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(Chest. 2005;128:256-262.)
© 2005 American College of Chest Physicians

Different Cycle Ergometer Outcomes in Severely Obese Men and Women Without Documented Cardiopulmonary Morbidities Before Bariatric Surgery*

Jacqueline G. Dolfing, MD; Emile F. Dubois, MD, PhD, FCCP; Bruce H.R. Wolffenbuttel, MD, PhD; Nienke M. ten Hoor-Aukema, BS and Dave H. Schweitzer, MD, PhD

* From the Departments of Gynecology and Obstetrics (Dr. Dolfing), and Endocrinology (Dr. Wolffenbuttel), University Hospital Groningen, Groningen, the Netherlands; and the Departments of Pulmonary Diseases (Dr. Dubois) and Internal Medicine and Endocrinology (Mr. ten Hoor-Aukema and Dr. Schweitzer), Hospital Reinier de Graaf Groep, Delft-Voorburg, the Netherlands.

Correspondence to: Emile F. Dubois, MD, PhD, FCCP, Department of Pulmonary Diseases, Reinier de Graaf Groep Delft and Voorburg, Fonteynenburglaan 5, PBX 998, 2270 AZ Voorburg, the Netherlands; e-mail: dubois{at}rdgg.nl


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: The number of severely obese patients undergoing bariatric surgery is increasing. No incremental cycle ergometer data are available in this category of patients. The current study was undertaken to provide information and to compare outcomes between severely obese men and women during physical exercise.

Design: Cross-sectional study.

Participants: Twenty-two men and 34 women, all with a body mass index (BMI) of at least 40 kg/m2, were selected from among persons participating in a dedicated weight management program that was carried out in the outpatient clinic of a large teaching hospital.

Measurements and results: Body composition was estimated with bioelectrical impedance. Oxygen uptake (O2) was obtained by breath-by-breath minute ventilation (ventilated hood) and was measured under resting energy expenditure (REE) conditions. Endurance was measured with an incremental cycle ergometer test. Male and female groups were balanced for mean (± SD) age (42.7 ± 7.6 vs 41.8 ± 8.9 years, respectively), BMI (43.0 ± 4.9 vs 41.3 ± 5.2 kg/m2, respectively), and fat weight (55.5 ± 14.0 vs 56.8 ± 2.2 kg, respectively). Fat-free mass (FFM), FFM index, fasting blood glucose level, insulin level, REE, and O2 at rest and during subjective maximal endurance were higher in the male group. However, maximal O2 (women, 119 ± 19% predicted; men, 92 ± 16% predicted) and anaerobic threshold were higher in the female group (women, 64 ± 12% predicted; men, 48 ± 76% predicted, respectively; p < 0.0001).

Conclusions: Severely obese men were more carbohydrate-intolerant and sustained less physical endurance than was predicted according to standards in comparison with obese women. The cycle ergometer data indicated that male gender was associated with less physical fitness.

Key Words: bicycle • exercise test • gender • severely obese


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The World Health Organization considers the problem of overweight and obesity as a matter of priority.1 Early mortality related to excess body weight was demonstrated in a previously reported metaanalysis.2 The burden of disease and costs due to overweight have been recently reviewed,3 and a call for urgent action has been placed for all clinicians who are dealing with obese patients.

Obesity is the principal driver for metabolic syndrome and diabetes. Thus far, substantial and sustained weight reduction with clinical improvements have been demonstrated only after bariatric surgery.4 In terms of comedications, long-term weight loss of at least 10% is necessary to reduce the number of prescriptions for diabetes and cardiovascular disease, whereas weight reduction of ≥ 15% is needed to prevent the issuing of new prescriptions.5 The National Institutes of Health consensus conference6 in 1991 established guidelines and indications for the surgical management of severe obesity that are now widely accepted. A body mass index (BMI) exceeding 40 kg/m2 indicates that a person is severely obese and therefore has an indication for surgery. Bariatric surgery may also be a feasible treatment option for people with a BMI between 35 and 40 kg/m2 who experience life-threatening problems like severe obstructive sleep apnea syndrome, with or without alveolar hypoventilation syndrome, and obesity-related cardiovascular disease or diabetes. Although cardiovascular disease and diabetes are specifically related to upper body obesity, guidelines do not differentiate between male-type (upper body) vs female-type (lower body) fat distribution.

The number of people with various obesity-related complaints who have undergone bariatric surgery in the United States has more than doubled within the last decade.7 Prior to surgery, many of these people report obesity-related dyspnea complaints, while other patients deny any dyspnea at all. Exercise ventilation monitoring appears to be an elegant tool to provide insight into the evaluation of dyspnea.8 Moreover, cardiopulmonary endurance analysis has been shown to be valuable in selecting patients who are at high risk for surgery-related complications.9 Yet, no such data have been obtained from groups of severely obese persons. The aim of the current study was to perform cardiopulmonary exercise capacity tests in severely obese patients who are scheduled for antiobesity surgery, using cycle ergometer tests (CETs) under standardized stress conditions. The aim of the current study was to document CET outcomes in consecutively referred individuals, independently from complaints, and to compare the obtained results of men and women.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
Patients were eligible for participation in the study if they had grade III severe obesity (BMI, ≥ 40 kg/m2), according to the classification of the World Health Organization.1 All patients participated in a dedicated weight management program (WMP) that was carried out in the outpatient clinic of a large teaching hospital, with the intent that they would undergo laparoscopic gastric banding. Our WMP offers a multidisciplinary approach to obese patients, aiming to reduce weight and to optimize general health before undergoing planned bariatric surgery. In a WMP, all patients receive general information about nutrition, lifestyle modification, and physical exercise. Each individual is seen by the same dietician and is advised to keep a mildly energy-restricted diet (2,092 kJ/d less than the daily requirement). Patients with a fasting blood glucose (FBG) concentration of ≥ 6.1 mmol/L (≥ 110 mg/dL) and those individuals with a BMI of ≥ 40 kg/m2, irrespective of FBG concentration, received additional pharmacotherapy with metformin at a maximal dose of 1,000 mg bid.10 Each individual was specifically asked about laxative use, purging, and whether they experienced binge eating attacks. Indeed, all patients reported frequently occurring unstoppable eating, and many experienced multiple binge eating attacks each day. Notably, gastric banding is a restrictive antiobesity procedure, which can be hazardous to anyone with extreme eating impulses. Based on these arguments, all patients were treated with fluoxetine, in a daily dose of 20 mg tid, prior to undergoing planned gastric banding. It is of note that a dosage of 60 mg of fluoxetine per day has been approved by the US Food and Drug Administration for the treatment of bulimia nervosa and obsessive-compulsive disorder.11

Excluded from participation were those patients with symptomatic coronary heart disease staged according the New York Heart Association class II and III, those with COPD disease of severity grade II and III (using Global Initiative for Chronic Obstructive Lung Disease criteria12), pregnant women, patients with general endocrine disorders, patients with known diabetes, patients who were treated with oral blood glucose-lowering agents and/or insulin before the start of the WMP, individuals who already had been treated with antiobesity drugs, antidepressants, or glucocorticoids, and patients who were incapable of performing an adequate CET.

At entry into the WMP, medical screening was performed in 70 consecutive patients, of whom 8 were receiving oral glucose-lowering agents, 2 were insulin users, and 2 had hypothyroidism. Written informed consent was obtained from the remaining 58 patients to participate in the study. One man and one woman were unable to perform a CET, hence, complete data were available for 56 patients, who were used in the study. The study was approved by the Medical Ethical Committee of Reinier de Graaf Groep Hospital.

Methods
At entry into the WMP, early morning fasting blood samples were taken and analyzed with commercially available assays. The following assessments were performed in men: total testosterone level (normal value, 9 to 35 nmol/L); and luteinizing hormone (LH) [normal value, 3 to 12 IU/L]. Both hormones were assayed with an auto-analyzer (Immulite; Diagnostic Products Co; Los Angeles, CA). The following assessments were performed in men and women: fasting insulin level (normal value, < 20 mU/L) [Coat-a-Count radioimmunoassay; Diagnostic Products Co), and FBG concentration (normal FBG value, < 6.1 mmol/L [< 110 mg/dL]; carbohydrate intolerance, 6.1 to 6.9 mmol/L [110 to 125 mg/dL]; overt diabetes, ≥ 7.0 mmol/L [≥ 126 mg/dL]) [using American Diabetes Association criteria13]. Androgen deficiency was defined as an early morning total testosterone level of ≤ 8 nmol/L, whereas in Leydig cell failure it was 8 to 15 nmol/L combined with an elevated LH level of > 18 IU/L (equal to 1.5 times the upper limit of the eugonadal reference range for young men).141516

After 3 months of the WMP, body composition was measured with bioelectrical impedance analysis (BIA) [Bodystat 1500; Bodystat Ltd; Isle of Man, UK] and fat-free mass (FFM), fat weight (FW), and FFM index (FFMI) [FFM x height2] were calculated. Resting energy expenditure (REE) was determined with the ventilated hood method and was calculated with the equation of Harris and Benedict.17 Breath-by-breath oxygen uptake (O2), carbon dioxide output, and minute ventilation (E) were measured (Oxycon {alpha} system; Erich Jaeger, GmbH; Wuerzburg, Germany). To establish REE conditions, all participants were asked to refrain from any food, beverage, and tooth brushing for at least 8 h prior to the analysis. Measurements were performed in a special light-dimmed laboratory after 30 min in semirecumbent position, and outcomes were corrected for a respiratory exchange ratio of 0.82.

CET was performed with a bicycle ergometer (Ergoline GmbH; Bitz, Germany). Prior to CET, an indwelling catheter was inserted into the radial artery, and arterial blood samples were taken for blood gas analysis and plasma lactate determination (normal resting value, 0.9 to 2.0 mmol/L) [i-STAT; Abbott Corp; East Winsor, NJ). After a 3-min warm-up period, the net O2 at 20% of the predicted maximum workload – O2 measured under REE conditions (O2unloaded) was calculated. This phase was followed by an interval-free slope-wise increase of workload with 10% of maximal predicted workload per subsequent minute starting at t = 3 min. The anaerobic threshold (AT) was determined with the ventilatory equivalent method (ie, an increase in the ventilatory equivalent of O2 [EqO2 = E/O2] without a simultaneous increase in the ventilatory equivalent of CO2 [EqCO2 = E/carbon dioxide output].18 AT was expressed in absolute values (milliliters per minute) and as the percent predicted of the maximum O2 (O2max).1920 In order to achieve the O2max, the CET was continued up to maximal subjective exhaustion, and otherwise was stopped in case of cardiocirculatory, ventilatory, or musculoskeletal limitations.212223 At the start of the CET and at subjective exhaustion, Borg scores for dyspnea and leg fatigue were assessed using standard questionnaires24 and objective measurements were also made (ie, O2max, heart rate reserve, and breathing reserve).

Statistical Analysis
All results are expressed as the mean ± SD. Comparisons between men and women were made with the unpaired, two-sided Student t test. Statistical significance was defined as a p value of < 0.05.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
A total of 56 patients (22 men and 34 women) were included in the study. There were no group differences in terms of age, BMI, and FW (Table 1 ). Men had a higher FFM than women, with a mean FFMI of 25 ± 2 kg/m2 in men vs 21 ± 1 kg/m2 in women (p < 0.0001). All men, except for one patient who had Leydig cell failure (testosterone, 10.4 nmol/L; LH, 18.2 U/L), were eugonadal. FBG concentrations and insulin levels were higher in the male group. FBG concentration was ≥ 6.1 mmol/L in 13 men (59%), of whom 8 men (36%) had diabetes and 5 men (23%) had carbohydrate intolerance (according to American Diabetes Association criteria13). FBG concentration was ≥ 6.1 mmol/L in 12 women (35%), of whom 4 women (12%) had diabetes and 8 women (24%) had carbohydrate intolerance.


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  		Table 1.. Demographic, Anthropometric, BIA, and Laboratory Data of Severely Obese Men and Women*

 
Calculated REE in men and women matched with predicted values (Table 2 ). The absolute O2 at 20% of maximal predicted workload and the net O2unloaded were similar between men and women (men, 570 ± 183 mL/min; women, 570 ± 107 mL/min; difference was not significant). Dividing net O2unloaded by FFM, representing the O2 per kilogram of leg muscle, revealed lower levels in men compared with women (6.9 ± 2.1 vs 9.8 ± 1.7 mL/min/kg, respectively; p < 0.0001). Furthermore, women performed better at subjective maximal endurance than predicted according to standards, while relative performance was lower in men. A similar picture emerged for O2 at AT (expressed as the O2max percent predicted), that is, it was higher in women compared with men (Table 2).


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  		Table 2.. Metabolic Rates and CET Outcomes Including Cardiopulmonary and Muscle Performance During Subjective Maximal Endurance in Severely Obese Men and Women

 
Men had a small but significantly lower PaO2 and a significantly higher PaCO2 at rest (Table 3 ). This might suggest an overall lower ventilation/perfusion ratio in men compared with women. The pathophysiology behind this observation can be explained in the first place by a higher circulating blood volume in men, or by the different distribution of body fat (ie, male type upper-body fat vs female-type lower body fat). Differences in fat distribution may lead to diminished ventilation in the lower parts of the lung due to "abdominal compression." This may explain a relatively lower vital capacity, which results in a relatively lower level of ventilation (Table 4 ).


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  		Table 3.. Resting and Exercise Arterial Blood Gas Analyses in Severely Obese Men and Women*

 

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  		Table 4.. Spirometry Outcomes During Subjective Maximal Endurance in Severely Obese Men and Women*

 
None of the patients experienced limitations other than physiologic cardiopulmonary limitations during CET, particularly at maximal subjective exhaustion. Moreover, men and women achieved similar breathing and heart rate reserves. Maximal fatigue, expressed as Borg scores for dyspnea and leg fatigue, as well as the increase of arterial lactate levels were similar between groups.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The current study demonstrated that severely obese men and women, without prior documentedcardiopulmonary morbidities, sustained subjective maximal exhaustion without cardiocirculatory, ventilatory, or respiratory limitations. In men and women, leg fatigue was the main reason to stop cycling, as shown in Borg scores. The aim of this study was also to compare fitness in untrained severely obese men and women during heavy exercise. First, it appeared that men were relatively less obese but more carbohydrate-intolerant, which suggests that these men were more sensitive toward the deregulation of carbohydrate metabolism in comparison with women. Second, men and women had similar net O2unloaded outcomes despite of a higher FFM in men. Third, men had a lower O2max and a lower AT, in comparison with the predicted values based on existing standards.

The results of the current study appear to be in contrast with those of a previously reported study25 that was also performed in severely obese men. These men had a similar BMI, but were able to achieve a higher peak of exercise at exhaustion and a higher AT, as predicted. The authors ascribed this phenomenon to the large muscle mass of these "big" men.25 The subjects studied were untrained Italian employees without cardiorespiratory disorders or obesity-related complaints, whereas in the current study all patients were white Dutch persons who had the intention of undergoing gastric banding surgery, which was indicated as treatment for their severe obesity. The discrepant results between the studies may be explained by differences in patient selection and ethnicity. The finding in the current study of more deregulation of carbohydrate metabolism in men is in agreement with that of a previously reported study looking at treadmill exercise in obese men and women. It was reported that the age-adjusted risk for having metabolic syndrome was 10.1 (95% confidence interval, 9.1 to 11.2) and was higher in men with a poor physical health compared with those who were in good shape. Differences in risk were also noted in obese women, albeit less than in men (age-adjusted risk for having metabolic syndrome, 4.9; 95% confidence interval, 3.8 to 6.3).26 This discrepancy in risk indicates "gender interaction" with physical fitness in obese subjects. Insulin resistance may also interact with fitness. It has been shown previously that insulin resistance interacts with cardiovascular components of the metabolic syndrome by impairing capillary recruitment in muscle.27 Furthermore, skeletal muscle tissue depends highly on lipid oxidation, particularly during exercise.28 Obese individuals, however, usually express high intramyocellular fat levels with a decreased capacity of muscular lipid oxidation.2930 Such an paradoxical relationship might be of importance because an increase in intramyocellular fat is also linked with insulin resistance in obese individuals.2931

A linear and inverse association between obesity and respiratory function has been previously shown in two large cohort studies.3233 This relationship was particularly present in men, and in both sexes with mainly male-type (upper-body) obesity.3233 In daily practice, however, obesity does not alter respiratory function, except in those individuals with extreme obesity (ie, weight [in kilograms]/height [in centimeters] of > 1).34 In the present study, men had significantly lower PaO2 and a significantly higher PaCO2 at rest, while PaO2 differences disappeared during maximal physical endurance. In agreement with these observations, it was also shown that vital capacities (percent predicted) were lower in men. Nevertheless, all patients included in the study fell within the generally accepted 95% confidence limits, as observed in the general population. Whether we should recommend routine CETs or other cardiopulmonary endurance tests to analyze patients before bariatric surgery cannot yet be answered. There are no convincing data to show which severely obese patient has an unacceptably high risk to sustain bariatric surgery without major complications. However, there is a body of evidence to suggest that the determination of O2max can provide crucial information about the health status of severely obese men. It has been shown previously that all-cause mortality was highest in obese men with a low O2max.35 Today, a consensus has been reached to consider all patients for bariatric who have a BMI of > 35 kg/m2 with significant comorbidities, or > 40 kg/m2 without comorbidities.36 One should realize, however, that many hospitals are unable to cope with the demand for antiobesity surgery. Waiting times are long, and duplicate referrals to other hospitals are common. It would be a challenge to implement cardiopulmonary exercise tests to establish a clinical triage for those patients who really benefit from antiobesity surgery. More studies on this issue are certainly needed.

The current study has a few limitations. First, in contrast with dual-energy radiograph absorptiometry (DXA), BIA does not provide information on body fat distribution. An assessment of the degree of agreement between DXA and BIA in nonobese and obese subjects revealed similar accuracies for both techniques.37 However, correlations of DXA and BIA were strongest in nonobese individuals.37 Second, only a limited number of subjects who had decided to request surgery as a definitive obesity treatment were included in the study. Thus far, there are no studies comparing the CET outcomes of randomly selected severely obese individuals with those of individuals with obesity-related complaints requesting for bariatric surgery.

Overall, this study has demonstrated that severely obese men and women without documented cardiopulmonary morbidities were capable of sustaining maximal subjective exhaustion without cardiopulmonary limitations. We hypothesize that male gender interacts negatively with fitness in the case of abundantly deposited fat tissue. Certainly, fat deposition studies in combination with CETs are needed to clarify the biological effects of male-type obesity (upper-body) vs those of female-type obesity (lower-body) within male or female groups. This type of research, although technically complicated, is certainly required in much larger individuals. Whether gender and the amount of male-type obesity (upper-body) should be used in operational definitions for obesity severity needs further answering.


   Acknowledgements
 
We are indebted to Ineke Bosman and to all employees of the Pulmonary Function Department of Hospital Reinier de Graaf Groep for their excellent laboratory and technical support.


   Footnotes
 
Abbreviations: AT = anaerobic threshold; BIA = bioelectrical impedance analysis; BMI = body mass index; CET = cycle ergometer test; DXA = dual-energy radiograph absorptiometry; FBG = fasting blood glucose; FFM = fat-free mass; FFMI = fat-free mass index; FW = fat weight; LH = luteinizing hormone; REE = resting energy expenditure; E = minute ventilation; O2 = oxygen uptake; O2max = maximum oxygen consumption; O2unloaded = maximum workload – oxygen uptake measured under resting energy expenditure conditions; WMP = weight management program

Received for publication September 4, 2004. Accepted for publication January 5, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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