Swimming exercise is an ideal and excellent form of exercise for patients with osteoarthritis (OA). However, there is no scientific evidence that regular swimming reduces vascular dysfunction and inflammation and elicits similar benefits compared with land-based exercises such as cycling in terms of reducing vascular dysfunction and inflammation in patients with OA. Forty-eight middle-aged and older patients with OA were randomly assigned to swimming or cycling training groups. Cycling training was included as a non–weight-bearing land-based comparison group. After 12 weeks of supervised exercise training, central arterial stiffness, as determined by carotid-femoral pulse wave velocity, and carotid artery stiffness, through simultaneous ultrasound and applanation tonometry, decreased significantly after both swimming and cycling training. Vascular endothelial function, as determined by brachial flow-mediated dilation, increased significantly after swimming but not after cycling training. Both swimming and cycling interventions reduced interleukin-6 levels, whereas no changes were observed in other inflammatory markers. In conclusion, these results indicate that regular swimming exercise can exert similar or even superior effects on vascular function and inflammatory markers compared with land-based cycling exercise in patients with OA who often has an increased risk of developing cardiovascular disease.
Swimming is a form of aerobic exercise that encompasses minimal weight-bearing stress, upper body exercise, and a reduced heat load and has been shown to improve vascular function in healthy older adults. For these reasons, swimming may serve as an excellent form of exercise for patients with osteoarthritis (OA) who suffer from an increased risk of cardiovascular disease. However, it is unknown whether swimming exercise would be beneficial for patients with OA, and there is no scientific evidence comparing swimming to land-based exercises in terms of reducing the risks of vascular disease in subjects with OA. The primary aim of the present study was to determine the effects of swimming and cycling exercise interventions on vascular function and blood markers that pertain to inflammatory disease pathways of OA. The working hypothesis was that both swimming and cycling exercises would result in improved central arterial stiffness and vascular endothelial function in middle-aged and older adults with OA. The secondary hypothesis was that improvements in vascular function with swimming exercise would be mediated by corresponding reductions in inflammatory cytokine levels.
Methods
A total of 48 sedentary middle-aged and older adults with radiographically verified OA were studied. Participants were recruited from the local community through flyers, e-mails, and information sharing. Among the 428 subjects responded, 364 were excluded through telephone screening, and 64 were further excluded through laboratory screening. Exclusion criteria were (1) strenuous physical activity > twice/week, (2) cardiac or pulmonary diseases, (3) joint replacement surgery, (4) intraarticular injection or systemic corticosteroid usage, (5) severe disabling co-morbidity, (6) aquaphobia, and (7) chronic tobacco smoking. The presence of OA was confirmed by x-rayusing the Kellgren–Lawrence grade. Institutional review board approved the study, and subjects gave their written informed consent.
Subjects were randomly assigned to either swimming or cycling exercise training groups. For the first few weeks, subjects received active coaching and instruction. Initially, participants exercised for 20 to 30 minutes/day and 3 days/week at an exercise intensity of 40% to 50% of heart rate reserve (HRR = [maximal heart rate − heart rate at rest] + heart rate at rest). The intensity and duration of exercise increased gradually with the goal of attaining 40 to 45 minutes/day and 3 days/week at an intensity of 60% to 70% of HRR. Exercise training lasted 12 weeks. During the course of the investigation, participants were instructed to maintain their usual lifestyle and dietary habits.
The swimming training was performed in the 25-yard long swimming pools, in which water temperature was held constant at 27 to 28°C. The cycling training was performed on a stationary cycle ergometer. Each participant received instructions to exercise continuously except during the time needed for checking a target intensity by heart rate monitor (Polar, Lake Success, New York).
Measurements were performed in the same order and at the same time of day on each participant after having refrained from food, alcohol, caffeine, and exercise for at least 8 hours before their arrival. All prescription and over-the-counter medicines and supplements were identical for 7 days before the pretesting and posttesting sessions. To avoid the acute effect of exercise, participants were studied at least 48 hours after their last exercise training session for the postintervention testing session. To minimize the “learning effect” or “training effect” associated with repeated tests, familiarization sessions were conducted before the initial testing sessions.
Three-day dietary records were collected and analyzed by the research bionutritionist using Nutritionist Pro software (Axxya Systems, Stafford, Texas). Physical activity level was assessed using a Godin questionnaire. Brachial and ankle blood pressure (BP), carotid-femoral pulse wave velocity (cfPWV), and heart rate were simultaneously measured by an automated vascular testing device (VP-1000plus; Omron Healthcare, Kyoto, Japan). Additionally, the right common carotid arterial diameter was imaged 1 to 2 cm proximal to the carotid bulb using an ultrasound machine equipped with a high-resolution linear array transducer (iE33 Ultrasound System; Philips Ultrasound, Bothell, Washington). Automated image analysis software (Carotid Analyzer; Medical Imaging Applications, Coralville, Iowa) was used to analyze all images. Analog output of carotid pressure waveforms was recorded (WinDaq 2000; Dataq, Akron, Ohio) for determination of central systolic BP and pulse pressure (PP) as well as for the subsequent determinations of carotid artery compliance (day-to-day coefficient of variation was 5 ± 2%), distensibility, and β stiffness index as previously described. Brachial artery flow-mediated dilation (FMD) was assessed using an ultrasound machine equipped with a high-resolution linear array transducer (Philips iE33 Ultrasound System) positioned 5 to 10 cm proximal to the antecubital fossa. A pneumatic cuff positioned 3 to 5 cm distal to the antecubital fossa was inflated to >100 mm Hg above systolic BP for 5 minutes (E20 Rapid Cuff Inflator, Hokanson, Bellevue, Washington). Diameter data were analyzed using automated image analysis software (Brachial Analyzer; Medical Imaging Applications).
Concentrations of immune/inflammatory markers were analyzed using a Millipore multiplex array in a Bio-Plex 200 analyzer (Bio-Rad, Hercules, California). Fasting blood concentrations of cholesterol, triglycerides, and glucose were determined enzymatically. Glycated hemoglobin concentration was measured using a commercially available kit (DCA Systems; Siemens, Tarrytown, New York).
The chi-square test was used to analyze group differences in categorical baseline variables, and continuous baseline variables were analyzed using an independent sample t test or the Mann–Whitney U test on the basis of the results from the Shapiro–Wilk test of normality. Data were analyzed using an intent-to-treat analysis with a multiple imputation. To ensure the validity of the intention-to-treat analysis, we also conducted per-protocol analysis of the 40 participants who completed the exercise intervention. A 2-way repeated measures analysis of variance was performed to compare outcomes of interest. When a significant effect was detected, paired samples t tests were used to assess intragroup differences.
Results
Most subjects were white (∼70%) and had OA in the lower limbs (∼90%). Baseline demographic and clinical characteristics are presented in Table 1 . At the baseline, swimming and cycling groups did not differ in age, gender distribution, and distribution of joint involved. The participants had excellent compliance to swimming (98%) and cycling (97%) training. The subjects in the swimming group used mostly freestyle (n = 10), breast stroke (n = 9), and a combination (n = 5). Four participants in each group dropped out before the end of the intervention. Intention-to-treat analysis of 48 participants, including 8 dropouts, was consistent with the per-protocol analysis of the 40 participants who completed the exercise interventions. Accordingly, we have only reported results from the intention-to-treat analysis.
| Variable | Cycling | Swimming | ||
|---|---|---|---|---|
| Before | After | Before | After | |
| Women/men (n) | 22/2 | – | 22/2 | – |
| Age (years) | 61±1 | – | 163±1 | – |
| Height (cm) | 163±2 | – | 59±2 | – |
| Body mass (kg) | 84.5±3.8 | 83.0±4.1 ∗ | 92.0±4.7 | 89.4±3.9 ∗ |
| Body mass index (kg/m 2 ) | 31.6±1.7 | 31.0±1.9 | 34.6±2.1 | 33.9±1.7 |
| Total caloric intake (kcal/day) | 1,831±160 | 1,864±175 | 1,856±167 | 1,894±179 |
| Protein intake (g/day) | 80±7 | 82±6 | 79±6 | 78±7 |
| Fat intake (g/day) | 73±9 | 78±6 | 72±5 | 74±6 |
| Carbohydrate intake (g/day) | 196 ± 15 | 199±11 | 189 ± 11 | 195 ± 12 |
| Alcohol intake (g/day) | 9±2 | 6±4 | 11±6 | 10±7 |
| Physical activity score (U) | 15±2 | 35±1 ∗ | 13±1 | 38±2 ∗ |
As depicted in Table 2 , there were no differences in brachial BP after either exercise intervention. Central systolic BP and PP decreased after both interventions (p <0.05; Table 2 ). Central arterial stiffness decreased (p <0.05; Figure 1 ), whereas carotid artery compliance increased (p <0.05) after both interventions ( Figure 2 ). Changes in carotid PP with exercise training were related to corresponding changes in carotid artery compliance (r = −0.43), carotid artery distensibility (r = −0.44), and cfPWV (r = 0.31; all p <0.05).
| Variable | Cycling | Swimming | ||
|---|---|---|---|---|
| Before | After | Before | After | |
| Systolic BP (mmHg) | 126±3 | 120±2 | 120±3 | 120±4 |
| Mean BP (mmHg) | 94±2 | 91±2 | 89±2 | 89±3 |
| Diastolic BP (mmHg) | 79±2 | 77±2 | 74±1 | 74±2 |
| Pulse pressure (mmHg) | 47±2 | 45±2 | 45±3 | 46±3 |
| Central Systolic BP (mmHg) | 105±8 | 100±9 ∗ | 100±8 | 97±11 ∗ |
| Central Pulse Pressure (mmHg) | 27±4 | 24±4 ∗ | 29±6 | 26±5 ∗ |
| Heart rate (bpm) | 68±2 | 68±2 | 67±2 | 62±2 |
| Carotid artery IMT (mm) | 1.4±0.4 | 1.2±0.4 | 1.2±0.4 | 1.2±0.3 |
As depicted in Figure 3 , endothelium-dependent vasodilatory function, as determined by brachial FMD, increased significantly after the swimming exercise (p <0.05). However, such increase in FMD was not observed after the cycling exercise.
There were no significant changes in fasting blood lipid profile or glucose concentration ( Table 3 ). However, glycated hemoglobin concentration decreased in both groups (p <0.05), whereas fasting glucose levels remained unchanged. Additionally, there were significant reductions in plasma cytokine concentrations of interleukin (IL)-6 in both groups.
