Health benefits of cycle ergometer training for older adults over 70: a review

As the number of older adults continues to increase worldwide, more attention is being paid to geriatric health care needs, and successful ageing is becoming an important topic in the medical literature. A preventive approach to the care of older adults is thus a priority in our aging societies. The purpose of this study was to update evidence for the health benefits of cycle ergometer training for older adults over 70. We searched online electronic databases up to September 2014 for original observational and intervention studies on the relationship between cycle ergometer training and health among older patients over 70. Twenty-five studies examined interventions aimed specifically at promoting cycling for older adults over 70. These studies reported a positive effect on the prevention of cardiovascular disease, and a significant improvement in metabolic responses. Improving functional status, muscle strength and cognitive performance are also well established. Overall, this review demonstrates a positive effect of cycle ergometer training with functional benefits and positive health outcomes for older adults over 70. Based on this evidence, clinicians can now encourage older adults to profit from the health benefits of cycle ergometer training to be able to pursue their daily activities independently.


Introduction
Physical activity (PA) is a modifiable behavior associated with health, functional status, and longevity, and encouraging a physically active lifestyle has become an accepted public health objective [1,2].
Concerning the general population, it is well known that regular physical activity (PA) ensures primary and secondary prevention of several chronic conditions [3]. Indeed, a large scale longitudinal 8-year study found that every additional 15 min of daily PA up to 100 min per day resulted in a further 4 % decrease in mortality from any cause [4].
The prevalence of sedentary behavior is higher in older adults, and is an independent health risk factor lead to an increase in the risk of developing numerous chronic diseases as well as all-cause mortality [5,6]. The risk of all of these diseases can be reduced by increased physical activity [7]. Further, evidence suggests that for older people, PA in later life can extend the period of active independent living, reduce disability and improve the quality of life [8]. Increasing PA thus helps minimize the burden on health and social care by improving healthy ageing [9,10].
It is well established that endurance exercise training is an effective strategy in older adults to reduce body fat mass, increase whole-body insulin sensitivity, and reduce the risk of cardiovascular disease [3,11]. It is also an effective strategy to protect older adults from falls and from some cancers (especially breast and colon cancer) [3].
The effectiveness of different modes of endurance exercise training on health such as cycle ergometer training (CET) [12], walking or jogging [13] and treadmill training [14] has been demonstrated in several studies. Among these modes of exercise, CET is particularly attractive because it is relatively easy and safe and causes no related injuries [15].
CET is usually a major component of any endurance exercise program that seeks to improve aerobic capacity and cardiovascular health [16]. Cycling is a healthy form of endurance exercise and, as a non-weight bearing activity, has less impact on the joints and is thus less stressful for the body than jogging or other running sports [17]. In addition, CET does not require as much postural control as walking on a treadmill and may be a better alternative for individuals with poor balance [18]. Finally, CET is feasible even for frail older individuals [19].
Up to now, the health benefits of CET for the general population are well established [20][21][22]. However, the effect of CET is less well documented in older adults [23][24][25][26] particularly those aged over 70 [27,28]. The aim of this review was thus to assess the health benefits of CET in this group.

Literature search
We conducted a systematic search for observational and intervention studies that examined the relation between cycle exercise training and the health of older adults published between April 1983 and June 2013. Published and peer-reviewed articles in English language journals were identified in electronic databases and on reference lists of articles available to the authors of this review.
The search terms 'exercise training, endurance training, or aerobic training and cycle ergometer, cycling or bicycle and health, health benefits and older adults, elderly, very old/elderly, aged, aging, oldest, old and over 70' were combined to search each of the eight electronic databases. The search resulted in a total of 4080 hits: Pubmed Central 3245, Medline 269, Scopus 237, Web of Science 129, SportDiscus 62, Embase 56, CINAHL Plus 50, Cochrane library 32. We also searched for previous systematic reviews, websites, and references therein.

Inclusion criteria and selection process
Based on the article titles and available abstracts, the reports were first evaluated for inclusion using the following criteria: Original research articles written in English, observational or intervention studies published in peer-reviewed journals with outcomes based on the use of bicycle ergometer, independently reported effects of cycle ergometer training (CET) in adults aged over 70, quantitative measures of CET for any purpose, measures of mortality or morbidity (including disease risk factors) and/or measures of health and cardiovascular function through CET.
Altogether 3964 articles were excluded for the following reasons: absence of controls studies, the outcomes were based on the use of real cycling, the studies focused on cycling injuries and accidents, and the studies evaluated physical activity in general, and not specifically CET.
A total of 116 potentially relevant papers were selected. Two authors independently evaluated them based on the inclusion criteria. This resulted in the additional exclusion of 85 studies. Thirty-one of the originally eligible studies were selected for detailed evaluation of the full text. After exclusion of six more papers based on the unanimous judgment of the two authors, 25 studies were selected for review (Fig. 1).

Data extraction
The selected studies were sorted according to authors, year of publication, mean age of sample, type of protocol and outcomes. The studies were divided into four groups based on four outcomes: cardiovascular function (Table 1), metabolic outcomes (Table 2), functional status (Table 3), and cognitive function (Table 4).

Effects on cardiovascular function
Effects on cardio-respiratory fitness Specific effects of cycle ergometer training (CET) on cardio-respiratory fitness were reported in eight of the 12 randomized studies [27,[29][30][31][32][33][34][35] (Table 1). Indeed, after a moderate endurance program on cycle ergometer, Lovell et al. [27,29] noted a significant increase in VO 2max (15 and 17 % respectively, p < 0.05) in the active group compared to the control group. Similarly, in older patients over 70, Buchner et al. [30] reported a 9 % increase in VO 2max (p < 0.05) after 78 endurance training sessions, with no significant change in the control group. Older subjects with a lower baseline VO 2max showed the greatest improvement in VO 2max (+29 %, p < 0.05) after CET, as shown by Babcock et al. [31]. In a small group of older people, Malbut et al. [32] reported a 15 % increase in VO 2max among women, and no significant change among men, after a 24-week program of CET at 75-80 % of VO 2max . In two small randomized studies, Coker et al. [33,34] observed a similar increase in aerobic fitness in both moderate and intermittent exercise groups as evidenced by a respective increase of 14 % and 21 % in VO 2max , as the result of CET. Conversely, Mangione et al. [35], reported no significant change in VO 2max in older patients in both high and low intensity cycle training groups.
According to these studies, moderate to high intensity of personalized CET, i.e., 30 min a day at least twice a week for a period of nine weeks seems to be useful for improving cardio-respiratory fitness among older adults over 70.

Effects on blood pressure
The benefits of CET on blood pressure in older subjects over 70 are less consistent and were reported in five studies [36,37,41,47,49] (Table 1). In a small randomized trial on healthy normotensive older patients, Nickel et al. [36] noted a significant decrease in systolic blood pressure (SBP) by 8 % after 15 min and in diastolic blood pressure (DBP) by 4 % after 24 h of CET at 50 % of heart rate reserve (HRR) in the active group compared to the control   CET cycle ergometer training, VO 2max maximum volume of oxygen, VT 1 first ventilatory threshold, MTP maximal tolerated power, HR heart rate, HRR heart rate reserve, VT 2 second ventilatory threshold, RPE rate of perceived effort,, VO 2 10 oxygen consumption of 10 ml/kg/min, P max maximal workload, SBP systolic blood pressure, DBP systolic blood pressure, IEx intermittent exercise, CEx continuous exercise, ↑ significant improvement within group, ↓ significant decrease within group, ↔ no change within group  CET cycle ergometer training, VO 2max maximum volume of oxygen, P max maximal workload, HRR heart rate reserve, BMI body mass index, MI moderate intensity, HI high intensity, ISGD insulin-stimulated glucose disposal, FT free testosterone, GH growth hormone, IGF-1 insulin like growth factor-1, SHBG sex hormone-binding globulin, LH luteinizing hormone, R a glycerol rate of appearance, FFA free fatty acid, ↑ significant improvement within group, ↓ significant decrease within group, ↔ no change within group Based on these studies, short-term CET seems to be associated in some extent with a significant decrease in SBP by 8-16 % and in DBP by 4-13 % in older adults over 70. This can be associated with a decrease in cardiac morbidity, stroke, and all-cause mortality.

Effects on endurance parameters
In this review, eight studies have shown that CET leads to significant improvement in endurance parameters of older adults over 70 [28,31,32,37,38,42,43,49] (Table 1). Vogel et al. [28] reported a significant increase in the first ventilatory threshold (VT 1 ) by 27.9 and 21.2 % (all, p < 0.05), respectively, in older men and women. Likewise, these authors reported a significant decrease in the heart rate (HR) at pre-training VT 1 (−6.2 and −5.2 %, respectively; p < 0.05) as well as in lactate concentrations at pretraining maximal tolerated power (MTP) (−23.4 and −20 %, respectively; p < 0.05), after nine weeks of CET. In a small group of older people, Morris et al. [38] reported that at the same relative intensity (50 % or 70 % of VO 2max ), interval exercise training resulted in a significant reduction in HR and oxygen uptake as opposed to continuous exercise training (p < 0.01). In a small group of older adults (72 ± 4.4 years old), Babcock et al. [31] reported a 21 % (p < 0.05) increase in oxygen uptake (VO 2 ) at VT 1 . However, they did not report any significant change in HR at VT 1 after 72 exercise sessions of CET. In another study in older men and women, Malbut et al. [32] reported a significant decrease in HR at VO 2 10 (heart rate at an oxygen consumption of 10 ml/kg/min) by 8 % (p < 0.05) and 15 % (p < 0.01) respectively, after 24 weeks of CET. Temfemo et al. [43] reported a significant increase in VT 1 (17 %, p < 0.05) in older patients after 8 weeks of CET at VT 1 . Finally, Schocken et al. [49], Haber et al. [42] and Finucane et al. [37] reported significant 10 % (p < 0.008), 16 and 16.5 % (p < 0.01) respective increases in the maximum workload, after 12 weeks of CET among older patients.
Based on these studies, short to medium-term of CET at an intensity of VT 1 appears to be an optimal way of improving endurance parameters among older adults over 70, specifically through an increase in the oxygen uptake by 21 %, in the mean VT 1 and maximum workload by 22 and 14 %, respectively. These improvements are important for seniors, and may contribute towards a better quality of life.

Effects on metabolic outcomes Effects on body composition
In this review, the effects of CET on body composition in older patients over 70 were evaluated in eight studies [27,33,34,37,40,41,46,51] (Table 2). Specifically, a 16-week CET program at 50-70 % of VO 2max resulted in a significant decrease in body mass and in the percentage of body fat (−2.6 and −5 % respectively; p < 0.05), with no significant change in fat-free mass in older patients [27]. In 100 healthy older adults, Finucane et al. [37] reported a significant decrease in total body mass (−10 %, p = 0.007), BMI (−0.4 %, p = 0.03), in waist circumference (−0.8 %, p = 0.02) and in intrahepatic lipids (−54 %, p = 0.024) in the exercise group compared with controls, whereas the same authors reported no significant alteration in fat mass and fat-free mass in the two groups after 12 weeks at 50-70 % of maximum power (P max ) of CET. However, there is evidence that the aforementioned exercise-induced adaptations can also occur independently of weight loss [51]. For example, Harber et al. [40] reported a significant decrease in fat mass (−3.9 %, p < 0.01) and in percentage body fat (−2.4 %, p < 0.01) with a significant increase in fat-free mass (−0.9 %, p < 0.01), without an overall decrease in body weight following 12-week of CET at 60 % of P max . Likewise, 16 weeks of CET at 70-85 % of HR max in older patients improved fat-free mass by 2 % (p < 0.05) without an overall decrease in body weight [46]. Conversely, three studies reported no significant change in body composition after 12 weeks of CET [33,34,41].
These outcomes suggest that 12-16 weeks of moderate to high intensity of CET may be an appropriate way to improve the body composition among older adults over 70, specifically by a significant decrease in the mean CET cycle ergometer training, HR max maximal heart rate, MMSEP mini mental state examination, ? significant improvement within group percentage of body fat and of body mass by 3.7 and 6.3 % respectively, and particularly by maintaining freefat mass. These data highlighted the importance of CET when designing weight management strategies among older patients over 70.

Effects on metabolic disorders
Specific effects of CET on metabolic disorders were reported in 4 studies [33,34,37,46] (Table 2). Indeed, Sial et al. [46] observed after 16 weeks of CET, a significant increase in the average rate of fat oxidation during exercise (33 %, p = 0.002), and a significant decrease in the average rate of carbohydrate oxidation during exercise (−19 %, p = 0.003). However, these authors did not report any significant change in the glycerol rate of appearance (Ra) and in the free fatty acid (FFA) rate of disappearance during exercise, but did report a significant 11 % decrease in glucose R a after the training program (p = 0.01) among older adults. Further, 12 weeks of CET 4-5 times per week (40 min per session) led to a significant increase in insulin-stimulated glucose disposal (ISGD) (28 %, p < 0.05) as well as in nonoxidative glucose disposal (NOGD) (30 %, p < 0.05) only in a high-intensity (HI) training group, with no significant change in the moderate-intensity (MI) training group [33]. In another study, 12 weeks of CET led to a slight (non-significant) increase in plasma adiponectin in both MI and HI training groups [34]. Conversely, Finucane et al. [37] reported no differences in fasting glucose, oral glucose insulin sensitivity and HbA1c between the training and control groups after 12 weeks of CET.
According to the above studies, short-term of CET can be in some extent an efficient strategy to prevent the metabolic disorders among older adults over 70, specifically through an increase in the fat oxidation and a decrease in the carbohydrate metabolism during exercise as well as by enhancing overall glucose disposal which have a positive effect on the regulation of glucose metabolism. This could have important clinical implications by increasing exercise capacity in this population.

Effects on endocrine function
Only two of the studies reviewed analyzed the effects of CET on endocrine function in older patients [29,50] ( Table 2). Zmuda et al. [50] reported a significant increase in serum testosterone, sex hormone-binding globulin (SHBG), total serum protein and the free testosterone index (39, 19, 13 and 23 % respectively; all p < 0.01) with no significant change in LH concentrations, during 60 min of CET at 50-80 % of HRR. After 48 sessions of CET, Lovell et al. [29] observed a significant 14 % increase in plasma concentration of testosterone, and of 15 % in free testosterone concentration (all, p < 0.05), with no significant change in growth hormone (GH), insulin like growth factor-1 (IGF-1) or in SHBG concentration.
According to these two reports, CET can have significant effects on the major male reproductive hormone, mainly through an improvement in the concentration of testosterone in plasma, which, in turn, may have cardiovascular protective effects in older adults over 70.

Effects on functional status Effects on muscle strength
This review shows that CET may be a sufficient stimulus to increase muscle strength and power in older patients over 70 through seven studies [27,29,30,32,40,41] (Table 3). For example, after 48 sessions of CET at 50-70 % of VO 2max (30-45 min/session), Lovell et al. [27] reported a significant increase in multiple muscle strength outcomes in older adults (i.e., leg strength (18 %), leg power (12 %), upper leg muscle mass (7 %), and total leg muscle mass (7 %), all p < 0.05). Similarly, Lovell et al. [29] observed a significant 18 % (p < 0.05) increase in leg strength and a 13.5 % (p < 0.05) increase in peak power after 16 weeks of CET in older patients. A 12-week exercise program (cycling 3-4 times/week, 20-45 min/session at 60-80 % of HRR) led to an 11 % improvement in quadriceps muscle volume, a 23 % increase in knee extensor power and a 31 % increase in knee extensor peak isometric force, as well as a 12 % increase in normalized power and a 20 % increase in normalized force (all, p < 0.05) [40]. Nine months of CET three times per week (∼35 min per session) increased the strength of the knee extensor by 10 % (p < 0.05), with no significant change in the strength of the other muscles [30]. Conversely, Perini et al. [41] did not report any significant change in quadriceps isometric strength or endurance after 8 weeks of CET. Likewise, Denison et al. reported no significant change between training and control groups in maximum grip strength after 12 weeks of CET at 50-70 of HR max . Finally, Malbut et al. [32] observed no effect of CET in isometric knee extensor strength, isometric elbow flexor strength or lower limb extensor power among older patients.
To summarize the above data, CET for 20-45 min, three times a week for 12-16 weeks at 50-70 % of VO 2max , is an efficient way of maintaining and improving muscle strength among older adults over 70, specifically through the development of leg and knee extension strength as well as the strength of the upper and total leg muscle mass.

Physical performance
Conflicting results have been reported concerning the effect of CET on the physical performance of older patients over 70 [30,35] (Table 3). In a randomized controlled trial, Buchner et al. [30] did not observe any significant improvement in gait and balance test, after 24 weeks of CET.
Denison et al., reported only a significant decrease in the 6 m timed up and go test (TUG) by 7 % (p = 0.04) in the training group compared to the control group, with no significant differences between groups in 3 m walk, eyes closed one-legged balance, and chair rise test after 12week of CET. In contrast, ten weeks of CET led to a significant improvement in chair rise time (−22 %, p < 0.001) and in the 6-minute walk test (9 %, p < 0.001) among older frail adults [35].
According to these three reports, short to medium-term CET modestly improve physical performance of older patients over 70, specifically through a decrease in the TUG as well as in chair raise time and an increase in the 6minute walk test. Nevertheless, further studies are needed to investigate the effects of long-term CET on the physical performance of this aged population.

Effect on cognitive function
To our knowledge, only one study has shown that CET can help improve cognition in frail older adults over 70 (Table 4). Indeed, Palleschi et al. [39] reported a significant improvement in cognitive performance, in particular an increase in the test of attentional matrix, the verbal span test, the supraverbal span test and the mini mental state examination (22,34, 71 and 12 % respectively; p < 0.0001), after 3 months of CET in a small group of older patients affected by Alzheimer's senile dementia.
According to the outcomes of this study, CET could be promoted in older adults as a cost-effective, efficient, and viable way to reduce cognitive dysfunction, but further studies are needed to confirm these finding among older patients over 70.

Principal findings
To our knowledge this is the first systematic review targeting the beneficial effects of cycle ergometer training (CET) on the health of older adults over 70.
According to the current evidence we suggest that CET is a suitable form of endurance training for promoting overall physical health among older adults over 70, particularly because it is relatively easy and safe and causes no related injuries. Further, as the upper body is less in motion in bicycle ergometer training than when the individual is walking on a treadmill, it is easier to record the vital signs and to collect blood samples especially for older frail individuals.
Overall, this systematic review included 25 published studies: 12 randomized studies and 13 non-randomized studies that analyzed the effect of CET on health outcomes among older adults over 70.
These studies suggest that CET has a positive impact on cardiovascular function through an improvement in cardiorespiratory fitness, blood pressure values and endurance parameters in older individuals over 70. Specifically, it helps control metabolic outcomes through an improvement in body composition, metabolic and endocrine disorders. CET also improves functional reserve capacity mainly by increasing muscle strength, with conflicting results concerning the physical performance. Finally, one study suggests that CET may improve also the cognitive performance in older adults over 70.

Comparison with other studies
Although several systematic reviews have already been published on the benefits of CET for the general population, to our knowledge, very few studies have focused on health benefits for older adults over 70.
Concerning the effect of cycling on cardio-respiratory performance, functional status and metabolic outcomes, our findings are in agreement with those of a systematic review by Oja et al. [20]. These authors analyzed the health benefits of cycling in middle-aged and older people. Their findings indicated clear improvement through enhancement of cardiovascular parameters, a consistent relationship between cycling and functional status through an improvement in muscle strength and regulation of metabolic function.
Although their review illustrates the potential positive relationship between cycling and health for the general population, it was not a systematic review focusing on a group of well-defined age, and it drew on a wide range of evidence. Our review provides more details on the health benefits of CET for older adults over 70, drawing on more specific intervention studies.
Valenzuela [52] studied the effect of progressive resistance training interventions in older adults aged between 80 and 89 in nursing homes. This study reported significant improvements in muscle strength and functional performance through a progressive resistance training exercise. Despite the difference in the type of training protocol, these results are in agreement with the results of our review because they also showed an improvement functional status.
On the other hand, concerning functional status, our review disagrees with the results of a review by Giné-Garriga et al. [53], who studied the effect of exercise training on functional status in frail older adults over 65. The authors of this review did not report any consistent effect of exercise training on functional status for older adults; this can probably be explained by the wide range of protocols they reviewed.
With increasing age, there is a well-described decline in voluntary physical activity, leading to an increased risk of frailty. In the present systematic review, we restricted the inclusion criteria to older adults aged over 70, whereas Keogh et al. [54] examined the effect of dancing in healthy older adults over 60. Despite the difference in the age of subjects and the type of training program, our review agrees with the results of the above review regarding the improvement in functional status and cardiorespiratory performance.
Finally, regarding functional status, our systematic review agrees with the review by Latham et al. [55], in which these authors demonstrate the beneficial effects of progressive resistance training in adults over 60.

Strengths and limitations of the review
The main strengths of this review are the comprehensive literary search and the inclusive approach to the types of interventions examined. We searched eight literature databases across a wide range of disciplines, while imposing as few limits as possible on our search.
The strong points of our review are first, we targeted a well-defined previously neglected population of older adults over 70, and second, we revealed robust performance outcomes.
As in all risk assessments, our review has a few limitations. First, we did not include publications that were not in English; so a language bias is possible. Second, the heterogeneity of the studies and of the training protocols made it difficult to establish precise outcomes concerning the intensity, frequency and duration of exercise training across studies. Third, the age limits we chose resulted in the exclusion of a large number of articles. However, given the current challenges of providing care for an aging population, we considered it important to select information that targeted this particular frail population.

Conclusion
Overall, this systematic review of studies on the effect of CET on the health of older adults over 70 revealed four different types of outcomes, cardiovascular function, metabolic outcomes, functional status, and cognitive performance.
Cycle ergometer training is particularly appropriate for older adults over 70 thanks to its ability to improve cardiorespiratory fitness, blood pressure values and endurance parameters. Further, CET is associated in some extent with a regulation of metabolic outcomes through an improvement in body composition and the prevention of metabolic and endocrine disorders. It has a positive effect on functional status by increasing muscle strength and in some extent enhancing physical performance. In this connection, it is worth emphasizing that this form of exercise is not only safer, but puts less stress on the joints of older adults than other typical components of exercise programs. Finally, CET may improve also the cognitive performance.
Clinicians can now use this evidence to formulate actions to enable older adults over 70 to profit from the health benefits of CET. This will reinforce the current public health efforts to improve the health of older adults, and to help them to continue pursuing their daily activities independently.