DAVIS Et Al 2008
DAVIS Et Al 2008
SORENESS BY PRE-RESISTANCE
CARDIOACCELERATION BEFORE EACH SET
W. JACKSON DAVIS,1 DANIEL T. WOOD,2 RYAN G. ANDREWS,2 LES M. ELKIND,3 AND W. BART DAVIS4
1
 Division of Physical and Biological Sciences; 2Office of Physical Education, Recreation, and Sports; 3Student Health Services,
University of California at Santa Cruz, Santa Cruz, California; and 4Engineering Division, Lawrence Berkeley National
Laboratory, University of California at Berkeley, Berkeley, California
                                                                   D
women), well-conditioned athletes paired by similar physical                     elayed-onset muscle soreness (DOMS) is a famil-
condition were assigned randomly to experimental or control                      iar and widespread adverse consequence of
groups. HR (independent variable) was recorded with HR                           unaccustomed or unusually intense physical
monitors. DOMS (dependent variable) was self-reported using                      activity or exercise. Symptoms can appear within
                                                                   hours, persist for as long as several days, and include pain (41),
Borg’s Rating of Perceived Pain scale. After identical pre-
                                                                   compromised muscle physiology and recovery (10,18,36,43),
training strength testing, mean DOMS in the experimental and
                                                                   reduced performance (18,19), increased risk of further injury
control groups was indistinguishable (P $ 0.19) for musculature
                                                                   (55), and reduced adherence to exercise programs (34,45).
employed in eight resistance exercises in both genders, vali-      Substantial research has therefore been devoted to strategies
dating the dependent variable. Subjects then trained three times   aimed at reducing DOMS, including behavioral approaches
per week for 9 (men) to 11 (women) weeks in a progressive,         (8,23,60,61), diet (12), supplements (37,54), systemic analge-
whole-body, concurrent training protocol. Before each set of       sics (3,38), and technological approaches (5).
resistance exercises, experimental subjects cardioaccelerated         Despite this research, DOMS has proved resistant to
briefly (mean HR during resistance training, 63.7% HR reserve),    amelioration. The most effective strategy for reducing DOMS
whereas control subjects rested briefly (mean HR, 33.5% HR         remains preceding exercise, termed the ‘‘repeated bout effect’’
reserve). Mean DOMS among all muscle groups and workouts           (44,47). The most successful behavioral strategies include
was discernibly less in experimental than control groups in men    yoga (8) and compression therapy (33), whereas the most
                                                                   effective dietary strategies include ingestion of the phospho-
(P = 0.0000019) and women (P = 0.0007); less for each
                                                                   lipid phosphatidylserine (30) or a carbohydrate-protein-
muscle group used in nine resistance exercises in both genders,
                                                                   antioxidant beverage (53). Supplements and analgesics have
discernible (P , 0.025) in 15 of 18 comparisons; and less in
                                                                   proven generally ineffective, although some technological
every workout, discernible (P , 0.05) in 32% (men) and 55%         approaches to DOMS reduction, such as transcutaneous
(women) of workouts. Most effect sizes were moderate. In both      nerve stimulation and its combination with cold (16), have
genders, mean DOMS per workout disappeared by the fourth           reduced DOMS moderately. Most strategies reported to
week of training in experimental but not control groups. Aerobic   reduce DOMS are ameliorative rather than preventive, none
cardioacceleration immediately before each set of resistance       has been shown directly to influence muscle recovery, and
                                                                   none has eliminated DOMS entirely.
                                                                      Finding a simple, effective, and inexpensive antidote and/or
Address correspondence to W. Jackson Davis, jackson@               prevention for DOMS could help to eliminate a major barrier
  MiracleWorkout.com.                                              to physical conditioning and exercise adherence at all levels.
1533-4287/22(1)/212–225                                            Moreover, any process or procedure that reduces or prevents
Journal of Strength and Conditioning Research                      DOMS may imply more rapid muscle recovery after an
Ó 2008, National Strength and Conditioning Association             exercise stimulus, which could benefit exercisers at all
             the                                         TM
levels—competitive athletics, recreational, and rehabilitative.   resistance exercises (1). Control subjects performed the same
In a research context, the discovery of an effective remedy for   resistance exercises at the same intensity, ensuring identical
DOMS could lead to a better understanding of its causes. We       eccentric muscle loading, but they rested briefly before each
therefore explored and report herein a new approach to the        set of resistance exercises to lower their HR during the sub-
management and elimination of DOMS induced by resistance          sequent resistance training to 20–39% of HRR, typical of
training; namely, aerobic elevation of heart rate (HR), or        anaerobic resistance exercises. Therefore, the primary
cardioacceleration, immediately before each set of anaerobic      difference between experimental and control groups was HR.
resistance exercises.                                                In both experiments, subjects reported DOMS for muscle
   The rationale for this approach to DOMS reduction is           groups used in every resistance exercise in every workout
based on its probable causes. DOMS is induced by eccentric        during several weeks of concurrent exercise training. The
or lengthening muscle contraction. In both human and animal       dependent variable (self-reported DOMS) was validated by
models, eccentric contraction immediately damages the             comparing DOMS induced by strength testing before and
muscle cytoskeleton and reduces contractile tension (20,39).      after resistance training, which was not discernibly different
Eccentric contraction also immediately compromises the            between the experimental and control groups. The in-
muscle membrane system, interfering with excitation-              dependent variable (HR) was validated by recording HR
contraction coupling (58), and alters the phospholipid            during resistance training and calculating mean values
membrane structure (22) and function (2,49). Eccentric            following the training program, which fell within the
exercise disrupts the sarcomere and myofibrils (e.g., 9 and 41,   prescribed ranges for experimental and control groups. The
but see 46). The collective cellular injury generates free        null hypothesis (elevated HR does not affect DOMS) was
radicals (6,36), edema (10), and inflammation products (17,42)    rejected in favor of the alternative hypothesis (elevated HR
that act as cellular mediators (24) to alter muscle sensory       reduces DOMS) if the mean DOMS reported by experimen-
systems (42), increase afferent discharge in muscle sensory       tal groups during resistance training was discernibly less than
receptors (56) and register centrally as the perception of        the mean DOMS reported by control groups at the 5% level
DOMS.                                                             (P , 0.05) and effect sizes (ES) were at least moderate.
   Elevated HR could intervene at any stage in this pre-
sumptive causal cascade to reduce DOMS and speed muscle           Subjects
recovery by increasing cardiac output and systolic blood          Identical experiments were conducted in successive years
pressure (1), enhancing muscle perfusion, and re-supplying        with 20 men and 28 women, undergraduate student-athletes
nutrients and other substances and clearing waste and injury      aged 18–22 years. The institutional review board evaluated
products faster. Resistance exercises that induce DOMS            and approved all aspects of the research program before
generally do not increase HR significantly (1), however,          implementation. After the recruitment of prospective subjects
because they are largely anaerobic, and the increase in blood     from university sport teams, the experiment was explained in
pressure caused by resistance exercises is brief and transient    a group setting without divulging its purpose. Each pro-
(40,48). In contrast, brief bouts of aerobic exercise performed   spective subject then signed a witnessed informed consent
immediately before each set of resistance exercises can           statement describing the risks, benefits, and responsibilities of
accelerate HR significantly, increasing cardiac output and        participation, and the option to withdraw at any time without
elevating systolic blood pressure chronically (1). Elevated       prejudice. Prospective subjects then underwent laboratory
HR could combine with exercise hyperemia (35,57) to               blood tests (lipid panel, electrolytes, fasting blood glucose)
increase muscle perfusion, accelerate sarcolemmal materials       and cardiovascular risk stratification (1). Athletes accepted as
flux, reduce or prevent eccentric contraction injury, promote     subjects were healthy, generally asymptomatic, and exhibited
faster muscle recovery, and reduce or prevent DOMS.               no more than one risk factor for coronary artery disease.
                                                                  After subjects were matched and assigned to experimental
METHODS                                                           and control groups as described below, mean demographics
Experimental Approach to the Problem                              were compared for the experimental and control groups (two-
Under this experimental rationale, we prospectively tested        tailed Wilcoxon matched-pairs sign-ranked tests). These com-
the hypothesis that aerobic cardioacceleration immediately        parisons revealed no discernible differences in age, body
before every set of resistance exercises reduces DOMS.            weight, height, or maximal aerobic capacity in men (Table 1)
Subjects matched as closely as possible were divided              (P = 0.10–0.95) or women (Table 2) (P = 0.11–0.65). Subject
randomly into experimental and control groups for several         demographics were therefore similar in the experimental and
weeks of concurrent exercise training. Experimental subjects      control groups.
performed brief, vigorous aerobic exercise immediately before
each set of resistance exercises to elevate their HR during       Procedures
subsequent resistance training to 60–84% of HR reserve            The overall design of this experiment included three phases
(HRR), typical of vigorous aerobic exercise and higher            (Figure 1a): pre-training assessments and instruction, con-
than can be achieved generally by conventional anaerobic          current exercise training and collection of data on the
   Figure 1. Graphic portrayal of the experimental design of this study. (a) Overview of the experiment. (b) Pre-training assessment and instruction sequence. (c, d)
   Training protocols used for experimental and control subjects, respectively. Within each section, the length of each horizontal bar is proportional to the duration of
   the corresponding component. The width of spaces between bars is not significant.
transmitter and wrist receiver during workouts to observe                                musculature, and recalled and reported most accurately
instantaneous HR, adjust aerobic work rate as required by the                            immediately upon completing the evaluation.
experimental design, and store mean HR data. DOMS was                                       Under a similar rationale, subjects recorded the RPE for
recorded for muscle groups used for each of the nine                                     each resistance exercise and the RPP for any non-DOMS pain
resistance exercises performed by each group, i.e., the eight                            experienced during that resistance exercise immediately upon
previously listed and weighted abdominal curl-ups on an                                  concluding the final set. At the end of each workout, subjects
inclined bench (Figure 1a). In every workout, subjects                                   recorded mean HR during the resistance exercise stage,
recorded the RPP for residual DOMS in the muscle group                                   stored in HR monitors; water consumption during the
used for each resistance exercise immediately after the third                            exercise session, measured to the nearest 0.1 l; data pertinent
(final) set using a purpose-designed workout log (15). The                               to a number of control variables, including aggregate RPE and
rationale for this procedure was that DOMS can be evaluated                              RPP for the entire exercise session; and other data. All data
most accurately during an exercise that utilizes the affected                            were recorded using a purpose-designed workout log (15).
   Experimental and control subjects performed three               (treadmill running), 10 minutes longer than the aerobic
vigorous workouts per week consisting of concurrent aerobic,       session of experimental subjects to help to compensate for
resistance, and range-of-motion (ROM) exercise (Figure 1c, d).     pre-resistance cardioacceleration time in experimental sub-
Experimental subjects performed integrated concurrent              jects and equalize the volume and intensity of aerobic exercise
training divided into three stages (Figure 1c): aerobic,           among the experimental and control groups. Control subjects
resistance, and a ROM cool-down. Experimental subjects             concluded each exercise session with the same ROM cool-
began each exercise session with a 20-minute aerobic               down as experimental subjects.
exercise warm-up (generally treadmill running) in which               During concurrent training, experimental and control
they rapidly attained and sustained a HR corresponding to          subjects performed the same nine resistance exercises in the
exercise of vigorous intensity, 60–84% of HRR (1), calculated      same sequence: lower body (seated inclined bilateral leg press,
using the Karvonen method. The rationale for prolonging the        seated leg [knee] extension, seated leg [knee] flexion or leg
warm-up was to induce sufficient cardiovascular fatigue to         curl) followed by upper body (seated front lat pull-down, flat
support more rapid subsequent cardioacceleration and to            bench press, overhead or military press, biceps or arm curl,
limit subsequent HR recovery in these well-conditioned             triceps kickback), and concluded with weighted abdominal
athletes, enabling experimental subjects to achieve and            curl-ups (crunches) on an inclined bench. The initial starting
sustain a higher HR during the resistance training that            weights for resistance exercises were 65% of 1RMs for men
immediately followed the warm-up.                                  and 50% of 1RMs for women. The rationale for beginning
   After the aerobic warm-up, experimental subjects began          with these relatively light weights was to minimize the risk of
integrated concurrent resistance training consisting of three      injury. The resistance weight was increased rapidly during the
sets each of the nine resistance exercises previously identified   first few exercise sessions to accommodate subjects’capacities
in the sequence listed. Immediately before every set of            (see below). The use of the same resistance exercises per-
resistance exercises, experimental subjects elevated their         formed at the same intensity ensured equivalent eccentric
HR to the upper portion of the vigorous range (60–84% of           muscle loading between experimental and control groups.
HRR) (1) by performing a short (0.5–1 minute) bout of              The use of different starting levels for resistance exercises
vigorous aerobic exercise (cardioacceleration), enabling them      between men and women did not influence the interpretation
to sustain an elevated HR through the subsequent set of            of results because all statistical comparisons were performed
resistance exercises. Experimental subjects used the cardio-       within genders.
vascular machine or exercise of their choice for cardioaccel-         To minimize extraneous variance and ensure equivalent
eration, usually treadmill running. Experimental subjects          eccentric muscle loading among groups, experimental and
concluded each exercise session with a cool-down consisting        control subjects used the same method of progression during
of 12 ROM exercises during which they reduced their HR             resistance training. For the first few exercise sessions, subjects
to the low end of the range corresponding to light exercise        in both groups were instructed to increase the weight used for
(20–39% of HRR) (1).                                               each resistance exercise as rapidly as necessary to achieve
   Control subjects performed serial concurrent training           three sets of eight repetitions for each resistance exercise with
divided into four stages (Figure 1d): warm-up, resistance,         an RPE no greater than 5 (‘‘strong’’ exertion) and an RPP no
aerobic, and a ROM cool-down. Control subjects began each          greater than 2 (‘‘weak’’ pain). This enabled subjects to increase
exercise session with a brief (5-minute) aerobic exercise          workloads rapidly but safely from the relatively light initial
warm-up in which they raised their HR to 60–84% of HRR             weight of 50% (women) to 65% (men) of 1RM weight to
using the cardiovascular exercise of their choice, usually         a heavier weight more appropriate to their capacities.
treadmill running. The rationale for abbreviating the warm-           After subjects reached this level, which occurred in the first
up was to minimize cardiovascular fatigue to support slower        two or three exercise sessions, advances in weight or
HR acceleration and faster HR recovery during subsequent           repetitions were prescribed for each resistance exercise when
resistance training, enabling control subjects to achieve and      the following five criteria were met: (a) the RPE for the
sustain a lower HR during the resistance training that             exercise assessed after the third (final) set was ‘‘strong’’ or less
immediately followed the warm-up.                                  (numerical value of 5 or less); (b) the aggregate RPE of the
   After the aerobic warm-up, control subjects began resis-        corresponding workout, recorded at its conclusion, was 5 or
tance training, consisting of three sets each of the same nine     less; (c) the RPP for DOMS during each resistance exercise
resistance exercises performed by experimental subjects and        assessed after the third set was ‘‘weak’’ or less (numerical value
in the same sequence. Immediately before every set of              of 2 or less); (d) the RPP for non-DOMS pain during each
resistance exercises, control subjects lowered their HR to the     resistance exercise assessed after the final set was 2 or less; and
low end of the range corresponding to light-intensity exercise     (e) aggregate RPP for the corresponding exercise session was
(20–39% of HRR) by resting briefly (0.5–1 minute) in a seated      2 or less.
position, enabling them to sustain a lowered HR during the            When these five criteria were met, either the number of
subsequent set of resistance exercises. Resistance training        repetitions per set or the weight per exercise was increased
was followed by 30 minutes of vigorous aerobic exercise            and entered immediately into workout logs as the
           the                                        TM
prescription for the corresponding resistance exercise in the      Quantitative results are reported as the mean 6 standard
next workout. Repetitions per set began at eight, increased on     error of the mean.
progression by one or two to a maximum of 12, and reverted
to eight when weight was increased. Weight was increased           RESULTS
upon progression by 5 lb for small muscle groups (generally        To evaluate and validate the dependent variable (self-reported
upper body) and 10 lb for large muscle groups (seated lat pull-    RPP for DOMS), the DOMS induced by identical strength
down and lower body). This method of progression was easy          testing was recorded by all subjects every 12 hours for 48
in practice for athletes to learn, and they implemented it         hours after both pre-and post-training 1RM trials. DOMS in
without difficulty within one or two workouts.                     the four measurements was recorded separately for muscle
   Several additional control and monitoring procedures were       groups used in each of eight resistance exercises listed in the
implemented to minimize extraneous variance and ensure             methods (abdominal curl-ups excluded). Before training in
identical eccentric muscle loading among groups. Experi-           men, mean DOMS per measurement for all eight muscle
mental and control training protocols were equalized for           groups after strength testing was not discernibly different
exercise modes, types, volume, intensity, and duration             between experimental and control groups (2.5 6 1.4 and
(approximately 1.8 hours). Experimental and control groups         2.6 6 1.4, respectively; two-tailed Wilcoxon test, n = 9, P =
exercised on different floors of the same training facility        0.19). Similarly, before training in women, mean DOMS
during the same morning hours (6:00 to 10:00 AM) of the            per measurement for all eight muscle groups after strength
same days (Tuesday, Thursday, and Saturday). Supervising           testing was not discernibly different between experimental
trainers alternated between the two groups several times in        and control groups (5.0 6 2.7 and 4.8 6 3.8, respectively;
each exercise session to preclude differential training effects    two-tailed Wilcoxon test, n = 13, P = 0.81). After training,
or motivational influences. Prescribed HR ranges for each          mean DOMS per measurement for all eight muscle groups
subject were registered in their HR monitor as lower and           after strength testing in women was not discernibly different
upper limits to assist compliance with HR prescriptions and        (3.5 6 3.1 and 4.5 6 3.5 for experimental and control groups,
were confirmed after training as reported in the results.          respectively; two-tailed Wilcoxon test, n = 8, P = 0.78). Mean
   Post-training assessments and debriefing (Figure 1a)            DOMS after training was not evaluated in men because of an
followed the same format, procedures, and sequence as              inadequate sample size resulting from incomplete data and
pre-training assessments, including measurements of muscle         withdrawal of some subjects.
strength, muscle endurance, and Vo _ 2max. To conclude each           DOMS after pre-training strength testing was then
experiment, every subject completed a written evaluation of        analyzed for each of the above eight muscle groups separately.
the training program in the form of a questionnaire that           Mean DOMS for lower body exercises exceeded that for
contained an embedded question asking the purpose of the           upper body exercises almost 2:1, discernibly different in both
experiment. No subject answered the question correctly,            genders (men: two-tailed t-test, n = 9, P = 0.001; women:
indicating that the experimental protocol was blind. Because       two-tailed t-test, n = 13, P = 0.001). For each of the muscle
subjects who were unaware of the purpose of the experiment         groups corresponding to the eight resistance exercises
also self-reported the dependent variable (DOMS), the              performed, the mean DOMS per measurement (Figure 2)
experimental protocol was double-blind.                            after identical strength testing was in no case discernibly
                                                                   different between experimental and control groups in either
Statistical Analyses                                               gender (two-tailed Wilcoxon tests; men: n = 9, P = 0.44–0.86;
All data were entered into electronic spreadsheets, and entries    women: n = 13, P = 0.23–1.0). Experimental and control
were confirmed by trained personnel before statistical analysis    groups in both genders therefore self-reported DOMS
and graphical display. The Wilcoxon test (29) was used for         induced by the same relative exercise exertion (maximal)
most comparisons of means. Student’s t-test was used to            similarly for every muscle group using the RPP scale. This
compare DOMS means in different exercise sessions (Figure 4)       outcome was prerequisite to the use of self-reported DOMS
because the underlying assumptions of normality and inde-          as the dependent variable and comprises a necessary and
pendence were justified. All hypotheses were tested at the 5%      sufficient validation of the dependent variable (RPP for
level (P # 0.05). Exact probabilities associated with most         DOMS) for use in the current experimental application.
tests are reported to permit critical evaluation of differences.      To test the main hypothesis (elevated HR reduces DOMS),
ES was calculated using the Cohen d method (51), and               DOMS induced by nine resistance exercises during training
differences in means were characterized using the ranges and       (the previously listed eight plus abdominal curl-ups) was first
descriptive terminology for highly trained individuals (ES ,       averaged among all muscle groups and all workouts
0.25, ‘‘trivial;’’ ES = 0.25–0.50, ‘‘small;’’ ES = 0.50–1.0,       separately for experimental and control groups. In men, the
‘‘moderate;’’ and ES . 1.0, ‘‘large.’’). Unless otherwise noted,   experimental group mean DOMS (1.4 6 0.5) was less than
statistical tests were one-tailed. Sample sizes varied because     one-fourth the control group mean (6.3 6 1.4), discernibly
of missing data from some subjects for some tests and are          smaller (Wilcoxon test, n = 28 workouts, P = 0.0000019;
therefore reported separately for each statistical test.           ES = 0.66, moderate). In women, the experimental group
                                                                                                                 DISCUSSION
                                                                                                                      The main finding of this study is
                                                                                                                      that physiologic DOMS caused
                                                                                                                      by conventional anaerobic re-
                                                                                                                      sistance exercises is reduced
                                                                                                                      immediately and eliminated
                                                                                                                      within 4 weeks by aerobically
                                                                                                                      elevating HR before each set in
                                                                                                                      comparison with control sub-
                                                                                                                      jects who did not elevate HR.
                                                                                                                      Several potentially confound-
                                                                                                                      ing variables, including differ-
                                                                                                                      ential eccentric muscle loading,
                                                                                                                      the method of using the RPP
                                                                                                                      scale to report DOMS, actual
                                                                                                                      and perceived exercise exer-
                                                                                                                      tion, water consumption during
    Figure 4. Time series showing mean delayed-onset muscle soreness (DOMS) per exercise session summed over          exercise sessions, and compli-
    all muscle groups used in nine resistance exercises during 9 weeks (men; a) to 11 weeks (women; b) of concurrent
                                                                                                                      ance with training sessions,
    exercise training. Experimental groups (cardioacceleration before each resistance exercise) reported less DOMS
    than control groups (rest before each resistance exercise) for every exercise session in both genders. *Control   were eliminated. None differed
    means discernibly larger than the corresponding experimental means (see Results). Error bars represent 2 SEMs.    discernibly between the exper-
                                                                                                                      imental and control groups. We
                                                                                                                      conclude that the reduction of
   We analyzed two additional potentially confounding                                  DOMS in experimental groups compared with control
variables that could, in principle, lead to different DOMS in                          groups was caused largely or exclusively by variation of the
the experimental and control groups; namely, water con-                                independent variable, i.e., by elevated HR. This finding
sumption during workouts and attendance at prescribed                                  implies that elevated HR during resistance training speeds
exercise sessions. Dehydration during exercise can induce or                           muscle recovery.
exacerbate muscle injury and potentially increase DOMS in                                 The discernible reduction of DOMS in experimental
hyperthermic men (11); therefore, differential water intake                            groups below that of control means in the first (men) or
during exercise sessions could yield differences in DOMS.                              second (women) workout suggests that cardioacceleration
Mean water consumption (Table 6) was not discernibly                                   before each set of resistance exercises rapidly reduces any
different, however, between experimental and control groups                            residual DOMS induced in the corresponding musculature by
in either gender (two-tailed Wilcoxon tests; men: n = 9; P =                           earlier exercise. Male subjects in particular began the training
0.77; women: n = 14, P = 0.11).                                                        program under the influence of residual DOMS induced by
   A second potentially confounding variable, differential                             earlier sport-related activities (see Methods). The smaller
compliance with prescribed exercise sessions between                                   mean DOMS in experimental groups in every exercise session
experimental and control groups, could lead to different                               after the first could reflect either the reduction of residual
             the                                             TM
      TABLE 5. Self-reported Rating of Perceived Exertion               TABLE 7. Compliance with exercise sessions.
      summed among all individual resistance exercises
      and all exercise sessions.                                        Gender           Experimental             Control
and disappearance in experimental subjects during training          exercises now act on an expanding peripheral vascular bed in
nonetheless provides empirical constraints on models of the         skeletal muscles to further enhance muscle perfusion (59),
underlying physiological mechanisms. The rapid initial              deliver nutrients and other substances and clear waste and
reduction of DOMS in experimental groups compared with              injury products faster, repair the cytoskeleton and sarco-
control groups in both genders (Figure 4) is congruent with         lemma more rapidly, restore the metabolic and contractile
the rapid dynamics of increased membrane flux that is               machinery, and reduce inflammation, eliminating DOMS
presumably induced in skeletal muscle by the higher cardiac         within a period of 4 weeks.
output and greater systolic blood pressure caused by pre-              This hypothetical two-stage model is based on the probable
resistance aerobic cardioacceleration (1). The slower disap-        causes of DOMS (see Introduction) combined with the
pearance of DOMS by the end of the fourth week in                   documented responses of muscle to exercise. The model
experimental subjects compared with control subjects in both        accounts for all features of the reduction and elimination of
genders (Figure 4), however, suggests a different mechanism         DOMS by aerobic elevation of HR before each set of
with a longer time constant, e.g., exercise-induced vascular-       resistance exercises observed in experimental groups in the
ization of skeletal muscle.                                         present study. The time course of the reduction in DOMS
   Increased muscle capillarization after exercise training is      from the repeated bout effect in control subjects was similar to
induced by both resistance and aerobic exercise (4,21,26,35).       the attenuation of DOMS in experimental subjects (Figure 4),
High-intensity intermittent endurance training increases the        suggesting that this two-stage model could operate in parallel
ratio of capillaries to muscle fibers in 4 weeks (26), similar to   with or through the mechanism(s) of the repeated bout effect
the time to disappearance of DOMS in experimental subjects          to enhance protection against eccentric contraction injury.
in the present study. Concurrent strength and endurance             The proposed model can be readily tested using cardioaccel-
training (but not strength or endurance training separately)        eration to regulate DOMS as the independent variable and
significantly increased vascularization in the vastus lateralis     physiological, biochemical, and ultrastructural measures as
muscle after 12 weeks of training (4), suggesting that              dependent variables.
concurrent training accelerates muscle vascularization dispro-
portionately. The increased capillarization of leg muscle           PRACTICAL APPLICATIONS
(tibialis anterior) in response to exercise is similar in men and   This study has two practical applications. First, it utilizes
women (50), consistent with the similar time course of DOMS         a new method of progression during resistance training,
reduction and elimination observed in our male and female           which optimizes exertion (RPE) and minimizes pain (RPP)
experimental groups (Figure 4). The known properties and            during sets of resistance exercises. This method promotes the
time course of muscle angiogenesis in response to a strong          fastest possible advances in training adaptations consistent
exercise stimulus are therefore congruent with the dynamics         with balancing the two competing goals of exercise programs:
of long-term DOMS reduction and disappearance observed in           maximizing effects and minimizing the risk of injury or
experimental groups of both genders in the present study.           overtraining. The training protocols used in this study were
   We propose the following hypothetical two-stage model to         designed to increase general strength and endurance by
account for the reduction and elimination of DOMS caused            combining medium weight, repetitions, and velocity with
by elevated HR during resistance exercises in experimental          strong exertion. The method of progression used herein can
subjects. In the first (early) stage, aerobic elevation of HR       be adapted, however, to specialized training purposes such as
immediately before each set of resistance exercises increases       athletic strength and power conditioning or patient re-
the flow of blood to skeletal muscle, enhancing muscle              habilitation by raising or lowering, respectively, the RPE
perfusion during resistance exercises (35,57), which accel-         threshold for progression.
erates lactate/H+ release from stressed muscle (27,28) and re-         Second, this study documents a new training protocol,
supplies nutrients such as glucose/glycogen and other               integrated concurrent exercise (15), which rapidly eliminates
substances more rapidly. In this first stage, therefore, the        DOMS. The rapid attenuation of DOMS during integrated
increased muscle perfusion induced by pre-resistance                concurrent training implies faster recovery of skeletal muscle
cardioacceleration retards cellular destruction induced by          after a strong exercise stimulus, which should support more
eccentric contraction and/or accelerates tissue repair, limit-      frequent training and faster progression during all high-
ing muscle inflammation and therefore reducing DOMS in              intensity training modes, including endurance, strength,
the first few workouts.                                             power, and agility. Even when DOMS is not an issue in a
   In the second (late) stage of this hypothetical model,           training program, integrated concurrent training would be
continued aerobic elevation of HR immediately before each           expected to support faster development. The present experi-
set of resistance exercises during integrated concurrent            ments entailed vigorous training with well-conditioned
training stimulates longer-term angiogenesis, accelerating          athletes, but integrated concurrent exercise may also reduce
the capillarization of skeletal muscle. The increased HR,           DOMS in medium- and low-intensity training applications
cardiac output, and systolic blood pressure induced by              with recreational exercisers, the elderly, and rehabilitating
continuing cardioacceleration before each set of resistance         patients. In this case, the prescription of integrated
concurrent exercise could help to eliminate a demonstrated                   7. Borg, G. G. Borg’s Perceived Exertion and Pain Scale. Champaign, IL:
barrier to exercise initiation, adherence, and progression at all               Human Kinetics, 1998.
levels and ages and could have potential clinical applications.              8. Boyle, CA, Sayers, SP, Jensen, BE, Headley, SA, and Manos, TM.
                                                                                The effects of yoga training and a single bout of yoga on delayed
                                                                                onset muscle soreness in the lower extremity. J Strength Cond Res 18:
ACKNOWLEDGMENTS                                                                 723–729, 2004.
This research was funded by the Division of Physical and                     9. Clarkson, PM and Hubal, MJ. Exercise-induced muscle damage in
                                                                                humans. Am J Phys Med Rehab 81: S52–S69, 2002.
Biological Sciences and the Office of Physical Education,
Recreation, and Sports, of the University of California at Santa            10. Clarkson, PM and Sayers, SP. Etiology of exercise-induced muscle
                                                                                damage. Can J Appl Physiol 24: 234–248. 1999.
Cruz. We are grateful to the 56 dedicated student-athletes
                                                                            11. Cleary, MA, Sweeney, LA, Kendrick, ZV, and Sitler, R. Dehydration
who initially served as subjects in these studies. For their                    and symptoms of delayed-onset muscle soreness in hyperthermic
cooperation and assistance in this research, we thank Greg                      males. J Athl Train 40: 288–297, 2005.
Harshaw, Athletic Director; Paul Holocher, men’s soccer                     12. Close, GL, Ashton, T, Cable, T, Doran, D, Noyes, C, McArdle, F,
coach; Michael Runeare, women’s soccer coach; Kim Musch,                        and MacLaren, DP. Effects of dietary carbohydrate on delayed onset
                                                                                muscle soreness and reactive oxygen species after contraction
swimming team coach; Selene Teitelbaum and Jonah Carson,
                                                                                induced muscle damage. Br J Sports Med 39: 948–953, 2005.
women’s volleyball coaches; Bob Hansen, men’s tennis
                                                                            13. Dannecker, EA, Hausenblas, HA, Kaminski, TW, and Robinson,
coach; and Gordie Johnson, men’s basketball coach. For                          ME. Sex differences in delayed onset muscle soreness. Clin J Pain 21:
technical support, we thank Cindy Hodges, Danielle Lewis,                       120–126, 2005.
Sarah Pinneo, and Sonia Williams-Kelley. For administrative                 14. Dannecker, EA, Koltyn, KF, Riley, JL, 3rd, and Robinson, ME. The
support, we thank Kate Aja, Dierdre Beach, Bruce Bridgeman,                     influence of endurance exercise on delayed onset muscle soreness. J
                                                                                Sports Med Phys Fitness 42: 458–465, 2002.
Caitlin Deck, Daniel Friedman, Dobie Jenkins, and Alice
Yang-Murray. Additional contributors to this research include               15. Davis, WJ. The Miracle Workout: The Revolutionary 3-Step Program for
                                                                                Your Perfect Body. New York: Ballantine. 2005, pp. 152–153.
Tamara Chinn, James Cisneros, Laura Engelken, Dianne
                                                                            16. Denegar, CR and Perrin, DH. Effect of transcutaneous electrical
Fridlund, Jill Fusari, Kathleen Hughes, Robert Irons, Camille                   nerve stimulation, cold, and a combination treatment on pain,
Jarmie, Kristin Onorato, Karen Ostermeier, Mischa Plunkett,                     decreased range of motion, and strength loss associated with delayed
Onelia Rodriquez, Zoe Scott, Justin Smith, and Kelly Vizcarra.                  onset muscle soreness. J Athl Train 27: 200–206, 1992.
After the completion of this research, the lead author became               17. Dennis, RA, Trappe, TA, Simpson, P, Carroll, C, Huang, BE,
                                                                                Nagarajan, NR, Bearden, E, Gurley, C, Duff, GW, Evans, WJ,
affiliated with The Miracle Workout, LLC, which developed
                                                                                Kornman, K, and Peterson, CA. Interleukin-1 polymorphisms are
a proprietary interest in Integrated Body ConditioningÒ,                        associated with the inflammatory response in human muscle to acute
a health, fitness, and training system that incorporates aspects                resistance exercise. J Physiol 560: 617–626, 2004.
of the integrated concurrent training protocol documented                   18. Dutto, DJ and Braun, WA. DOMS-associated changes in ankle and
in this study (patent pending). The results of this study do not                knee joint dynamics during running. Med Sci Sports Exerc 36:
                                                                                560–566, 2004.
constitute endorsement of this product by the authors or the
                                                                            19. Folland, JP, Chong, J, Copeman, EM, and Jones, DA. Acute muscle
National Strength and Conditioning Association.
                                                                                damage as a stimulus for training-induced gains in strength. Med Sci
   Note: W. Jackson Davis is now with The Miracle Work-                         Sports Exerc 33: 1200–1205, 2001.
out, LLC, P.O. Box 2221, Boulder, Colorado 80306.                           20. Frieden, J and Lieber, RL. Eccentric exercise-induced injuries to
                                                                                contractile and cytoskeletal muscle fibre components. Acta Physiol
                                                                                Scand 171: 321–326, 2001
REFERENCES
                                                                            21. Haga, S, Mizuno, M, Bae, SY, Toshinai, K, Miyazaki, H, Hamaoka, T,
 1. American College of Sports Medicine. Guidelines for Exercise Testing
                                                                                Esaki, K, Shimomitzu, T, Okawara, T, and Ohno, H. The effect of
    and Prescription (7th ed.). Philadelphia: Lippincott Williams &
                                                                                12-week intensive endurance training on muscle oxygen utilization
    Wilkins, 2006. pp. 4, 21–28, 51–54, 74, 78, 81–90, 119, 135, 144–145,
    154, 158.                                                                   and its relation to capillary proliferation in human thigh muscles.
                                                                                Med Sci Sports Exerc 32: S5, S362, 2000.
 2. Asp, S, Daugaard, JR, Kristiansen, S, Kiens, B, and Richter, EA.
    Exercise metabolism in human skeletal muscle exposed to prior           22. Helge, JW, Therkildsen, KJ, Jorgensen, TB, Wu, BJ, Storlien, LH, and
    eccentric exercise. J Physiol (Lond) 509: 305–313, 1998.                    Asp, S. Eccentric contractions affect muscle membrane phospho-
                                                                                lipids fatty acid composition in rats. Exp Physiol 86: 599–604, 2001.
 3. Barlas, P, Robinson, J, Allen, J, and Baxter, GD. Managing delayed-
    onset muscle soreness: Lack of effect of selected oral systemic         23. High, DM, Howley, ET, and Franks, BD. The effects of static
    analgesics. Arch Phys Med Rehab 81: 966–972, 2000.                          stretching and warm-up on prevention of delayed-onset muscle
                                                                                soreness. Res Q Exerc Sport 60: 357–361, 1989.
 4. Bell, GJ, Syrotuik, D, Martin, TP, Burnham, R, and Quinney, HA.
    Effect of concurrent strength and endurance training on skeletal        24. Hirose, L, Nosaka, K, Newton, M, Laveder, A, Kano, M, Peke, J, and
    muscle properties and hormone concentrations in humans. Eur J               Suzuki, K. Changes in inflammatory mediators following eccentric
    Appl Physiol 81: 418–427, 2000.                                             exercise of the elbow flexors. Exerc Immunol Rev 10: 75–90, 2004.
 5. Bennett, M, Best, TM, Babul, S, Taunton, J, and Lepawsky, M.            25. Hoffman, MD, Shepanski, MA, Ruble, SB, Valic, Z, Buckwalter, JB,
    Hyperbaric oxygen therapy for delayed onset muscle soreness and             and Clifford, PS. Intensity and duration threshold for aerobic-
    closed soft tissue injury. Cochrane Database Syst Rev 19: CD004713.         exercise-induced analgesia to pressure pain. Arch Phys Med Rehab 85:
    2005.                                                                       1183–1187, 2004.
 6. Best, TM, Fiebig, R, Corr, DT, Brickson, S, and Ji, L. Free radical     26. Jensen, L, Bangsbo, J, and Hellsten, Y. Effect of high intensity training
    activity, antioxidant enzyme, and glutathione changes with muscle           on capillarization and presence of angiogenic factors in human
    stretch injury in rabbits. J Appl Physiol 87: 74–82, 1999.                  skeletal muscle. J Physiol 557: 571–582, 2004.
             the                                             TM
27. Juel, C. Muscle pH regulation: Role of training. Acta Physiol Scand      45. Minor, MA and Sanford, MK. Physical interventions in the
    162: 359–366, 1998.                                                          management of pain in arthritis. Arthritis Care Res 6: 197–206, 1993.
28. Juel, C, Clarksov, C, Nielsen, JJ, Krustrup, P, Mohr, M, and             46. Nosaka, K, Newton, M, and Sacco, P. Delayed-onset muscle soreness
    Bangsbo, J. Effect of high-intensity intermittent training on lactate        does not reflect the magnitude of eccentric exercise-induced muscle
    and H+ release from human skeletal muscle. Am J Physiol Endicronol           damage. Scand J Med Sci Sports 12: 337–346, 2002.
    Metab 286: E245–251, 2004.
                                                                             47. Nosaka, K, Newton, M, Sacco, P, Chapman, D, and Lavender, A.
29. Kanji, GK. 100 Statistical Tests. New York: Sage Publications Ltd.,          Partial protection against muscle damage by eccentric actions at
    1999.                                                                        short muscle lengths. Med Sci Sports Exerc 37: 746–753, 2005.
30. Kingsley, ML, Kilduff, LP, McEneny, J, Dietzig, RE, and Benton, D.       48. Palatini, P, Mos, L, Munari, L, Valle, F, Del Torre, M, Rossi, A,
    Phosphatidylserine supplementation and recovery following                    Varotto, L, Macor, F, Martina, S, Pessina, AC, and Dal Palù, C. Blood
    downhill running. Med Sci Sports Exerc 38: 1617–1625, 2006.                  pressure changes during heavy-resistance exercise. J Hypertens Suppl
31. Koltyn, KF. Exercise-induced hypoalgesia and intensity of exercise.          7: S72–S73, 1989.
    Sports Med 32: 477–487, 2002.
                                                                             49. Pilegaard, H, and Asp, S. Effect of prior eccentric contraction on
32. Koltyn, KF and Umeda, M. Exercise hypoalgesia and blood pressure.            lactate/H+ transport in rat skeletal muscle. Am J Physiol Endicronol
    Sports Med 36: 207–214, 2006.                                                Metab 274: E554–559, 1998.
33. Kraemer WJ, Bush, JA, Wickham, RB, Denegar, CR, Gomez, AL,               50. Porter, MM, Stuart, S, Boij, M, and Lexell, J. Capillary supply of the
    Gotshalk, LA, Duncan, ND, Volek, JS, Putukian, M, and Sebastia-              tibialis anterior muscle in young, healthy, and moderately active men
    nelli, WJ. Influence of compression therapy on symptoms following            and women. J Appl Physiol 92: 1451–1457, 2002.
    soft tissue injury from maximal eccentric exercise. J Orthop Sports
    Phys Ther 31: 282–290, 2001.                                             51. Rhea, MR. Determining the magnitude of treatment effects in
                                                                                 strength training research through the use of the effect size.
34. Kraus, H, Nagler, W, and Melleby, A. Evaluation of an exercise
                                                                                 J Strength Cond Res 18: 918–920, 2004.
    program. Am Fam Physician 28: 153–158, 1983.
                                                                             52. Rodenburg, JB, Steenbeek, D, Schiereck, P, and Bar, PR. Warm-up,
35. Laughlin, MH, Korthuis, RJ, Duncker, DJ, and Bache, RJ. Control of
                                                                                 stretching and massage diminish harmful effects of eccentric
    blood flow to cardiac and skeletal muscle during exercise. In Rowell,
    LB, and Shepherd, JT. (eds.). Handbook of Physiology. New York:              exercise. Int J Sports Med 15: 414–419, 1994.
    American Physiological Society and Oxford University Press. 1996,        53. Romano-Ely, M, Todd, K, Saunders, MJ, and St. Laurent, T. Effect of
    pp. 705–769.                                                                 an isocaloric carbohydrate-protein-antioxidant drink on cycling
36. Lee, H, Goldfarb, AH, Rescino, MH, Hedge, S, Patrick, S, and                 performance. Med Sci Sports Exerc 38: 1608–1616, 2006.
    Apperson, K. Eccentric exercise effect on blood oxidative stress         54. Shafat, A, Butler, P, Jensen, RL, and Donnelly, AE. Effects of dietary
    markers and delayed onset muscle soreness. Med Sci Sports Exerc              supplementation with vitamins C and E on muscle function during
    34: 443–448, 2002.                                                           and after eccentric contractions in humans. Eur J Appl Physiol 93:
37. Lenn, J, Uhl, T, Mattacola, C, Boissonneault, G, Yates, J, Ibrahim, W,       196–202, 2004.
    and Brucker, G. The effects of fish oil and isolfavones on delayed       55. Smith. LL. Causes of delayed onset muscle soreness and the impact
    onset muscle soreness. Med Sci Sports Exerc 34: 1605–1612, 2002.             on athletic performance: A review. J Appl Sport Sci Res 6: 135–141,
38. Loram, LC, Mitchell, D, and Fuller, A. Rofecoxib and tramadol do             1992.
    not attenuate delayed-onset muscle soreness or ischaemic pain in         56. Taguchi, T, Sato, J, and Mizumura, K. Augmented mechanical
    human volunteers. Can J Phyisol Pharmacol 83: 1137–1145, 2005.
                                                                                 response of muscle thin-fiber sensory receptors recorded from
39. Lovering, RM and De Deyne, PG. Contractile function, sarcolemma              rat muscle-nerve preparations in vitro after eccentric contraction.
    integrity, and the loss of dystrophin after skeletal muscle eccentric        J Neurophysiol 94: 2822–2831, 2005.
    contraction-induced injury. Am J Physiol Cell Physiol 286: 230–238,
    2003.                                                                    57. Tschavkovsky, ME and Sheriff, DD. Immediate exercise hyperemia:
                                                                                 contributions of the muscle pump vs. rapid vasodilation. J Appl
40. MacDougall, JD, Tuxen, D, Sale, DG, Moroz, JR, and Sutton, JR.               Physiol 97: 739–747, 2004.
    Arterial blood pressure response to heavy resistance exercise. J Appl
    Physiol 58: 785–790, 1985.                                               58. Warren, GL, Ingalls, CP, Lowe, DA, and Armstrong, RB. Excitation-
                                                                                 contraction uncoupling: Major role in contraction-induced muscle
41. MacIntyre, DL, Reid, WD, and McKenzie, DC. Delayed muscle                    injury. Exerc Sport Sci Rev 29: 82–87, 2001.
    soreness: The inflammatory response to muscle injury and its clinical
    implications. Sports Med 20: 24–40, 1995.                                59. Weber, MA, Krakowski-Roosen, H., Delorme, S, Renk, H,
                                                                                 Krix, M, Millies, J, Kinscherf, R, Kunkele, A, Kauczor, HU, and
42. Marqueste, T, Decherchi, P, Messan, F, Kipson, N, Grelot, L, and
    Jammes, Y. Eccentric exercise alters muscle sensory and motor                Hildebrandt, W. Relationship of skeletal muscle perfusion measured
    control through release of inflammatory mediators. Brain Res 1023:           by contrast-enhanced ultra-sonography to histological microvas-
    222–230, 2004.                                                               cular density. J Ultrasound Med 25: 583–591, 2006.
43. Martin, V, Millet, GY, Lattier, G, and Perrod, L. Effects of recovery    60. Zainuddin, Z, Newton, M, Sacco, P, and Nosaka, K. Effects of
    modes after knee extensor muscles eccentric contractions. Med Sci            massage on delayed-onset muscle soreness, swelling, and recovery of
    Sports Exerc 36: 1907–1915, 2004.                                            muscle function. J Athl Train 40: 174–180, 2005.
44. McHugh, MP. Recent advances in the understanding of the repeated         61. Zainuddin, Z, Sacco, P, Newton, M, and Nosaka, K. Light concentric
    bout effect: The protective effect against muscle damage from                exercise has a temporarily analgesic effect on delayed-onset muscle
    a single bout of eccentric exercise. Scand J Med Sci Sports 13: 88–97,       soreness, but no effect on recovery from eccentric exercise. Appl
    2003.                                                                        Physiol Nutr Metab 31: 126–134, 2006.