During an incremental cycle test, large muscle groups are involved, and therefore, this is one of the most common used tests to assess aerobic exercise capacity (3). Although this test is thought primarily to reflect the capacity of the cardiovascular and respiratory system, expressed as peak oxygen uptake (2peak">V̇o2peak) or peak work rate (WRpeak) (7), the incremental cycle test also reflects other systems as the neural system and the skeletal muscles involved (21) Furthermore, muscle fiber distribution affects exercise testing to the extent that the proportion of type 1 muscle fibers is positively correlated to V̇o2 consumption (21).
It is well known that V̇o2 and WR are closely related (19,34). However, at peak exercise, it has been found that WR can increase while V̇o2 is leveling off (3). Furthermore, it has been shown that in elite sprint cycling, performance was more dependent on WR than on 2peak">V̇o2peak during cycling (23). Thus, WR may reflect different aspects of exercise capacity than V̇o2 especially toward maximal WR. In elite sprint runners, the maximal speed was found to be associated with functional strength tests of the legs, such as squat jump and countermovement jump (29). Lower extremity muscular strength has also been shown to affect performance in field-based cardiorespiratory tests in male subjects although a nonsignificant correlation between maximal strength measured by isokinetic dynamometry and a maximal treadmill test was also revealed (13). Patton et al. (25) have shown a significant positive relation between peak power assessed with a Wingate test and isokinetic peak power at the knee in untrained but physically active men. To the best of our knowledge, no study has addressed the relationship between exercise capacity and lower extremities muscle strength and muscle endurance in sedentary subjects during cycling.
Surface electromyography (sEMG) has been used to examine muscle activity during movement. Assessed by this method, WR in elite cyclists at maximal seated cycling is produced foremost by the muscles of the knee (49%) and hip (32%) (24). A similar involvement of knee and hip muscles was seen in subjects with recreational cycling experience during exercise on a cycle ergometer (10). The sEMG, however, has been criticized because it involves a normalization procedure with maximal voluntary contraction (MCV) at an isometric position, and therefore, MCV at the right speed and angle may not be captured (20). Other options to examine the load on the lower extremities include isokinetic dynamometry. This method allows separate measurements of muscular strength and muscular endurance of different skeletal muscle systems at different velocities and angles, measuring, for example, peak torque and total work (22).
The aim of this study was thus to examine the relationship between exercise capacity during an incremental cycle test, assessed by 2peak">V̇o2peak and WRpeak and knee muscular strength and muscular endurance, assessed by isokinetic dynamometry. A further aim was to investigate the relative contribution of fiber-type proportion, muscular strength, and muscular endurance in performing an incremental cycle test.
Experimental Approach to the Problem
This is an observational study in a single group of sedentary male subjects focusing on the relation between physiological variables of exercise capacity.
We used 2 measures of exercise capacity, maximum work rate (WRpeak), and maximal oxygen consumption (2peak">V̇o2peak) as dependent variables. Even if these are closely correlated, they differ somewhat as oxygen consumption levels off at high work loads (4). Nondependent variables were measurements of muscle fiber distribution, muscular strength, and muscular endurance of the legs as described below.
Thirty-nine sedentary healthy male subjects participated voluntarily in the study, as a part of a larger study on heritage of type 2 diabetes (T2D). Their mean age was 38.4 ± 4.5 (SD) years, height 181 ± 6 cm, weight 92.2 ± 13.0 kg, body mass index (BMI) 28.4 ± 3.3 kg·m−2, waist 97.7 ± 9.6 cm, hip 104.9 ± 5.8 cm, and waist/hip ratio 0.93 ± 0.05. All subjects had a normal glucose tolerance test. There were no significant differences in subject and study characteristics between the subjects with heritage for T2D and subjects without. They were therefore analyzed as 1 group. None of the subjects included in the study were participating in 30 minutes or more of moderate intensity physical activity in 3 days or more of the week for the last 3 months and were therefore considered sedentary (1). The study was approved by the regional ethical review board at Lund, Sweden. Written informed consent was obtained from all subjects.
Muscle biopsies were taken 4-6 days before an incremental cycle test. The subjects performed an incremental cycle test to examine exercise capacity and isokinetic dynamometry to determine knee muscle strength and muscle endurance. Isokinetic dynamometry was performed 4-6 days after the cycle test. Before testing, the subjects were told not to eat, drink coffee, or smoke 2 hours before the test sessions. They were also told not to perform any heavy exercise 48 hours before the tests.
An incremental exercise test was performed on a cycle ergometer (Marquette Hellige Medical Systems 900 ERG, Milwaukee, WI, USA). Work load began at 50 W and increased with 15 W·min−1. The work load was held constant at 40% of 2peak">V̇o2peak (estimated from a previous submaximal cycle test ) for 4 minutes (36) as a part of a study on V̇o2 kinetics, not included in this manuscript. Pedaling rate was maintained at 60 rpm using both visual feedback and verbal encouragement. V̇o2, VCO2, and ventilation (VE) were measured breath-by-breath (Oxycon Mobile, Jeager, Hoechberg, Germany). Heart rate (HR) was monitored continuously during the test (Polar T 61, Polar, Oulu, Finland). The subjects were verbally encouraged to exercise to exhaustion and 2peak">V̇o2peak was not considered to be reached until the respiratory exchange ratio (RER) exceeded 1.1. Calibration of the gas sensors was performed before each test with a certified gas mixture. Air flow was calibrated before each test using a calibration syringe.
Knee Muscular Strength and Muscular Endurance Measurements
The knee muscle strength and endurance measurements were performed using isokinetic dynamometry. Each subject performed the strength and endurance tests in the same order, starting with a 5-minute warm-up on an ergometer cycle with a work load of 1 W·kg−1 body weight.
The isokinetic tests were performed on a computerized dynamometer (Biodex Multi-Joint System III, Biodex Medical Systems, Inc., Shirley, NY, USA), and the dynamometer calibration was verified before each test day. Subjects were seated in a comfortable position with the backrest angled at 100° to the seat. Velcro straps were placed across the thigh, pelvis, and chest to minimize body movements and to isolate the movement of the knee joint. The arms were crossed over the chest during the test. The mechanical axis of the dynamometer was aligned with the transverse axis of the knee joint, with the lateral femoral epicondyle used as the bony landmark. The weight of the leg was recorded and gravity adjustment was made using the computer software. The range of movement was from 10° to 100° of knee flexion (KF). Isokinetic concentric knee extension (KE) and KF muscle strength and endurance of the right knee were assessed, using 2 test protocols. To analyze muscle strength 5 maximal concentric knee extensor-flexor cycles at 60°·s−1, with no rest between the repetitions, was performed. After a 60-s rest, the subjects performed 30 consecutive maximal extensor-flexor cycles at 180°·s−1 to analyze muscle endurance. Before each test protocol, the subjects performed 2 submaximal extensor-flexor cycles at the preselected angular velocity. Each subject was instructed to exert maximal voluntary effort by performing each contraction as hard and as fast as possible.
Muscle Biopsy Preparations and Measurements
Muscle biopsies were taken from the right vastus lateralis muscle in the fasting state under local anesthesia (Lidocaine 10%), using a 6-mm Bergström needle (Stille AB, Sweden) (11). The participants were instructed to be rested and not perform any vigorous exercise within 48 hours before the biopsy. The biopsy was immediately desiccated, frozen in liquid nitrogen, and stored at −80° C until analysis. The muscle biopsies were thawed, and serial sections (10 μm) were cut using a cryostat at −20° C. Myofibrillar ATPase histochemistry was performed after preincubation at pH 4.4, 4.6, and 10.3 to identify muscle fiber types (6) or by amylase-Periodic Acid Shiff (PAS) (2) (Figure 1). The median number of fibers counted was 387.5 (range 226-685). Computer image analysis was performed using BioPix IQ 2.0.16 software (BioPix AB, Gothenburg, Sweden).
The absolute 2peak">V̇o2peak (L·min−1) was defined as the highest recorded value during the last minute of the incremental cycle test (33). WRpeak was the highest recorded value during the test measured in watts (W). Maximum HR (HRpeak) and the RER were also analyzed.
Knee Muscle Strength and Muscle Endurance Measurements
Peak torque (Nm) was defined as the single highest torque produced during the 5 consecutive muscular contractions performed at the angular velocity of 60°·s−1 (22). Total work (Nm·s−1) was the amount of work accomplished for the entire set of 30 contractions performed at the angular velocity of 180°·s−1. Peak torque is considered to represent muscle strength at a specific angular velocity. Total work reflects a measure of muscular endurance (22). Peak torque 60°·s−1 will further on be referred to as strength and total work 180°·s−1 as endurance.
Values throughout are given as mean ± SD. Pearson's correlation was used to analyze relationships between variables. Stepwise multiple linear regression analyses, both backward and forward, were performed. In the backward regression, independent variables were excluded because of collinearity during the multiple regression analysis. When no collinearity was found between independent variables, a forward regression analysis was performed. Dependent variables were 2peak">V̇o2peak and WRpeak. Independent variables were KE and KF muscle strength, KE and KF muscle endurance, and fiber-type composition (type I, IIa and IIb fibers). Models are reported together with the adjusted R 2 values as assessments of the goodness of fit. SPSS (Version 13.0, SPSS Inc. Chicago, IL, USA) was used for the statistical analyses. The p ≤ 0.05 criterion was used for establishing statistical significance.
To determine the reliability of the equipment and procedures used for 2peak">V̇o2peak and WRpeak measurements 6 male subjects (age: 33.0 ± 8.7 years, height: 185 ± 6 cm, weight: 82.1 ± 5.7 kg) performed a test-retest on the cycle ergometer with 24 hours between the tests. V̇o2, VCO2, and ventilation were measured during an incremental maximal test. The coefficient of variance (CV) and method error (ME) were determined, and CV 2.5% and ME ±0.08 L·min−1 were recorded. Corresponding values on the reliability of load measurement during ergometry cycling was CV 3% and ME ± 3 W. The system was also validated against measurements with Douglas bags showing a CV of 3% for V̇o2(8,14,27,28).
Results of the tests are presented in Tables 1 and 2. A correlation matrix for exercise capacity, KE and KF strength, and endurance and fiber-type composition is presented in Table 3.
There was a close relationship between 2peak">V̇o2peak and WRpeak (r = 0.87, p < 0.001). A significant correlation was found between KE strength and 2peak">V̇o2peak and WRpeak (r = 0.45 and r = 0.44, p < 0.001, respectively). There was also a significant correlation between KF endurance and 2peak">V̇o2peak and WRpeak (r = 0.47 and r = 0.45, p < 0.001, respectively). KE endurance correlated significantly to WRpeak (r = 0.32, p < 0.05) and almost to 2peak">V̇o2peak (r = 0.28, p = 0.058) (Table 3).
In Tables 4 and 5, the multiple regression models are summarized. The analyses showed that KE strength, KF endurance, and the percentage of type I fibers could explain up to 40% of the variation in 2peak">V̇o2peak and WRpeak. Notably, the percentage of type I fibers contributed only about 10% to 2peak">V̇o2peak and WRpeak. The KF endurance was the most dominant factor for 2peak">V̇o2peak (20%) and KE strength for the WRpeak model (18%).
The major finding of this study was that the performance of a maximal incremental cycle test in sedentary male subjects was highly affected by lower extremity muscle strength and muscle endurance. Also, fiber-type composition contributes to a smaller extent to peak exercise capacity.
The subjects in this study were moderately overweight according to measurements of BMI (35), waist (31,35), hip, waist/hip ratio (26,35), and thigh girth (35). Muscle fiber type composition (Table 2) was similar to what has been reported earlier in healthy sedentary subjects (17,32,37). 2peak">V̇o2peak (Table 1) was comparable to previously presented normative data for age, height, and physical activity (33). Isokinetic KE and KF peak torque measurements at 60°·s−1 (Table 2) were slightly higher than normative values for this population. The subjects were comparable to the 70th percentile for the age group (15). Thereby, this study group seems representative for sedentary, healthy men in this age group.
Both KE strength and KF endurance were significantly related to 2peak">V̇o2peak and WRpeak at about the same degree (Table 3), reflecting the well-known close relation between 2peak">V̇o2peak and WRpeak. Stepwise multiple regression analysis revealed that KF endurance was the most dominant factor to explain the variance of 2peak">V̇o2peak, whereas KE strength explained most of the variance of WRpeak (Tables 4 and 5). Because WRpeak is known to increase after 2peak">V̇o2peak has been reached during an incremental cycle test, a certain degree of anaerobic, strength-related capacity must be involved in this parameter. The tendency for KE strength to be more compliant to WRpeak than to 2peak">V̇o2peak is therefore expected. Conversely, because 2peak">V̇o2peak is considered to be a measure of aerobic capacity, our finding that 2peak">V̇o2peak was dominated primarily by knee muscle endurance rather than strength is also expected.
In previous sEMG studies, muscle activity in different leg muscle groups during the propulsive phase in cycling has been analyzed. It has been demonstrated that knee extensors contribute to WRpeak with 39-49% and knee flexors with 9-10% (10,24). This is in accordance with the findings of our study, where KE strength was the most important contributor to the variation in WRpeak explaining up to 18%. However, considering the alleged importance of quadriceps muscles compared to hamstring muscles in cycling performance (10,24), the dominance of KF instead of KE endurance is somewhat surprising. Differences in methods to assess muscle load may to some extent explain the differences in our findings compared to those of earlier sEMG studies. The sEMG measures only the total amount of muscle activity, whereas in isokinetic dynamometry, it is possible to obtain separate indices of muscular strength and muscular endurance (10,24). The KF endurance may, however, be of greater importance at peak exercise than earlier accounted for (10,24).
Our finding of a correlation between peak torques values and 2peak">V̇o2peak similar to that between total work and 2peak">V̇o2peak may be less expected in our study group of sedentary individuals. In successful endurance trained cyclists who are known to have a high proportion of type I muscle fibers, a similar finding could be more easily explained. A competitive cyclist's choice of cadence has been shown to be dependent on muscle fiber distribution (12,18). High cadence gives lower force per pedal rate, which is thought to require less type II muscle fibers (12). This allows a cyclist with a high proportion of type I fibers to cope with the large total force required when performing close to 2peak">V̇o2peak. Our group of sedentary subjects, however, has a normal proportion of type I muscle fibers. Also, the relatively low cadence that is used in an incremental cycle test should have influenced the subjects in our study toward recruiting a larger proportion of type II fibers. Instead, the high correlation between peak torque values and 2peak">V̇o2peak in our study group is probably because of the previously discussed high correlation between 2peak">V̇o2peak and WRpeak. This study examined the relationship between peak exercise capacity and isokinetic KE and KF strength and endurance in sedentary subjects. Therefore, the results in this study may not be applicable to elite cyclists. Although the proportion of force produced by knee and hip muscle might be similar (10,24), patterns of ankle muscle recruitment could differ between novice and elite cyclists (9). It is possible that a difference in recruitment also exists for KE and KF muscles. Further studies are required to confirm these findings in other populations.
The variance of both 2peak">V̇o2peak and WRpeak was explained not only by KF muscle endurance and KE muscle strength but also to a lesser degree also by a high percentage of type I muscle fibers (Tables 4 and 5). The proportion of type I muscle fibers has earlier been shown to contribute to 2peak">V̇o2peak (5), which was also found in our study (Table 4). Previous studies of nonathletic individuals with a high proportion of type I fibers in the knee muscles have also demonstrated high muscle endurance (total work) during isokinetic testing, whereas individuals with a low proportion of type I fibers have high strength (peak torque) values (30). The significant correlation between knee muscle endurance and 2peak">V̇o2peak that was found in our study was therefore anticipated. Muscular strength, assessed as 1 RM, in weightlifters has been shown to relate to type II muscle fiber distribution, especially type II a muscle fibers (16). This is comparable to the relation between KE muscular strength and KE muscular endurance and type II fibers in our study despite the sedentary population in our study (Table 3). Although, it has been suggested that type II fiber distribution may contribute to other forms of high-power activates (16), neither Patton et al (25) nor we could show this relation between power produced during cycling and type II a fiber distribution. Power produced during highly repetitive activity such as cycling may be more dependent on type 1 muscle fibers (Tables 4 and 5).
In conclusion, the performance of 2peak">V̇o2peak and WRpeak in sedentary subjects in a maximal incremental cycle test is highly affected by knee muscle strength and endurance. Fiber type composition also contributes to WRpeak but to a smaller extent.
The performance of a maximal incremental cycle test in sedentary male subjects was highly affected by knee muscular strength and muscular endurance. Also, muscle fiber type composition contributed to peak exercise capacity. When prescribing exercise training to increase exercise capacity in sedentary male subjects, it should be kept in mind that muscular strength and muscular endurance also will contribute to the exercise capacity and not only cardiorespiratory indices. Resistance training of the legs may help improve cycling performance.
1. ACSM's Guidelines for Exercise Testing and Prescription
(8th ed.). Baltimore, MD: Lippincott Williams & Wilkins, 2010.
2. Andersen, P. Capillary density in skeletal muscle of man. Acta Physiol Scand
. 95: 203-205, 1975.
3. Åstrand, P, Rodahl, K, Dahl, H, and Strømme, S. Textbook of Work Physiology-Physiological Bases of Exercise
(4th ed.). Champaign, IL: Human Kinetics, 2003. pp. 280-281.
4. Astrand, PO and Ryhming, I. A nomogram for calculation of aerobic capacity (physical fitness) from pulse rate during sub-maximal work. J Appl Physiol
7: 218-221, 1954.
5. Bergh, U, Thorstensson, A, Sjodin, B, Hulten, B, Piehl, K, and Karlsson, J. Maximal oxygen uptake and muscle fiber types in trained and untrained humans. Med Sci Sports
10: 151-154, 1978.
6. Brooke, MH and Kaiser, KK. Three “myosin adenosine triphosphatase” systems: The nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem
18: 670-672, 1970.
7. Bruce, RA, Blackmon, JR, Jones, JW, and Strait, G. Exercising testing in adult normal subjects and cardiac patients. Ann Noninv Electrocardiol
9: 291-303, 2004.
8. Carter, J and Jeukendrup, AE. Validity and reliability of three commercially available breath-by-breath respiratory systems. Eur J Appl Physiol
86: 435-441, 2002.
9. Chapman, AR, Vicenzino, B, Blanch, P, and Hodges, PW. Patterns of leg muscle recruitment vary between novice and highly trained cyclists. J Electromyogr Kinesiol
18: 359-371, 2008.
10. Ericson, M. On the biomechanics of cycling. A study of joint and muscle load during exercise on the bicycle ergometer. Scand J Rehabil Med Suppl
16: 1-43, 1986.
11. Eriksson, KF, Saltin, B, and Lindgarde, F. Increased skeletal muscle capillary density precedes diabetes development in men with impaired glucose tolerance. A 15-year follow-up. Diabetes
43: 805-808, 1994.
12. Faria, EW, Parker, DL, and Faria, IE. The science of cycling: Physiology and training-Part 1. Sports Med
35: 285-312, 2005.
13. Flouris, AD, Metsios, GS, and Koutedakis, Y. Contribution of muscular strength in cardiorespiratory fitness tests. J Sports Med Phys Fitness
46: 197-201, 2006.
14. Foss, O and Hallen, J. Validity and stability of a computerized metabolic system with mixing chamber. Int J Sports Med
26: 569-575, 2005.
15. Freedson, P, Giliam, T, Mahoney, T, Mailszweski, A, and Kastango, K. Industrial torque levels by age group and gender. Isokinet Exerc Sci
3: 34-42, 1993.
16. Fry, AC, Schilling, BK, Staron, RS, Hagerman, FC, Hikida, RS, and Thrush, JT. Muscle fibre characteristics and performance correlates of male olympic-style weightlifters. J Strength Cond Res
17: 746-754, 2003.
17. Gollnick, PD, Armstrong, RB, Saubert, CW IV, Piehl, K, and Saltin, B. Enzyme activity and fibre composition in skeletal muscle of untrained and trained men. J Appl Physiol
33: 312-319, 1972.
18. Hansen, EA and Sjogaard, G. Relationship between efficiency and pedal rate in cycling: Significance of internal power and muscle fiber type composition. Scand J Med Sci Sports
17: 408-414, 2007.
19. Hansen, JE, Casaburi, R, Cooper, DM, and Wasserman, K. Oxygen uptake as related to work rate increment during cycle ergometer exercise. Eur J Appl Physiol Occup Physiol
57: 140-745, 1988.
20. Hug, F and Dorel, S. Electromyographic analysis of pedaling: A review. J Electromyogr Kinesiol
19: 182-198, 2009.
21. Jones, A and Poole, D. Oxygen Uptake Kinetics in Sport, Exercise and Medicine
. New York, NY: Routledge, 2005. pp. 261-293.
22. Kannus, P. Isokinetic evaluation of muscular performance: Implications for muscle testing and rehabilitation. Int J Sports Med
15(Suppl 1):S11-S18, 1994.
23. Martin, JC, Davidson, CJ, and Pardyjak, ER. Understanding sprint-cycling performance: The integration of muscle power, resistance, and modelling. Int J Sports Physiol Perform
2: 5-21, 2007.
24. McDaniel, JG, Lex, D, Tomas, A, Hunter, EL, Grisham, JD, McNeil, JM, Carroll, C, Thompson, FT, Davidsson, CJ, and Horscroft, RD. Joint power distribution at 60, 90, and 120 rpm during seated maximal cycling. Med Sci Sports Exerc
37: 123, 2005.
25. Patton, JF, Kraemer, WJ, Knuttgen, HG, and Harman, EA. Factors in maximal power production and in exercise endurance relative to maximal power. Eur J Appl Physiol
60: 222-227, 1990.
26. Potteiger, JA, Jacobsen, DJ, Donnelly, JE, and Hill, JO. Glucose and insulin responses following 16 months of exercise training in overweight adults: The Midwest exercise trial. Metabolism
52: 1175-1181, 2003.
27. Rietjens, GJ, Kuipers, H, Kester, AD, and Keizer, HA. Validation of a computerized metabolic measurement system (Oxycon-Pro) during low and high intensity exercise. Int J Sports Med
22: 291-294, 2001.
28. Rosdahl, H, Gullstrand, L, Salier-Eriksson, J, Johansson, P, and Schantz, P. Evaluation of the Oxycon Mobile metabolic system against the Douglas bag method. Eur J Appl Physiol
29. Smirniotou, A, Katsikas, C, Paradisis, G, Argeitaki, P, Zacharogiannis, E, and Tziortzis, S. Strength-power parameters as predictors of sprinting performance. J Sports Med Phys Fitness
48: 447-454, 2008.
30. Thorstensson, A and Karlsson, J. Fatiguability and fibre composition of human skeletal muscle. Acta Physiol Scand
98: 318-322, 1976.
31. Vella, CA, Zubia, RY, Burns, SF, and Ontiveros, D. Cardiac response to exercise in young, normal weight and overweight men and women. Eur J Appl Physiol
105: 411-419, 2009.
32. Wade, AJ, Marbut, MM, and Round, JM. Muscle fibre type and aetiology of obesity. Lancet
335: 805-808, 1990.
33. Wasserman, K, Hansen, J, Sue, D, Stringer, W, and Whipp, B. Principles of Exercise Testing and Interpretation
(4th ed.). Philadelphia, PA: Lippincott Williams & Wilkins, 2005. pp. 162-165.
34. Wasserman, K and Whipp, BJ. Exercise physiology in health and disease. Am Rev Respir Dis
112: 219-249, 1975.
35. Wells, JC, Cole, TJ, and Treleaven, P. Age-variability in body shape associated with excess weight: The UK National Sizing Survey. Obesity
16: 435-441, 2008.
36. Wisen, AG and Wohlfart, B. Determination of both the time constant of vO2 and DeltavO2/DeltaW from a single incremental exercise test: Validation and repeatability. Clin Physiol Funct Imaging
24: 257-265, 2004.
37. Zoladz, JA, Semik, D, Zawadowska, B, Majerczak, J, Karasinski, J, Kolodziejski L, Duda, K, and Kilarski, WM. Capillary density and capillary-to-fibre ratio in vastus lateralis muscle of untrained and trained men. Folia Histochem Cytobiol
43: 11-17, 2005.
Keywords:© 2011 National Strength and Conditioning Association
isokinetic dynamometry; incremental cycle test; 2peak">V̇o2peak; WRpeak