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Glycemic Status Affects Cardiopulmonary Exercise Response in Athletes with Type I Diabetes


Medicine & Science in Sports & Exercise: August 2010 - Volume 42 - Issue 8 - p 1454-1459
doi: 10.1249/MSS.0b013e3181d1fdb3
Clinical Sciences

Purpose: This study aimed to (a) examine the influence of type I diabetes on the cardiopulmonary exercise response in trained subjects and (b) determine whether glycemic control affects these responses.

Methods: The cardiopulmonary responses to maximal incremental cycle ergometry were compared in 12 Ironman triathletes with type I diabetes and 10 age- and sex-matched control subjects without diabetes. Athletes with type I diabetes were then stratified into low- (glycosylated hemoglobin (HbA1c) < 7%, n = 5) and high-HbA1c (HbA1c > 7%, n = 7) groups for comparison. Cardiac output, stroke volume, arterial blood pressure, and calculated systemic vascular resistance along with airway function were measured at rest and during steady-state exercise.

Results: During peak exercise HR, stroke volume and cardiac output were not different between the groups with and without diabetes; however, forced expiratory flow at 50% of the forced vital capacity was lower in subjects with diabetes (P < 0.05). Within the group with diabetes, HbA1c was lower in the low-HbA1c versus high-HbA1c group (6.5 ± 0.3 vs 7.8 ± 0.4, respectively; P < 0.05), but training volume was not different. At rest, the low-HbA1c group had greater cardiac output and lower systemic vascular resistance than the high-HbA1c group, and all pulmonary function measurements were greater in the low-HbA1c group (P < 0.05). During peak exercise, the V˙O2, workload, HR, stroke volume, and cardiac output were greater in the low-HbA1c versus the high-HbA1c group (P < 0.05). In addition, all indices of pulmonary function were higher in the low-HbA1c group (P < 0.05). Finally, within the subjects with diabetes, there was a weak inverse correlation between HbA1c and exercise training volume (r 2 = −0.352) and stroke volume (r 2 = −0.339). These data suggest that highly trained individuals with type I diabetes can achieve the same cardiopulmonary exercise responses as trained subjects without diabetes, but these responses are reduced by poor glycemic control.

1Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ; and 2Arizona Department of Pharmacy Practice and Science, University of Arizona, Tucson, AZ

Address for correspondence: Eric M. Snyder, Ph.D., Department of Pharmacy Practice and Science, University of Arizona, 1703 E. Mabel, Tucson, AZ 85721; E-mail:

Submitted for publication August 2009.

Accepted for publication November 2009.

People with type I diabetes have lower cardiac output (7,20) and muscle blood flow (6) during a given exercise intensity compared with age-, weight-, and sex-matched individuals with similar exercise history. In addition, pulmonary function (2,11) and diffusing capacity (20,35) are reduced in subjects with type I diabetes. Despite these diabetes-related reductions in the ability to oxygenate and deliver blood to peripheral tissues, some studies have found that V˙O2max is not different between subjects with type I diabetes and subjects without diabetes matched for age, sex, body composition, and physical activity (7,20,21,34).

The development of advanced glycation end products (AGE) secondary to chronic hyperglycemia may be responsible for pulmonary and cardiovascular complications associated with diabetes (8,32,36). Consistent with this idea, the magnitude of hyperglycemia seems to affect the extent of cardiovascular and pulmonary impairment and explain why some (7,20), but not all (34), studies show that type I diabetes is associated with a lower V˙O2max. Impaired exercising leg blood flow (16), pulmonary function (22), and pulmonary diffusion (20,22) are more severe in patients with diabetes with poor glycemic control. In addition, V˙O2max is reduced in patients with type I diabetes with high levels of glycosylated hemoglobin (HbA1c) but not in those who maintain normoglycemia (20). These findings suggest that careful glycemic control may attenuate diabetes-associated changes in the cardiopulmonary response to exercise.

Regular aerobic training improves V˙O2max by increasing cardiac output and possibly whole-body arteriovenous oxygen difference in individuals without diabetes (3,23). Individuals with type I diabetes are encouraged to participate in all forms of exercise (31); however, no study has determined whether athletes with type I diabetes are capable of the same relative or absolute cardiovascular or pulmonary training adaptations as athletes without diabetes. Training does not seem to improve glycemic control in patients with type I diabetes (17,37), and there is a paucity of data that have prospectively determined whether glycemic control influences the cardiovascular response to exercise in endurance-trained athletes with diabetes. The purpose of this study was twofold. We sought 1) to compare the cardiovascular and pulmonary responses to exercise in endurance-trained subjects with type I diabetes versus trained subjects without diabetes and 2) to determine the effect of glycemic control on the cardiovascular and pulmonary responses to exercise in endurance-trained athletes with type I diabetes. We hypothesized that peak cardiac output, stroke volume, and V˙O2 would be lower in trained subjects with type I diabetes versus trained subjects without diabetes. We also hypothesized that peak cardiac output, stroke volume and V˙O2 would be greater in trained subjects with type I diabetes with good (HbA1c < 7%) versus poor (HbA1c > 7%) glycemic control.

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Twelve nonsmoking subjects with type I diabetes who were training for an Ironman triathlon and 10 nonsmoking control subjects without diabetes matched for age, sex, and training volume were recruited for this study. The protocol was reviewed and approved by the University of Arizona Institutional Review Board, all participants provided written informed consent before study, and all aspects of the study were performed according to the Declaration of Helsinki.

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Subjects were requested to come into the laboratory in a fasting state. Venous blood samples were collected at rest for measurement of HbA1c and blood glucose. Resting measures of cardiac output, blood pressure (systolic blood pressure (SBP), diastolic blood pressure (DBP), and mean arterial blood pressure), and pulmonary function (forced vital capacity (FVC), forced expiratory flow at 1 s (FEV1), and forced expiratory flow at 50% of the forced vital capacity (FEF50)) were performed before exercise. All exercise tests were performed on the same cycle ergometer (Corival Lode BV, Groningen, The Netherlands). The workload for the exercise testing protocol was subject-specific, with the initial and incremental increase in workload differing between subjects to accommodate body size and training differences. The cycle ergometry test initiated with a workload ranging from 25 to 55 W after 1 min of unloaded pedaling (0 W) on the cycle ergometer. Workloads increased incrementally every 3 min until exhaustion was reached as determined by the subject's inability to maintain a pedal rate between 60 and 80 rpm, an RER > 1.15, or an RPE of 18 of 20 (4). Total exercise duration ranged between 15 and 21 min.

After peak exercise, subjects completed a recovery phase of 3 min of pedaling at the initial workload and 5 min of stationary recovery while remaining seated on the bike. Oxygen uptake (V˙O2), carbon dioxide production (V˙CO2), respiratory rate, tidal volume, and minute ventilation were continuously monitored and averaged for data analysis every 3 s during all stages of the exercise test. For flow and gas exchange analyses, a Medical Graphics CPX/D (St. Paul, MN) metabolic cart was interfaced with a Perkin-Elmer MGA-1100 mass spectrometer (Perkin-Elmer 1100, Welsley, MA) as described previously (28,29). Before and during exercise, the subject's HR was monitored with a 12-lead ECG (Marquette Electronics, Milwaukee, WI).

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Assessment of cardiovascular function.

Cardiac output was assessed with a previously validated 8- to 10-breath acetylene rebreathe technique using a 5-L rebreathe bag containing 0.7% C2H2 and 9% He (13,30). Briefly, a pneumotachograph was connected to a nonrebreathing Y valve (Hans Rudolph, Kansas City, MO) with the inspiratory port connected to a pneumatic switching valve that allowed for rapid switching from room air to the test gas mixture. Gases were sampled using a mass spectrometer (Perkin-Elmer) that was integrated with custom analysis software for the assessment of . The volume of gas used to fill the rebreathe bag was determined by the tidal volume of the subject with 500 mL added to the subject's tidal volume to ensure the bag did not collapse at the end of inspiration. The bag volume was adjusted during exercise accordingly. Consistent bag volumes were ensured using a timed switching circuit, which, given a consistent flow rate from the tank, resulted in the desired volume (14). The switching circuit and tank were checked before each test for accurate volumes. At the end of a normal expiration (end-expiratory lung volume), the subjects were switched into the rebreathe bag and instructed to nearly empty the bag with each breath for 10 consecutive breaths. After each cardiac output maneuver, the rebreathe bag was emptied with a suction device and refilled immediately before the next maneuver. At the start of each maneuver, there was no residual gas in the dead space of the apparatus or from the exhaled air from the subjects, as determined through gas sampling with the mass spectrometer.

Blood pressure was obtained using the auscultation technique, with the same technician performing all measures. Stroke volume was calculated from and HR. Mean arterial pressure (MAP) was calculated using the equation: MAP = DBP + 1/3(SBP − DBP), where DBP is diastolic blood pressure and SBP is systolic blood pressure. Systemic vascular resistance was calculated using the formula: (MAP − pulmonary capillary wedge pressure (assumed to be 10 mm Hg)) × 80)/.

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Assessment of airway function.

Airway function was assessed by having subjects perform a maximal expiratory flow volume maneuver in triplicate at rest, during each stage of exercise, and into recovery as described previously (29). We have previously shown that this maneuver can be reproducibly performed in various populations during exercise, including patients with asthma and patients with heart failure (1,12). All subjects were carefully instructed on performing the maximal expiratory flow volume maneuver with a special emphasis on taking a gradual but maximal inspiration before the forced exhalation.

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Assessment of glucose and HbA1c.

HbA1c was measured by high-performance liquid chromatography, and glucose was determined by glucose oxidation, both at the University of Arizona Medical Center Pathology Laboratory.

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Statistical analysis.

All statistical analyses were performed using the SPSS statistical software package (v.12; SPSS, Inc., Chicago, IL). All data were found to have normal distribution, and a two-sample paired t-test was used to examine group differences at rest and during exercise. Pearson correlation coefficients were used to describe linear relationships between selected variables. An α level of 0.05 used to determine statistical significance. All data are presented as mean ± SD.

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Group with diabetes versus group without diabetes.

Table 1 shows that groups were well matched for age, sex, training volumes, and aerobic capacity. As expected, HbA1c (7.3% ± 0.8% vs 5.2% ± 0.5%) and blood glucose (204 ± 52 vs 93 ± 7 mg·dL−1) were higher in subjects with versus subjects without diabetes, respectively (P < 0.05). Resting and peak exercise cardiovascular and pulmonary data are shown in Table 2. SBP, DBP, and MAP were not different between the groups. Similarly, cardiac output and systemic vascular resistance were not different between the groups at rest; however, HR was 18 beats lower, and stroke volume was 23 mL lower on average in subjects with diabetes versus subjects without diabetes (P < 0.05). FVC and FEV1 were the same, but subjects with diabetes had a lower FEF50 than subjects without diabetes (P < 0.05).





During peak exercise, there were no differences in blood pressure or systemic vascular resistance between groups (P > 0.05). Stroke volume, HR, and cardiac output were not different between groups during peak exercise. In addition, there were no differences in FVC or FEV1 between groups at peak exercise, but the group without diabetes had higher FEF50. These data are summarized in Table 2.

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Subjects with diabetes with low versus high HbA1c.

The group with type I diabetes was also stratified into subjects with HbA1c < 7% (low-HbA1c; five subjects), and those with HbA1c > 7% (high-HbA1c; seven subjects). Mean HbA1c were 6.5% ± 0.3% and 7.8% ± 0.4% (P < 0.05) in the low-HbA1c versus high-HbA1c, respectively. Training volumes were not different between the groups, and there were no differences in resting SBP, DBP, or MAP (P > 0.05). The high-HbA1c group had a lower resting cardiac output and a higher systemic vascular resistance than the low-HbA1c group (P < 0.05). Despite being 18 mL lower, mean resting stroke volume was not different between groups (P = 0.057). FVC and FEF50 were both lower in the high-HbA1c group at rest (Table 3).



Table 3 also summarizes peak exercise group comparisons. During peak exercise, workload was 24% higher, and V˙O2 was 10% higher in the low-HbA1c group (P < 0.05). Peak stroke volume was 20 mL greater, and HR was 23 beats greater (P < 0.05), resulting in a 25% higher cardiac output in the low-HbA1c group (P < 0.05). SBP, DBP, and MAP were not different between groups (P > 0.05) because lower systemic vascular resistance in the low-HbA1c group (P < 0.05) canceled out the effect of greater cardiac output. All pulmonary function parameters were lower in subjects of the high-HbA1c group during peak exercise (P < 0.05). HbA1c was inversely correlated with training volume (Fig. 1; r 2 = 0.35) and peak stroke volume (Fig. 2; r 2 = −0.34; P < 0.05).





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This study showed that the cardiovascular response to peak exercise was the same in endurance-trained subjects with type I diabetes versus subjects without diabetes. These findings are consistent with some (9,34), but not all (7,21), studies showing that the cardiovascular response to exercise is not affected by type I diabetes. Interestingly, FEF50, an indicator of airway function, was lower during peak exercise in the group with type I diabetes, suggesting that subjects with diabetes have an attenuated bronchodilation during peak exercise. The main finding of this study was that, within the athletes with type I diabetes, the cardiopulmonary response to exercise was affected by glycemic control. Despite similar training volumes, subjects with type I diabetes with high-HbA1c had lower peak workload, V˙O2peak, and peak cardiac output than those with low-HbA1c. Pulmonary function measures were also lower in the high-HbA1c group during peak exercise. These data suggest that cardiopulmonary training adaptations are greater in patients with type I diabetes who maintain good glycemic control.

Contrary to our hypothesis, we found no difference in aerobic capacity or cardiopulmonary exercise response between athletes with diabetes and athletes without diabetes (with the exception of FEF50). Our interpretation of these data is that subjects with diabetes are capable of the same cardiopulmonary training adaptations as trained subjects without diabetes. Nonetheless, the athletes with diabetes in this study competed at a higher level and trained approximately 1 h·wk−1 more than athletes without diabetes (P > 0.05), raising the possibility that we compared highly trained athletes with diabetes with less highly trained athletes without diabetes. We do not believe this is the case because the athletes with diabetes and athletes without diabetes had nearly identical peak workload and V˙O2. In addition, when V˙O2peak was adjusted for age and sex, the control athletes and athletes with diabetes achieved values of 123% and 126% predicted.

Our data may help explain why some studies find that V˙O2max is reduced in subjects with type I diabetes (7,21), whereas others do not (9,34). Veves et al. (34) compared trained and untrained groups with type I diabetes and found that V˙O2max was not different in the healthy group with diabetes and in the group without diabetes with similar training histories. They, like others (21), also reported an inverse linear correlation between aerobic capacity and HbA1c and suggested that "fit diabetic patients were likely to have better glycemic control." Interestingly, Veves et al. (34) found no correlation between training volume and HbA1c. The present study prospectively determined that V˙O2peak was greater in trained athletes with type I diabetes with good versus poor glycemic control, despite similar training volumes. Similar results were published in untrained subjects when Niranjen et al. (20) randomly assigned untrained patients with type I diabetes into groups that maintained "normoglycemia" (HbA1c = 5.6) or hyperglycemia (HbA1c = 8.8) for 6 yr. After their intervention, which included no exercise training, peak workload, maximal HR, and V˙O2max were reduced in the hyperglycemic but not in the normoglycemic group. In this context, our findings and those of Niranjen et al. (20) confirm a relationship between aerobic fitness and glycemic control and suggest that careful glycemic control improves aerobic capacity in trained and untrained subjects. In contrast, it is unclear whether aerobic training improves glycemic control.

The mechanism through which poor glycemic control influenced cardiac and pulmonary responses to maximal exercise is an interesting area for further study. Autonomic dysfunction may have influenced the hemodynamic exercise response in the high-HbA1c group. Several studies have reported a blunted sympathoadrenal response to exercise in subjects with diabetes (9,10,15), which may be more obvious in those with poor glycemic control (15). We did not measure catecholamines in this study; however, average peak HR was 23 beats lower in the high- versus the low-HbA1c group, a finding seen previously in patients with diabetes with mild neuropathy (10). Neurological impairment in subjects with type I diabetes is strongly linked with glycemic control (33). The high-HbA1c group in this study had only modestly high HbA1c levels (7.8%); nonetheless, it is possible that their glycemic status limited peak HR responses in this study. Finally, we do not believe this finding represented a disproportionate inability to achieve "peak" workloads in the high-HbA1c group because the RER for all subjects exceeded 1.10 at maximal effort.

Pulmonary function is similarly affected by hyperglycemia. Approximately 75% of young, nonsmoking individuals with type I diabetes exhibit abnormal lung function (24). These diabetes-specific limitations are most likely associated with decreased pulmonary elasticity and loss of alveolar microvascular volume caused by protein glycosylation in the lung parenchyma and vascular endothelium (25,26). These physical restrictions manifest as decreased FVC, FEV1, and FEF50 (18,20), which mimic our findings in the high-HbA1c group during peak exercise. The formation of AGE is considered "permanent," and there is debate as to whether AGE-induced changes in protein structure are reversible without pharmacological intervention. Our finding that cardiac and pulmonary capacities were impaired in the high- versus the low-HbA1c group, combined with the previous finding that 6 yr of normoglycemia improves aerobic capacity without any exercise training (20), highlights the potential importance of chronic glycemic control for athletes with type I diabetes.

It is unclear whether endurance training improves glycemic control in patients with type I diabetes. In contrast to studies on type II diabetes, where exercise training is clearly associated with improved glycemic control (27), the effects of endurance training on glycemic control in individuals with type I diabetes are equivocal (5,17,37). In the present study, there was an inverse correlation between weekly training volume and HbA1c in the subjects with diabetes (r 2 = −0.35, P < 0.05). These data and others (5,19) may indicate that endurance training modestly improves glycemic control. However, we believe that the most important interpretation of the present data is that endurance athletes with type I diabetes may receive a greater cardiopulmonary training response if they combine responsible glycemic control with aerobic training regimens. The low-HbA1c group had an average HbA1c of 6.5%, which is widely considered "good" glycemic control in this population (33). Although better glycemic control may have further improved the cardiopulmonary response to exercise in the low-HbA1c group, potential gains should be balanced by the increased risk of exercise hypoglycemia when blood glucose levels are maintained too low. For this reason, it would seem prudent for athletes with type I diabetes to consult a physician before intensive glycemic control during heavy physical training.

In summary, the cardiopulmonary response of endurance-trained subjects with type I diabetes and age- and sex-matched trained subjects without diabetes was not different. However, cardiopulmonary responses to peak exercise were greater in identically trained athletes with diabetes who maintained good versus poor glycemic control. These findings suggest that the cardiopulmonary capacity of athletes with type I diabetes is influenced by both training and glycemic control.

This study was funded by the University of Arizona and the Arizona Biomedical Research Commission.

The results of this study do not constitute endorsement by the American College of Sports Medicine.

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