J Appl Physiol 114: 3–10, 2013.
First published October 11, 2012; doi:10.1152/japplphysiol.01107.2012.
New records in aerobic power among octogenarian lifelong endurance athletes
Scott Trappe,1 Erik Hayes,1 Andrew Galpin,1 Leonard Kaminsky,1 Bozena Jemiolo,1 William Fink,1
Todd Trappe,1 Anna Jansson,3 Thomas Gustafsson,2 and Per Tesch3,4
1
Human Performance Laboratory, Ball State University, Muncie, Indiana; 2Department of Laboratory Medicine, Clinical
Physiology Karolinska Instutet, Stockholm, Sweden; 3Mid Sweden University, Östersund, Sweden; and 4Department of
Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
Submitted 11 September 2012; accepted in final form 9 October 2012
aging; exercise; heart rate; oxygen consumption; skeletal muscle
MAXIMAL OXYGEN UPTAKE (V̇O2MAX) in humans was initially described in the 1920s by A. V. Hill (27, 28). Since then, V̇O2max
has been extensively profiled in numerous populations with the
upper limit ⬎90 ml·kg⫺1·min⫺1 in a 22-yr-old highly trained
elite cross-country skier (12). In contrast, a V̇O2max of ⬃17.5
ml·kg⫺1·min⫺1 [five metabolic equivalents (METs)] is the
prognostic exercise capacity for increased risk of mortality and
has recently been shown to be a more powerful predictor of
mortality than established risk factors for cardiovascular disease (41). The ⬃73 ml·kg⫺1·min⫺1 (21 METs) difference in
V̇O2max from the elite endurance athlete and prognostic exercise capacity for mortality represents the largest possible cardiorespiratory reserve in humans. Aerobic capacity is variable
Address for reprint requests and other correspondence: S. Trappe, Human
Performance Laboratory, Ball State Univ., Muncie, IN 47306 (e-mail: strappe
@bsu.edu).
http://www.jappl.org
(33), can be improved on the magnitude of 15–30% with
endurance training (21, 29), and is linked to genetic factors that
influence upper limits and trainability (56). Although V̇O2max
gradually declines across the life span and is well documented
among athletes and nonathletes from age 20 yr to ⬃75 yr (26,
43, 59), little information on V̇O2max and corresponding cardiorespiratory reserve in relationship to lifelong physical activity patterns is available in individuals ⬎80 yr of age.1 This
is an emerging knowledge gap for aerobic capacity given that
individuals living beyond age 80 yr are the fastest expanding
age demographic in our society (63).
We recently had the opportunity to examine aerobic capacity
in two cohorts of healthy independently living men ⬎80 yr old
with differing lifelong physical activity habits. One group
consisted of lifelong elite endurance athletes, who were still
actively engaged in competitive events, while the other group
only performed activities of daily living, with no history of
structured exercise. To complement the V̇O2max testing, we
obtained skeletal muscle biopsies from their legs to examine
the oxidative profile at the cellular and molecular level. We
hypothesized that the lifelong endurance athletes would have a
greater aerobic profile compared with the age-matched untrained men. The unique aspect of this investigation is that it
offers insight into cardiovascular and skeletal muscle health in
two distinct phenotypes of healthy octogenarians and establishes new upper limits for aerobic power in men 80 –91 years
of age.
METHODS
Subjects
Nine lifelong endurance athletes were recruited from a national list
of master’s cross-country skiers in Sweden. Criteria for inclusion to
the lifelong exercise group included a minimum of 50 yr of consistent
exercise training with no more than 6 mo of no training at any time
point in the past 50 yr. These endurance athletes included a former
two-time Olympic champion and several national and regional champions, with a history of vigorous aerobic exercise (4 – 6 days/wk) and
participation in endurance events (cross-country skiing, track and
field, and orienteering) throughout their entire adult lives. On average,
these veteran athletes had trained ⬃8 h/wk (range ⫽ 3–20 h) for the
past 50⫹ years. Six men with no history of consistent exercise
(beyond activities of daily living) were recruited from Muncie, Indiana, and served as healthy untrained controls. Subject profiles are
shown in Table 1.
All subjects were carefully screened for past exercise history by
filling out an extensive exercise and medical questionnaire and personal interview. All participants underwent a physical examination,
which included medical history, blood samples for general health
1
This article is the topic of an Invited Editorial by Joyner and Barnes (32a).
8750-7587/13 Copyright © 2013 the American Physiological Society
3
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Trappe S, Hayes E, Galpin A, Kaminsky L, Jemiolo B, Fink
W, Trappe T, Jansson A, Gustafsson T, Tesch P. New records in
aerobic power among octogenarian lifelong endurance athletes. J
Appl Physiol 114: 3–10, 2013. First published October 11, 2012;
doi:10.1152/japplphysiol.01107.2012.—We examined whole body
aerobic capacity and myocellular markers of oxidative metabolism in
lifelong endurance athletes [n ⫽ 9, 81 ⫾ 1 yr, 68 ⫾ 3 kg, body mass
index (BMI) ⫽ 23 ⫾ 1 kg/m2] and age-matched, healthy, untrained
men (n ⫽ 6; 82 ⫾ 1 y, 77 ⫾ 5 kg, BMI ⫽ 26 ⫾ 1 kg/m2). The
endurance athletes were cross-country skiers, including a former
Olympic champion and several national/regional champions, with a
history of aerobic exercise and participation in endurance events
throughout their lives. Each subject performed a maximal cycle test to
assess aerobic capacity (V̇O2max). Subjects had a resting vastus lateralis muscle biopsy to assess oxidative enzymes (citrate synthase and
␤HAD) and molecular (mRNA) targets associated with mitochondrial
biogenesis [peroxisome proliferator-activated receptor-␥ coactivator
1␣ (PGC-1␣) and mitochondrial transcription factor A (Tfam)]. The
octogenarian athletes had a higher (P ⬍ 0.05) absolute (2.6 ⫾ 0.1 vs.
1.6 ⫾ 0.1 l/min) and relative (38 ⫾ 1 vs. 21 ⫾ 1 ml·kg⫺1·min⫺1)
V̇O2max, ventilation (79 ⫾ 3 vs. 64 ⫾ 7 l/min), heart rate (160 ⫾ 5 vs.
146 ⫾ 8 beats per minute), and final workload (182 ⫾ 4 vs. 131 ⫾ 14
W). Skeletal muscle oxidative enzymes were 54% (citrate synthase)
and 42% (␤HAD) higher (P ⬍ 0.05) in the octogenarian athletes.
Likewise, basal PGC-1␣ and Tfam mRNA were 135% and 80%
greater (P ⬍ 0.05) in the octogenarian athletes. To our knowledge, the
V̇O2max of the lifelong endurance athletes is the highest recorded in
humans ⬎80 yr of age and comparable to nonendurance trained men
40 years younger. The superior cardiovascular and skeletal muscle
health profile of the octogenarian athletes provides a large functional
reserve above the aerobic frailty threshold and is associated with
lower risk for disability and mortality.
4
V̇o2 max in Octogenarian Lifelong Athletes
Table 1. Subject profile
Variable
Octogenarian Athletes
Untrained Octogenarians
Age, yr
Height, cm
Weight, kg
BMI, kg/m2
LBM, kg
Hb, g/dl
Hct, %
Glucose, mg/dl
Cholesterol, mg/dl
Daily Steps**
81 ⫾ 1
172 ⫾ 2
68 ⫾ 3
23 ⫾ 1*
50 ⫾ 2
14.0 ⫾ 0.3
42 ⫾ 1
95 ⫾ 3
183 ⫾ 11
8026 ⫾ 1210*
82 ⫾ 2
172 ⫾ 4
77 ⫾ 5
26 ⫾ 1
50 ⫾ 2
14.6 ⫾ 0.7
43 ⫾ 1
98 ⫾ 5
157 ⫾ 15
4347 ⫾ 1050
BMI, body mass index; LBM, lean body mass; Hct, hematocrit. *P ⬍ 0.05.
**Does include daily exercise for athletes.
Medications
Four of the nine octogenarian athletes were not taking any prescribed medication, three were taking cholesterol medication, and two
were taking blood pressure medication. One of the untrained controls
was not taking any prescribed medication. The other five men were
taking various cholesterol (n ⫽ 4), blood pressure (n ⫽ 2), thyroid
(n ⫽ 2), bladder/prostate (n ⫽ 3), or acid reflux medications (n ⫽ 1).
All subjects took over-the-counter pain medication on occasion.
Daily Physical Activity
Daily physical activity was indirectly assessed using a pedometer
(Lifecorder EX, New LifeStyles, Lees Summit, MO). Subjects were
asked to wear the pedometer for 2 wk and to put on the pedometer first
thing upon waking and take it off just prior to going to bed each night.
Total steps each day were assessed if the subject wore the pedometer
for a minimum of 12 h as noted by the first and last movement
recorded on each day. Any periods of time ⬎60 min of no recorded
movement was not included in the determination of the 12 h.
Body Composition
Following 30 min of supine rest, subjects were assessed for body
composition via dual X-ray absorptiometry (Lunar Prodigy full-body
scanner, Madison, WI). Data were analyzed using enCore 2008
software by GE Health Care. The scanner was calibrated each day
prior to the first scan.
Maximal Oxygen Consumption (V̇O2max)
Subjects performed a continuous incremental cycle ergometer test
with a 12-lead ECG to volitional exhaustion. The endurance athletes
warmed up at a 50-W load for two min at 60 RPM. Following the
warm-up, the watt load on the cycle ergometer was increased by 15
W/min in a ramped fashion until the subject reached volitional fatigue
or could not maintain a cadence of 60 rpm. Similarly, the untrained
men warmed up for 2 min at a 20-W load followed by a ramped
increase of 10 W/min until volitional fatigue or could not maintain a
cadence of 60 rpm. Oxygen uptake was measured breath-by-breath
Trappe S et al.
and averaged in 20-s intervals using indirect calorimetry via an
automated open circuit system (Ball State: Parvo Medics, Sandy, UT;
Karolinska: SensorMedics Vmax, Encore, 229; Viasys Respiratory
Care, Yorba Linda, CA). Both systems were calibrated with standardized gases before each test. In addition, the respective pneumotachs
were also calibrated before each test using a standard volume of air
(3-liter syringe).
Successful test criteria included a plateau in oxygen uptake with
increasing workload, achievement of age-predicted maximum heart rate,
a respiratory exchange ratio (RER) of ⬎1.10 or a rating of perceived
exertion ⬎19. A physician monitored all testing to ensure subject safety.
The average of the highest three consecutive 20-s time points during the
last 120 s of the test was used for the measure of maximal oxygen uptake,
maximum ventilation, and respiratory exchange ratio. Maximal heart rate
was determined from the 12-lead ECG and peak workload from the
highest watt output for a completed 20-s stage.
To compare the Karolinska Institute and Ball State University metabolic carts, a member of the investigative team (S. Trappe) performed a
cycle test on each system ⬃10-days apart. Because the highest workload
obtained by the subjects was 198 W, a comparison evaluation was
performed at 100, 150, and 200 W. The V̇O2 (l/min) data were nearly
identical between systems with values of 1.50, 2.11, and 2.78 l/min and
1.50, 2.08, 2.72 l/min, respectively on the two different metabolic cart
systems. The V̇O2 at these workloads was in agreement with the predicted
oxygen uptake and power output relationship (23).
Muscle Biopsy
The overall approach for the muscle biopsies was identical for the
octogenarian athletes and age-matched untrained men. Subjects were
asked to refrain from structured exercise and any physical activity
outside of normal activities of daily living for 24 h prior to the muscle
biopsy. Subjects consumed their normal evening meal and were
instructed not to ingest any additional food or caloric beverage until
after the muscle biopsy. Subjects arrived at the laboratory in the early
morning (⬃7:30 AM) by car and had a short walk into the laboratory.
Once in the laboratory, subjects rested quietly in the supine position
for 30 min. Following this rest period, a muscle biopsy was obtained
from the vastus lateralis (4). Muscle samples were divided into several
pieces, quickly frozen in liquid nitrogen, and stored at ⫺190°C for
later analysis of enzyme activity and mRNA levels.
Skeletal Muscle Enzymes
Oxidative enzymes were determined from a 10- to 20-mg portion
of the muscle specimen. Citrate synthase activity was determined
through the reduction of DTNB by the release of CoA-SH in the
cleaving of acetyl-CoA (13). ␤-hydroxyacyl-CoA dehydrogenase (␤HAD) was determined fluorometrically by an indirect measurement of
NADH disappearance (13). All samples were analyzed at the same
time using the same chemicals to limit any differences due to potential
variations in assays.
Skeletal Muscle mRNA
Total RNA extraction and RNA quality check. Total RNA was
extracted in TRI reagent (Molecular Research Center, Cincinnati,
OH). The quality and integrity [RNA integrity number of 8.32 ⫾ 0.06
(SE)] of extracted RNA [0.11 ⫾ 0.01 (SE) ␮g/␮l] were evaluated
using an RNA 6000 Nano LabChip kit on an Agilent 2100 Bioanalyzer (Agilent Technologies, Palo Alto, CA).
Reverse transcription and quantitative PCR. Oligo (dT) primed
first-strand cDNA was synthesized (150 ng total RNA) using SuperScript II RT (Invitrogen, Carlsbad, CA). Quantification of mRNA
levels (in duplicate) was performed in a 72-well Rotor-Gene 3000
centrifugal real-time cycler (Corbett Research, Mortlake, NSW, Australia). Housekeeping gene (HKG) GAPDH was used as a reference
gene, as we have previously described (31, 45). The expression of
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markers, resting ECG, and blood pressure. Participants were excluded
if they had any major acute or chronic illness, cardiac, pulmonary,
liver, or kidney abnormalities, uncontrolled hypertension, insulin- or
noninsulin-dependent diabetes, abnormal blood chemistries, arthritis,
a history of neuromuscular problems, or if they smoked tobacco.
Prior to volunteering for this research, all subjects were briefed on
the project objectives and testing procedures by a member of the
investigative team. Subjects were informed of the risks and benefits of
the research and gave their written consent in accordance with the
Human Subjects Institutional Review Boards at Ball State University,
Karolinska Institutet, and Mid Sweden University. This study was
conducted in accordance with the Declaration of Helsinki.
•
V̇o2 max in Octogenarian Lifelong Athletes
Table 2. Maximal aerobic power test data
Variable
Octogenarian Athletes
Untrained Octogenarians
2.56 ⫾ 0.06*
38 ⫾ 1*
52 ⫾ 2*
79 ⫾ 3*
160 ⫾ 5
16.1 ⫾ 0.5*
1.12 ⫾ 0.02
182 ⫾ 4*
1.62 ⫾ 0.14
21 ⫾ 1
32 ⫾ 2
63 ⫾ 6
146 ⫾ 8
11.4 ⫾ 1.4
1.19 ⫾ 0.03
131 ⫾ 14
V̇O2, l/min
V̇O2, ml 䡠 kg⫺1 䡠 min⫺1
V̇O2, ml 䡠 kg LBM⫺1 䡠 min⫺1
V̇E, l/min
Heart rate, bpm
O2 pulse, ml O2/beat
RER
Final workload, W
bpm, beats per minute. *P ⬍ 0.05.
Statistical Analysis
5
Trappe S et al.
the appropriate significance value based on whether equality of
variance was assumed or unassumed as determined by Levene’s
equality of variance test. Nonnormally distributed data were analyzed with a nonparametric independent t-test. The Pearson correlation test was used for the correlation analyses. All data are
presented as means ⫾ SE.
RESULTS
Maximal Aerobic Capacity
The mean ⫾ SE values for V̇O2max, ventilation, heart rate, O2
pulse, RER, and final workload achieved during the maximal
cycling test are shown in Table 2. Absolute V̇O2max (l/min) was
58% higher (P ⬍ 0.05) in the octogenarian athletes. When
expressed relative to body weight, V̇O2max (ml·kg⫺1·min⫺1)
was 80% higher (P ⬍ 0.05). The octogenarian athletes also had
25% higher ventilation and 41% higher O2 pulse (P ⬍ 0.05).
Although the maximal heart rate was, on average, 14 beats per
minute (bpm) higher in the endurance-trained men, this was
not significant because of the wide range in observed maximal
heart rates. No difference in the maximal RER was observed,
with both groups of men achieving levels above 1.10, which
was further confirmation of achieving maximal cardiorespiratory values. The maximal workload achieved during the test
was 51 W (⫹39%) greater (P ⬍ 0.05) in octogenarian athletes
compared with the untrained octogenarians.
Individual V̇O2max (ml·kg⫺1·min⫺1) data points for the octogenarian athletes and untrained octogenarians are shown in
Fig. 1. For comparison, representative V̇O2max data across the
life span are shown along with a prognostic value for exercise
capacity and mortality (5 METs).
Skeletal Muscle Enzymes
Normality of each variable measured was determined using a
qq-plot and the Shapiro-Wilk test. Those data that displayed a normal
distribution were analyzed using a parametric independent t-test with
70
Figure 2 shows oxidative enzyme activity for citrate synthase and ␤-HAD. Citrate synthase (⫹54%) and ␤-HAD
Octogenarian Athletes
Untrained Octogenarians
Normative Values for Healthy Men
Across the Lifespan (n=44,549)
60
95th P
.
VO2max (ml kg-1 min-1 )
ercen
tile - S
50
50th P
uperio
r
Fig. 1. Individual V̇O2max data from the octogenarian lifelong endurance athletes and
healthy untrained octogenarians. The dotted
line represents the prognostic exercise capacity [5 metabolic equivalents (METs),
17.5 ml·kg⫺1·min⫺1] generally necessary for
an independent lifestyle and associated with
an increased risk for mortality as described
by Meyers et al. (41). The normative values
for healthy men across the life span (n ⫽
44,549) were originally obtained from the
Cooper Institute in Dallas, TX, and have
been summarized by the American College
of Sports Medicine (1).
ercen
40
30
5th Pe
rcenti
tile
le - Ve
ry Poo
r
20
Independence
Dependence and
Risk of Mortality
10
0
20
30
40
50
60
70
80
90
100
Age (y)
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GAPDH was normalized to a second HKG, RPL01, to compare
GAPDH basal level between groups. All primers used in this study
were mRNA specific (on different exons and crossing over an intron)
and designed for quantitative PCR analysis (qPCR; Vector NTI
Advance 9 software) using SYBR green chemistry. Details about
primer characteristics and sequences for muscle peroxisome proliferator-activated receptor-␥ coactivator 1␣ (PGC-1␣) and mitochondrial transcription factor A (Tfam) have been reported previously by
our laboratory (14, 24, 64). A melting curve analysis was generated to
validate that only one product was present. The details about RT and
PCR reaction parameters have been reported previously (14).
The PGC-1␣ and Tfam gene expression between groups was
compared using the 2⫺⌬CT (arbitrary units) quantification method
(36). A serial dilution curve (cDNA made from 500 ng of total RNA
of human skeletal muscle; Ambion, Austin, TX) was generated for
each qPCR run to evaluate reaction efficiencies. The amplification
calculated by the Rotor-Gene software was specific and highly efficient (efficiency ⫽ 1.04 ⫾ 0.01; R2 ⫽ 0.99 ⫾ 0.00; slope ⫽ 3.22 ⫾
0.02).
•
6
V̇o2 max in Octogenarian Lifelong Athletes
-1)
20
*
Octogenarian Athletes
Untrained Octogenarians
18
-1
16
14
*
Enzyme Activity (
12
10
8
6
4
2
0
Citrate Synthase
-HAD
(⫹42%) were higher (P ⬍ 0.05) in the octogenarian athletes
compared with the untrained octogenarians.
Skeletal Muscle Basal Gene Expression
Basal levels of PGC-1␣ and Tfam mRNA were 135% and
80% greater (P ⬍ 0.05), respectively, in the octogenarian
athletes compared with the untrained octogenarians (Fig. 3).
Correlations
A positive correlation between V̇O2max and final workload
was observed (r ⫽ 0.94; P ⬍ 0.05). A low correlation was
observed between V̇O2max and maximal heart rate (r ⫽ 0.27).
V̇O2max was positively correlated to maximal ventilation (r ⫽
0.67; P ⬍ 0.05) and O2 pulse (r ⫽ 0.89; P ⬍ 0.05). Additionally, similar positive correlations were observed between
V̇O2max and each of the four skeletal muscle oxidative markers
(citrate synthase, ␤-HAD, PGC-1␣, and Tfam) from the vastus
lateralis muscle (r ⫽ 0.55– 0.61; P ⬍ 0.05).
Trappe S et al.
among octogenarians. The high aerobic power profile was
complemented by a robust skeletal muscle oxidative profile at
the cellular and molecular level. These data provide insight
into cardiovascular and skeletal muscle health in two distinct
phenotypes of healthy octogenarians and establish new records
for aerobic power in men 80 –91 yr of age.
The V̇O2max range for the nine lifelong exercisers was fairly
homogeneous (34 – 42 ml·kg⫺1·min⫺1), with seven men ⱖ36
ml·kg⫺1·min⫺1 and two men ⬎40 ml·kg⫺1·min⫺1 (Fig. 1). The
most unique individual in our group was a 91-yr-old former
Olympic champion with an aerobic capacity of 36 ml·kg⫺1·min⫺1
(2.36 l/min). Likewise, the untrained healthy octogenarians had a
homogeneous V̇O2max (17–24 ml·kg⫺1·min⫺1), with four of the
six men ⬎20 ml·kg⫺1·min⫺1 and the other two near the 5 MET
prognostic exercise capacity for increased risk of dependence and
mortality. For comparison, we identified 21 published studies that
measured aerobic capacity in individuals ⬎80 yr of age, and these
are summarized in Table 3. From these studies, a total of 464
individuals were identified with 42% men and 58% women. We
aggregated an average V̇O2max from reported mean data and, in
some cases, estimated individual data points presented graphically
in the papers. Overall, the average V̇O2max was 21 ⫾ 4
ml·kg⫺1·min⫺1 from the 195 men and 18 ⫾ 4 ml·kg⫺1·min⫺1
from the 269 women. For the men, this was identical to the
21 ⫾ 1 ml·kg⫺1·min⫺1 of the untrained men in our study. The
physical characteristics and physical activity levels from these 195
men were comparable to the untrained men in our study, and thus,
it is not surprising that the V̇O2max was similar. Only one study had
a subject population that was comparable to the octogenarian
athletes in our study. Harridge et al. (25) reported a V̇O2max of
27 ⫾ 5 ml·kg⫺1·min⫺1 (1.80 l/min) in five men ⬎80 yr with a
history of lifelong endurance exercise and were described as
highly active at the time of the physiological assessment. On
average, the octogenarian athletes in the current study had ⬃40%
greater aerobic capacity in both relative and absolute terms compared with the lifelong exercisers tested by Harridge et al. (25),
and ⬃80% greater than the age-matched untrained men profiled
by us and the other study populations summarized in Table 3.
DISCUSSION
Octogenarian Athletes
35
30
Arbitrary Units
The unique aspect of this investigation was the physiological
assessment of two cohorts of healthy independent living men
⬎80 yr old with different lifelong physical activity habits. The
endurance athletes had been engaged in vigorous aerobic
exercise their entire adult lives and were still active in various
competitive events and exercised 4 – 6 days/wk. The agematched untrained men had no history of structured exercise
but must also be considered a unique group of individuals
given their age, independent lifestyle, overall health profile,
and full engagement in the maximal testing efforts performed
in this study. The exercise routine and activities of daily living
resulted in the lifelong endurance athletes averaging ⬃3,700
more steps per day compared with the nonexercisers. However,
the ⬃4,300 steps/day of the untrained octogenarians constitutes a respectable amount of physical activity for individuals
in this age group, and it further highlights their overall mobility
and health status. The primary finding from this investigation
was the remarkably high aerobic capacity of the lifelong
endurance-trained athletes that are the highest ever reported
Untrained Octogenarians
*
*
25
20
15
10
5
0
PGC-1
Tfam
Fig. 3. Basal peroxisome proliferator-activated receptor-␥ coactivator 1␣
(PGC-1␣) and mitochondrial transcription factor A (Tfam) mRNA levels in
skeletal muscle from octogenarian lifelong endurance athletes and healthy
untrained octogenarian men.
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Fig. 2. Citrate synthase and ␤-hydroxyacyl-CoA dehydrogenase (␤-HAD)
skeletal muscle enzyme activity from octogenarian lifelong endurance athletes
and healthy untrained octogenarian men.
•
32
11
83 ⫾ 4
84 ⫾ 4
8
23
83 ⫾ 4
77–87
9
23
81 ⫾ 3
80–87
17
1
6
4
1
2
7
1
1
10
18
5
11
5
Men, n
90
⬎80
80–87
84
80
79–82
80–87
ⱖ80
ⱖ80
⬎80
83 ⫾ 4
80–87
83 ⫾ 3
80–90⫹
81 ⫾ 1
Age, yr
2
11
34
26
12
32
101
19
9
3
13
2
2
3
Women, n
T
T
T
T
C
C
C
T
C
T
C
C
C
C
C⫹T
T
T
T
T
T
C
C
1.23
1.31
1.61
1.81
1.49
1.47
1.30
1.80
1.38
1.30
1.52
1.31
144
18.2
138
137
21.8
22.2
15.8
15.1
16.2
18.5
18.3
19.4
22.9
26.3
133
131
154
154
144
25.9
18.4
139
141
Heart Rate,
bpm
23.0
23.8
21.1
15.4
27.1
21.1
21.0
21.7
V̇O2max,
ml 䡠 kg⫺1 䡠 min⫺1
Men
0.79
0.91
0.97
1.39
1.07
V̇O2max,
l/min
13.8
16.2
15.4
15.2
14.4
16.3
15.0
16.1
23.1
19.5
28.7
23.0
18.2
18.0
19.7
VO2max,
ml 䡠 kg⫺1 䡠 min⫺1
Women
126
129
144
138
135
131
143
128
Heart Rate,
bpm
Estimated from figure. bMean data presented in paper. C, Cycling; T, Treadmill. Two articles were not presented in the table because they were data from the same training program (18, 52).
Evans et al., 2005 (19)b
Healthy nonactive
Trained (24 wk AE)
Healthy nonactive
Trained (36 wk program)
Healthy nonactive
Trained (36 wk program)
Healthy nonactive
Trained (6 mo AE)
Healthy nonactive
Trained (40–48 wk AE)
Healthy active
Active
Healthy nonactive
Healthy nonactive
Healthy nonactive
Healthy nonactive
Not reported
Varied
Active (3d/wk)
Healthy nonactive
Vigorous Exercisers
Healthy nonactive
Healthy nonactive
Healthy active
Not clearly stated
Healthy active
Fitness Profile
V̇O2max,
l/min
Trappe S et al.
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J Appl Physiol • doi:10.1152/japplphysiol.01107.2012 • www.jappl.org
a
Independent living
Vaitkevicius et al., 2002 (61)b
living
living
living
living
living
Independent
Independent
Independent
Independent
Independent
Binder et al., 2002 (7)b
Independent living
Independent living
Physiologist
Senior center
Independent living
Independent living
Independent living
“Medically stable”
Independent living
Independent living
Independent living
Lifelong endurance
Independent living
Independent living
Independent living
Independent living
Independent living
Subject Population
Test
Mode
•
Training Studies
Malbut et al., 2002 (40)b
Lötscher et al., 2007 (37)a
Harridge et al., 1997 (25)b
Binder et al., 1999 (6)b
Paterson et al., 1999 (42)b
Malatesta et al., 2004 (38)b
Stathokostas et al., 2004 (53)a
Simar et al., 2005 (50)b
Cross-sectional Studies
Dill and Wasserman, 1964 (17)
Posner et al., 1987 (44)a
Fleg and Lakatta, 1988 (20)a
Babcock et al., 1992 (3)a
Toth et al., 1994 (57)a
Malbut et al., 1995 (39)b
de Wild et al., 1995 (16)a
Takeshima et al., 1996 (54)a
Reference
Table 3. Summary of literature on V̇O2max in men and women ⬎80 yr
V̇o2 max in Octogenarian Lifelong Athletes
7
8
V̇o2 max in Octogenarian Lifelong Athletes
Trappe S et al.
59). Although the high variability in maximal heart rate limits
our interpretation, these data provide a preliminary indication
that lifelong vigorous endurance exercise may attenuate the
decline in maximal heart rate among individuals ⬎80 yr of age.
The higher O2 pulse observed in the octogenarian athletes is
in agreement with previous studies on master athletes compared with age-matched nonexercisers (22, 43, 47). Oxygen
pulse, an indirect indicator of stroke volume, is typically ⬃25
ml/min in young endurance athletes (59) and declines ⬃40%
(to ⬃18 ml/min) in ⬃70-yr-old master athletes (43, 59). The 16
ml/min O2 pulse of the octogenarian athletes suggest a modest
⬃12% reduction with the additional 10 –20 yr of aging and
continued endurance training. It has been well established that
the cardiac tissue stiffens with age, which decreases compliance and overall performance of the heart (35). However,
lifelong endurance exercisers (⬃65–75 yr) have been shown to
maintain a large proportion of their cardiac function as they age
(2, 10, 48). A higher blood volume is associated with training
status and may be higher in older active individuals, which
would aid in heart dynamics (15, 32). Although we do not have
more detailed heart data or blood volume measures, the higher
O2 pulse and high correlation to V̇O2 max suggest enhanced
cardiac function among the octogenarian athletes compared
with the untrained men.
We observed higher maximal ventilation among the octogenarian athletes (range ⫽ 65–97 l/min) compared with the
untrained men (range ⫽ 34 –78 l/min). Seven of the nine
octogenarian athletes (78%) had maximal ventilation ⬎75
l/min, while only one of the untrained men (16%) achieved this
level. We observed a positive correlation between ventilation
and V̇O2 max, which has been previously reported among older
individuals with varying habitual activity levels (43). The
ventilatory efficiency (minute ventilation/V̇O2) was ⬃25%
lower among the octogenarian athletes and was comparable to
young (25 yr) and master-level (45– 65 yr) endurance-trained
men (22, 47, 59), suggesting that efficiency at the lungs was
relatively unchanged despite the diminished capacity observed
in the life-long endurance athletes.
The muscle biopsy data presented are the first from highly
endurance-trained octogenarian athletes. We observed a higher
oxidative profile of mitochondrial markers in the octogenarian
athletes compared with the untrained octogenarians. These data
suggest that lifelong endurance training enhances mitochondrial function in individuals ⬎80 yr of age. Similarly, middleaged (45–50 yr) and older (70 yr) lifelong endurance athletes
have a higher oxidative profile compared with untrained counterparts (30, 58). The differences in mitochondrial function
between the octogenarian athletes and untrained octogenarians
were comparable in magnitude to improvements with endurance training in young individuals (11, 21). It is important to
note that mitochondrial function normally declines with age,
and this decline does not appear to be reversible with endurance training in sedentary adults ⬎80 yr old or very old
animals (5, 18, 49). Consequently, maintaining a higher oxidative profile as a result of lifelong endurance training likely
provides these athletes with greater metabolic flexibility that
would be unique for this age category and result in numerous
positive health benefits. It must also be considered that in
addition to the lifelong endurance exercise of the octogenarian
athletes, genetic networks favorable for mitochondrial biogen-
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Recent studies have shown that all-cause mortality risk with
increasing exercise capacity reaches an asymptote at 10 METs
for men (8, 34). The ⬃11 MET exercise capacity of the
octogenarian athletes places them in the lowest mortality risk
category and further highlights the extraordinary cardiorespiratory fitness level of these men. For every 1-MET level
increase in exercise capacity above 5 METs, the mortality risk
is 12% lower (34, 41). On the basis of exercise capacity, the
octogenarian athletes have a ⬃50% lower all-cause mortality
risk compared with the untrained octogenarians. While exercise capacity is typically a modifiable risk factor, the trainability of the cardiorespiratory and skeletal muscle systems appears attenuated among octogenarians (19, 51). Thus, the large
cardiorespiratory reserve of the octogenarian athletes (⬃6 METs),
which is nearly equivalent to the exercise capacity of the untrained
men, may be even more important to remain above the threshold
for aerobic frailty, subsequent disability, and mortality (9, 34, 62).
It is also noteworthy that the high aerobic power achieved by
the octogenarian athletes is comparable to healthy nonendurance-trained men ⬃20 yr younger (75th percentile), ⬃40 yr
younger (50th percentile), and ⬃60 yr younger (20th percentile) (Fig. 1) (1). While the lifelong vigorous exercise routine of
these aging athletes was a key element to their high aerobic
capacity measured in our study, their elite athletic achievements as young adults (age 20 –30 yr) suggest they had aerobic
capacities at the upper range for humans. An estimated V̇O2 max
of 80 ml·kg⫺1·min⫺1 during their prime competitive years
would translate to a ⬃7.5% decline per decade in aerobic
capacity. This is comparable to previous longitudinal and
cross-sectional studies that have shown the decline in aerobic
capacity of highly trained master runners to be ⬃5–7% per
decade (26, 43, 59). However, data from these studies were
based upon subjects tested at ages ranging from ⬃45 to ⬃70 yr
old. Although data from the aging athletes of the current study
are limited to a single time point, they support the idea that a
5–7% decline in V̇O2 max with age can be extended to lifelong
endurance athletes in their 80s and 90s.
Decreases in maximal heart rate have generally been viewed
as the primary cause for a reduction in aerobic capacity with
age (22, 26, 55), although this is not universally accepted in
aging (⬎60 yr) athletes (47). The average maximal heart rate
of 160 beats/min in the octogenarian athletes was the highest
reported to date for this age group, but it should be interpreted
with some caution, given the high variability that we observed
among them (range ⫽134 –181 bpm). Six of the nine octogenarian athletes (67%) had a maximal heart rate ⬎160 bpm,
which included the 91-yr-old Olympian (169 bpm). Likewise,
the untrained men were also quite variable (range ⫽ 126 –168
bpm), with only two individuals (33%) that had a maximal
heart rate ⬎160 bpm. The untrained men’s average maximal
heart rate was similar to reports in the literature (Table 3). The
variability in heart rate among our subject populations was
higher than typically observed across the life span (⬍80 yr)
(55). The reason for this large variability is unknown, but may
be related to the age of the subjects, as several studies have
reported a large range in maximal heart rate in individuals ⬎80
yr of age (18, 25, 37, 42, 52). None of our subjects were taking
heart medications that would have directly influenced heart
rate. The higher heart rate of the octogenarian athletes challenges the idea that the decline in maximal heart rate with age
is typically independent of activity level (10, 22, 26, 43, 55,
•
V̇o2 max in Octogenarian Lifelong Athletes
ACKNOWLEDGMENTS
We would like to thank Tommy Lundberg, Rodrigo Fernandez Gonzalo,
and Kevin Murach for their technical assistance.
GRANTS
This research was supported by the National Institutes of Heath (NIH; Grant
AG038576 to S. Trappe), National Aeronautics and Space Administration
(NASA; Grant NNJ04HF72G to S. Trappe), Swedish National Space Board (P.
Tesch), Swedish Medical Research Council (T. Gustafsson), and Marianne &
Marcus Wallenberg Foundation (T. Gustafsson).
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the authors.
AUTHOR CONTRIBUTIONS
Author contributions: S.T. and P.A.T. conception and design of research;
S.T., E.H., A.G., L.K., B.J., W.F., T.T., A.J., T.G., and P.T. performed
experiments; S.T., E.H., B.J., and W.F. analyzed data; S.T., E.H., and L.K.
interpreted results of experiments; S.T. prepared figures; S.T. drafted manuscript; S.T., E.H., A.G., L.K., B.J., W.F., T.T., T.G., and P.T. edited and
revised manuscript; S.T., E.H., A.G., L.K., B.J., W.F., T.T., A.J., T.G., and
P.T. approved final version of manuscript.
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•