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J Appl Physiol 103: 932-940, 2007. First published June 21, 2007; doi:10.1152/japplphysiol.01221.2006
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Do skeletal muscle phenotypic characteristics of Xhosa and Caucasian endurance runners differ when matched for training and racing distances?

Tertius A. Kohn,1 Birgitta Essén-Gustavsson,2 and Kathryn H. Myburgh1

1Department of Physiological Sciences, University of Stellenbosch, Matieland, South Africa; and 2Department of Large Animal Clinical Sciences, Swedish University of Agricultural Sciences, Uppsala, Sweden

Submitted 28 October 2006 ; accepted in final form 18 June 2007


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Although East African black athletes dominate endurance running events, it is unknown whether black and white endurance runners with similar racing ability, matched for training, may differ in their skeletal muscle biochemical phenotype. Thirteen Xhosa (XR) and 13 Caucasian (CR) endurance runners were recruited and matched for 10-km performance, average preferred racing distance (PRDA), and training volume. Submaximal and maximal exercise tests were done, and vastus lateralis muscle biopsies were taken. XR were significantly lighter and shorter than CR athletes but had similar maximum oxygen consumption corrected for body weight and peak treadmill speed (PTS). XR had lower plasma lactate concentrations at 80% PTS (P < 0.05) compared with CR. Also, XR had more type IIA (42.4 ± 9.2 vs. 31.3 ± 11.5%, P < 0.05) and less type I fibers (47.8 ± 10.9 vs. 63.1 ± 13.2%, P < 0.05), although oxidative enzyme activities did not differ. Furthermore, XR compared with CR had higher lactate dehydrogenase (LDH) activity in homogenate muscle samples (383 ± 99 vs. 229 ± 85 µmol·min–1·g dry weight–1, P < 0.05) and in both type IIa (P < 0.05) and type I (P = 0.05) single-fiber pools. A marked difference (P < 0.05) in the composition of LDH isoform content was found between the two groups with XR having higher levels of LDH5-4 isoforms (skeletal muscle isozymes; LDH-M) than CR, which was not accounted for by fiber-type differences alone. These results confirm differences in muscle phenotype and physiological characteristics, particularly associated with high-intensity running.

African runners; fiber type; myosin heavy chain isoforms; enzyme activities; single fibers

RUNNING EVENTS from the middle distances (800–10,000 m) to long distances (half- and full-marathon) are dominated by East African black runners (34, 42). These populations may have a genotypic or phenotypic advantage when it comes to endurance running. Several investigators have searched for phenotypic differences between black and white endurance athletes from South Africa, Kenya, and Eritrea (8, 16, 36, 47, 59, 60).

The South African studies have presented some consistent but also some inconsistent findings. Two studies indicated that black runners ran at a higher percentage of their maximum oxygen consumption (VO2max) during either a simulated treadmill marathon (8) or at 10-km race pace (60) compared with their white counterparts. VO2max differed in one (60) but not the other study (8). Similarly, one study has found no difference in running economy at either 17 or 21 km/h (16), while another found a significant difference (60). A more consistent finding was that South African black endurance runners had lower blood lactate concentrations during submaximal exercise tests (8, 16, 59).

Their ability to sustain running intensities close to their VO2max (41, 60) and to resist fatigue in unfavorable conditions (38) may be related to central control of whole body homeostasis during exercise (41) or to the smaller body size of the black runners or to a more favorable muscle metabolic profile (59). Biopsy data from the vastus lateralis have shown that the South African black runners tend to have a lower proportion of type I muscle fibers compared with white endurance runners (8, 16). Higher citrate synthase (CS) and 3-hydroxyacyl-CoA dehydrogenase (3-HAD) activities have also been found in the vastus lateralis of black endurance runners (59). This finding seemed difficult to explain given the literature showing that type I fibers are associated with higher CS and 3-HAD activities (21).

Nonetheless, Kenyan runners, compared with Scandinavian runners, also had higher mean 3-HAD activity albeit in the gastrocnemius muscle, and the ratio of lactate dehydrogenase (LDH) isozymes was different between the two groups (47). Kenyans had a higher ratio of LDH1-2:LDH4-5 (LDH-H:LDH-M), but after the Scandinavians trained for 14 days at altitude, the difference between the groups for these ratios became nonsignificant. However, these findings might have been influenced by the low subject numbers (5 Kenyans and 6 Scandinavians), that women were included in the Scandinavian group, and that the Kenyan subject group consisted of senior and junior runners, as well as altitude effects. Nonetheless, similar to the studies on South African runners, it was shown that the Kenyans had lower plasma lactate levels at submaximal intensities compared with Scandinavian runners (48). No differences were found between the two groups for VO2max and hemoglobin concentrations, suggesting a peripheral rather than a cardiovascular cause for the lower lactate accumulation during exercise.

The above-mentioned studies have advanced our scientific understanding of differences in the endurance phenotype of black and white distance runners, indicating that running economy may be a factor in the better performance of the African runners. However, several studies have indicated that black athletes also have a metabolic phenotype of low lactate accumulation that is not adequately explained, since the muscle fiber types and biochemical phenotypes have not been investigated in detail. Finally, both training volume and habitual racing distance could influence these parameters but were inconsistent between groups in some of the previous studies, possibly confounding the conclusions. When black and white athletes are well-matched for racing ability, racing distance, and training, we hypothesize that that there will be inherent skeletal muscle phenotypic differences.

The aim of the present study was to do a comprehensive phenotypic comparison between subelite black endurance runners from distinct ethnic origin (Xhosa) and white endurance runners of Caucasian descent who were closely matched for the aforementioned factors. This study investigated possible differences in whole body physiology and muscle characteristics, with special emphasis on fiber type and enzyme activities, including LDH activities and isozyme proportions and single muscle fiber analyses. Focus was also placed on increasing the sample size compared with previous studies.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Subject recruitment and training volume assessment.   The Stellenbosch University Research Administration Subcommittee C Ethics Committee for research on human subjects approved this study. Twenty-six athletes (13 Caucasian and 13 ethnic Xhosa) were recruited from local athletic clubs. Athletes were informed about all the tests and possible risks involved. If a subject was unfamiliar with the language, an interpreter was used. Each athlete signed a written informed consent before testing.

Exclusion criteria included not currently competing in races, a current 10-km road race time of >37 min, any illness or injury in the previous 6 mo, and training < 45 km/wk. Caucasian athletes were from British or Dutch European descent, the two groups representing most Caucasians living in South Africa. Xhosa athletes were from Xhosa-speaking family lineage, a lineage that descends from the Nguni of Southern Zaire in Central Africa (10). Other Nguni descendents in South Africa include the Zulu, but distinctions have long been made between the South Nguni (Xhosa) and the North Nguni (Zulu) (10, 26). The Xhosa ethnicity of the subjects was based on the stated first language reported for both parents and all four grandparents. Although it is regarded from an anthropological perspective that Xhosa people rarely intermarry with other African tribes, and this is supported by genetic evidence from Lane et al. (33), we do not assume a homogeneous genetic background.

Each athlete completed a detailed questionnaire reporting favorite race distance for road, track, and cross-country competitions, recent 10-km personal-best time (PB), and typical training volume per week specifically for the previous 3 mo. An average preferred specialization distance (PRDA) was calculated for each athlete by taking the average of the three favorite racing distances, one for each of the three disciplines mentioned above. In some cases, athletes participated in only two of these disciplines, but no athletes competed in only one. Athletes were matched for weekly training volume, 10-km PB, and PRDA (Table 1).


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  		Table 1. Matching of Caucasian and Xhosa athletes according to usual training volume, recent 10-km personal best race time, and average preferred racing distance

 
Exercise tests and muscle biopsies were performed on separate days, allowing recovery from previous running tests for at least 2 days. Athletes were encouraged to be well rested and to perform very-low-intensity training the day before testing. All athletes were thoroughly familiarized on the treadmill (including exposure to low- and high-speed running on the treadmill) before running tests.

VO2max testing and peak treadmill speed.   Athletes performed two incremental maximal exercise tests to fatigue on a treadmill (RunRace, TechnoGym), with continuous measurement of heart rate (Polar), oxygen consumption (VO2), respiratory exchange ratio (RER), and minute ventilation (VE) (Jaeger Oxycon Pro) throughout the test. After a 5-min warm-up on the treadmill, tests started at 14 km/h, and thereafter the treadmill speed was increased by 0.5 km/h every 30 s until fatigue. Athletes were said to have attained their maximal ability when two of the following criteria were fulfilled: 1) heart rate within 5 beats/min of theoretical maximum heart rate (220 – age); 2) RER > 1.10; and 3) a plateau in VO2 (53). A plateau was considered as less than one-half the expected rise in oxygen consumption for the workload compared with the linear relationship between oxygen consumption and speed during the incremental test. Whenever these criteria were not fulfilled, athletes had to perform the same test on the next visit and were encouraged verbally during the test to perform better. Peak treadmill speed (PTS; in km/h) was calculated as follows taking every second into account:

Formula

Submaximal exercise test and blood sampling.   Before warm-up and submaximal testing, athletes were fitted with an intravenous catheter (Jelco 22G, Johnson & Johnson) and a three-way stopcock, which were flushed with saline containing 0.04% heparin (Heparin Novo, Novo Nordisk).

The submaximal workloads corresponded to 64, 72, and 80% of each individual's PTS (the highest attained during 1 of the 2 maximal tests). Athletes ran for 5 min at each workload, and breath-by-breath measurements were recorded as described for the incremental test. Values collected for the 5th minute were considered for data analysis. During the 1-min rest interval, 3-ml blood samples were collected in sealed test tubes containing fluoride oxalate (Vacutainer, BD), mixed, and stored on ice. Blood was centrifuged directly after the test at 3,000 rpm, and the plasma was stored at –87°C until analysis. Running economy was determined for the speed 16.1 km/h from x-y plots of VO2 and treadmill speed.

Muscle biopsy.   A needle biopsy was obtained from the vastus lateralis muscle using the suction-assisted technique described by Evans et al. (22). The biopsy site was at the same depth (2 cm) and in a similar position for all athletes, corresponding to one-third along the total length of the upper leg, distal to the hip joint. The biopsy was split into three parts: two were frozen in liquid nitrogen for subsequent homogenate and single fiber analyses, and the third was mounted in embedding medium (Jung Tissue Freezing Medium, Leica Instruments) and rapidly frozen in isopentane, precooled with liquid nitrogen. All biopsy samples were stored at –87°C.

Plasma lactate concentration.   Plasma lactate concentrations (mmol/l) were determined using a commercially available kit based on enzymatic conversion of plasma lactate (Lactate PAP, BioMérieux) and a spectrophotometer (Bio-Tek Instruments).

Morphology of fibers.   Fiber typing of muscle samples was based on the method by Brooke and Kaiser (11). Three serial cross sections (10 µm) were cut onto glass slides and placed into preincubation medium set at exactly pH 4.30, 4.60, and 10.30, after which the samples were treated similarly. Sections were visualized and photographed (Nikon CoolPix Microscope System). Fibers were identified as either types I, IC, IIC, IIAC, IIA, IIAX, or IIX according to the staining intensities described by Staron (54), and expressed as a percentage of the total number of fibers counted. In this study, fiber types IC, IIC, and IIAC numbers were pooled and termed type I/IIA because of low counts in each of the aforementioned subgroups. Cross-sectional area (CSA, µm2) and fiber diameter (FD, µm) were determined using a computer software program (SimplePCI version 1.0, Nikon) on the same slides photographed for the fiber typing. Fibers were divided into two groups, namely type I (pure type I fibers only) and type II fibers, the latter comprising of fiber types I/IIA, IIA, IIAX, and IIX.

Enzyme activities and myosin heavy chain composition in homogenate samples.   Muscle biopsy samples previously frozen in liquid nitrogen were freeze-dried overnight. A small piece was weighed and crushed in a test tube, and a ratio of 1 mg:400 µl chilled 100 mM potassium phosphate buffer, pH 7.30, was added. Samples were kept on ice and sonicated (Virtis Sonicators) three times for 10 s on ice, with a 10-s delay between intervals. Phosphofructokinase (PFK), CS, LDH, and 3-HAD activities were determined using the fluorometric methods described by Essén-Gustavsson and Henriksson (21), with slight modifications. Reagent and sample volumes were decreased to accommodate the microplate reader (Bio-Tek Instruments). The enzyme reagent was always 250 µl; sample volumes for PFK, CS, and 3-HAD were 5 µl and 3 µl for the LDH assay. The emission at 460 nm was recorded for 5 min with 30-s intervals using an excitation wavelength of 340 nm. Enzyme activities are expressed as micromoles per minute per gram dry weight (dw).

Myosin heavy chain (MHC) isoform contents of homogenate samples were determined using SDS-PAGE according to the method of Talmadge and Roy (56) with beta-mercaptoethanol added to the upper running buffer to a concentration of 0.12% before electrophoresis (7, 32). Electrophoresis was carried out using a large-gel system (Bio-Rad) for 28 h at constant 70 V at 4°C. Gels were stained with Coomassie blue R250 and subsequently scanned using a computer scanner. Relative percentages of the bands were quantified using a software package (CREAM 1D, KEM-EN-TEC).

Single-fiber identification and enzyme activities.   Single muscle fibers were dissected from freeze-dried samples in a humidity-controlled room (40% humidity, 20°C). A total of 2,857 (mean of ± 130 fibers/sample) fibers were dissected. A small piece of each fiber was cut off, transferred to a capillary tube containing SDS denaturing buffer, and left overnight to dissolve. The remaining piece was sealed and stored in a labeled glass capillary tube at –87°C. Identification of the fiber types was carried out electrophoretically on the dissolved fragment, using the same protocol described above. Gels were silver stained (Amersham), and fibers were identified as expressing either pure fibers (MHC I, IIa, or IIx), or hybrid fibers (MHC I/IIa or MHC IIa/IIx).

LDH activities in pools of pure type I and pools of pure type IIa fibers were determined for each subject. The pooled fibers were weighed on a microbalance (to 3 decimals of a milligram), calibrated with known weights. Pool weights ranged between ~40 and ~100 µg. After weighing on an electrobalance (Cahn 25), the samples were transferred to a microtube, and 400 µl chilled 100 mM potassium phosphate buffer (pH 7.30) was added per 1 mg sample. Sonication and enzyme activity determination were carried out in the same way as for the homogenate samples. Enzyme activities are expressed as micromoles per minute per gram dry weight.

LDH isoform content in homogenate samples.   LDH isoform content of homogenate muscle samples was analyzed electrophoretically on nondenaturing polyacrylamide gels using modifications to existing protocols (19, 62). Freeze-dried samples were diluted with 15 µl 0.1 M potassium phosphate buffer (pH 7.30) per milligram, homogenized by hand on ice, and centrifuged (10 min at 600 g at 4°C). The protein concentration of the supernatant was determined (9). Part of the supernatant was diluted with 40% sucrose to yield a final protein concentration of 5 mg/ml. The gels consisted only of a separating gel that contained 5% acrylamide, 0.13% bisacrylamide, 0.25 M Tris (pH 8.90), 0.12% ammonium persulfate and 0.1% TEMED. The electrophoresis buffer had a final pH of 9.50 and contained 5 mM Tris and 25 mM glycine. Electrophoresis of 20 µg total protein per well was carried out using a minigel system (Bio-Rad) at 8 mA for 2 h at 4°C. Gels were incubated for a minimum of 10 min at 37°C in a solution containing 1.3% sodium lactate, 0.03% nitroblue tetrazolium, 0.003% phenazine methosulfate, 50 mM Tris·HCl, and 0.06% NAD+. Gels were subsequently scanned using a computer scanner. Relative percentages of the five separated bands were quantified using a software package (CREAM 1D, KEM-EN-TEC).

Statistical analysis.   Values are expressed as means ± SD. Statistical comparisons between population groups were performed using the Wilcoxon signed rank test for nonparametric matched pair data. However, because of lower sample numbers in the single-fiber enzyme pools, statistical significance was determined with the Mann-Whitney U-test for nonparametric unpaired data (see Fig. 4). Significance for all analyses was set at P < 0.05. Correlation coefficients were calculated using the two-tailed Pearson's correlation test to assess specific associations 1) between fiber type and other muscle phenotypic characteristics, and 2) between submaximal exercise test physiological parameters (including plasma lactate accumulation) and muscle phenotypic characteristics.


Figure 1
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  		Fig. 1. Plasma lactate concentration during the submaximal exercise test in Caucasian and Xhosa athletes. Values are means ± SD (n = 12 pairs). PTS, peak treadmill speed. *Significantly different from Xhosa (P < 0.05).

 

Figure 2
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  		Fig. 2. Fiber types (A; n = 9 pairs) and myosin heavy chain (MHC) isoform content (B; n = 13) in homogenate muscle samples of Caucasian and Xhosa athletes. Values are means ± SD. *Significantly different from Caucasian (P < 0.05).

 

Figure 3
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  		Fig. 3. Enzyme activities in homogenate muscle samples (n = 9 pairs) of Caucasian and Xhosa athletes. Values are means ± SD. CS, citrate synthase; PFK, phosphofructokinase; 3-HAD, 3-hydroxyacyl-CoA dehydrogenase; LDH, lactate dehydrogenase; dw, dry weight. *Significantly different from Caucasian, P < 0.01. #Different from Caucasian (P = 0.07).

 

Figure 4
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  		Fig. 4. LDH activities in pools of single fibers and homogenate muscle samples of Caucasian and Xhosa athletes who could not be paired for this analysis. Values are means ± SD. *Significantly different from Caucasian (P < 0.05). #Different from Caucasian (P = 0.05). Sample size is indicated within each bar.

 

   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Good matching of athletes for training volume, 10-km PB, and PRDA was obtained. As can be seen in Table 1, athletes were coded according to matching pairs, and for matching, none of the three variables considered was given first priority; rather all three were taken into account. A final consideration was whether the pairs’ muscle biopsies were similarly analyzed (see {dagger} in Table 1).

Table 2 reports the subject characteristics, as well as the maximal exercise test results, the latter taken from the highest PTS of the two tests. Xhosa athletes were lighter and shorter than their matched counterparts (P < 0.01). VO2max expressed relative to body weight was similar in the recruited athletes. However, when values were not corrected for body weight, significant differences were apparent (see VO2max and VE expressed in l/min, Table 2). Both groups reached similarly high peak treadmill speeds and maximum RER, as would be expected for subjects matched for performance, and this indicated that both groups were similarly familiar with treadmill running at maximal capacity.


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  		Table 2. Subject characteristics and maximal exercise test results of Caucasian and Xhosa athletes

 
At all the submaximal workloads, no differences were observed for RER, heart rate, and VO2 expressed relative to body mass (Table 3), with the exception of VO2 at 80% PTS, which showed a trend to be higher in Xhosa compared with Caucasian athletes (P = 0.09). VE was significantly lower in Xhosa athletes at 64 and 72% PTS workloads but became nonsignificant at the higher workload (80% PTS). Economy at 16.1 km/h expressed relative to body mass and relative to body mass scaled to 0.75 (kg0.75), was similar in both groups. During the submaximal test, there were no differences in the mean plasma lactate concentrations between the groups at the 64 and 72% PTS workloads (Fig. 1). However, at 80% PTS, the Xhosa athletes had lower mean plasma lactate concentrations than their Caucasian counterparts (P < 0.05).


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  		Table 3. A comparison of Caucasian and Xhosa athlete physiological parameters, including running economy and metabolic profile relative to PTS

 
Xhosa athletes had less type I fibers with a concomitantly higher proportion of type IIA fibers than their Caucasian counterparts (Fig. 2A, P < 0.05) determined with ATPase histochemistry in nine pairs. This was further confirmed with the MHC isoform analysis in 13 pairs who showed lower MHC I and higher MHC IIa expression in Xhosa athletes (Fig. 2B, P < 0.05). There was no difference between Xhosa and Caucasian athletes for the proportions of type I/IIA, IIAX, and IIX fibers. Morphometry of type I and type II muscle fibers of nine pairs of Caucasian and Xhosa biopsies revealed no differences in CSA (µm2) and FD (µm) for either fiber type between groups (Table 4). A large variability is apparent for both fiber types in both groups.


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  		Table 4. Cross-sectional area and fiber diameter of Caucasian and Xhosa muscle biopsy samples

 
Enzyme activities were analyzed in homogenate muscle samples of nine pairs and were similar in range to those reported by Essén-Gustavsson and Henriksson (21) for endurance-trained athletes. No differences were observed for CS, PFK, and 3-HAD activities (Fig. 3). However, LDH activity was higher in Xhosa athletes compared with Caucasian athletes (P < 0.01), with PFK activity showing a trend to be higher in Xhosa athletes (P = 0.07).

LDH activities in distinct fiber type pools and homogenate samples are represented graphically in Fig. 4. Only subjects with activities for both pools and homogenates were used in this figure (Caucasian: n = 6; Xhosa: n = 7). The homogenate LDH activity was higher in Xhosa compared with Caucasian athletes. The range of activities between the two fiber types was similar in range to that reported by Essén-Gustavsson and Henriksson (21). Statistical analysis between fiber types within each group showed that the mean LDH activity of type I fiber pools was significantly lower than the mean for the type IIa pools for both Caucasian and Xhosa athletes (P < 0.05). However, the mean LDH activities in type I and type IIa pools of Caucasian athletes were significantly lower than the mean for type I and type IIa pools in Xhosa athletes (P < 0.05).

Figure 5 illustrates the LDH isoform content in muscle homogenate samples of Caucasian and Xhosa athletes. Xhosa athletes expressed higher levels of the LDH5 and LDH4 isoforms (LDH-M), with the remaining three isoforms (LDH3-1) lower than their Caucasian counterparts (P < 0.05).


Figure 5
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  		Fig. 5. LDH isoform (LDH 5, LDH 4, LDH 3, LDH 2, LDH 1) content in homogenate muscle samples of Caucasian and Xhosa athletes. Values are means ± SD. *Significantly different from Caucasian (P < 0.05).

 
Relationships were observed between LDH activity and either the MHC I or MHC IIa contents of muscle samples (MHC I: r = –0.57, P < 0.05; MHC IIa: r = 0.63, P < 0.01, Fig. 6) and similarly between PFK activity and MHC proportions (MHC I: r = –0.63, P < 0.01; MHC IIa: r = 0.58, P < 0.05) in homogenate samples. No relationship was observed between plasma lactate at 80% PTS and LDH [r = –0.31, not significant (NS)], or MHC IIa (r = 0.23, NS) content of muscle samples. However, there was a significant relationship between the ratio of LDH activity and MHC IIa in homogenates (LDH activity/%MHC IIa) and the plasma lactate at 80% PTS (r = –0.56, P < 0.05). This relationship indicates that the higher the LDH activities are, despite normalizing for fiber type, the lower is the accumulation of plasma lactate.


Figure 6
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  		Fig. 6. Relationship between homogenate muscle LDH activity and MHC IIa. Pearson's correlation coefficient of r = 0.63, P < 0.01.

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
The present study confirms the main finding of most of the previous related studies, namely that there were lower plasma lactate concentrations during the submaximal exercise tests in black endurance athletes compared with white athletes, particularly at higher relative intensities. This study, comparing the phenotypes of athletes from two distinctly different genotypic groups, shows that Xhosa athletes had lower type I fiber proportions, which had been suggested before, but not conclusively proved (16, 59). The most novel findings were that Xhosa athletes had a higher proportion of type IIa fibers and higher LDH activities in muscle homogenate samples, type IIa pools, as well as type I fiber pools, than their Caucasian counterparts. This indicates that the higher activity in the homogenate samples of the Xhosa runners were not simply a result of higher proportions of fast-twitch fibers. Unlike most of the other studies, running economy did not differ. Neither did oxidative enzyme activities differ. Both these findings confirm, on the one hand, the close matching of the athletes for training and racing distances, and on the other their subelite status.

Physical and physiological characteristics of athletes.   Past studies on black and white athletes, both elite and subelite, were not able to match the two groups of athletes for body size. Studies on South African black runners all reported that black athletes are shorter and lighter than their Caucasian counterparts (8, 16, 38, 59). Body size does play a significant role in absolute VO2max and in lung volume, which differs extensively between population groups (61). According to Svedenhag (55), it is more correct to express oxygen uptake as millimeters per minute per kilogram0.75 than millimeters per minute per kilogram. Both calculation methods were applied, but neither resulted in a difference in maximal oxygen consumption between Xhosa and Caucasian athletes. On the one hand, this could be due to the fact that the athletes were all subelite in the present study, but on the other, this finding is in accordance with previous studies on South African black and white athletes, as well as Caucasian and Kenyan runners, and Spanish and Eritrean distance runners (16, 36, 47, 59). It is well known that VO2max is only one of many factors contributing to the endurance phenotype (40).

Muscle fiber types.   Although one factor proposed to contribute to elite endurance performance on the road is a high percentage of type I fibers (17), Xhosa athletes, however, had less type I fibers and more type IIA fibers (Fig. 2A) than their Caucasian counterparts. This was confirmed by MHC isoform content analysis (which also takes into account any MHC I or IIa coexpression in hybrid fibers) (Fig. 2B). In previous studies, black runners also showed tendencies to have fewer type I fibers, but those findings were not statistically significant (16, 59). This might have been due to low subject numbers or less stringent matching. The present study also reports more fiber-type subdivisions than the previous studies performed on South African athletes. A possible explanation for the lower type I fiber proportions in Xhosa athletes could be that they have trained longer at a higher intensity than their Caucasian counterparts, as was suggested in an earlier study (16). That study reported that black South African runners trained for a longer period of time per week above 80% of their VO2max. Recently, it was shown that marathon training increased type I fiber proportions in recreational subjects (58), whereas higher training intensities (as well as high-frequency electrical stimulation in animal models) may convert type I fibers to faster fiber types (2, 43). Scandinavian elite cross-country skiers had less type I fibers than recreationally active subjects (~31% vs. ~62%) (31), suggesting that even elite endurance athletes may benefit more from moderate type II fiber proportions than was suggested earlier (17, 46).

Both the present data and an earlier Kenyan-Scandinavian study (47) indicate the presence of some pure type IIX fibers within the fiber type distribution in the muscles of both groups. This finding is surprising as it is commonly accepted that endurance training results fairly easily in conversion of type IIX fibers into type IIA (3, 4), and molecular mechanisms controlling this conversion are currently fairly well understood (30, 49). However, in athletes running at very high speeds, molecular mechanisms may promote the continued expression of MHC IIx concurrently with MHC IIa, possibly in response to demands for a mechanical power rather than the demand for prolonged cyclical activation.

The proportion of type I fibers in distance runners (3,000–10,000 m) and in senior Kenyan athletes are reported to be higher (~65–75%) (27, 47) than found in the present study. Despite a PRDA of 11.6 ± 5.2 km, type I fiber proportions of Xhosa athletes were more closely related to that reported earlier for middle distance runners (800–1,500 m) (27). Whether this phenotype in Xhosa endurance athletes is related to genotype or environment (e.g., training intensity) remains to be determined. Black sedentary subjects from Central and West Africa had less type I fibers (33 vs. 41%) than sedentary Caucasians, and it was speculated that this finding may explain why the sprinting events are dominated by African-American blacks originating from that part of Africa (1). However, genetic diversity amongst African athletes has precluded identification of distinct genotypes promoting endurance performance (51, 52) despite geographical clustering (42, 50).

Other factors playing an important role in power generation are the CSA of muscle fibers (25, 57) and the expression of the {alpha}-actinin-3 isoform (36). No differences in CSA and FD were observed between Xhosa and Caucasian athletes, which is similar to findings comparing Kenyan and Scandinavian athletes (47). Neither were the CSA of the fibers associated with PRDA (r = 0.16 and r = 0.23 for type I and II, respectively). This may indicate that in endurance runners, it is fiber type itself that confers greater or lesser capacity for power production. The above statement is supported by the recent work by Trappe et al. (58), who showed that 13 wk of marathon training decreased fiber diameter of MHC I and MHC IIa single fibers but increased peak force and maximal shortening velocity in the same fiber types.

Biochemistry.   In the present study, differences in variables related to lactate metabolism were observed at whole body level (plasma lactate), tissue level (homogenate LDH activities), single-fiber level (LDH activities in pools of identified pure fiber types), and protein level (isoforms of LDH expressed). Previously, lower plasma lactate levels were observed for South African black athletes at relatively low running intensities where oxidative metabolism of both fat and carbohydrate would be predominant (8). Lower submaximal lactate levels were also observed in two other South African studies (16, 59) and in Kenyan compared with Scandinavian runners during submaximal exercise tests (48), whereas the opposite finding was reported comparing Eritrean and Spanish distance runners for submaximal tests (36). The lower plasma lactates at various submaximal running speeds could in previous studies be explained by correlations with the higher CS activity found in the muscle samples of the South African black runners compared with white runners (59) and the higher 3-HAD activity in Kenyan runners (47). Especially the latter would indicate less reliance on carbohydrate and more reliance on fat as a fuel during submaximal exercise. Such a correlation was not found in the present study, possibly because there was no difference between groups in plasma lactate at lower submaximal intensities, but differences were found at 80% PTS when the RER of 0.99 (Caucasian) and 1.00 (Xhosa) indicated substantial carbohydrate flux only. Future studies should investigate this carbohydrate flux in more detail by assessing lactate turnover kinetics during exercise, as has been done previously following training (5, 37). Although it is possible that the Xhosa athletes had a more economical running style once the running speed was sufficiently elevated, this would seem a less likely explanation for the lower lactate accumulation than enhanced lactate removal, since no differences were evident in the whole body oxygen uptake (see Table 3). Also, MacRae et al. (37) specifically showed that at higher intensities of exercise, training improved lactate clearance, despite similarly high rates of appearance, compared with pretraining.

The higher mean LDH activity and tendency for higher PFK activity in Xhosa athletes, with no difference in the activities of CS or 3-HAD (Fig. 3), are consistent with a higher capacity for carbohydrate flux, specifically glycolytic flux without evidence of higher fat or carbohydrate oxidation capacities. No difference in oxidative capacity could be explained by the close matching of training distances between subjects in the present study, whereas the subjects in the study by Weston et al. (59) were matched only for performance over 10-km races, rather than for a combination of training, preferred racing distance, and performance. It is possible that the higher LDH activities may have been influenced by habitual, or recent, higher intensities of training in the Xhosa athletes.

The Xhosa athletes did have more type IIA fibers (which in general have higher LDH and PFK activities than type I fibers), and this may therefore partly explain the higher LDH and PFK activities observed in homogenates (21). However, LDH activity was significantly higher in pools of type I and in pools of type IIa fibers of Xhosa athletes compared with Caucasian athletes, indicating that this was not a fiber type-related phenomenon (Fig. 4). Indeed, regression analysis revealed that the proportion of MHC IIa could explain only ~36% of the variation in LDH activity (Fig. 6). This suggests the possibility of a training-induced adaptation, as suggested above, or differences in expression of the five LDH isoforms.

The heart isozymes (LDH1-2, also called LDH-H) are thought to favor conversion of lactate to pyruvate, whereas skeletal muscle isozymes (LDH4-5, also called LDH-M) are thought to favor pyruvate-to-lactate conversion (18). Also, even in cardiac muscle where the LDH-H predominates, there is some evidence of compartmentation of lactate metabolism (15). All five isozymes may be expressed in skeletal muscle in various amounts, and 4 wk of endurance training in previously healthy moderately, recreationally active subjects caused a modest but significant shift in proportional expression toward the isozymes associated with the heart (39) and a concomitant reduction in submaximal plasma lactate accumulation. Kenyan runners exhibited more LDH1-2 isoforms in their gastrocnemius muscle, possibly influencing lower lactate accumulation (47). It has also been suggested that the LDH isozymes may be compartmentalized since LDH is present in both sarcoplasmic and mitochondrial sites (14, 20). An intracellular lactate shuttle has been proposed that allows lactate produced during glycolysis to be shuttled immediately to the mitochondria in the same fiber where it can be converted back to pyruvate and subsequently metabolized (12, 24). Data from some laboratories have questioned that mitochondrial LDH exists (44, 45), but convincing evidence of spatial compartmentalization of LDH in intimate proximity to the mitochondria has been provided recently (28), similar to that seen for monocarboxylate transporter 1 (MCT1) (29).

In the present study, the higher LDH5-4 isoform content and the higher LDH activity in Xhosa athletes were associated with less lactate accumulation in the plasma in these athletes. This observation may be related to the lactate shuttle system suggested by Brooks (13). More research is required to fully understand the role of specifically the LDH5-4 isoforms in skeletal muscle and lactate shuttling. A recent study has suggested that exercise training requiring a higher power output (albeit in their case eccentric resistance training) results in elevation of these particular LDH isoforms’ mRNA, with no changes observed in the heart LDH mRNA (23). It is therefore possible that training intensity is another factor that could explain differences in lactate phenotype between groups.

Recently, it was shown that male Kenyan runners performing training at higher speeds had a significantly higher VO2max and better 10-km performance time than Kenyan athletes training at lower speeds (6). Similarly, another study reported that Xhosa runners did more high-intensity training than their white counterparts (16). Also, after a 12-wk endurance training program, Kenyan boys from a village were able to complete a 5,000-m competitive run in less time than Kenyan town boys (18.5 ± 1.2 vs. 20.3 ± 1.5 min), which might be attributed to the fact that the village boys trained at a significantly higher speed (intensity) than the town boys (13.8 ± 1.6 vs. 12.4 ± 1.5 km/h) (35). Although these studies quantified training intensity, none could relate it to muscle enzyme characteristics.

In summary, South African Xhosa athletes had more type IIA and fewer type I fibers and lower plasma lactate concentrations at a high submaximal exercise intensity than their Caucasian counterparts. Furthermore, Xhosa athletes had no difference in muscle oxidative capacity but had higher LDH activities in homogenate samples and in pools of type I and in pools of type IIa fibers, as well as a different LDH isozyme profile. In conclusion, the skeletal muscle phenotype of Xhosa athletes does differ substantially from their Caucasian counterparts even when the two groups of athletes are very closely matched for racing distance preference, racing ability, and training volume. Whether fiber type and enzymatic differences in skeletal muscle are training intensity dependent remains to be proven.


   GRANTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
ACKNOWLEDGMENTS
 REFERENCES
 
This study was supported by the Harry Crossley Foundation, Swedish Institute Scholarship to Tertius A. Kohn (2000) and a joint venture between the National Research Foundation of South Africa and Swedish International Development Cooperation Agency (2002–2004).


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
REFERENCES
 
We thank the athletes for participation and Dr. Jannie Brink for performing the muscle biopsies. Thanks are extended to Jesper Løvind Andersen (Copenhagen Muscle Research Centre), Kristina Karlström (Swedish Agricultural University), and Karen van Tubbergh (Stellenbosch University) for assistance during the learning of techniques used in muscle analysis. Abrie Eksteen, Robyn Bowen, and Jo-Anne du Toit are thanked for assistance during exercise testing.


   FOOTNOTES
 

Address for reprint requests and other correspondence: K. H. Myburgh, Dept. of Physiological Sciences, Univ. of Stellenbosch, Private Bag X1, Matieland 7602, South Africa (e-mail: khm{at}sun.ac.za)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 

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