Archives of Gerontology and Geriatrics 31 (2000) 121 – 132 www.elsevier.com/locate/archger

Effects of aerobic physical exercise in the elderly with type 2 diabetes mellitus Daniel Tessier a,b,*, Julie Me´nard a, Tama`s Fu¨lo¨p b, Jean-Luc Ardilouze a, Marie-Andre´e Roy b, Nicole Dubuc b, Marie-France Dubois b, Pierre Gauthier b a Research Group in Diabetology, Centre de recherche clinique, Centre uni6ersitaire de Sante´ de l’Estrie, Sherbooke, Quebec, Canada b Research Centre in Gerontology and Geriatrics, Sherbrooke Geriatric Uni6ersity Institute, 375 Argyll, Sherbrooke, Quebec, Canada J1J 3H5

Received 17 May 2000; received in revised form 3 August 2000; accepted 4 August 2000

Abstract The objective of this study was to determine the impact of an aerobic physical exercise program in the treatment of a group of elderly patients with type 2 diabetes mellitus (DM) in relation to metabolic control, physical capacity, quality of life (QOL) and attitudes toward diabetes. Patients were randomly assigned to either an experimental (n=19) or a control (n=20) group. The following measurements were conducted at baseline and after week 16: glycosylated hemoglobin (hbA1c), fructosamine, 3 h oral glucose tolerance test, treadmill test (Balke–Naughton), and a questionnaire on QOL and attitudes toward DM. After the intervention, the experimental group showed a significant decrease of glucose excursion during the oral glucose tolerance test (OGTT) (area under the curve) (16.6 93.8 vs. 15.393.1, PB 0.05) and an increase in total time on the treadmill (s) (423 9 207 vs. 4719230, P B0.05). An improvement in the attitudes toward DM was observed in the experimental group (P =0.01) but not in the control group. Female gender, higher body mass index and hbA1c were factors associated with a response to the intervention. This study suggests that physical exercise has significant effects on glucose excursion during an OGTT and exercise tolerance in elderly patients with type 2 DM. © 2000 Elsevier Science Ireland Ltd. All rights reserved.

* Corresponding author. Tel.: +1-819-8211170, ext. 3254; fax: +1-819-8297145. E-mail address: [email protected] (D. Tessier). 0167-4943/00/$ - see front matter © 2000 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 1 6 7 - 4 9 4 3 ( 0 0 ) 0 0 0 7 6 - 5

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Keywords: Type 2 diabetes; Physical exercise; Quality of life

1. Introduction Type 2 diabetes mellitus (DM) has been characterized by an increase in hepatic glucose production, a deficit in insulin secretion and an increased resistance to its action (DeFronzo et al., 1992). Studies on normal and middle-aged diabetic subjects have shown that physical exercise results in numerous beneficial adaptations in skeletal muscles, including an increase in the expression of the glucose transporter GLUT 4 thus resulting in an increased sensitivity to the action of insulin (LeBlanc et al., 1981; Goodyear and Kahn, 1998). In the same population, physical exercise of either low or high intensity, was associated with a significant increment in insulin sensitivity (Braun et al., 1995; Mayer-Davis et al., 1998). The phenomenon of insulin resistance has been shown to characterize type 2 DM in elderly subjects (Meneilly et al., 1996) and in particular in the more obese group (Meneilly and Elliott, 1999). However, limited data are available on the role of physical exercise in the treatment of type 2 DM in the elderly. In a study with a small group of 14 diabetic men who were not on oral antidiabetic agent and who followed a training program over 2 years, Skarfors observed an improvement of physical performance but without observable metabolic change (Skarfors et al., 1987). In a recent study, a support program to promote physical activity failed to measure any change in the amount of physical exercise in an older population with type 2 DM (Samaras et al., 1997). In this respect, a position paper from the American Diabetes Association underlined the importance of physical training in the control of type 2 DM in subjects of all ages (American Diabetes Association, 1997). Two other studies suggested that in patients already taking sulfonylureas, the combination of physical exercise plus the oral agent is significantly more hypoglycemic than either modality of treatment alone (Massi-Benedetti et al., 1996; Gudat et al., 1998). However in daily practice, after the introduction of oral agents to control glycemia in type 2 DM, the role of physical training in the improvement of metabolic control is still not clear. It has been proposed that concepts related to personal-model beliefs and socialenvironmental barriers are pertinent to the self-management of DM (Glasgow et al., 1997). A survey study reported that in diabetic subjects, a lower level of physical activity was associated with a lower score on the assessment of the quality of life (QOL) (Glasgow et al., 1997). However, the effects of a structured physical exercise program in an older population with type 2 DM on parameters regarding QOL and attitudes, is an unanswered question. Consequently, a randomized study was conducted to examine the impact of an aerobic physical exercise program on parameters linked to metabolic control, physical performance, QOL and attitudes in a group of elderly ambulatory patients under treatment for type 2 DM.

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2. Subjects and methods

2.1. Study subjects The study protocol was approved by the Ethics Committee of the Sherbrooke Geriatric University Institute. Candidates for this study had to be 65 years and older at randomization, ambulatory outpatients, no acute medical illness in the last 6 months, stable pharmacological treatment for the last 3 months, no insulin injections or oral steroids and no active participation in a supervised exercise program. All subjects provided written consent before participating in the study.

2.2. Experimental design. After a baseline visit, each subject underwent a 3 h oral glucose tolerance test (OGTT), a blood evaluation for HbA1c, fructosamine [the methodology for these parameters has been previously published (Tessier et al., 1999)], a questionnaire on QOL and attitudes toward type 2 diabetes and a Balke–Naughton treadmill test. Afterward, each participant was then randomized to either an active physical training program (E) or to a control group (C). Subjects in the control group received instructions to continue with their usual activity regimen. The baseline assessment was repeated with each subject at week 16.

2.3. OGTT and laboratory parameters All subjects consumed a diet containing at least 200 g of carbohydrates per day for 3 days prior to each test. Studies were started at 08:30 h after a 12 h overnight fast. A dose of 75 g of glucose was ingested (Glucodex, Rougier, Canada). Blood specimens were drawn at baseline, 30, 60, 90, 120, 150 and 180 min for measurements of glucose and insulin after the ingestion of glucose. Glucose was measured by a glucose oxydase colorimetric method (Vitros, Johnson & Johnson Clinical Diagnostics, Rochester, NY), insulin by a radioimmunoassay procedure (Coat-ACount, Diagnostic Products, Los Angeles, CA), glycosylated hemoglobin (A1c labile fraction removed) by HPLC (Pharmacia, Upsala, Sweden), fructosamine by colorimetric method (Vitros, Johnson & Johnson Clinical Diagnostics, Rochester, NY).

2.4. Physical exercise program Patients in the (E) group trained three times a week under supervision during 16 weeks. Each session comprised: a warm-up phase (10 min (%)), a cardiovascular portion of rapid walk (20%), a strength/endurance portion consisting of two sets of 20 repetitions of major muscle groups (20%) and finally, stretching exercises and relaxation (10%) (Ericksonn, 1999). From baseline, exercise intensity required 35– 59% of the HRmax (which would be equivalent to 30–49% VO2max (American Diabetes Association, 1999a)) to reach 60–79% of the HRmax at week 4 (this should correspond to approximately 50–74% of the VO2max) until the end of this study.

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2.5. Treadmill test The Balke – Naughton treadmill protocol was used for this study. After a period of adaptation (10 – 30 s) with the treadmill speed at 2.25 miles/h, the first step was to increase treadmill speed to 2.5 miles/h on a horizontal plane for 2 min. On each successive step the treadmill slope was increased by 3°. With the goal of reaching a value of VO2max between 5 and 8 mets, this should correspond to a duration between 6 and 12 min on the treadmill test. The speed and slope changes for the treadmill test were in conformity with the recommendations of the American Heart Association (Fletcher et al., 1990). Blood pressure and electrocardiographic tracings were recorded during a minimum of 6 s at the end of every step (2 min) for heart rate calculation. Every test was conducted under the direct supervision of a physician and a skilled physical training educator. Each patient was asked to remain as long as possible on the treadmill although the subjects could terminate the test when they felt that they were giving their maximum effort. The physician could also interrupt the treadmill test according to the criteria established by the American College of Sports Medicine (American College of Sports Medicine, 1995). The calculation of the estimated maximum heart rate (HRmax) was carried out according to the Karvonen formula (estimated HRmax = 220− age).

2.6. QOL and attitudes questionnaire For the QOL concept, a self-administered questionnaire was used which has been developed by combining the Diabetes Quality of Life–DCCT Research Group (DCCT Research Group, 1988) and the Modified Quality of Life Measure for Youths (Ingersoll and Marrero, 1991). A score of 1 corresponds to the best QOL. In regard to the evaluation of attitudes, a questionnaire derived and translated from the one used by Dunn and colleagues was used (Dunn et al., 1986; Gosselin and Bergeron, 1991). A score of 5 reflects the most positive attitudes.

2.7. Dietary assessment No specific advice was given to change anything in the dietary habits of the subjects during this protocol. The total daily caloric intake was estimated with three 24-h dietary recalls on non-consecutive days, including a week-end day (Beaton et al., 1979; Dubois and Boivin, 1990; Payette and Gray-Donald, 1991; Tarasuk and Beaton, 1992).

2.8. Statistical analysis Considering the size of the sample, non parametric procedures were utilized. For between group comparisons, variables were analysed using the Mann–Whitney test for independent samples. Fisher’s Exact test served to compare the groups regarding the gender. The Wilcoxon signed rank test was used to make within group comparisons. The total area under the curve (AUC) for glucose and insulin was

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Table 1 Population description Experimental

Control

N Age (years) Female/male Duration of diabetes (months) Total energy intake (kcal/day)

19 69.3 9 4.2 7/12 51.39 51.0 1746 9 583

20 69.5 95.1 9/11 101.5 9 84.2 1588 9327

Drug treatment (mg/day) Glyburide (n)a Metformin (n)

11.0 96.6 (10) 13219 639 (14)

12.1 9 6.3 (12) 1400 9507 (15)

a

Number of patients under this medication.

calculated according to the trapezoidal rule. Results are expressed as mean9 1 S.D. All P values were computed for two-tailed tests.

3. Results Forty-five patients were randomized in this study. Six patients were lost to follow-up after randomization: five subjects in the experimental group and 1 subject in the control group. These six subjects were lost early in the study and refused to participate for personal reasons. Characteristics of the 39 other subjects are reported in Table 1. All the subjects were of caucasian origin. Parameters related to metabolic control are shown in Table 2. At baseline, there was no significant Table 2 Diabetes control, time on the treadmill and attitudes related parameters Experimental

HbA1c (%) Fructosamine (mmol/g prot) Fasting glycemia (pmol/l) Fasting insulinemia (pmol/l) AUC glycemia AUC insulinemia BMI (kg/m2) Weight (kg) Time on treadmill (s) Attitudes a

Baseline

Week 16

Baseline

Week 16

7.5 9 1.2 3.8 90.6 8.8 92.7 147 987 16.69 3.8 438 9 276 30.7 95.4 83.1 9 18.0 423 9207 3.439 0.44

7.6 9 1.2 3.7 90.5a 9.2 92.5 171 987 15.3 93.1b 400 9212 30.6 95.4 83.0 917.6 471 9 230b,c 3.55 90.41b,c

7.3 91.7 3.9 90.6 8.4 92.5 110 971 16.1 9 2.9 231 9108 29.49 3.7 79.4 914.3 405 9222 3.32 90.32

7.8 9 1.5 3.9 90.6 8.4 92.3 170 9 69 15.9 93.0 269 9131 29.4 93.8 79.5 914.6 401 9216 3.31 9 0.32

P= 0.08. PB0.05, versus baseline in the same group. c PB0.05 versus control group. b

Control

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Table 3 Female/male comparisons in the experimental group Female (n =7)

Hb A1c (%) Fructosamine (mg/g prot) Fasting glycemia (mmol/l) AUC glycemia Time on treadmill (s) Weight (kg)

Male (n =12)

Baseline

Week 16

Baseline

Week 16

7.4 9 1.3 3.8 9 0.6 9.5 93.5 17.6 95.1 316 9219 78.6 9 19.3

7.4 91.4 3.6 9 0.6 9.6 9 4.0 14.8 94.5a,b 369 9 201c 78.3 920.2

7.5 9 1.2 3.9 90.6 8.5 92.2 16.0 9 3.0 486 9180 85.8 917.4

7.5 9 1.1 3.8 9 0.5 8.9 9 1.1 15.5 9 2.2 543 9231 85.7 916.2

a

PB0.05. PB0.05 for change between groups. c PB0.01 versus baseline in the same group. b

difference between the experimental (E) and the control (C) groups. Compliance was measured by counting presence at each exercise session and was found to be \ 90% in the experimental group. Total daily caloric intake (kcal/day) did not change significantly in the control group during this study. A significant decrease in total daily caloric intake was observed in the experimental group (baseline: 17469 583, week 16: 1544 9 498, P B 0.01). However, it is not thought that this result is clinically significant since no weight loss was observed in this group (Table 2). When comparisons were made at week 16, a significant decrease was observed within the (E) group regarding the AUC for glycemia during the OGTT (P B 0.05) with no change in the AUC for insulin (Table 2). In the (E) group, a significant increase was observed for time on the treadmill (PB 0.05) (Table 2) with no significant change in the percentage of maximal heart rate reached (baseline: 88911%, week 16: 8999%, P \ 0.05). Consequently, it was hypothesized that the additional time spent on the treadmill is not the result of additional pressure being placed on the subjects to perform better during the second treadmill test. A trend was observed regarding the change of fructosamine in the (E) group (P= 0.08) (Table 2). No significant changes were observed in either group in regard to HbA1c, fasting glycemia, BMI and weight (Table 2). No significant change was observed in the dosage of either glyburide or metformin in patients taking these drugs: the changes that were observed in the AUC for glycemia during OGTT are not related to a change in the oral hypoglycemic drug dosage. Subgroup analyses was undertaken to delineate some characteristics of responders vs non responders within the (E) group. Considering the size of the sample, multivariate analysis was not possible. Compared to men, women had a significant decrease of the AUC for glycemia during the OGTT (PB 0.05) and a significant increase in time on the treadmill (PB 0.05) (Table 3). In regard to the baseline values for the women in the (E) group, a trend was noted for a higher AUC for glycemia during OGTT and a lower time on the treadmill, however, this was not statistically significant. Patients with a higher BMI had a significant improvement in

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Table 4 High/low BMI comparisons in the experimental group

HbA1c (%) Fructosamine (mg/g prot) Fasting glycemia (mmol/l) AUC glycemia Time on treadmill (s) Weight (kg)

High BMI (\30) (n =9)

Low BMI (B30) (n = 10)

Baseline

Week 16

Baseline

Week 16

7.6 9 1.1 3.7 9 0.5 8.99 2.5 15.8 92.9 3479 187 95.69 16.4d

7.49 1.1 3.6 9 0.4a 8.9 9 3.0 13.7 91.4b,d 441 9187c 95.3 915.7

7.4 91.3 3.9 90.7 8.8 93.0 17.2 94.6 491 9 209 71.9 910.4

7.8 91.4 3.8 90.6 9.5 92.1 16.7 9 3.6 505 9281 72.0 910.8

a

P= 0.1. PB0.05. c PB0.01 versus baseline in the same group. d PB0.05 between groups. b

the AUC for glucose during OGTT, fructosamine (PB 0.05) and time on treadmill (PB0.01) (Table 4). In subjects with higher values of HbA1c, a significant decrease of fructosamine and of AUC for glucose was observed during the OGTT (PB 0.05), however, no significant change was noted for HbA1c (Table 5). All these changes were observed in the absence of significant weight loss in the (E) group. Absence of significant change in regard to the HbA1c is probably related to the relatively short duration of this study. In regard to the QOL assessment, no significant change was observed for the total score in the 2 groups ([E], baseline: 1.81 9 0.47, week 16, 1.76 9 0.49, [C], baseline: 1.999 0.44, week 16: 1.9090.35, P \0.05). With respect to attitudes, the analysis on the total score showed a significant difference between the two groups in favor of the (E) group (P B 0.05) (Table 2). Table 5 High/low HbA1c comparisons (experimental group)

Hb A1c (%) Fructosamine (mg/g prot) Fasting glycemia (mmol/l) AUC glycemia Time on treadmill (se) Weight (kg) a

PB0.05. PB0.01 between groups. c PB0.05. d P= 0.1, with baseline. b

High HbA1c (\7.3%) (n =10)

Low HbA1c (B7.3%) (n =9)

Baseline

Week 16

Baseline

Week 16

8.391.0a 4.390.4b 11.0 92.4 18.6 94.2b 372 9169 89.7 921.5

8.3 91.1 4.1 90.5c 10.6 9 2.7 16.2 93.3c 432 9187d 89.3 9 21.2

6.7 90.6 3.4 90.5 6.9 9 1.0 14.8 9 2.4 468 9236 77.2 9 12.3

6.9 90.9 3.4 90.3 7.9 9 1.6 14.5 9 2.9 506 9 269 77.3 912.1

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Table 6 Summary of randomized trials on exercise in edlerly subjects with type 2 diabetes mellitus Program content/duration (weeks)

N

Age (year)a

Effectsa

Reference

1 2 2 1

64

62.49 5.9

38

56.7 96.2

Agurs-Collins et al., 1997 Raz et al., 1994

Monthly sessions (26 weeks)

26

60.5 9 7.8

2 sessions/week in a gymnasium, 1 session/week at home (104 weeks)

14

59.0 9 1.4

¡ weight 2.8% ¡ Hb A1c 1.1% ¡ Hb A1c 0.5%   work capacity 15% HbA1c: no change   VO2max 15.7% Hb A1c: no report

session/week for 12 weeks sessions/week for 12 weeks sessions/week in a gymnasium session/week at home (12 weeks)

a

Samaras et al., 1997 Skarfors et al., 1987

In the experimental group.

4. Discussion Mechanisms underlying the improved glucose tolerance in type 2 DM in conjunction with physical training include an increase in the glucose clearance rate associated with increased muscular blood flow and an increased ability to extract glucose (LeBlanc et al., 1981; Braun et al., 1995; Dela et al., 1995; Goodyear and Kahn, 1998; Mayer-Davis et al., 1998). A number of therapeutic intervention studies in middle-aged patients with type 2 DM have demonstrated that physical activity can play a role in the improvement of glucose tolerance and insulin sensitivity (Krotkiewski et al., 1985; Ro¨nnemaa et al., 1986; Schneider et al., 1992, 1994; Vanninen et al., 1992). These studies are either case controlled (Krotkiewski et al., 1985; Schneider et al., 1992, 1994) or randomized (Ro¨nnemaa et al., 1986; Vanninen et al., 1992). Simultaneous intervention with diet therapy was carried out in a number of these trials (Krotkiewski et al., 1985; Schneider et al., 1992; Vanninen et al., 1992). Significant weight loss was reported in three studies (Ro¨nnemaa et al., 1986; Schneider et al., 1992; Vanninen et al., 1992) and on occasion in the control group (Vanninen et al., 1992). Two other trials observed that the isolated dietary intervention is probably equivalent to the same intervention plus a physical exercise program in improving metabolic control in middle-aged subjects with type 2 DM (Bogardus et al., 1984; Larsen et al., 1997). These observations cast some doubt on the value of the physical training intervention in that population. In the present study conducted in elderly with type 2 DM, a significant improvement of AUC was observed for glucose and increased time on the treadmill with an exercise program alone without any dietary intervention and weight loss. Thus, the data suggest that physical training has a distinct effect per se on parameters linked to diabetes control and its influence appears to be independent of the dietary intervention.

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A limited number of randomized studies that have examined the effect of physical exercise, have targeted the elderly population with type 2 DM (Table 6). Skarfors did not observe any metabolic improvement in a small number of male subjects after a 2 year physical training program. In contrast, it was observed that females seemed to benefit more than males from physical training even in the absence of significant weight loss. This differential effect between females and males was also reported by another study in a middle-aged population with type 2 DM (Schneider et al., 1994). The exact reason for this gender difference cannot be determined at this point. One possible explanation for this observation is that insulin sensitivity appears to increase in females after either a low intensity or a high intensity physical training program (Braun et al., 1995). Another study recruited elderly overweight diabetic African–American subjects and randomized them to an experimental group and a control group (Agurs-Collins et al., 1997). The experimental group received dietary advice and physical training. Most of the subjects had an HbA1c higher than 10%. This study documented an improvement in HbA1c as well as a weight decrease in the experimental group after 6 months. Our study documented that caucasian subjects having an HbA1c B 10% associated with a pharmacological intervention and moderate obesity may also experience some benefits from an exercise program. However in our study, fructosamine demonstrated better correlation with glycemic changes than HbA1c. This is probably the result of the relatively short duration of the program (16 weeks with a graduation period in the first 4 weeks). In addition, no benefit from physical training could be demonstrated in patients with an HbA1c B 7.3%: the UKPDS study suggested that through an intensive pharmacological approach, a level of HbA1c close to 7% represents an optimal control (American Diabetes Association, 1999b), thus it is probably much more difficult to detect a statistically significant change by an additional intervention such as in this study. Meneilly observed that obese elderly patients with type 2 DM tend to be more insulin resistant than subjects with a lower BMI (Meneilly and Elliott, 1999). In this study, metabolic and exercise tolerance improvements have been observed primarily in those subjects with a higher BMI. The explanation is that by increasing physical activity, resistance to the action of insulin was lowered in the population with more insulin resistance and again, this study documented this phenomenon in the absence of significant weight loss. Since studies in middle aged patients with type 2 DM have shown that diet alone improves glycemic profile (Markovic et al., 1998; Williams et al., 1998), this study suggests that physical exercise has a complementary effect on diet treatment in obese patients with type 2 DM. We could not demonstrate any significant change between the two groups regarding the QOL. A major factor was the limited power due to the size of the sample. Most likely as the result of a ‘healthier volunteer’ selection bias, the QOL score that was obtained was on the ‘better side’ and consequently, the capacity to demonstrate an improvement was proportionally reduced. One also has to take into consideration the relatively short duration of the program. On the other hand, the intervention program did not negatively affect the QOL of the subjects in the experimental group despite three visits per week to the gymnasium. Motivation of

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the subjects in the experimental group was based on the presence of a qualified physical educator, social interaction with other participants and the variety of the physical training program. In this respect, subjects in the experimental group expressed their satisfaction in regard to the amount of time available for physical exercise as compared with the control group. The DCCT trial did not report a deterioration of the QOL in patients with type 1 DM who underwent intensive treatment of their disease (Anonymous, 1996). In summary, the evaluation did not detect any deterioration in the QOL in the older subjects who took part in a supervised physical training program. The assessment of attitudes toward DM is a relatively unexplored area in older patients with type 2 DM. This study observed an improvement in attitudes toward diabetes in an older population in spite of having to travel three times per week to a gymnasium. This improvement was identified without providing the subjects with any specific intervention to improve theoretical knowledge about DM. This point underlines that teaching may be successful in the older population with type 2 DM through the use of a behavioral approach based on positive reinforcement, and by avoiding confrontation in failure situations (Ahroni, 1996)). Personal beliefs have been mentioned as an obstacle for the subject with DM to integrate physical exercise into the treatment of this disease (Glasgow et al., 1997). In the authors’ opinion, the presence of a support group is an important element in treatment adherence and helps to bypass the obstacles thus facilitating the integration of a physical exercise program into the lifestyle of an older diabetic population (Gilden, 1992). In conclusion, regular physical exercise is a feasible and acceptable modality of treatment in the older ambulatory population with type 2 DM when optimal glycemic control has not been reached through diet and oral agents.

Acknowledgements We would like to thank the physical educator Claire Trempe for her active supervision of the exercise sessions, Krystyna Kouri from the Centre d’Expertise en Ge´rontologie et Ge´riatrie (CEGG Inc.) and the Quebec Diabetes Association for funding this study.

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