Delayed onset muscle soreness (DOMS) may follow exercise that involves eccentric loading of skeletal muscle. Symptoms associated with DOMS include, but are not limited to, significant discomfort at the site of injury and tendon insertion points (16), inflammation, edema (5), compromised muscular function, loss of range of motion across an affected joint (14,19), and reduction in maximal force generating capacity of the affected muscle (4,5,16). Typically, muscle soreness tends to develop within the first 24 h after the exercise session and may persist for up to 10 d (4). Loss of force generating power or torque has commonly been reported to be compromised within 2 h of the muscle damaging bout of exercise (16,20,22). Compromised range of motion and force generating capability of muscle due to DOMS appears to increase the cost of transport of running and alter locomotion patterns sufficiently to cause stride length to decrease at a given submaximal running speed (2). Changes in gait subsequent to soreness or damage to muscle tissue could result in further injury and could adversely affect running performance. Downhill running provides a good mechanism to eccentrically load muscles of the ankle and knee, as the amount of energy absorption has been found to approximately double at both joints when running at 4.5 m·s−1 on a −8.3% slope (3).
DOMS has been found to cause a significant decrease in stride length at a given running speed (2). The spring-mass model has been used to describe the mechanics of running, and in particular it has been shown that to increase stride rate at a given speed, the vertical stiffness of the leg system must increase (7). Because changes in stride length and stride rate at a given speed are inversely proportional to each other, if stride length decreases with DOMS, the stride rate would increase. This increase would be due to an increase in vertical leg stiffness.
A decrease in stride length at a given speed should be accompanied by changes in joint kinematics, particularly if the change in stride length was driven by the DOMS inducing factor, as has been demonstrated in a previous study of running (11). Additionally, a significant decrease in stride length with DOMS has been recently reported in a group of trained male runners (2). The purpose of this study was to determine whether changes in ankle and knee angular kinematics occurred with DOMS in a group of well-trained distance runners. Specifically, the range of motion was assessed as well as the peak angular velocity during flexion and extension. It was hypothesized that ROM of both the knee and ankle would decrease due to DOMS, with a corresponding decrease in angular velocity. Based on previous research of downhill running, greater changes might be observed in the knee as it undergoes greater flexion (thus greater eccentric loading) during early stance while running down a slope (3). Decreased ROM of these joints implies that the joints become “stiff.” To assess this mechanically, joint torsion stiffness of both the knee and ankle during portions of stance were measured to determine if the rotational stiffness parameters of these joints changed with DOMS. Leg stiffness was calculated from the knee joint torsion stiffness for congruency with the hypothesis that increased stride rate would be accompanied by an increase in vertical leg stiffness (7). This study was based on previously published effects of DOMS on physiological and stride parameters in a group of well-trained male runners (2). Specifically, after a 48-h period, DOMS was shown to significantly increase measured V̇O2 (increased by 1 mL·kg−1·min−1), increase blood lactate concentrations (increased by 0.61 mmol·L−1) and self-reported amount of muscle soreness (by 3 points on a 6-point scale), and to decrease stride length by 3.2% (2).
METHODS
Subjects and procedures.
Nine, well-trained, male endurance athletes (triathletes = 3; distance runners = 6) participated in the investigation. Before inclusion in the study, subjects were informed of the risks associated with their participation, and each subject completed a university-approved consent form and a medical history questionnaire. Descriptive characteristics have been presented previously (2) but are presented again here in Table 1. Preliminary measures included determination of thigh and foot length, determination of body composition using skinfolds and assessment of maximal aerobic capacity (V̇O2peak) using a graded treadmill test (2). During this test, gas exchange was measured continuously using an automated gas analysis system (TrueMax 2400, ParvoMedics, Salt Lake City, UT). After a warm-up period, the initial treadmill velocity was set at 53.6 m·min−1 below the subject’s estimated 5-km race pace. Treadmill velocity was increased by 26.8 m·min−1 every 3 min until the subject achieved a running speed that was 26.8 m·min−1 faster than the estimated race pace. From this point, grade was increased by 2% every 2 min until the subject achieved volitional exhaustion. Data obtained from the graded exercise test (V̇O2 and treadmill speed) were entered into a linear regression to predict treadmill velocities that would be used for running economy testing. Running economy was assessed among all subjects at a treadmill speed that would elicit 75% (3.77 ± 0.53 m·s−1) of V̇O2peak.
;)
TABLE 1: Descriptive characteristics of the participants (N = 9).
The first running economy session (RE1) occurred a minimum of 48 h after the graded exercise test, and general procedures have been presented previously (2). After a brief warm-up, retro-reflective markers were fixed on the left leg over the following bony landmarks: head of the fifth metatarsal (fixed to the shoe), over the lateral calcaneus (fixed to the shoe), the lateral malleolus, the lateral epicondyle of the femur, and the greater trochanter. The runner then maintained the speed associated with 75% of V̇O2peak for 5 min. A 10-s video recording of the sagittal motion of the runner was made at 2.5 min of the 5 min run, followed by the collection of expired gas for the final 2 min. During the video recording of the running motion, the runner was able to run freely without the apparatus used to collect expired gas, which was given to the runner following video recording. All video was recorded at 120 Hz with a high speed video camera (Pulnix, Sunnyvale, CA).
Between 48 and 96 h of the first RE1, each participant ran on a treadmill with a −10% grade at a speed that elicited approximately 70% of V̇O2peak for 30 min. Exactly 48 h after the downhill run, a second running economy session (RE2) occurred, with procedures identical to those of RE1. A postdownhill exercise time interval of 48 h was chosen as it falls in the time range associated with peak muscle soreness (4). No exercise was performed during the 48-h period between the completion of the downhill run and RE2 testing. Subjects were also required to refrain from the use of anti-inflammatory agents during the study. The general degree of muscle soreness was assessed using a 0- to 6-point scale where 0 corresponded to “no pain” and 6 to “unbearable pain” during step downs from a 33-cm bench and descending stairs (2).
Data reduction.
Video records were digitized and recorded markers were smoothed using a second-order, dual-pass Butterworth filter using a cut-off frequency of 15 Hz (Motion Analysis Corporation, Santa Rosa, CA). Between 10 and 12 (depending upon the speed) consecutive strides were identified from the digitized data, using combinations of kinematic trajectories of toe and heel markers (12) and observing the video to determine heel strike and toe-off events. For each stride, ankle and knee angles and angular velocity were determined. Angles at heel-strike and toe-off, range of motion during stance and swing, and maximum flexion and extension angular velocity values were measured.
Joint torsion stiffness was determined by a method similar to that presented by Li (15). Joint stiffness of the knee (kknee) was estimated by the following equation:
where “I” is the person’s mass multiplied by the length of the thigh squared (m·l2thigh), ω is the knee angular velocity (rad·s−1), and θ is the knee angular position. Figure 1 provides an example of how Δω2·(Δθ2)−1 was determined for the knee. Torsion stiffness was measured for two periods of stance. The first portion of stance lasted from heel strike until maximum knee flexion velocity, for which knee torsion stiffness (kknee1) was determined. Knee torsion stiffness for the second part of stance (kknee2) was measured from maximum knee flexion velocity to the point of maximum knee flexion. Torsion stiffness was not determined after maximum knee flexion due to variability in the relationship between Δω2 and Δθ2 across participants, consequently knee torsion stiffness values were obtained for only the first half of stance.
FIGURE 1: Knee stiffness (kknee) was determined from the slope of the relationship between the knee angular position squared and the knee angular velocity squared. Knee stiffness was determined for two portions of stance—from heel strike to maximum angular velocity of knee flexion (kknee1) and from maximum angular velocity of knee flexion to maximum knee flexion angle (kknee2). Regression lines were fit for the data during these portions of stance. In this example plot from one subject, the two regression lines with corresponding equations are shown. The coefficients that indicate the slope of the line were used in subsequent calculations. The general kinematic pattern was similar across subjects for the two portions of stance included in this study. Also apparent in this plot is the difference between RE1 and RE2.
Joint stiffness of the ankle was estimated for four portions of stance as shown in Figure 2. The equation used was similar to equation 1 above, except that “I” was calculated as the person’s mass multiplied by the length of the foot (ankle to fifth metatarsal) squared (m·l2foot); ω was the ankle angular velocity (rad·s−1) and θ was the ankle angular position. Ankle stiffness (kankle1) was determined for the period from just after heel strike to maximum angular velocity of ankle dorsiflexion. The next phase of stance for which ankle stiffness was determined (kankle2) was from maximum dorsiflexion velocity to maximum dorsiflexion, which coincides with mid-stance. Ankle stiffness was also determined from maximum dorsiflexion to maximum angular velocity of plantarflexion (kankle3). Finally, a fourth phase from maximum angular velocity of plantarflexion to toe-off was also obtained (kankle4).
FIGURE 2: Ankle stiffness (kankle) was determined from the slope of the relationship between the ankle angular position squared and angular velocity squared during stance. Ankle stiffness was determined for four portions of stance—from just after heel strike to maximum angular velocity of dorsiflexion (kankle1), from maximum angular velocity of dorsiflexion to maximum dorsiflexion angle (kankle2), from maximum dorsiflexion to maximum angular velocity of plantarflexion (kankle3), and from maximum angular velocity of plantarflexion to toe-off (kankle4). Regression lines were fit for the data during these portions of stance. In this example plot from one subject, the two regression lines with corresponding equations are shown. Coefficients that indicate the slope of the line were used in subsequent calculations. The general kinematic pattern was consistent across participants. Also depicted in the graph is the difference between RE1 and RE2.
Leg stiffness (kleg) was estimated from the knee torsion stiffness using the following equation:
where “l” is the length of the thigh, and Δθ is the change of angle of the knee during particular phase of stance. Leg stiffness was determined for each of the phases of stance for which joint stiffness were determined. Typically, leg stiffness is determined over the stride by calculating the ratio of peak vertical force to displacement of the center of mass (7), which requires the use of a force measuring platform. Due to the limitations of the physiological measurements, leg stiffness was determined from joint kinematics and individual subject morphology, which was shown to produce similar values to the force plate method (14).
Statistical analysis.
Changes in the following dependent variables were assessed: knee and ankle ROM, heel strike and toe-off angles, and peak flexion and extension angular velocity for both the stance and swing phase of running. Also, ankle and knee torsion stiffness values and overall leg stiffness were compared. Data obtained from 10–12 strides for a dependent variable were collapsed into a single mean value for statistical analysis. For each variable of interest, an ANOVA with repeated measures was computed using SPSS 11.0 (SPSS, Inc., Chicago, IL). Statistical significance was set at α = 0.05.
RESULTS
Angular kinematic patterns observed for the ankle and knee were typical of the running stride (Fig. 3). Ankle motion was not statistically different for most of the running stride. A strong trend was present for the average ROM during stance (P = 0.06) and during swing (P = 0.17) of the ankle to decrease with DOMS (Table 2). Differences between RE1 and RE2 for the ROM of the ankle during stance were roughly 2.7°. Peak angular velocity of dorsiflexion during the initial portion of stance was lower at RE2, and the peak angular velocity of dorsiflexion during swing tended to be slower at RE2 (P = 0.09).
FIGURE 3: The angular kinematic patterns for both the ankle (A) and knee (B) were very similar between RE1 and RE2 for this subject. Only slight differences (primarily during stance) between RE1 and RE2 are observed. Data represent the ensemble average of 10 strides of one participant. Standard errors bars are not included but are quite small due to the consistent patterns exhibited by individual participants from stride-to-stride. For the ankle, 90° represents anatomical position, decreasing angle was dorsiflexion, and an increasing angle was plantarflexion. For the knee, decreasing angle is flexion and an increasing angle is extension.
TABLE 2: Angular kinematic measurements of the ankle.
Differences were also observed in knee angular kinematic measurements (Table 3). The knee tended to be slightly more extended at heel strike at RE2 (P = 0.10) but not different at toe-off (Table 3). There was a strong trend for the ROM of the knee to decrease during stance at RE2 (P = 0.06), due to a lower maximum knee flexion angle (as seen in Fig. 3). Another result of the lower ROM was significantly lower flexion and extension peak angular velocity values during stance. ROM during swing was also lower at RE2 (Table 3).
TABLE 3: Angular kinematic measurements of the knee.
There were no differences in torsion stiffness of the ankle during foot stance with DOMS (Table 4). At RE2, torsion stiffness of the knee was lower during kknee2 (Table 4). Leg stiffness was not significantly different between the two conditions. On average, leg stiffness was higher during the initial portion of stance due perhaps to a higher torsion stiffness of the knee during the initial stance (heel strike to maximum knee flexion velocity;Fig. 1. The significant decrease in kknee2 did not translate into lower leg stiffness during the second portion of stance, as leg stiffness remained essentially the same.
TABLE 4: Ankle and knee torsion stiffness parameters and vertical leg stiffness.
DISCUSSION
The downhill run produced significant DOMS in the runners (2). Ankle and knee ROM during stance tended to be reduced with DOMS at 48 h after an intense eccentric bout of exercise. Both ankle and knee angular velocity were lower during the initial portion of stance, when both joints are flexing (dorsiflexion in the ankle). Ankle joint stiffness was not statistically different with DOMS (although showed a trend to be slightly lower later in stance). Knee torsion stiffness decreased during the second portion of stance, but had no effect on vertical leg stiffness. Vertical leg stiffness showed a trend to be greater at contact, but knee torsion stiffness did not. Changes in angular motion were most apparent during the early portion of stance, perhaps to protect the ankle and knee musculature during the initial eccentric portion of stance.
Changes in knee kinematics with DOMS are similar to previously reported results, where knee ROM was found to decrease (11). ROM reported by Hamill et al. (11) referred to the ROM over the entire stride. In this current study, the ROM during both swing and stance decreased with DOMS. Hamill et al. (11) found stride length to remain constant with DOMS despite changes in angular kinematic measures. We have previously reported stride length to significantly decrease with DOMS by 3.2% (2). This decrease in stride length was consistent with altered angular kinematics particularly the reduced range of motion of both the ankle and knee. It was somewhat surprising that larger changes associated with DOMS were not found by Hamill et al. (11) as participants performed a run on a −26% grade (compared with the −10% grade used in this current study). Differences in results presented here and those of Hamill et al. may be due to a higher intensity used on the downhill run. Runners in this study performed the downhill run at an intensity of approximately 95% of maximal heart rate, whereas the subjects in the study of Hamill et al. (11) performed at 73.5% of maximum heart rate.
Calculated ankle joint stiffness was similar to that reported in previous studies of running, where joint stiffness values of around 7 N·m·°−1 that are somewhat independent of running speed have been reported (10,13,23). Knee joint stiffness values of 13–24 N·m·°−1 over a range of running speeds and proportional to running speed have been reported (1,10,23). Leg stiffness values that are reported here are very similar to those observed previously during running (7).
To maintain similar speed when stride length was decreased, a subsequent increase in stride rate has to occur (since running velocity is the product of stride rate and stride length). Increasing stride rate at a particular running speed has been found to be associated with increased vertical leg stiffness (7). Because stride rate increased with DOMS, vertical leg stiffness should also increase. Indeed this appears to be the case with DOMS, because vertical leg stiffness increases during the first portion of stance. It was encouraging that the behavior of leg stiffness as measured from kinematics was similar to leg stiffness measured from force plate records with an increase in stride frequency at a given speed. Leg stiffness tended to increase during the first portion of the stride from heel strike to maximum knee flexion angular velocity. Increased vertical leg stiffness was probably due to the slight increase in knee torsion stiffness during this same time period. This had the effect of reducing the ROM and decreasing the angular velocity of the knee, possibly as a protective mechanism against the pain associated with muscle soreness. Results from studies of hopping have found that adjustments in leg stiffness are typically made by adjusting the joint stiffness of the ankle (8,9). In running, control of leg stiffness appears to occur at the knee (1,10). Impaired function of knee musculature due to DOMS alters knee joint stiffness and affects the stiffness of the leg system. These changes in the function of the knee may also increase the risk of injury due to altered impact dynamics during the initial portion of stance.
Results from previous research suggest that the musculature of the knee were primarily responsible for increasing the shock absorption capability of the leg (17,18). It has been found that the knee musculature absorbs the additional energy associated with impact (6). When the runner has DOMS, this alters the ability of the musculature to respond to increased shock absorption requirements. The knee tended to be more stiff during the initial portion of stance, decreasing the ability of the knee to absorb the energy of impact and increasing risk of injury either due to transmission of force through the skeletal system to sensitive structures such as the spine and head or due to increased energy absorption by passive structures such as ligaments and connective tissue that crosses the joint. Because the runner may be at increased risk of injury, it might be recommended that runners only engage in light exercise or a different mode of exercise until recovered from DOMS. Reductions in range of motion and in force generating capacity are two previously reported consequences of DOMS (4,5,14,16,19). Effects of DOMS may be attenuated somewhat by engaging in light exercise on days subsequent to the muscle damaging exercise (21), although results of a separate investigation found no effect of light exercise on recovery from DOMS (24).
Inclusion of additional runners might strengthen the results of the present analysis. Included results do show that there was a trend of leg stiffness to increase during early stance with DOMS due primarily to changes in motion of the knee. Further study of the changes in mechanics of running due to DOMS are warranted.
REFERENCES
1. Arampatzis, A., G. P. Bruggeman, and V. Metzler. The effect of speed on leg stiffness and joint kinetics in human running. J. Biomech. 32: 1349–1353, 1999.
2. Braun, W. A., and D. J. Dutto. The effects of a single bout of downhill running and ensuing DOMS on running economy performed 48 hours later. Eur. J. Appl. Physiol. 90: 29–34, 2003.
3. Buczek, F. L., and P. R. Cavanagh. Stance phase knee and ankle kinematics and kinetics during level and downhill running. Med. Sci. Sports Exerc. 22: 669–677, 1990.
4. Clarkson, P. M., K. Nosaka, and B. Braun. Muscle function after exercise-induced muscle damage and rapid adaptation. Med. Sci. Sports Exerc. 24: 512–520, 1992.
5. Clarkson, P. M., and S. P. Sayers. Etiology of exercise-induced muscle damage. Can. J. Appl. Physiol. 24: 234–248, 1999.
6. Derrick, T. R., J. Hamill, and G. E. Caldwell. Energy absorption of impacts during running at various stride lengths. Med. Sci. Sports Exerc. 30: 128–135, 1998.
7. Farley, C. T., and O. Gonzalez. Leg stiffness and stride frequency in human running. J. Biomech. 29: 181–186, 1996.
8. Farley, C. T., H. H. P. Houdijk, C. van Strien, and M. Louie. Mechanism of leg stiffness adjustment for hopping on surfaces of different stiffnesses. J. Appl. Physiol. 85: 1044–1055, 1998.
9. Farley, C. T., and D. C. Morgenroth. Leg stiffness primarily depends on ankle stiffness during human hopping. J. Biomech. 32: 267–273, 1999.
10. Gunther, M., and R. Blickhan. Joint stiffness of the ankle and the knee in running. J. Biomech. 35: 1459–1474, 2002.
11. Hamill, J., P. S. Freedson, P. M. Clarkson, and B. Braun. Muscle soreness during running: biomechanical and physiological considerations. Int. J. Sport Biomech. 7: 125–137, 1991.
12. Hreljac, A., and N. Stregiou. Phase determination during normal running using kinematic data. Med. Biol. Eng. Comput. 38: 503–506, 2000.
13. Kuitunen, S., P. Komi, and H. Kyrolainen. Knee and ankle joint stiffness in sprint running. Med. Sci. Sports Exerc. 34: 166–173, 2002.
14. Lee, H., A. H. Goldfarb, M. H. Rescino, S. Hedge, S. Patrick, and K. Apperson. Eccentric exercise effect on blood oxidative-stress markers and delayed onset of muscle soreness. Med. Sci. Sports Exerc. 34: 443–448, 2002.
15. Li, L. Equilibrium point and knee joint modeling: advances in bioengineering.
Proceedings of the ASME International Mechanical Engineering Congress and Exposition, Nashville, TN, 1999, pp. 299–300.
16. MacIntyre, D. L., W. D. Reid, and D. C. McKenzie. Delayed muscle soreness: the inflammatory response to muscle injury and its clinical implications. Sports Med. 20: 24–40, 1995.
17. Mercer, J. A., P. Devita, T. R. Derrick, and B. T. Bates. Individual effects of stride length and frequency on shock attenuation during running. Med. Sci. Sports Exerc. 35: 307–313, 2003.
18. Mizrahi, J., O. Verbitsky, and E. Isakov. Shock accelerations and attenuation in downhill and level running. Clin. Biomech. 15: 15–20, 2000.
19. Rawson, E. S., B. Gunn, and P. M. Clarkson. The effects of creatine supplementation on exercise-induced muscle damage. J. Strength Cond. Res. 15: 178–184, 2001.
20. Rodenburg, J. B., P. R. Bar, and R. W. De Boer. Relations between muscle soreness and biochemical and functional outcomes of eccentric exercise. J. Appl. Physiol. 74: 2976–2983, 1993.
21. Sayers, S. P., P. M. Clarkson, and J. Lee. Activity and immobilization after eccentric exercise: II. serum CK. Med. Sci. Sports Exerc. 32: 1593–1597, 2000.
22. Sorichter, S., A. Koller, C. Haid, et al. Light concentric exercise and heavy eccentric muscle loading: effects on CK, MRI and markers of inflammation. Int. J. Sports Med. 16: 288–292, 1995.
23. Stefanyshyn, D., and B. Nigg. Dynamic angular stiffness of the ankle joint during running and sprinting. J. Appl. Biomech. 14: 292–299, 1998.
24. Weber, M. D., F. J. Servedio, and R. W. Woodall. The effects of three modalities on delayed onset of muscle soreness. J. Orthop. Sports Phys. Ther. 20: 236–242, 1994.
