining each arterial blood gas sample, 5 mL of arterial blood was rapidly withdrawn to eliminate the dead space and to see blood temperature increases (5-mL Luer-Lok Tip; Becton-Dickinson; Franklin Lakes, NJ). The highest recorded temperature seen from the thermocouple during this withdrawal was recorded as the arterial blood temperature. Immediately after the 5-mL withdrawal, another 2 mL was withdrawn for actual blood gas analysis using a special syringe (Arterial Blood Sample Syringe, with dry lithium heparin for gases and electrolytes; SIMS Portex Inc; Keene, NH). These blood gas samples were withdrawn over a 10-s period to reduce the fluctuations of blood gas tensions over a given respiratory cycle. Any bubbles were expelled within 5 s of sampling. The samples were stored on ice and analyzed within 10 min of sampling.

Arterial blood Po2, and Pco2 were measured directly with a blood gas analyzer (ABL725 Blood-Gas Analyzer; Radiometer; Copenhagen, Denmark). Arterial oxygen saturation was also directly measured on the analyzer (ABL725; Radiometer) using cooximetry (ie, multiwavelength oximetry). The ideal alveolar gas equation was used to calculate Pao2 such that the P(A-a)O2 could be calculated.9 The ratio of the physiologic dead space (ie, the sum of the anatomic and alveolar dead space) to tidal volume was calculated as (Paco2 − PECO2)/Paco2, where PECO2 is the partial pressure of mixed expired CO2 and was calculated as the barometric pressure taken as 760 − 47 mm Hg (water vapor pressure) multiplied by the concentration of mixed expired CO2.

Statistical Analysis

Linear regressions were performed between the dependent variables P(A-a)O2, Pao2, and Paco2, and the W/H ratio. As well, linear regressions were performed between the same dependent variables and waist circumference and BMI. A two-sided, two-sample t test of means was used to compare predicted spirometry parameters with the measured values. As well, since we assumed a priori that morbidly obese men would have a larger W/H ratio compared to morbidly obese women, a one-sided, two-sample t test of means was used to compare Pao2, P(A-a)O2, Paco2, and the W/H ratio between genders. The 95% confidence interval of the mean difference between genders was included, too. The data were analyzed using a statistical software package (MedCalc, version 7.3.0.1; MedCalc Software; Mariakerke, Belgium). Statistical significance was declared when p < 0.05.

Subject Characteristics

Table 1 describes the subject characteristics and lipid profile of the 17 morbidly obese women and 8 morbidly obese men. Metabolic syndrome, defined by the patient having at least three of five clinical markers listed in the National Cholesterol Education Program Adult Treatment Panel III report,10 was diagnosed in 12 of 25 patients (6 men, 6 women). Seven subjects were superobese (ie, BMI, ≥ 50 kg/m2). The mean Pao2 at rest was 88 ± 7 mm Hg, the mean P(A-a)O2 was 19 ± 9 mm Hg, and the mean Paco2 was 38 ± 3 mm Hg. The variance in the W/H ratio explained 32% of the variance in P(A-a)O2 and 36% of the variance in Pao2 (p < 0.004) [Fig 1, 2 ]. The variance in the W/H ratio explained 20% of the variance in Paco2 (p < 0.05) [Fig 3 ]. The men tended to have poorer pulmonary gas exchange due to their larger W/H ratio compared to women (Fig 123). There was a significant relationship between the waist circumference and pulmonary gas exchange, but the r2 was less compared to using the W/H ratio (P[A-a]O2 vs waist circumference r2 = 0.18; Pao2 vs waist circumference r2 = 0.27; Paco2 vs waist circumference r2 = 0.16; p ≤ 0.05 for all). However, there was no significant relationship between BMI and P(A-a)O2, Pao2, or Paco2 (r2 = 0.0 for all).

There was a significant difference in the mean W/H ratio (men, 1.08 ± 0.07; women, 0.93 ± 0.10; p < 0.01) and a nearly significant difference in pulmonary gas exchange between genders. Specifically, the mean difference for Pao2 was −7.3 mm Hg compared to women (95% CI of the difference, −17.0 to 2.4; p = 0.06), the mean difference for P(A-a)O2 was 6.2 mm Hg compared to women (95% CI of the difference, −1.8 to 14.1; p = 0.06), and the mean difference for Paco2 was 0.8 mm Hg compared to women (95% CI of the difference, −3.7 to 2.0; p = 0.27) between genders.

The purpose of this study was to examine the effect of the W/H ratio on pulmonary gas exchange in morbidly obese persons at rest. We found that the men had larger W/H ratios compared to women, and that it explained a large part of the variance in pulmonary gas exchange (Fig 123). Furthermore, the obese men tended to have worse gas exchange compared to obese women.

Due to the limited number of men sampled in this study, we have reported near significance in Pao2 and P(A-a)O2 between genders (p = 0.06 for both [one-tailed]). As 1 −(p/2) is the probability that the true effect is positive, then the probability that Pao2 is lower and P(A-a)O2 is higher in men compared to women is 1 − (0.12/2) = 0.94 or 47:1, which are pretty good odds.

There were other variables that may have been associated with pulmonary gas exchange, such as waist circumference and BMI. The waist circumference may actually be a better predictor of gas exchange impairment in morbidly obese individuals because the waist circumference reflects the amount of fat mass surrounding the abdomen. The abnormally high P(A-a)O2 and low Pao2 may be attributed to ventilation-perfusion abnormalities, as the lower portions of the lung have been found to be underventilated and overperfused in obese individuals.11 Since the expiratory reserve volume is commonly reduced in obese persons, it follows that the obese person breaths closer to residual volume. Therefore, when seated upright, ventilation to lower lung zones is impaired, resulting in abnormally low ventilation-perfusion ratios11; those with large waist circumferences could have larger mismatching between ventilation and perfusion and more atelectasis compared to those whose waist circumference is smaller. Vaughan et al3 have demonstrated that as waist circumference decreased in morbidly obese patients, the P(A-a)O2 decreased (r2 = 0.35; p < 0.05), meaning that pulmonary gas exchange is related to abdominal obesity. As well, they showed a significant relationship between changes in expiratory reserve volume and Pao2 (r2 = 0.35) and P(A-a)O2 (r2 = 0.58), demonstrating that as expiratory reserve volume increased from surgical weight loss due to the reduction in waist circumference, gas exchange improved.,3

However, while there were significant relationships between pulmonary gas exchange and waist circumference, they were not as strong as the relationship between pulmonary gas exchange and W/H ratio. We can only speculate as to why this is. Perhaps a large fat mass surrounding the hips offers protective effects against the abdominal fat mass such that the gas exchange impairment is reduced. In fact, a large fat mass surrounding the hips may help to keep the abdominal fat mass from sagging toward the ground. A sagging abdominal fat mass may result in more atelectasis and ventilation-perfusion mismatching compared to a nonsagging abdominal fat mass. Typically, women have more of a gynoid-shaped physique in which the fat mass is concentrated around the hips, while men tend to have a more android-shaped physique in which the fat mass is concentrated around the abdomen. From Figures 123, it can be seen that if one has a large fat mass surrounding the abdomen but also a large fat mass surrounding the hips and thighs (ie, women), the gas exchange impairment is not as severe. As to the reason why BMI is not associated with pulmonary gas exchange impairment, it could be that height has particular protective effects, too. In fact, 65% of the variance in height in our obese subjects could be explained by FVC (p < 0.001), and a large FVC indicates that there should be a larger surface area for oxygen diffusion through the alveolar-capillary membrane, especially in the upper part of the lung. This would compensate for the lower portions of the lung, which are underventilated and overperfused in obese individuals.11 However, a post hoc analysis showed that there was no relationship of height or FVC to pulmonary gas exchange in our subjects.

We would assume that morbidly obese individuals would have worse gas-exchange problems lying down compared to sitting upright. In the supine position, both chest wall and abdominal fat will, without doubt, result in a reduction in functional residual capacity between the sitting and the supine position. Functional residual capacity is reduced in nonobese healthy people going from the sitting to the supine position, which is well known, and the effects will be greater in obese people. This may well lead to airway closure during tidal breathing in these types of patients, which will result in additional hypoxemia and an increase in P(A-a)O2. Airway closure will probably reduce alveolar ventilation of alveoli distal to those closed airways, causing ventilation-perfusion inequality, and, if they are severe, may even result in alveolar collapse beyond the closed airways, causing a shunt to develop.

Some studies have reported that morbid obesity is associated with an abnormally high P(A-a)O2 at rest (> 15 mm Hg).3,5,12 Other studies3,56 have shown that some obese patients have mild hypoxemia (Pao2, approximately 78 to 83 mm Hg) with normal Paco2 values at rest, while in morbidly obese patients who are diagnosed with respiratory insufficiency (either obstructive sleep apnea or obesity-hypoventilation syndrome) severe hypoxemia has been observed with profound hypercapnia.,1314 None of our morbidly obese subjects had respiratory insufficiency, as the Paco2 values in all subjects were < 47 mm Hg at rest.

In conclusion, morbidly obese men tend to have poorer pulmonary gas exchange compared to morbidly obese women, and a significant part of the blood gas status in these patients is associated with the W/H ratio. There was both an oxygenation problem, as reflected by the P(A-a)O2 and Pao2 values, and a minor ventilatory constraint, as reflected by the Paco2 values, which was related, in part, to the W/H ratio. The waist circumference explained a small part of the variance in pulmonary gas exchange between morbidly obese subjects, but the W/H ratio explained a larger part of the variance. There was no relationship between BMI and pulmonary gas exchange.

Abbreviations: BMI = body mass index; LLN = lower limit of normal; P(A-a)O2 = alveolar-arterial oxygen pressure difference; V̇o2 = oxygen consumption; W/H = waist-to-hip

Dr. Zavorsky was the recipient of the 2005 Baxter Corporation Award in Anesthesia from the Canadian Anesthesiologists’ Society and was a Research Scholar-Junior 1 from the Quebec Health Research Foundation (Fonds de la Recherche en Santé du Québec). This project was partially funded by the Canadian Anesthesiologists’ Society.

The authors have reported to the ACCP that no significant conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Table Graphic Jump Location
Table 1. Body Parameters and Spirometry Results for the Subjects*
* 

BSA = body surface area; V̇e = minute ventilation; RER = respiratory exchange ratio; HR = heart rate; Vd/Vt = physiologic dead space ventilation; PEF = peak expiratory flow; HDL = high-density lipoprotein; LDL = low-density lipoprotein; HbA1C = glycosylated hemoglobin; T/L = ×1012 cells/L; G/L = ×109 cells/L; BTPS = body temperature and pressure saturated. Predicted values were significantly different than measured values (p < 0.05). Pulmonary function values in men as a percentage of the normal values predicted for men and women of the same height and age are from Hankinson et al.7

 

Calculated as 0.0097 × (height [in centimeters] + weight [in kilograms]) − 0.545.

Figure Jump LinkFigure 1. Linear regression of the relationships between W/H ratio and P(A-a)O2. • = men; ○ = women.Grahic Jump Location
Figure Jump LinkFigure 2. Linear regression of the relationships between W/H ratio and Pao2. • = men; ○ = women.Grahic Jump Location
Figure Jump LinkFigure 3. Linear regression of the relationships between W/H ratio and Paco2. • = men; ○ = women.Grahic Jump Location

The authors would like to thank the volunteers for being a part of this research study, and the anesthesiologists from the Department of Anesthesia at the Montreal General Hospital, who performed the arterial cannulations on the subjects.

Whipp, BJ, Davis, JA (1984) The ventilatory stress of exercise in obesity.Am Rev Respir Dis129,S90-S92. [PubMed]
 
Wang, LY, Cerny, FJ Ventilatory response to exercise in simulated obesity by chest loading.Med Sci Sports Exerc2004;36,780-786. [PubMed]
 
Vaughan, RW, Cork, RC, Hollander, D The effect of massive weight loss on arterial oxygenation and pulmonary function tests.Anesthesiology1981;54,325-328. [PubMed] [CrossRef]
 
Dolfing, JG, Dubois, EF, Wolffenbuttel, BH, et al Different cycle ergometer outcomes in severely obese men and women without documented cardiopulmonary morbidities before bariatric surgery.Chest2005;128,256-262. [PubMed]
 
Refsum, HE, Holter, PH, Lovig, T, et al Pulmonary function and energy expenditure after marked weight loss in obese women: observations before and one year after gastric banding.Int J Obes1990;14,175-183. [PubMed]
 
Thomas, PS, Cowen, ER, Hulands, G, et al Respiratory function in the morbidly obese before and after weight loss.Thorax1989;44,382-386. [PubMed]
 
Hankinson, JL, Odencrantz, JR, Fedan, KB Spirometric reference values from a sample of the general U.S. population.Am J Respir Crit Care Med1999;159,179-187. [PubMed]
 
Sartorio, A, Malavolti, M, Agosti, F, et al Body water distribution in severe obesity and its assessment from eight-polar bioelectrical impedance analysis.Eur J Clin Nutr2005;59,155-160. [PubMed]
 
Johnson, RL, Jr, Heigenhauser, GJF, Hsia, CCW, et al Determinants of gas exchange and acid-balance during exercise. Rowell, LB Shepard, JT eds.Handbook of physiology: Section 12. Exercise: regulation and integration of multiple systems1996,515-584 Oxford University Press. New York, NY:
 
Grundy, SM, Brewer, HB, Jr, Cleeman, JI, et al Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition.Circulation2004;109,433-438. [PubMed]
 
Holley, HS, Milic-Emili, J, Becklake, MR, et al Regional distribution of pulmonary ventilation and perfusion in obesity.J Clin Invest1967;46,475-481. [PubMed]
 
Hakala, K, Mustajoki, P, Aittomaki, J, et al Improved gas exchange during exercise after weight loss in morbid obesity.Clin Physiol1996;16,229-238. [PubMed]
 
Sugerman, HJ, Fairman, RP, Baron, PL, et al Gastric surgery for respiratory insufficiency of obesity.Chest1986;90,81-86. [PubMed]
 
Lopata, M, Onal, E Mass loading, sleep apnea, and the pathogenesis of obesity hypoventilation.Am Rev Respir Dis1982;126,640-645. [PubMed]
 

Figures

Figure Jump LinkFigure 1. Linear regression of the relationships between W/H ratio and P(A-a)O2. • = men; ○ = women.Grahic Jump Location
Figure Jump LinkFigure 2. Linear regression of the relationships between W/H ratio and Pao2. • = men; ○ = women.Grahic Jump Location
Figure Jump LinkFigure 3. Linear regression of the relationships between W/H ratio and Paco2. • = men; ○ = women.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1. Body Parameters and Spirometry Results for the Subjects*
* 

BSA = body surface area; V̇e = minute ventilation; RER = respiratory exchange ratio; HR = heart rate; Vd/Vt = physiologic dead space ventilation; PEF = peak expiratory flow; HDL = high-density lipoprotein; LDL = low-density lipoprotein; HbA1C = glycosylated hemoglobin; T/L = ×1012 cells/L; G/L = ×109 cells/L; BTPS = body temperature and pressure saturated. Predicted values were significantly different than measured values (p < 0.05). Pulmonary function values in men as a percentage of the normal values predicted for men and women of the same height and age are from Hankinson et al.7

 

Calculated as 0.0097 × (height [in centimeters] + weight [in kilograms]) − 0.545.

References

Whipp, BJ, Davis, JA (1984) The ventilatory stress of exercise in obesity.Am Rev Respir Dis129,S90-S92. [PubMed]
 
Wang, LY, Cerny, FJ Ventilatory response to exercise in simulated obesity by chest loading.Med Sci Sports Exerc2004;36,780-786. [PubMed]
 
Vaughan, RW, Cork, RC, Hollander, D The effect of massive weight loss on arterial oxygenation and pulmonary function tests.Anesthesiology1981;54,325-328. [PubMed] [CrossRef]
 
Dolfing, JG, Dubois, EF, Wolffenbuttel, BH, et al Different cycle ergometer outcomes in severely obese men and women without documented cardiopulmonary morbidities before bariatric surgery.Chest2005;128,256-262. [PubMed]
 
Refsum, HE, Holter, PH, Lovig, T, et al Pulmonary function and energy expenditure after marked weight loss in obese women: observations before and one year after gastric banding.Int J Obes1990;14,175-183. [PubMed]
 
Thomas, PS, Cowen, ER, Hulands, G, et al Respiratory function in the morbidly obese before and after weight loss.Thorax1989;44,382-386. [PubMed]
 
Hankinson, JL, Odencrantz, JR, Fedan, KB Spirometric reference values from a sample of the general U.S. population.Am J Respir Crit Care Med1999;159,179-187. [PubMed]
 
Sartorio, A, Malavolti, M, Agosti, F, et al Body water distribution in severe obesity and its assessment from eight-polar bioelectrical impedance analysis.Eur J Clin Nutr2005;59,155-160. [PubMed]
 
Johnson, RL, Jr, Heigenhauser, GJF, Hsia, CCW, et al Determinants of gas exchange and acid-balance during exercise. Rowell, LB Shepard, JT eds.Handbook of physiology: Section 12. Exercise: regulation and integration of multiple systems1996,515-584 Oxford University Press. New York, NY:
 
Grundy, SM, Brewer, HB, Jr, Cleeman, JI, et al Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition.Circulation2004;109,433-438. [PubMed]
 
Holley, HS, Milic-Emili, J, Becklake, MR, et al Regional distribution of pulmonary ventilation and perfusion in obesity.J Clin Invest1967;46,475-481. [PubMed]
 
Hakala, K, Mustajoki, P, Aittomaki, J, et al Improved gas exchange during exercise after weight loss in morbid obesity.Clin Physiol1996;16,229-238. [PubMed]
 
Sugerman, HJ, Fairman, RP, Baron, PL, et al Gastric surgery for respiratory insufficiency of obesity.Chest1986;90,81-86. [PubMed]
 
Lopata, M, Onal, E Mass loading, sleep apnea, and the pathogenesis of obesity hypoventilation.Am Rev Respir Dis1982;126,640-645. [PubMed]
 
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