The Kenyan runners. Review

Transcription

1 Scand J Med Sci Sports 2015: 25 (Suppl. 4): doi: /sms ª 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Review The Kenyan runners H. B. Larsen 1, A. W. Sheel 2 1 The Copenhagen Muscle Research Centre, Rigshospitalet, Copenhagen, Denmark, 2 School of Kinesiology, University of British Columbia, Vancouver, BC, Canada Corresponding author: Henrik B. Larsen, The Copenhagen Muscle Research Centre, Rigshospitalet, Copenhagen, Denmark. Tel.: , hl@boag.nu Accepted for publication 26 August 2015 Today the Kenyan dominance in middle- and long-distance running is so profound that it has no equivalence to any other sport in the world. Critical physiological factors for performance in running include maximal oxygen consumption (VO 2max ), fractional VO 2max utilization and running economy (energetic cost of running). Kenyan and non-kenyan elite runners seem to be able to reach very high, but similar maximal oxygen uptake levels just as there is some indication that untrained Kenyans and non- Kenyans have a similar VO 2max. In addition, the fractional utilization of VO 2max seems to be very high but similar in Kenyan and European runners. Similarly, no differences in the proportion of slow muscle fibers have been observed when comparing Kenyan elite runners with their Caucasian counterparts. In contrast, the oxygen cost of running at a given running velocity has been found to be lower in Kenyan elite runners relative to other elite runners and there is some indication that this is due to differences in body dimensions. Pulmonary system limitations have been observed in Kenyan runners in the form of exercise-induced arterial hypoxemia, expiratory flow limitation, and high levels of respiratory muscle work. It appears that Kenyan runners do not possess a pulmonary system that confers a physiological advantage. Additional studies on truly elite Kenyan runners are necessary to understand the underlying physiology which permits extraordinary running performances. During the past four decades, African runners or runners of African ancestry have produced some of the most remarkable results in athletic events at world-class level. While the West Africans have excelled in short distance races ( m), the East Africans, especially Kenyans, have excelled in middle-distance ( m) and steeplechase, and also, together with the Ethiopians, in long-distance races (5000 m-marathon). The dominance of Africans has been more and more profound during these four decades. During the same time period, the dominance of European runners has been reduced dramatically. Thus, 38 years ago, all distances from 800 m to marathon were dominated by Europeans (Matthews, 1987). The average proportion of European achievements in the six all-time top 20 lists in the distances from 800 m to marathon including steeplechase was 48.3% while the percentage of African results was 26.6% of which the Kenyans produced 13.3%. Moreover, the majority of world record holders were Europeans, and European gold medal winners at the Olympic games and world championships were not a rarity. Today, the proportion of European achievements is reduced to 4.2%, whereas the percentage of Africans in the top has increased to 91.7%, of which 53.3% are Kenyans (IAAF, All Time Outdoor Lists, June 2015, Fig. 1). The markedly reduced occurrence of Europeans in the list is not due to them necessarily running slower now than earlier. It is simply related to the fact that runners from East Africa in particular now run so much faster (IAAF, 2015; Matthews, 1987). The performances of Kenyan men in middle- and longdistance events at the Olympic games, world championships on track and world cross-country championships underscore the Kenyan superiority. Most of the top Kenyan performers come from a group of eight small tribes called Kalenjin, which number only approximately five million people. Among the Kalenjin tribes, the Nandis have performed the best although they constitute only approximately 2% of the general Kenyan population. The question that arises is why do Kenyan runners perform so extraordinarily well in middle- and long-distance races? This question has inspired considerable interest, speculation and debate among athletes, coaches, exercise physiologists and academics. Those interested in understanding the dominance of these athletes have wondered whether the secret can be found in the socialization experiences and 110

2 Kenyan runners All-time TOP 20 (%) 53.3 Asia Kenya South America Africa excl. Kenya North America Europe Maximal oxygen uptake Performance Fractional utilization Running economy Fig. 2. Main physiological factors critical for distance running performance Fig. 1. Relative distribution (%) between the continents of the all-time top 20 performances in middle- and long-distance running for men in the six major distances from 800 m to marathon incl. steeplechase in June, Black Americans are regarded as Africans excl. Kenyans. lifestyles of Kenyan children (e.g., the effects of running to school as children). Others point to the impacts of living and growing up at high altitude, and/or to the diet of these athletes. While it has been suggested that Kenyans may benefit from biological advantages over groups in other regions of the world we recognize that this is controversial (Hoberman, 2004). Attempting to understand the intersecting spheres of biology, anatomy, physiology, psychology, sociology and how it is they explain possible racial differences in athletic performance is contentious among scholars of different disciplines [for contrasting perspectives see: (Hoberman, 2004) and (Pitsiladis et al., 2004)]. We are cognizant of this controversy and have purposely narrowed the scope of our manuscript to the physiology of Kenyan runners. The study of elite athletes has long been used to better understand human physiology and address questions of O 2 transport, muscle metabolism, cardiorespiratory control and the neural control of muscular contraction. It is generally agreed upon that there are three biological prerequisites for a runner to be successful: high capacity for aerobic energy output (VO 2max ), the ability to use a high fraction of it for long periods and a good running economy (i.e., low energy cost at race pace throughout the race) (Joyner & Coyle, 2008) (Fig. 2). When studying athletic performance and the physiology of running one should consider each of the abovementioned factors. Our brief review is concerned with the available evidence that contrasts Kenyan and non-kenyan runners with respect to VO 2max, fractional utilization of VO 2max and running economy. We also highlight recent findings, which consider the pulmonary system as a potential limitation to exercise performance. Maximal oxygen uptake Since the early work of A. V. Hill (Hill & Lupton, 1923), exercise physiologists have associated the limits of human endurance with the ability to consume oxygen at a high rate. Indeed, it is now well established that there is a high correlation between of VO 2max and running performance in groups of runners of quite different abilities. A high maximal O 2 uptake during exercise represents the ability to integrate the components of transport and utilization: cardiac output, pulmonary gas exchange, hemoglobin, blood flow, muscle O 2 extraction, and the rate of aerobic ATP resynthesis. Elite male athletes typically have a VO 2max between ml/kg/min with women having values approximately 10% lower owing to a lower hemoglobin concentration and higher levels of body fat (Saltin & Astrand, 1967). When groups of athletes with similar athletic performance abilities or athletes with a relatively narrow range of VO 2max are studied VO 2max becomes a less sensitive predictor of performance (Sj odin & Svedenhag, 1985). There have been several investigators that have made direct VO 2max comparisons between Kenyan runners with runners of non-african descent (Saltin et al., 1995b; Prommer et al., 2010; Tam et al., 2012) while others have exclusively studied Kenyan athletes and made comparisons with previously published values (Billat et al., 2003; Foster et al., 2014; Santos-Concejero et al., 2015). Saltin et al. (1995b) revealed that Kenyan elite long-distance runners studied at sea level have a very high VO 2max (79.9 ml/kg/min), but it was not higher than the level observed in Scandinavian elite runners (79.2 ml/kg/min). In addition, another group of 111

3 Larsen & Sheel Kenyan elite runners studied at altitude (2000 m) had similar VO 2max values when compared to Scandinavian elite runners (66.3 vs 67.3 ml/kg/min). Furthermore, three groups of junior runners studied at altitude had VO 2max values of 68.2, 65.5 and 58.7 ml/kg/min, respectively. However, as the entire Kenyan group of elite runners encompassed six Olympic or world champions, several silver and bronze medalists at the world championships, one world record holder and two junior runners who later broke the senior world record the possibility exists that these runners, when top-trained and studied at sea level, have values higher than the mean of 79.9 ml/kg/min. In fact, only two of the very best Kenyan runners (top five in the world in their respective distances) were in the group of runners studied at sea level. In addition, the results of Peter Koech (world record holder at 3000 m steeplechase) studied at altitude and John Ngugi (Olympic champion in 5000 m and five times world champion in crosscountry running) (studied at sea level at submaximal speeds) indicate that these runners would have VO 2max values close to 85 ml/kg/min. Thus, we feel safe to conclude that Kenyan runners performing well in long-distance running on the international arena are characterized by VO 2max values between 80 and 85 ml/kg/min although there are examples of world-class runners like Julius Korir having 77 ml/ kg/min but still winning major races. This is consistent with findings on two former Kenyan world record holders, Kipchoge Kip Keino had a VO 2max of 84.8 ml/kg/min and Henry Rono had 84.3 ml/kg/min (Larsen, 2012). It is of note, that these values are comparable to former non-kenyan world record holder Dave Bedford who had a VO 2max of 85.0 ml/kg/min and Steve Prefontaine who had 84.4 ml/kg/min (Larsen, 2012). It is not mandatory to have a VO 2max above 80 ml/kg/min to be successful. Indeed, a study of Kenyan marathon runners having an average best performance time of 2:07:17 (h:min:s) has shown VO 2max values of 63.1 ml/kg/min when the athletes were studied at altitude (2000 m) in Kenya and 67.5 ml/kg/min when studied in Italy (1300 m) (Tam et al., 2012). In line with this, a study by Prommer et al. (2010) has shown that Kenyan distance runners can run a 10 km in 28:29 (min:sec) with a relatively low mean VO 2max value of 71.5 ml/kg/min. In addition, several studies of black South African elite distance runners have shown that they can perform well without having a very high VO 2max (Bosch et al., 1990; Coetzer et al., 1993; Weston et al., 2000). Moreover, two of these studies demonstrated that Black South African runners with the same race time as White South African runners, have a lower VO 2max than the White runners. Thus, a relatively low VO 2max of Black South African runners seems to be a common feature at a given performance level compared to other runners in the world. A key question is whether untrained Kenyans of Kalenjin ancestry have a high VO 2max at a young age. To answer this question untrained adolescent Nandi town boys were studied (Saltin et al., 1995b; Larsen et al., 2005). When studied at an altitude of ~2000 m, Kenyan boys had VO 2max values, which were in the same range as untrained Caucasian teenagers studied at sea level (Andersen et al., 1987). It can be argued that the maximal oxygen uptake of the Kenyan boys would be higher if they were tested at sea level. For example, VO 2max is approximately 10% reduced when tested at 2000 m (Squires & Buskirk, 1982). However, it appears that high-altitude natives do not gain much in VO 2max when tested at sea level (Favier et al., 1995). Although there may be a small difference, one also has to consider that the body mass of the Nandi boys was only ~54 kg, which is ~12 kg less than that of Caucasian boys of the same age. If VO 2max is normalized for differences in body mass with the exponent of 0.75, the Kenyan boys will actually have a lower VO 2max than the Caucasian boys. The fact that no difference was observed with respect to VO 2max between untrained Kenyan and Danish boys is in line with findings of others (Boulay et al., 1988). Fractional utilization of VO 2max The ability to sustain a high percentage of VO 2max during competition has long been identified as a predictor of endurance performance. Is the success of Kenyan runners explained by a high fractional utilization of VO 2max? The answer to this question is difficult as the number of data points in the literature are few. It was shown in one runner, Kip Keino, that he utilized his whole VO 2max when running 5000 m and above 97 98% of VO 2max in a 10-km race (Karlsson et al., 1968). This original observation is consistent with more recent findings where Kenyan runners are able to sustain 93 96% of the velocity associated with VO 2max at m speed during treadmill running (Billat et al., 2003). Moreover, in the above-mentioned study by Tam et al. (2012) the fractional utilization of VO 2max were calculated and compared with European athletes of almost the same performance level (2:08:24 in the marathon). This study indicated that the fractional utilization of VO 2max sustained during the marathon was extremely high but similar in the Kenyan and European runners. Finally, when the average heart rate during a 5000 m competition was recorded in Nandi town and village boys they utilized 97.3% of their maximal heart rate (Larsen et al., 2005). Here, we present a summary of published values in Kenyan runners that 112

4 Kenyan runners are physiological indices of a high fractional utilization of VO 2max. Muscle fiber type The majority of factors that may explain superiority in exercising at a high fractional utilization of VO 2max are related to the features of the muscles involved in the action of running. There is a moderate-to-strong relationship between distance running performance and the proportion of type I muscle fibers (Costill et al., 1973; Sj odin & Svedenhag, 1985) which also appears to be the case in well-trained cyclists (Coyle et al., 1988). It has been suggested that the percentage of type I muscle fibers may be an indicator of the potential trainability of the musculature (Sj odin et al., 1982). However, extreme endurance training has been demonstrated to induce a similarly high mitochondrial oxidative capacity of type I and type II muscle fibers, in line with the fact that the contractile characteristics of a fiber and transformation of the main fiber types are not so easily affected by training, whereas the metabolic capacity is; also in the type II fibers (Jansson & Kaijser, 1977). Both Kenyan and Scandinavian elite runners have a high proportion of type I muscle fibers (Saltin et al., 1995a). Kenyan junior runners have a proportion of type I muscle fibers that is high and not much different from Kenyan elite runners (~70% type I fibers). South African distance runners appear to differ from Kenyan runners, having less type I fibers (Coetzer et al., 1993). In sum, there is contradictory evidence to suggest that Kenyan elite distance runners may have a higher proportion of type I muscle fibers relative to other runners. These conflicting results are difficult to resolve and we emphasize that the number of muscle biopsies obtained from Kenyan runners to date have been remarkably few and additional study is required. Leg muscle oxidative enzymes Muscle mitochondrial enzyme capacity is linked with the substrate metabolism during exercise. The more mitochondria, the larger the muscle lipid consumption during exercise and in turn, the level of blood lactate at a given work rate is lower, the higher the activity of the oxidative enzymes (Ivy et al., 1980). Thus, a direct link exists to the oxidative potential of the muscles engaged in running and the performance level, as a running speed has to be high before blood lactate starts to become elevated (Sj odin & Jacobs, 1981). There is a positive correlation between the activity of three oxidative enzymes, citrate synthase (CS), succinate dehydrogenase, and glycerol-3 phosphate dehydrogenase, and performance in running. When comparing the CS activity of Kenyan and Scandinavian elite runners, no differences were found regardless of whether the comparisons were made between the vastus lateralis or the gastrocnemius muscle in the two groups of runners (Saltin et al., 1995a). Capillaries Capillarization is one of the key factors determining the oxidative profile of the musculature and it is closely related to VO 2max. Capillary density has also been shown to correlate positively with the running velocity at which blood lactate begins to accumulate (Sj odin & Jacobs, 1981). A moderate correlation is found between muscle capillarity and the mean marathon running velocity during competition (Sj odin & Jacobs, 1981). When comparing the capillarization of Kenyan vs Scandinavian elite runners there appears to be only a tendency for a higher capillarization of the Kenyan elite runners (Saltin et al., 1995a). Plasma lactate and ammonia responses The blood lactate response to submaximal running is a good predictor of endurance running performance and primarily reflects the local metabolic response in the running muscles. Kenyan elite runners have lower blood lactate levels, both at altitude and at sea level, when running at a given exercise intensity compared to other elite runners. The difference is most pronounced at high exercise intensities. With the accumulation of lactate in the blood the ammonia concentration usually also increases. This is also true for Kenyan elite runners but only at very high exercise intensities and then to a lower extent than other elite runners (Saltin et al., 1995a). In addition, the peak ammonia concentration following a maximal test was only half to one third in the Kenyan runners as compared to other elite runners. Following a period of endurance running, the blood ammonia level was reduced in Kenyan town and village boys (Larsen et al., 2005). These blood ammonia data warrant further exploration, as they may explain some metabolic regulations in the muscles of Nandi runners, in turn affecting critical fatiguing factors, either peripherally in the muscle or at a more central level. Running economy Running economy is expressed as the steady state submaximal oxygen uptake at a given running velocity. The lower the VO 2 at a given submaximal running speed, the better the running economy. Studies from the 1930s were the first to suggest differences in the amount of oxygen that different athletes require 113

5 Larsen & Sheel when running at the same speed (Dill et al., 1930) and the submaximal oxygen requirement (ml/kg/ min) has been shown to vary considerably between subjects (Svedenhag & Sj odin, 1984). The oxygen cost of running at a given running velocity normalized for differences in body mass has been found to be lower in Kenyan elite runners relative to other elite runners (Saltin et al., 1995b). In addition, when comparing some of the most efficient Kenyan runners (Julius Korir and John Ngugi) without normalizing for differences in body mass these runners are still superior compared to top-swedish runners (Saltin et al., 1995b). In fact, their running economy is very comparable with the one found in two of the most efficient Caucasian runners (Derek Clayton and Frank Shorter) ever measured (Pollock, 1977). Furthermore, their data are in line with or slightly better compared to the best ever economy curves (Joyner, 1991). Other researchers have found no association between running economy and running performance in Kenyan runners which was interpreted to mean that running economy is compensated for by other factors to afford distance running success (Mooses et al., 2015). It should be noted that others have critiqued this work [see (Santos-Concejero & Tucker, 2014)] and suggested that the importance of running economy in Kenyan runners cannot necessarily be downplayed. Classical studies of human locomotion (Cavagna et al., 1964) show that the work of moving the limbs comprises a substantial part of the metabolic cost of running, just as load-carrying experiments have shown that adding a few grams of mass on the feet/ ankle evokes an increase in the metabolic rate (Myers & Steudel, 1985). Some have speculated that successful Kenyan runners are characterized as having slender limbs with low masses allowing them to run with a minimal energy used for swinging the limbs. Evidence to support this postulate comes from studies which show that elite Kenyan runners had longer legs (approximately 5%) relative to Scandinavian runners and they had thinner and lighter calf musculature and that Kenyan boys have a low body mass and a very low BMI relative to boys of similar age from other continents (Saltin et al., 1995b; Larsen et al., 2004). If slimness and low body mass indeed is important prerequisites for becoming a world elite runner it is probably easier to produce this kind of athletes in Kenya than most other places in the world due to a much higher prevalence of people having this body shape in Kenya. With respect to body dimensions the study by Tam et al. (2012) raises several important points. The Kenyan and European marathon runners who had a comparable running economy also had similar body dimensions (height, weight, and BMI). In contrast, the study by Saltin et al. (1995b) demonstrated that the Scandinavian elite runners having inferior running economy compared to Kenyan elite runners were taller, heavier and had a higher BMI compared to the Kenyans. This lends support to the hypothesis that body dimensions are crucial for running economy. Tam et al. (2012) also noted that Kenyan and European runners who performed equally well in the marathon achieved the results with a very similar combination of VO 2max, fractional utilization of VO 2max and running economy. Pulmonary system limitations to exercise It is commonly held that the structural capacity of the normal lung is over-built and exceeds the demand for pulmonary gas transport in the healthy, exercising human (Dempsey, 1986). However, the adaptability of the pulmonary system structures to habitual physical training is substantially less than other links in the O 2 transport system (Dempsey & Wagner, 1999). Accordingly, in some highly fit individuals the lung s diffusion surface, airways, and/or chest-wall musculature are underbuilt relative to the demand for maximal O 2 transport (Dempsey, 1986). Two specific pulmonary limitations to exercise performance in the highly trained have been reported: (a) exercise-induced arterial hypoxemia (EIAH) secondary to excessive widening of the alveolar-to-arterial O 2 difference, inadequate hyperventilation and metabolic acidosis; and (b) highly fatiguing levels of respiratory muscle work which effectively steals blood flow from locomotor muscles via a sympathetically mediated reflexes and heightens perceptions of limb and respiratory discomfort. While these limitation have been shown by several research groups to occur in highly trained athletes, it is unknown if Kenyan runners experience these pulmonary limitations during exercise. Here, we briefly summarize the available data, which speaks to pulmonary system limitations in Kenyan runners. Exercise-induced arterial hypoxemia Arterial O 2 desaturation of 3 15% below resting levels has been observed to occur at or near maximum exercise intensities. EIAH has been reported in highly trained young males, as sedentary males do not experience EIAH. Of note is that the relationship between VO 2max and the severity of EIAH is modest. We emphasize that the true prevalence of EIAH and susceptibility remains unresolved. EIAH is usually viewed as occurring only in very heavy or maximum exercise, it is underappreciated that many of those experiencing EIAH begin to show decrements of PaO 2 even in submaximal exercise. PaO 2 is reduced below resting levels due to a widened alveolar-to- 114

6 Kenyan runners arterial difference in O 2 (AaDO 2 ) and/or insufficient increase in alveolar PO 2. HbO 2 desaturation is further exaggerated by a rightward shift of the dissociation curve due to metabolic acidosis and increased temperature. The precise cause(s) of EIAH have not been fully identified exercise-induced ventilation/perfusion inequality most likely contributes to a widened AaDO 2. During heavy exercise a diffusion limitation and perhaps even stress-failure of the alveolar-capillary interface remains plausible, but evidence for their existence is indirect in exercising humans. From an athletic performance perspective, it has now been well established that naturally occurring reductions in arterial oxygenation have a significant effect on exercise performance. Foster et al. (2014) observed significant gas exchange impairments in Kenyan runners that would be of sufficient magnitude to compromise O 2 delivery. Young Kenyan runners (10M, 4F; 25 years) were instrumented with a radial artery catheter and esophageal temperature probe for determination of blood gases and core temperature. Participants competed in national and international running events with a range of racing accomplishments. Several subjects had principally competed at local, modest high altitude ( m) in Kenya. One female participant was former medalist at the Jr. World Cross- Country Running Championships, while two male participants competed internationally at major marathons. Subjects performed incremental treadmill running to exhaustion at 1545 m, which corresponds to an FIO 2 of approximately at sea level. Significant decreases in the PaO 2 and oxyhemoglobin saturation (SaO 2 ) and a widening of the alveolar-to-arterial difference in O 2 from rest to peak exercise were observed (Fig. 3). At maximal exercise, the reduced SaO 2 was caused by a combination of reduced PaO 2 (~60%) along with acid shifts (~40%) in arterial blood and increases in core temperature. We emphasize that there were notable between-subject differences in gas exchange during submaximal exercise where several subjects had reductions in PaO 2 during the initial treadmill stage, whereas others maintained PaO 2 values close to resting levels until near-maximal exercise intensity. Humans who are native to high altitude (at least 3 generations) appear to exhibit an enhanced lung structure and function relative to their lowland counterparts where pulmonary gas diffusion during exercise appears enhanced (Dempsey et al., 1971). Moreover, it has been consistently shown that moderate high-altitude exposure accelerates developmental growth of the mammalian lung. However, to date it is unknown if these purported altitude-induced lung enhancements are present in elite Kenyan runners of high-altitude ancestry. High levels of respiratory muscle work The ventilation associated with heavy exercise causes significant increases in the total work of breathing including inspiratory and expiratory muscle work as well as the resistive and elastic work of breathing. The elastic work of inspiration is particularly high if expiratory flow limitation occurs and the subject is made to breathe in a relatively hyperinflated state. The metabolic and circulatory costs of the hyperventilation of heavy exercise are substantial and have (a) (b) (c) Fig. 3. Arterial blood gas and gas exchange values in Kenyan runners at rest and incremental percentages of maximal workload. (a) PAO 2, alveolar partial pressure for oxygen and PaO 2, arterial partial pressure for oxygen. (b) SaO 2, arterial oxygen saturation. Values for SaO 2 were determined in three ways; (1) direct measure from blood gas analyzer (closed circles); (2) calculated based on current PaO 2 applied to an ideal dissociation curve (ph = 7.40, temperature = 37 C, PaCO 2 = 40 mmhg) (open triangles); and (3) individual resting PaO 2 applied to a curve shifted due to current ph, temperature and PaCO 2 (open diamonds); (c) A-aDO 2, alveolar-to-arterial difference in oxygen and PaCO 2, arterial partial pressure for carbon dioxide. *Significantly different from rest (P < 0.05). From Foster et al. (2014). 115

7 Larsen & Sheel been estimated to represent 10% of the VO 2max in the untrained and upwards of 15 16% of VO 2max and of maximum cardiac output in highly trained males (Sheel & Romer, 2012). Highly trained subjects are capable of achieving very minute ventilations but the maximum flow-volume envelope is unchanged from that of the untrained subjects. As such, the expiratory flow during normally occurring tidal breathing intersects with the maximum flowvolume envelope. End-expiratory lung volume subsequently forced upward in order to increase flow rate further. However, this increase in flow is accomplished at the expense of lung hyperinflation and high work of breathing. It is now known that the high work of breathing during sustained exercise >85% maximum results in diaphragmatic fatigue. Exercise performance can be affected, whereby the fatigued respiratory muscles trigger a metaboreflex from, which in turn causes a decrease in O 2 transport to locomotor muscles in response to a fatigue-induced increase in sympathetic vasoconstrictor outflow. Foster et al. (2014) found that during maximal treadmill exercise most male and female Kenyan runners demonstrated significant flow limitation where the tidal breath intersected with the expiratory side of the maximum flow-volume curve or impending flow limitation where their tidal flow-volume loop approached the maximal curve and developed its characteristic shape, but did not fully intersect. Subjects were instrumented with an esophageal balloontipped catheter for the determination of the work of breathing. Throughout exercise there was a progressive and curvilinear increase in the work of breathing which was commensurate with values seen in non- Kenyan athletes. It is unknown if the diaphragm of maximally exercising Kenyan runners fatigues. However, many of the predisposing factors for fatigue of the diaphragm appear present including: expiratory flow limitation, a high work of breathing and significant metabolic acidosis. Furthermore, Kenyan runners appear to demonstrate expiratory flow limitation and high levels of respiratory muscle work that are consistent with observations other aerobically trained athletes. The flow limitation observed was of sufficient magnitude to restrain the increase in ventilation during exercise. These findings suggest that pulmonary system limitations are present in runners of Kenyan ancestry. Based on the available evidence, it appears that Kenyan runners do not possess a pulmonary system that confers a physiological advantage. Perspectives Different geographical regions including Finland, Australia and New Zealand have dominated international running races over the last 100 years. Runners from East Africa, and in particular Kenya, currently dominate international competition. As argued by Joyner and Coyle (2008) this geographical diversity argues against a simple genetically-based set of answers to the complex problem of elite endurance performance. On the other hand, the above-mentioned countries have far from been as dominant as the African countries are today. Until the legendary Kipchoge Keino made his breakthrough in 1965, the Kenyans did not run for competition. Keino did not only show the world that Kenyans could run but he also showed the Kenyans that they could run. When studying the Kenyan phenomenon in middle- and long-distance running there is no doubt that the interactions between biology, motivational and sociological factors must be considered. Much of what we know about Kenyan runners, from a physiological perspective, is based upon a limited number of studies with small sample sizes and difficulties in study-design. The pertinent question is; what is the appropriate control group? In order to compare Kenyan runners born/raised at modestly high altitude the comparative group must be fully acclimatized across physiological systems (e.g., ventilatory, hematological, metabolic and cardiovascular). We stress that when it comes to conclusions between Kenyan and non-kenyan runners it must be considered that most studies may not have made the desired comparison. For example, comparing top-level European marathon runners with Kenyans with an equivalent marathon time (e.g., 2:08:00) is difficult as the Kenyan runners cannot be characterized as toplevel. The mean performance time in the two groups of runners corresponds to number 16 in the all-time best performance list of European marathon runners (IAAF, June, 2015) but to number 162 among Kenyan marathon runners. Future studies need to consider the above factors when attempting to understand the current success of Kenyan runners. Key words: Elite runner, oxygen consumption, pulmonary system, running economy. Acknowledgements Twenty-five years ago, Bengt Saltin initiated the studies in Kenya of the physiology of Kenyan runners. Being a very strong runner himself, the physiology of running had for many years been one of his main interests. Therefore, after first the Ethiopians and as the Kenyans had shown a still increasing dominance in middle- and long-distance running, Bengt Saltin had a strong desire to study the underlying physiological reasons for this. As he said: If you are interested in running of course you would like to know why the Kenyan runners are the best. There is only one way to find out and that is to go there and study them. Therefore, he took the initiative and established a small laboratory in Kenya in the area from where the most 116

8 Kenyan runners successful runners originates. Since then studies from different research groups have been going on in Kenya. Without his great enthusiasm and scientific curiosity these studies would never have been possible. We have been fortunate to be a part of these studies and we are very grateful to Bengt Saltin. References Andersen LB, Henckel P, Saltin B. Maximal oxygen uptake in Danish adolescents years of age. Eur J Appl Physiol 1987: 56: Billat V, Lepretre PM, Heugas AM, Laurence MH, Salim D, Koralsztein JP. Training and bioenergetic characteristics in elite male and female Kenyan runners. Med Sci Sports Exerc 2003: 35: Bosch AN, Goslin BR, Noakes TD, Dennis SC. Physiological differences between black and white runners during a treadmill marathon. Eur J Appl Physiol 1990: 61: Boulay MR, Ama PF, Bouchard C. Racial variation in work capacities and powers. Can J Sport Sci 1988: 13: Cavagna GA, Saibene FP, Margaria R. Mechanical work in running. J Appl Physiol 1964: 19: Coetzer P, Noakes TD, Sanders B, Lambert MI, Bosch AN, Wiggins T, Dennis SC. Superior fatigue resistance of elite black South African distance runners. J Appl Physiol 1993: 75: Costill DL, Thomason H, Roberts E. Fractional utilization of the aerobic capacity during distance running. Med Sci Sports 1973: 5: Coyle EF, Coggan AR, Hopper MK, Walters TJ. Determinants of endurance in well-trained cyclists. J Appl Physiol 1988: 64: Dempsey JA. J.B. Wolffe memorial lecture. Is the lung built for exercise? Med Sci Sports Exerc 1986: 18: Dempsey JA, Reddan WG, Birnbaum ML, Forster HV, Thoden JS, Grover RF, Rankin J. Effects of acute through life-long hypoxic exposure on exercise pulmonary gas exchange. Respir Physiol 1971: 13: Dempsey JA, Wagner PD. Exerciseinduced arterial hypoxemia. J Appl Physiol 1999: 87: Dill DB, Talbott JH, Edwards HT. Studies in muscular activity: VI. Response of several individuals to a fixed task. J Physiol 1930: 69: Favier R, Spielvogel H, Desplanches D, Ferretti G, Kayser B, Hoppeler H. Maximal exercise performance in chronic hypoxia and acute normoxia in high-altitude natives. J Appl Physiol 1995: 78: Foster GE, Koehle MS, Dominelli PB, Mwangi FM, Onywera VO, Boit MK, Tremblay JC, Boit C, Sheel AW. Pulmonary mechanics and gas exchange during exercise in Kenyan distance runners. Med Sci Sports Exerc 2014: 46: Hill AV, Lupton H. Muscular exercise, lactic acid, and the supply and utilization of oxygen. Quart J Med 1923: 16: Hoberman J. African atheltic aptitude and the social sciences. Equine Comp Exerc Physiol 2004: 1: Ivy JL, Withers RT, Van Handel PJ, Elger DH, Costill DL. Muscle respiratory capacity and fiber type as determinants of the lactate threshold. J Appl Physiol 1980: 48: Jansson E, Kaijser L. Muscle adaptation to extreme endurance training in man. Acta Physiol Scand 1977: 100: Joyner MJ. Modelling: optimal marathon performance on the basis of physiological factors. J Appl Physiol 1991: 70: Joyner MJ, Coyle EF. Endurance exercise performance: the physiology of champions. J Physiol 2008: 586: Karlsson J, Hermansen L, Agnevik G, Saltin B. Running (in Swedish). Stockholm, Sweden: Framtiden, Larsen HB. Dominance of Kenyan Kalenjins in middle- and longdistance running. East African Running: toward a cross-disciplinary perspective. Routledge, 2012: 1(38): Larsen HB, Christensen DL, Nolan T, Sondergaard H. Body dimensions, exercise capacity and physical activity level of adolescent Nandi boys in western Kenya. Ann Hum Biol 2004: 31: Larsen HB, Nolan T, Borch C, Sondergaard H. Training response of adolescent Kenyan town and village boys to endurance running. Scand J Med Sci Sports 2005: 15: Matthews P. World and Continental Records. Athletics 87 International Track and Field Annual. London: London and International Publishers Ltd., 1987: Mooses M, Mooses K, Haile DW, Durussel J, Kaasik P, Pitsiladis YP. Dissociation between running economy and running performance in elite Kenyan distance runners. J Sports Sci 2015: 33: Myers MJ, Steudel K. Effect of limb mass and its distribution on the energetic cost of running. J Exp Biol 1985: 116: Pitsiladis YP, Onywera VO, Geogiades E, O Connell W, Boit MK. The dominance of Kenyans in distance running. Equine Comp Exerc Physiol 2004: 1: Pollock ML. Submaximal and maximal working capacity of elite distance runners. Part I: cardiorespiratory aspects. Ann N Y Acad Sci 1977: 301: Prommer N, Thoma S, Quecke L, Gutekunst T, Volzke C, Wachsmuth N, Niess AM, Schmidt W. Total hemoglobin mass and blood volume of elite Kenyan runners. Med Sci Sports Excerc 2010: 42: Saltin B, Astrand PO. Maximal oxygen uptake in athletes. J Appl Physiol 1967: 23: Saltin B, Kim CK, Terrados N, Larsen H, Svedenhag J, Rolf CJ. Morphology, enzyme activities and buffer capacity in leg muscles of Kenyan and Scandinavian runners. Scand J Med Sci Sports 1995a: 5: Saltin B, Larsen H, Terrados N, Bangsbo J, Bak T, Kim CK, Svedenhag J, Rolf CJ. Aerobic exercise capacity at sea level and at altitude in Kenyan boys, junior and senior runners compared with Scandinavian runners. Scand J Med Sci Sports 1995b: 5: Santos-Concejero J, Billaut F, Grobler L, Olivan J, Noakes TD, Tucker R. Maintained cerebral oxygenation during maximal self-paced exercise in elite Kenyan runners. J Appl Physiol 2015: 118: Santos-Concejero J, Tucker R. Comment on Dissociation between running economy and running performance in elite Kenyan distance runners. J Sports Sci 2014: In press: 1 3. Sheel AW, Romer LM. Ventilation and respiratory mechanics. Compr Physiol 2012: 2: Sj odin B, Jacobs I. Onset of blood lactate accumulation and marathon running performance. Int J Sports Med 1981: 2:

9 Larsen & Sheel Sj odin B, Jacobs I, Svedenhag J. Changes in onset of blood lactate accumulation (OBLA) and muscle enzymes after training at OBLA. Eur J Appl Physiol 1982: 49: Sj odin B, Svedenhag J. Applied physiology of marathon running. Sports Med 1985: 2: Squires RW, Buskirk ER. Aerobic capacity during exposure to simulated altitude, 914 to 2286 meters. Med Sci Sports Exerc 1982: 14: Svedenhag J, Sj odin B. Maximal and submaximal oxygen uptakes and blood lactate levels in elite male middle- and long-distance runners. Int J Sports Med 1984: 5: Tam E, Rossi H, Moia C, Berardelli C, Rosa G, Capelli C, Ferretti G. Energetics of running in top-level marathon runners from Kenya. Eur J Appl Physiol 2012: 112: Weston AR, Mbambo Z, Myburgh KH. Running economy of African and Caucasian distance runners. Med Sci Sports Exerc 2000: 32: