The Impact of Training on the Loss of Cardiorespiratory Fitness in Aging Masters Endurance Athletes

lite masters endurance athletes are considered models of optimal healthy aging due to the maintenance of high cardiorespiratory tness (CRF) until old age. Whereas a drop in VO 2max in masters athletes has been broadly investigated, the modifying impact of training still remains a matter of debate. Longitudinal observations in masters endurance athletes demonstrated VO 2max declines between 5% and 46% per decade that were closely related to changes in training volume. Here, using regression analyses, we show that 54% and 39% of the variance in observed VO 2max decline in male and female athletes, respectively is explained by changes in training volume. An almost linear VO 2max decrease was observed in studies on young and older athletes, as well as non-athletes, starting a few days after training cessation, with a decline of as much as 20% after 12 weeks. Besides a decline in stroke volume and cardiac output, training cessation was accompanied by considerable reductions in citrate synthase and succinate dehydrogenase activity (reduction in mitochondrial content and oxidative

was observed in studies on young and older athletes, as well as non-athletes, starting a few days after training cessation, with a decline of as much as 20% after 12 weeks. Besides a decline in stroke volume and cardiac output, training cessation was accompanied by considerable reductions in citrate synthase and succinate dehydrogenase activity (reduction in mitochondrial content and oxidative capacity). This reduction could largely be rescued within similar time periods of training (re)uptake. It is evident that training reduction or cessation leads to a considerably accelerated VO 2max drop, as compared to the gradual aging-related VO 2max decline, which can rapidly nullify many of the bene ts of preceding long-term training efforts. Keywords: aerobic exercise capacity; exercise training; training cessation; training (re)uptake; aging 1. Introduction Highly functional older individuals in general [1] and elite masters endurance athletes in particular are considered models of optimal healthy aging [2], which is characterized by the maintenance of a high level of cardiorespiratory tness (CRF) in older age. CRF can be assessed by individual maximal aerobic power (VO2max) [3,4]. Ample evidence attests a close association between CRF and endurance exercise performance with longevity [5–8]. Conversely, a decline in CRF is related to reduced endurance performance and an elevated risk of morbidity and mortality [9,10]. A landmark study by Saltin and colleagues [11] convincingly demonstrated a rapid loss of CRF when healthy and physically active indi- viduals became physically inactive (i.e., 20 days of bed rest). A relatively fast recovery and an increase in VO2max above baseline was observed during a subsequent 8-week training period [11]. Accordingly, high CRF, even if acquired and maintained through regular exercise training for many years (i.e., a typical condition for masters athletes), rapidly drops when training is ceased, e.g., due to injury or illness, jeopardizing the hard-earned exercise bene ts [12]. Whereas the aging-related decline in VO2max has been comprehen- sively evaluated in general and endurance-trained populations [6,13,14], the importance of maintaining appropriate training loads and, in particular, the consequences of short- and long-term training reduction/cessation and those of training (re)uptake in masters endurance athletes have been much

e.g., due to injury or illness, jeopardizing the hard-earned exercise bene ts [12]. Whereas the aging-related decline in VO2max has been comprehen- sively evaluated in general and endurance-trained populations [6,13,14], the importance of maintaining appropriate training loads and, in particular, the consequences of short- and long-term training reduction/cessation and those of training (re)uptake in masters endurance athletes have been much less investigated. However, regular and appropriate Int. J. Environ. Res. Public Health2022,19, 11050.

Int. J. Environ. Res. Public Health2022,19, 11050 2 of 19 training stimuli are of utmost importance to improve or maintain muscular performance and CRF [11,12]. Thus, here, we aim to evaluate and summarize longitudinal observations on VO2max changes related to training variations of masters endurance athletes in the long and short term. 2. Materials and Methods The present narrative review is reported following the IMRAD (introduction, methods, results, discussion) format [15]. A comprehensive search and screening strategy was used to identify relevant literature. PubMed and Web of Science were searched using combinations of terms covering the topics of training-related VO2max changes in masters endurance (primarily runners) athletes: (masters OR master OR endurance athletes OR elite runners) AND (VO2max OR aerobic power OR aerobic capacity) AND (humans) AND (aging OR older) AND (training). Studies that assessed VO2max changes longitudinally and reported associated changes in at least one parameter of training load were considered eligible for inclusion. We focused on studies that followed participants over several time points and/or evaluated participants of different age groups. In addition, we performed a literature search on studies reporting effects of short- term (up to 12 weeks) training cessation or training (re)uptake (beginning with training or training reuptake after training cessation) on VO2max and associated physiological changes. Because such data on masters athletes are scarce, a representative range of studies including young and older healthy subjects (initial VO2max > 25 mL/min/kg) was considered, with a focus on studies that followed participants over several time points. Data are presented descriptively. Multiple linear regression (stepwise variable selec- tion) was applied to evaluate the predictive importance of independent variables with respect to VO2max changes. Training volume, age, sex, the observation period (in years) and baseline VO2max (at the beginning of the longitudinal observation) were considered as independent variables. 3. Results Results of six long-term studies that satis ed our inclusion criteria on masters athletes reporting longitudinal changes in VO2max with aging and related changes of training characteristics are shown in Table. The number of the predominantly male participants in the various age groups ranged between 6 and 34. The

of the longitudinal observation) were considered as independent variables. 3. Results Results of six long-term studies that satis ed our inclusion criteria on masters athletes reporting longitudinal changes in VO2max with aging and related changes of training characteristics are shown in Table. The number of the predominantly male participants in the various age groups ranged between 6 and 34. The age of participants after follow-up varied between 46.5 and 82.8 years, and the observation periods ranged between 6 and 22 years (Table). The VO2max (mL/min/kg) decline per decade ranged from 5% to 46% per decade and was closely related to the changes in training volume (running, km/week) (Table, Figure). Studies reporting training intensities (running, min/km) indicate that training volume reductions parallel intensity reductions, except one of the female groups of a study by Eskurza et al., who increased training volume but reduced training intensity during follow- up [16]. Male masters who maintained near-normal training volume (not more than 10% reduction or maintenance of high training volume) showed a VO2max decline of between 5% and 6.5% per decade [17–21]. Those who reduced training volume by between 11% and 20% or were moderately trained showed a VO2max decline of between 8% and 26% per decade [17–21], and those with training volume reductions of more than 20% or who became almost sedentary had a VO2max decline of between 15% and 46% per decade [17–21]. Eskurza et al. and Hawkins et al. reported data on female athletes, also indicating a training-dependent loss of VO2max [16,21]. Regression analysis including male athletes [17–21] revealed a close association between reported VO2max reductions and related changes in training volumes with aging. Fifty-four percent of the variance in the observed VO2max decline was explained by training-volume changes (Figure), and this percentage increased to 70% when the age of the athletes was considered. No other variables improved the explanation

Int. J. Environ. Res. Public Health2022,19, 11050 3 of 19 of the VO2max decline. Within the groups of females [16,21], 39% of the variance in VO2max change was explained by changes in the training volume (Figure). Table 1. Longitudinal changes in VO 2max with aging and related changes of training characteristics in masters endurance athletes. Positive values of the training intensity measure (min/km) indicate a decrease in intensity. Reference N m (Males) f (Females) Observation Period (Years) Age (Years) Post VO2Max (mL/min/kg) Pre vs. Post (% Change) Change Per Decade Training V: Volume, km/Week I: Intensity, min/km Pre vs. Post (% Change) Eskurza et al., 2002 [16] 6 f 6 61.0 45.2 2.1 vs. 42.1 2.1 ( 7%) 12% V: 38.0 vs. 45.8 (+20) I: 5.3 vs. 5.6 (+5%) Eskuzra et al., 2002 [16] 10 f 6 56.0 50.0 2.2 vs. 43.8 2.2 ( 12%) 20% V: 62.0 vs. 42.0 ( 32%) I: 5.3 vs. 5.6 (+5%) Hawkins et al., 2001 [21] 31 m 9 53.5 58.7 1.7 vs. 50.4 1.5 ( 14%) 16% V: 61.8 vs. 43.6 ( 29%) Hawkins et al., 2001 [21] 34 m 8 62.2 53.4 1.4 vs. 46.2 1.4 ( 13%) 17% V: 56.2 vs. 43.3 ( 23%) Hawkins et al., 2001 [21] 13 m 9 71.1 46.2 2.5 vs. 36.4 2.6 ( 21%) 23% V: 43.8 vs. 37.5 ( 14%) Hawkins et al., 2001 [21] 8 m 7 82.8 41.5 3.1 vs. 28.4 2.7 ( 32%) 46% V: 49.4 vs. 26.7 ( 46%) Hawkins et al., 2001 [21] 24 f 8 51.2 48.7 1.6 vs. 45.2 1.2 ( 7%) 9% V: 55.1 vs. 37.7 ( 22%) Hawkins et al., 2001 [21] 16 f 8 58.3 46.7 1.3 vs. 40.8 1.8 ( 13%) 16% V: 39.4 vs. 31.8 ( 19%) Hawkins et al., 2001 [21] 9 f 8 73.2 39.4 1.6 vs. 31.8 2.8 ( 19%) 24% V: 43.6 vs. 26.6 ( 39%) Pollock et al. 1997 [19] 9 m 9.2 60.4 8.5 55.4 8.7 vs. 52.1 6.8 ( 6%) 6.5% V: 61 vs. 55 ( 10%) I: 4.9 vs. 5.2 (+6%) Pollock et al.

39.4 vs. 31.8 ( 19%) Hawkins et al., 2001 [21] 9 f 8 73.2 39.4 1.6 vs. 31.8 2.8 ( 19%) 24% V: 43.6 vs. 26.6 ( 39%) Pollock et al. 1997 [19] 9 m 9.2 60.4 8.5 55.4 8.7 vs. 52.1 6.8 ( 6%) 6.5% V: 61 vs. 55 ( 10%) I: 4.9 vs. 5.2 (+6%) Pollock et al. 1997 [19] 9m 10 70.4 8.5 52.1 6.8 vs. 43.2 6.3 ( 17%) 17% V: 55 vs. 35 ( 36%) I: 5.2 vs. 5.9 (+14%) Pollock et al. 1997 [19] 10 m 10 59.5 10.3 54.2 7.7 vs. 50.0 6.9 ( 8%) 8% V: 49 vs. 38 ( 12%) I: 4.9 vs. 5.4 (+10%) Pollock et al. 1997 [19] 10 m 10 69.8 10.2 50.0 6.9 vs. 40.8 9.5 ( 18%) 18% V: 38 vs. 27 ( 29%) I: 5.4 vs. 6.3 (+17%) Katzel et al. 2001 [20] 7 m 8.7 70 51.3 2.4 vs. 48.6 1.8 ( 5%) 6% highly trained (no essential change) Katzel et al. 2001 [20] 21 m 8.7 71 49.8 1.1 vs. 38.2 0.9 ( 23%) 26% moderately trained (volume and intensity reduction) Katzel et al. 2001 [20] 12 m 8.7 74 49.4 2.2 vs. 33.8 1.8 ( 32%) 36% not trained (rather sedentary) Rogers et al. 1990 [18] 15 m 8 62 54.0 1.7 vs. 51.8 1.8 ( 4%) 5% highly trained Trappe et al. 1996 [17] 10 m 22 46.5 68.8 vs. 59.2 ( 14%) 6% highly trained Trappe et al. 1996 [17] 18 m 22 46.5 64.1 vs. 48.9 ( 24%) 11% moderately trained Trappe et al. 1996 [17] 15 m 22 46.5 70.7 vs. 46.7 ( 34%) 15% not trained Few data on training cessation or training (re)uptake responses (physiological char- acteristics) in older masters are available. Thus, results of studies on young and older endurance athletes and healthy individuals reporting short-term changes in VO2max and related physiological changes due to training cessation or training (re)uptake were consid- ered for this analysis (Table).

acteristics) in older masters are available. Thus, results of studies on young and older endurance athletes and healthy individuals reporting short-term changes in VO2max and related physiological changes due to training cessation or training (re)uptake were consid- ered for this analysis (Table).

Int. J. Environ. Res. Public Health2022,19, 11050 4 of 19Int. J. Environ. Res. Public Health 2022, 19, x FOR PEER REVIEW 4 of 20 Figure 1. Relationship between VO2max decline and the reduction in training volume with aging of masters athletes (from data presented in Table 1) [16–21]. Circles indicate males, and triangles indi- cate females. Changes in the training volume explain 54% and 39% of the variance in VO2max changes in male and female masters athletes, respectively. Few data on training cessation or training (re)uptake responses (physiological char- acteristics) in older masters are available. Thus, results of studies on young and older en- durance athletes and healthy individuals reporting short-term changes in VO2max and related physiological changes due to training cessation or training (re)uptake were con- sidered for this analysis (Table 2). Table 2. Effects of short-term (up to 12 weeks) training cessation and training (re)uptake on VO2max and related changes of physiological parameters (cardiorespiratory parameters are maximal val- ues). Reference N m (Males) f (Females) Duration (Days) of Training Cessation (ce) Training (Re)Uptake (re) Age (Years) VO2max (mL/min/kg) Pre vs. Post (% Change) Changes in Related Physiological Parameters (% Change) Coyle et al., 1984 [22] 6 m 1 f 12 (ce) 29.1 ± 3.2 62.1 ± 3.3 vs. 57.7 ± 2.6 (−7%) heart rate (+4%) stroke volume (−10%) cardiac output (−7%) arteriovenous O2diff (+0.4%) oxygen pulse (−11%) citrate synthase (−17.1%) succinate dehydrogenase (−18.5%) Coyle et al., 1984 [22] 6 m 1 f 21 (ce) 29.1 ± 3.2 62.1 ± 3.3 vs. 59.7 ± 3.1 (−7%) heart rate (+4%) stroke volume (−11%) cardiac output (−8%) arteriovenous O2diff (+2%) oxygen pulse (−11%) citrate synthase (−23.7%) succinate dehydrogenase (−23.9%) Coyle et al., 1984 [22] 6 m 1 f 56 (ce) 29.1 ± 3.2 62.1 ± 3.3 vs. 53.2 ± 2.1 (−14%) heart rate (+6%) stroke volume (−14%) cardiac output (−9%) arteriovenous O2diff (−4%) oxygen pulse (−19%) citrate synthase (−40.6%) Figure 1. Relationship between VO 2max decline and the reduction in training volume with aging of masters athletes (from data presented in Table) [ 16–21]. Circles indicate males, and triangles indicate females.

± 3.2 62.1 ± 3.3 vs. 53.2 ± 2.1 (−14%) heart rate (+6%) stroke volume (−14%) cardiac output (−9%) arteriovenous O2diff (−4%) oxygen pulse (−19%) citrate synthase (−40.6%) Figure 1. Relationship between VO 2max decline and the reduction in training volume with aging of masters athletes (from data presented in Table) [ 16–21]. Circles indicate males, and triangles indicate females. Changes in the training volume explain 54% and 39% of the variance in VO 2max changes in male and female masters athletes, respectively. Table 2. Effects of short-term (up to 12 weeks) training cessation and training (re)uptake on VO 2max and related changes of physiological parameters (cardiorespiratory parameters are maximal values). Reference N m (Males) f (Females) Duration (Days) of Training Cessation (ce) Training (Re)Uptake (re) Age (Years) VO2max (mL/min/kg) Pre vs. Post (% Change) Changes in Related Physiological Parameters (% Change) Coyle et al., 1984 [22] 6 m 1 f 12 (ce) 29.1 3.2 62.1 3.3 vs. 57.7 2.6 ( 7%) heart rate (+4%) stroke volume ( 10%) cardiac output ( 7%) arteriovenous O2diff (+0.4%) oxygen pulse ( 11%) citrate synthase ( 17.1%) succinate dehydrogenase ( 18.5%) Coyle et al., 1984 [22] 6 m 1 f 21 (ce) 29.1 3.2 62.1 3.3 vs. 59.7 3.1 ( 7%) heart rate (+4%) stroke volume ( 11%) cardiac output ( 8%) arteriovenous O2diff (+2%) oxygen pulse ( 11%) citrate synthase ( 23.7%) succinate dehydrogenase ( 23.9%) Coyle et al., 1984 [22] 6 m 1 f 56 (ce) 29.1 3.2 62.1 3.3 vs. 53.2 2.1 ( 14%) heart rate (+6%) stroke volume ( 14%) cardiac output ( 9%) arteriovenous O2diff ( 4%) oxygen pulse ( 19%) citrate synthase ( 40.6%) succinate dehydrogenase ( 38.4%)

Int. J. Environ. Res. Public Health2022,19, 11050 5 of 19 Table 2.Cont. Reference N m (Males) f (Females) Duration (Days) of Training Cessation (ce) Training (Re)Uptake (re) Age (Years) VO2max (mL/min/kg) Pre vs. Post (% Change) Changes in Related Physiological Parameters (% Change) Coyle et al., 1984 [22] 6 m 1 f 84 (ce) 29.1 3.2 62.1 3.3 vs. 50.8 1.9 ( 18%) heart rate (+5%) stroke volume ( 13%) cardiac output ( 10%) arteriovenous O2diff ( 7%) oxygen pulse ( 20%) citrate synthase ( 39.6%) succinate dehydrogenase ( 32.5%) Cullinane et al., 1986 [23] 15 m 10 (ce) 28.2 5.6 61.3 6.2 vs. 61.2 5.6 ( 1.6%) heart rate (+5%) ventilation (+1.5%) stroke volume ( 2.6%) Doherty et al., 2003 [24] 7 f 10 (ce) 21.0 2.6 49.8 1.3 vs. 46.0 1.3 ( 7.6%) heart rate (+1.5%) stroke volume ( 1%) cardiac output ( 0.5%) arteriovenous O2diff ( 7%) Drinkwater and Horwath, 1972 [25] 7 f 90 (ce) 14-17 47.8 1.8 vs. 40.4 1.0 ( 15.4%) heart rate (+1.5%) ventilation ( 10.3%) Giada et al., 1998 [26] 12 m 60 (ce) 55 5 43 7 vs. 36 7 ( 16.3%) Giada et al., 1998 12 m 60 (ce) 24 6 59 10 vs. 49 9 ( 16.9%) Heath et al., 1983 [27] 6 m 2 f 10 (ce) 28 3 58.6 2.2 vs. 57.6 2.1 ( 1.7%) Houmard et al., 1992 [28] 9 m 3 f 14 (ce) 20.1 1.4 61.6 2.2 vs. 58.7 1.8 ( 4.6%) heart rate (+4.7%) plasma volume ( 5.1%) citrate synthase ( 25.3%) Katzel et al., 1997 [29] 10 m 90 (ce) 59 8 50 5 ( 11 to 20%) Martin et al., 1986 [30] 5 m 1 f 42 (ce) 26 1 62.7 4.0 ( 6.5%), 21 days; ( 20.3%), 56 days stroke volume 21 days ( 10%) 56 days ( 17%) Murias et al., 2010 [31] 8 m 21 (re) 68.0 7.0 28.3 7.1 vs. 30.7 6.0 (+8.4%) heart rate ( 3.5%) stroke volume (+6.8%) cardiac output (+7%) arteriovenous O2diff (+3.7%) Murias et al., 2010 [31] 8 m 21 (re) 23.0 5.0

4.0 ( 6.5%), 21 days; ( 20.3%), 56 days stroke volume 21 days ( 10%) 56 days ( 17%) Murias et al., 2010 [31] 8 m 21 (re) 68.0 7.0 28.3 7.1 vs. 30.7 6.0 (+8.4%) heart rate ( 3.5%) stroke volume (+6.8%) cardiac output (+7%) arteriovenous O2diff (+3.7%) Murias et al., 2010 [31] 8 m 21 (re) 23.0 5.0 48.0 6.1 vs. 53.8 7.6 (+12%) heart rate ( 2.1%) stroke volume (+5.5%) cardiac output (+3.1%) arteriovenous O2diff (+7.5%) Murias et al., 2010 [31] 8 m 42 (re) 68.0 7.0 28.3 7.1 vs. 32.8 7.6 (+15.9%) heart rate ( 2.1%) stroke volume (+9.1%) cardiac output (+11.3%) arteriovenous O2diff (+5.2%) Murias et al., 2010 [31] 8 m 42 (re) 23.0 5.0 48.0 6.1 vs. 52.5 6.4% (+9.4%) heart rate ( 2.1%) stroke volume (+7.9%) cardiac output (+5.4%) arteriovenous O2diff (+4.8%) Murias et al., 2010 [31] 8 m 63 (re) 68.0 7.0 28.3 7.1 vs. 34.0 5.8 (+20.1%) heart rate ( 1.4%) stroke volume (+15.2%) cardiac output (+17.9%) arteriovenous O2diff (+3.7%)

This review evaluates the impact of training on VO2max changes in aging masters athletes.