Introduction

Due to its high worldwide prevalence, obesity is currently the most common metabolic disease in the world. In fact, there is growing concern, because the global figures for obesity have progressively increased from an estimate of 200 million people affected in 1995 to the current 300 million, which is a 50% increase in only 7 years. Moreover, this increase in obesity prevalence is a global trend, not confined to affluent societies but also seen in emerging countries such as China (1). Obesity is a life-threatening condition associated with higher rates of cardiovascular morbidity and mortality (2, 3), anatomical and functional cardiopulmonary alterations (4, 5, 6), and poor physical fitness (7, 8). It is accepted that surgically induced weight loss in patients with severe obesity is associated with a better quality of life (9) and relief of dyspnea symptoms (10). However, it is not clear whether this is due to a reduction in the energy expenditure required to perform any physical activity (11) or to the improvement in cardiopulmonary function (12, 13).

The cardiopulmonary stress test offers an objective measure of patients' functional capacity and cardiac reserve (14, 15). Several studies have evaluated cardiopulmonary function in this type of population, but the conclusions differ for both the general obese population (16, 17) and in studying the changes in subjects with induced weight loss (18). In addition to the differences in study design and population characteristics, an important problem arises because oxygen consumption (VO₂)¹ is usually expressed relative to body mass, which can be confusing because the ratio method penalizes heavier individuals (19). To eliminate the potential confounding effect of body mass, it has been proposed that maximumVO₂ (VO_2max) should be presented relative to fat free mass (FFM) (7).

The aim of this study was to investigate the effects of surgically induced weight loss on energy expenditure, cardiovascular stress, exercise capacity, and cardiovascular function. We performed a symptom-limited cardiopulmonary exercise test with respiratory gas exchange analysis and indexed VO₂ to FFM, which was determined with the DXA method.

Research Methods and Procedures

Subjects

We studied 31 morbidly obese (MO) patients of both sexes from the MO Unit of our hospital who were included in a bariatric surgery program (complex techniques vs. biliopancreatic diversion). All individuals participating in the study presented with a normal cardiovascular examination and had normal electrocardiograms. None of them habitually performed any sporting activity or were taking any medication that could interfere with the stress test result. BMI (kilograms per meter squared) was taken as a measure of obesity, and MO was defined as BMI 40. In all cases, obesity had been present for at least 15 years. The Hospital Clinical Investigation Committee approved the study protocol, and all participants signed an informed consent.

Testing Procedures

Cardiopulmonary Exercise Testing.

Symptom-limited cardiopulmonary treadmill exercise testing on an ergometer (Enraf Nonius Holland, Delft, The Netherlands) with respiratory gas exchange analysis was carried out. After testing a patient whose weight was 244 kg, we designed a protocol suited to patients of this type. The treadmill speed and grade for each stage were as follows: Stage 1, 2.5 km/h, 0% ; Stage 2, 2.5 km/h, 2% ; Stage 3, 2.5 km/h, 4% ; Stage 4, 2.5 km/h, 6% ; Stage 5, 2.5 km/h, 8% ; Stage 6, 3 km/h, 10% ; Stage 7, 3 km/h, 12% ; Stage 8, 3 km/h, 14% ; Stage 9, 3 km/h, 16% ; Stage 10, 3 km/h, 18% ; Stage 11, 3.5 km/h, 20% ; Stage 12, 3.5 km/h, 22% ; Stage 13, 3.5 km/h, 24% ; and Stage 14, 3.5 km/h, 25% ; from this point on, the speed and grade were unchanged. Each stage was 2 minutes in duration. Subjects were encouraged to exercise until they felt unable to continue. Heart rate (HR) and arrhythmia were monitored from the electrocardiogram, and blood pressure (BP) was measured by the cuff method in the standing position before, at 2-minute intervals during the test, and during recovery. We used a cuff diameter appropriate to the arm circumference. For analysis of expired gases during the exercise and rest period, an ergometer (Oxycon-4, Mijnhardt, Odjik, Netherlands) was used with a unidirectional Hans Rudolf mask (Hans Rudolf, Inc., Kansas City, MO) to determine the values of tidal volume (milliliters), respiratory frequency (breaths per minute), minute ventilation (V_E; liters per minute), VO₂ (milliliters per minute), carbon dioxide production (milliliters per minute), and respiratory gas exchange ratio (carbon dioxide production/VO₂) every 30 seconds. The system was calibrated before each session with standard gases of known oxygen and carbon dioxide concentrations.

The efficiency of the cardiovascular system during maximal exercise was evaluated with the oxygen pulse (VO₂/HR) (7). This parameter is calculated by dividing VO₂ by the simultaneously measured HR. Its values are dependent on the stroke volume and the difference between the arterial and mixed venous blood O₂ content. The maximum arteriovenous oxygen difference during exercise has a physiological limit of 15 to 17 volume % (14); hence, if maximum effort is achieved, the O₂ pulse can be used to estimate stroke volume. An exercise response with a higher VO₂/HR than predicted indicates a better than average cardiorespiratory function. Peak O₂ pulse was defined as peak VO₂ divided by peak HR and was expressed as milliliters per beat.

The following criteria were used to estimate the relative stress of the cardiovascular system during exercise: age-predicted maximum HR and the respiratory exchange ratio (RER). We used the following equation to estimate the maximum HR: 220 - age (years). The achievement of a predicted maximal HR is taken to imply that cardiovascular limit has been reached (20). The RER represents the amount of carbon dioxide produced divided by the amount of oxygen consumed. At high levels of exercise, CO₂ production exceeds VO₂; thus, RER values > 1.0 often indicate that the subject is giving a maximal level of effort (14).

Measurement of Body Composition.

Total body composition was measured by DXA using a Lunar Prodigy densitometer (Lunar Corporation, Madison, WI). We measured total fat mass and FFM. Using an external calibrator, daily precision control was carried out. The margin of error of total corporal mass was 1% .

Statistical Analysis

Categorical variables are expressed as frequency and percentage and continuous variables as mean SD. Normality for continuous variables was assessed with the Shapiro-Wilk test. Pre- and post-intervention comparisons were made using a paired Student's t test. Comparisons between category variables were made with a ² test. A general linear model was used to test the changes during effort test, including pre- and post-status as a fixed effect and id-subject (i.e., patient number) as a random effect. Statistical analyses were conducted using SPSS version 12.0 (SPSS Inc., Chicago, IL), with the significance level set at p < 0.05 for all analyses.

Results

Clinical Characteristics

The 31 patients (20 women and 11 men) who were enrolled in the study all completed the protocol. Their mean age was 38 8 years and their height 1.64 0.11 m; 25% were diabetics, and 32% had arterial hypertension. Blood hemoglobin contents were normal in both groups. The physical characteristics of the participants at baseline and at 1-year follow-up are given in Table 1. As expected, significantly lower values for weight, BMI, fat mass, and FFM were found after surgery.

Table 1. - Physical characteristics of obese people before and 1 year after surgery.

Full table

Hemodynamic data at rest and during maximal exercise are presented in Table 2. Although at rest the systolic pressure was significantly higher before surgery, during maximal exercise, the peak systolic pressure was similar in both groups. The mean resting O₂ consumption was higher before weight loss (p < 0.001), but the peak VO₂ was similar before and after surgery. When we adjusted VO₂ for weight, the value was higher before surgery, both at rest and at peak exercise (p < 0.002). However, when we adjusted for FFM, there were no differences between the groups before and after weight loss. At rest, there were no differences in the ventilatory pattern (respiratory frequency and V_E), but at peak exercise, the V_E was higher after weight loss (p < 0.02).

Table 2. - Exercise parameters and gas exchange variables at rest and on maximal exercise in MO patients before and 1 year after bariatric surgery.

Full table

Energy Expenditure

The increased cost of performing mechanical work for obese people before surgery is indicated by a significantly higher O₂ uptake, HR, systolic arterial pressure (SAP), and V_E, at each work load, during the time that they were able to exercise (Figure 1). At 1-year follow-up, the surgical group displayed a significant weight loss of 51 kg (35% of the initial weight), and they were able to exercise at each work load with lower energy expenditure. This reduced cost enabled them to significantly increase the exercise duration time (13.8 3.8 vs. 21.6 4.2 minutes, pre- and post-surgery, respectively; p < 0.001).

Figure 1.

Results of effort test before and after bariatric surgery. From the beginning of the exercise, obese patients after weight loss presented a lower cardiovascular and respiratory response, as indicated by lower VO₂ uptake, HR, SAP, and V_E. This comparison refers only to the time for which the MO patient was able to exercise before surgery (general linear model). Data are presented as mean, SE. Presurgery and postsurgery figures listed below the panels represent the number of subjects who reached each workload.

Full figure and legend (101K)

Cardiovascular Stress

At the end of the exercise, HR and RER were higher in postoperative patients. Before surgery, MO patients reached only 83% of age-predicted maximum HR, and their RER at the end of exercise was 0.87 0.07, suggesting a submaximal exercise test. After surgery, they reached 90% and 1.03 0.09, respectively (p < 0.01 and p < 0.001) (Table 2), which represents higher cardiovascular stress.

Peak Oxygen Pulse

The peak O₂ pulse (milliliters per beat) was higher in obese people before surgery (15.7 4 vs. 13.9 3, p < 0.002), but when we calculated the O₂ pulse after adjusting peak VO₂ for FFM (milliliters per kilogram of FFM per beat), there were no statistical differences between the groups (0.26 0.05 vs. 0.25 0.05) (Figure 2).

Figure 2.

The upper graph shows the comparison of peak O₂ pulse (VO₂/HR) before and after surgery, showing higher values before weight loss (p < 0.002). Data are expressed in milliliters per beat. The lower graph shows comparison of peak O₂ pulse before and after surgery with VO₂ adjusted for FFM (O₂ pulse/FFM). The differences between both groups disappeared. Data are expressed in milliliters per kilogram of FFM per beat (paired Student's t test) and are presented as means SD.

Full figure and legend (35K)

With the aim of analyzing cardiac function in both groups at the same level of exercise, we compared preoperative peak O₂ pulse with postoperative O₂ pulse obtained at the same HR that each individual achieved before surgery at the end of the test. As expected, again, the O₂ pulse was significantly higher before surgery (15.7 4 vs. 12.9 3.5, p < 0.001). However, after normalizing VO₂ by FFM, the differences in O₂ pulse between the groups disappeared (0.26 0.05 vs. 0.24 0.04) (Figure 3).

Figure 3.

Comparison of O₂ pulse before and after surgery at the same level of effort. We compared peak O₂ pulse (VO₂/HR) achieved for each patient before surgery with the O₂ pulse obtained after surgery, when their HR was equal to the peak HR achieved before surgery. In the upper graph, the O₂ pulse is significantly higher before weight loss. Data are expressed in milliliters per beat. In the lower graph, there were no differences in O₂ pulse between both groups after adjusting VO₂ for FFM. Data are expressed in milliliters per kilogram of FFM per beat (paired Student's t test) and are presented as means SD.

Full figure and legend (39K)

Discussion

This study showed that large weight loss in MO patients was associated with a marked increase in exercise capacity. A weight reduction of 35% significantly increased treadmill endurance duration. Although similar results have been published previously and have been attributed to cardiac function improvement (12, 13), we demonstrated that this was due to both a reduction in energy expenditure at any level of work rate and a better use of cardiac reserve. We did not find any significant improvement in cardiovascular function.

It has been described that it is physiologically more difficult for the obese individual to do the same amount of work as a person of normal weight (21). In our study, from the beginning of the exercise, MO patients presented a greater cardiovascular and respiratory response, as indicated by higher VO₂ uptake, HR, SAP, and V_E (Figure 1). A part of the subjects' cardiovascular reserve is consumed to supply the energy required to move their enlarged bodies. After weight reduction, the patient performs the same amount of external work with lower cardiorespiratory response. Öhrström et al. (11) obtained similar results showing a reduction in energy expenditure after surgery, and Karason et al. (10) showed an increase in leisure-time physical activity. Although exertional dyspnea in obesity may have multifactorial causes, it seems clear that the reduction in the energy cost of exercise is one of the factors that allows prolonged exercise time. All of these findings suggest that the energy expended to move large bodies is a limiting factor in aerobic activities.

Some authors believe that increased requirements for muscular activity may stretch the cardiopulmonary reserve, leading to exhaustion (12). In our study, patients achieved different levels of exercise intensity before and after surgery. The attainment of an HR that reaches the age-predicted maximal HR and RER 1 are taken as an indication that cardiovascular limitation has been reached (14, 20). Before surgery, the obese patients achieved only 83% of the predicted maximal HR, and their RER was <0.9. Thus, before surgery, the obese group did not reach its maximal exercise capacity. After weight loss, these values were 90% and 1, respectively, almost reaching a maximal effort (Table 2). It seems that before surgery, obese patients reached their work limit capacity before the cardiovascular system was maximally stressed, suggesting that the limiting factor in aerobic activities is not the cardiorespiratory system (7). Marinov et al. (22) found that obese children had an increased awareness of fatigue that limited their physical capacity. The perception of effort is an important factor that limits exercise, which is volitionally terminated when the sense of effort in the motor cortex becomes more intense than is tolerable (20, 23). On average, obese patients used as much as 58% of their peak VO₂ walking at a speed of 2.5 km/h, whereas normal subjects use only 34% (24). This might explain why obese people cannot follow the advice to exercise through long and brisk walks (21). Surgically induced weight loss is associated with marked relief in symptoms of dyspnea in direct proportion to the weight loss achieved. Any complementary exercise program after surgery should start with low-intensity non-weight-bearing activities such as bike riding or swimming. The rate of perceived exertion can be used to prescribe exercise intensity by increasing the level progressively as patients lose weight.

Discrepancy persists regarding cardiovascular function in obese patients (6, 16, 21, 25, 26) and its modification with weight loss. Some researchers have published results showing significant reductions in cardiac mass (18), but others have not found any effect on cardiac left-ventricular structure (27). Aside from echocardiographic studies, comparisons of cardiopulmonary stress testing before and after weight loss are lacking. Kanoupakis et al. (12) found that obese individuals improved their cardiopulmonary exercise performance after surgical weight loss, and reported an increase in peak VO₂ consumption related to body weight. In our study, despite lower cardiovascular stress, the absolute values for peak O₂ pulse were higher before surgery (Figure 2), which could suggest that greater obesity had better cardiovascular function. Confusion exists about normalization procedures to enable comparison of VO_2max between people of different sizes. In obese individuals, the maximum VO₂ values are low when related to actual body weight but are usually normal when related to height or FFM (7). Recently, Loftin et al. (19) showed that the influence of mass is not removed by the ratio method and, in fact, penalizes heavier individuals. In our case, when we adjusted peak O₂ pulse with FFM, the differences between the groups disappeared (Figure 2), suggesting that the stroke volume was similar before and after surgery. The improvement in exercise capacity after surgery cannot be attributed to an improvement in cardiovascular function.

This study has some limitations. First, the slope in the relationship between VO₂ and workload performed depends on the rate of work increase. If this rate of increase is high, a proportion of the energy generated comes from anaerobic sources, and the VO₂ slope will be less pronounced (28). These considerations are important because we compared the slope of two population groups that experienced changes in workload differently due to different weight. Second, the effort test that we designed for patients with extreme obesity has limitations. During cycling ergometry, the VO₂ is displaced upwardly by 5.8 mL/min per kilogram of body weight. For treadmill exercise, a predictable adjustment for body weight is not possible because of complex mechanical factors that are weight dependent (28). Third, it would be considered inappropriate to compare the peak O₂ pulse obtained in each group because the intensity level of the exercise was different before and after surgery. For this reason, we analyzed both groups at the same level of effort. We compared the peak O₂ pulse/FFM achieved for each patient before surgery with the O₂ pulse/FFM obtained after surgery, measured at the point at which their HR was equal to the peak HR obtained before surgery. Again, we did not find any statistical differences between the groups (Figure 3).

In conclusion, this study demonstrated that, after surgically induced weight loss, obese patients performed the same amount of external work with lower O₂ uptake, HR, SAP, and V_E and, hence, with lower energy consumption. At the same time, after surgery, they achieved higher peak HR and RER, optimizing the use of cardiac reserve. Both factors explain the increased exercise capacity. Increased exercise capacity cannot be attributed to an improvement in cardiac function because we did not detect any difference in the peak O₂ pulse adjusted by FFM before and after surgery.

Notes

¹ Nonstandard abbreviations: VO₂, oxygen consumption; VO_2max, maximum VO₂; FFM, fat free mass; MO, morbid obesity, morbidly obese; HR, heart rate; BP, blood pressure; V_E, minute ventilation; RER, respiratory exchange ratio; SAP, systolic arterial pressure.

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Acknowledgments

This study was supported by a research grant from the Health Investigation Fund (Fondo de Iinvestigación Sanitaria, 99/1021). We thank Ana Canton for help in collecting data.