10 October 2014

Blisters in mountain ultramarathon running

This is my 100th post at this blog. I am fairly happy with my choice of subjects for my posts so far and I have personally learnt tremendously when writing them and hope this will have benefited my running at least to some positive extent. If the posts on these subjects also have benefited other runners I am even more happy. There are however some subjects I still have not written about that constantly come to my mind when I think about what to write about next. The effects on ultrarunning on the heart, a very controversial subject, is definitively one. It is however a rather complicated subject, to put it mildly, and even though I have collected most scientific articles on the subject I have simply not had time to dig into them and write a short summary of these numerous studies and divergent findings and opinions.

Another subject I have thought long to write about is the most common problem all mountain ultramarathon runners are facing when racing – blisters. If you wonder why it is so common just look at this picture from somewhere in the Italian Alps during Petite Trotte à Léon (PTL) earlier this year – while a talus field is really beautiful for the eyes it is the darkest nightmare for your feet, at least when descending.
 
Talus fields - the worst nightmare for your feet at least when descending
It is not the amount of data that has made me hesitate to write about blisters as almost every runner writes about it and has an opinion, but rather the lack of good scientific studies on the subject.  I was therefore very happy when I came across a new scientific study about blister formation in mountain ultramarathon racing by Scheer and colleagues (Scheer et al “The enemy of the feet: blisters in ultraendurance runners” J Am Podiatr Med Assoc 2014; 104: 473). In this study, blister frequency, localization, severity and preventive measures of 50 runners of the 2010 and 2011 Al Andalus Ultra Trail, a 5-day 219 km multistage trail during the summer in high temperatures in southern Spain, were investigated.  Quite interesting, the blister formation occurred almost linearly over the first three days, with 34% having blisters after Day 1, 54% after Day 2 and 72% after Day 3. After 4 days of racing (182 km) 76% of the runners had blisters (see figure below).
 

Most of the blisters formed on the toes (65%), followed by blisters at the ball of the foot (16%), heel (14%) and sole (5%). Blisters were more painful towards the end of the race, and those of the sole and heel tended to be the most painful (although not statistically significant). Most interesting, the prophylactic measures studied (type and fabric of socks; application of antiperspirants, talcum powder, or lubricant to feet; and prophylactic taping) did not show any reduction in blister rates. The only predictive marker for reduced blister incidence was previous ultramarathon experience in men (r = -0.44, P < 0.05). I think these findings agree well with my experiences from Tor des Geants (TDG) and Petite Trotte à Léon (PTL) were my feet withstood the stress for approximately 80 hours before severe blister formation in TDG last year and around 100 hours before blister formation in PTL this year. The study also reinforces my belief that you have to find a solution to prevent blisters that works for you personally and that this solution might be different for each runner and even for each race depending on the conditions.

Looking at what others have written about blisters there exists barely an ultrarunning running blog without something about it. A really good post is by Andy Cole in his blog “Running Late” from last year entitled “Bad News and Blisters” and I can definitively recommend it. If you really want to dig into the subject “Fixing your feet. Injury prevention and treatments for athletes ”, now in its 5th edition, by John Vonhof is the reference book. It is very much written with endurance runners in mind.
 
In the scientific literature a lot has been written about friction blisters and sock fiber composition for instance, but no good prospective randomized controlled trials have been conducted to my knowledge of different types of socks, or any other intervention for that matter, in ultramarathon runners. Other studies also confirm the findings by Scheer and colleagues that blister formation is very common as they appear to represent 17-40% of injuries at continuous ultramarathons and 33-74% of injuries during multistage ultramarathons (for review see Hoffman et al “Medical services at ultra-endurance foot races in remote environments: Medical issues and consensus guidelines” Sports Med 2014; 44: 1055-1069).

08 October 2014

Lung function and respiratory muscle training in ultramarathon running

Fall has arrived here in Uppsala and the brightly colored trees and piles of leaves under makes my daily commute runs to and from work an absolute treat. The nights are cold with freezing temperatures, but the days have been unusually warm.

Fyrisån in Uppsala an early fall morning in the end of September
I am finally free from the lingering weakness and repeated respiratory infections I had after Petite Trotte à Léon (PTL) and can run slowly to work without arriving completely exhausted and out of breath. During the past month since the race I have really noticed that it was not only my legs and feet that suffered, but to a great extent also the rest of my body and perhaps in particular my respiratory system. It was likely influenced by the fact that I developed a rather severe respiratory infection already during the race, but as I do not think that could explain everything I started to look at how mountain ultramarathon running affected the lung function and respiratory muscles. The following overview is regretfully rather technical, as lung physiology is, at least for me, rather complicated, but I have tried to simplify the findings in the studies done so far.

Incidentally, there were in the past months two scientific studies published looking at changes in lung function during mountain ultramarathons. The first article is published by Vernillo and co-workers and is another study of runners completing Tor des Géants (TDG) 330-km long mountain ultramarathon with 24000 meter D+ in the Aosta Valley in Italy (Vernillo et al “Changes in lung function during an extreme mountain ultramarathon” Scand J Med Sci Sports 2014; Epub ahead of print).  In this study of 23 male finishers of TDG with a mean age of 46.0 ± 8.0 years and an average finish time of 124 hours 19 minutes and 2 seconds the lung (pulmonary) function was analyzed by a variety of volitional (voluntary) measurements using so called spirometer. A clear significant decline in the overall lung function was observed and the authors attribute this to the high levels of ventilation required in a harsh mountainous environment. The respiratory muscle endurance, as assessed by the maximal voluntary ventilation during 12 seconds (MVV12), declined by 11.8% during the race and very interestingly there was a correlation between the MVV12 values before the race and finish time. This is similar to the findings by Blaber and colleagues of a correlation between prerace MVV10-30 values and 100-km race times in eight Canadian elite runners (Blaber et al “Cardiopulmonary physiology and responses of ultramarathon athletes to prolonged exercise” Can J Appl Physiol 2004; 29: 544-63). Also very interestingly, the inspiratory lung function appeared to decrease to a larger extent than the expiratory (see table below). The authors conclude with the speculation that, as the changes in lung function might be a possible limiting factor for the race performance, specific respiratory muscle training might be beneficial to improve mountain ultramarathon performance.

The second article is published by Wütrich and colleagues and is a study of 23 runners completing Ultra Trail du Mont Blanc (UTMB) in 2012, which was shortened to 110 km and 5862 meters D+ due to severe weather conditions (Wütrich et al “Aspects of respiratory muscle fatigue in a mountain ultramarathon” Med Sci Sport Exerc 2014; Epub ahead of print).  The runners were 42.9 ± 9.4 years and completed the race in an average time of 20.1 ± 3.4 hours. In this study, the focus was more on the respiratory muscle strength and fatigue rather than only lung function and voluntary maximal inspiratory pressure (MIP) and maximal expiratory pressure (MEP) were measured with a mouth pressure meter. Non-volitional inspiratory muscle strength was measured with mouth twitch pressure (Pm,tw) in response to cervical magnetic stimulation. Interestingly, the runners developed significant respiratory muscle fatigue in both expiratory (MEP -21%) and inspiratory muscles (-19%) together with a reduction in all flow mediated lung function parameters. Peripheral inspiratory muscle fatigue contributed significantly to the decrease in volitional inspiratory muscle strength as shown by a reduction in Pm,tw (-19%), while central voluntary muscle activation only decreased by -3%. The later finding is surprising and in contrast to previous findings of an important central component of fatigue in leg locomotor muscles following mountain ultramarathons (Millet et al 2011; Temesi et al 2014). One of the speculative conclusions the authors make of their findings in this study is that the combination of respiratory and leg muscle fatigue both might contribute to changes in the postural control and thus an elevated risk of fall and injuries in these events when running on challenging undergrounds.

In addition to these two recent studies by Vernillo et al and Wütrich et al, three older studies have been published about the effect of ultramarathon races on lung function (see table below). All of these studies have shown a rather large decrease in the lung function following long endurance running.


Study
Distance
(km)
Subj
Expiratory tests
Inspiratory tests
Resp end
 
 
 
FVC
FEV1
PEF
MEP
PIF
IC
MIP
MVV12
Vernillo
2014
330
(MUM)
23
- 9.5%
 -9.7%
-8.7%
-
-16.8%
-20.7%
 
-11.8%
Wüthrich
2014
110
(MUM
22
-1.8%
-7.3%
-13.8%
-21%
-16.8%
 
-19%
-16.8%
Ker
1996
87
(UM)
10
-
-
-
-
No difference in MIP, but a reduction of -26.5%
 in Tlim endurance time 3-d post race
Warren
1989
100 – 214 (24-h UM)
10
-6.5 %
-3.0%
-11.0%
-22.3%
-
ND
-7.2%
 -17.0%
Mahler
1981
80.6 or 100 (UM)
15
- 12.4%
-9.5%
-13.7%
-
-
-
-
-


An indirect sign of the effects of ultramarathon running on the lungs is that changes in lung blood flow appears to also lead to changes in the right ventricle (RV) of the heart which support the lungs with blood. This is a rather new observation, as traditionally the running effects of the heart appeared to be more located to the left ventricle (LV).  For instance a study by Oxborough and colleagues of 16 runners of the 100 mile (161 km) Western States Endurance Run (WSER) in 2009 with advanced cardiac imaging with both conventional two-dimensional and speckle tracking echocardiography showed clear RV dilatation and reduction in function (Oxborough et al “Dilatation and dysfunction of the right ventricle immediately after ultraendurance exercise” Circ Cardiovasc Imaging 2011; 4: 253-263). The authors speculate that the changes might be due to pulmonary hypertension. Another study by Dávila-Roman and colleagues of 14 runners of the 100 mile (163 km) Hardrock 100 mountain ultramarathon race at high altitude (2350 – 4300 meters) in 1994 showed that 5/14 (36%) developed wheezing, pulmonary hypertension and marked RV dilatation and dysfunction (Dávila-Roman et al “Transient right but not left ventricular dysfunction after strenuous exercise at high altitude” J Am Coll Cardiol 1997; 30: 468-473). These two studies exemplify that the effects on the lungs during a mountain ultramarathon probably also lead to acute changes in heart function. However, further studies are clearly needed to verify this and to study the exact mechanisms behind this.

A higher pressure in the pulmonary arteries could also contribute to accumulation of water in the lungs, so called pulmonary edema. There are other mechanisms that also could lead to this, for instance the diffusion capacity between the air and blood in the lungs. Already in 1978 in the Comrades 90-km ultramarathon in South Africa two highly trained runners were observed developing acute pulmonary edema (McKechnie et al “Actue pulmonary oedema in two athletes during a 90-km running race” South Africa Med J 1979; 56: 261-265) and recently it has been shown in studies of marathon runners that around 20-50% develop mild to severe interstitial lung edema during a race (Zavorsky et al “Interstitial lung edema triggered by marathon running”  Respir Physiol Neurobiol 2014; 190: 137-141 and Zavorsky et al “Small changes in lung function in runners with marathon-induced lung edema” Physiol Rep 2014; 2: e12056). However, in most cases these changes appear to not be correlated to a decrease in lung function and not associated with exercise induced arterial hypoxemia (EIAH) so perhaps not leading to limiting endurance performance as respiratory muscle fatigue and exercise-induced asthma (EIA) and exercise-induced bronconstriction (EIB) (the later not discussed in this overview as it is not specific to ultramarathon running). However, speculations about the mechanisms behind how the respiratory function limit endurance performance has led to a debate whether the lungs can be defined as “overbuilt” or “underbuilt” for facing strenuous exercise and much indicates, paradoxically, that the fitter someone is, the more likely he or she is to experience respiratory limitations (reviewed in Demsey “Is the healthy respiratory system (always) built for exercise?” J Physiol 2006; 567: 339-340 and Bussotti et al “Respiratory disorders in endurance athletes – how much do they really have to endure” Open Acc J Sport Med 2014; 5: 47-63).

If inspiratory respiratory muscle fatigue indeed is a major limiting factor in ultramarathon performance the natural question is whether it is possible to train these muscles and how this could be done. Regretfully, almost no studies have been done on respiratory muscle training (RMT), or specifically inspiratory muscle training (IMT), in endurance running. This is in contrast to other sports where a large number of studies have been conducted and where there appears to be beneficial effects (see review and metaanalysis in HajGhanbari et al “Effects of respiratory muscle training on performance in athletes” J Strength Cond Res 2013; 27: 1643-1663 and Illi et al “Effect of respiratory muscle training on exercise performance in healthy individuals: a systematic review and meta-analysis” Sports Med 2012; 42:707-24). There are some early studies showing promising effect of respiratory core muscle training for shorter running distances (see for instance Tong et al “'Functional' inspiratory and core muscle training enhances running performance and economy” J Strength Cond Res 2014; Epub ahead of print). For ultramarathon races and in particular mountain ultramarathons, where the problems might be even more enhanced, no studies have been done to my knowledge. To speculate, I would think some kind of respiratory training would be beneficial, in particular for elite runners of shorter mountain ultramarathons. Personally, not being an elite runner, I will not specifically incorporate respiratory muscle training except to the extent that I will perhaps focus more on these muscle groups when doing core and climbing training and also make sure I include enough speed and/or hill training early in the season so that my respiratory apparatus is trained to a greater extent than they are compared to during slow distance training runs.

26 September 2014

Killer shoes - The importance of footwear traction in mountain trail running

Catching my breath I finally took the time to turn around and look out over the valley. There were still thick veils of mist lower down, but the rain had finally abated after constantly falling since last night. Looking out over the snow-clad mountains on the other side of the valley I could see the first stars of the new night breaking through the rapidly vanishing clouds. I turned off the headlight and let the night surround me. It was warm without any wind and I was surprised that I anyway could feel soft movements from the thick wet grass around my ankles. Slowly turning around towards the slope I touched the wet grass with my hands. I leaned forward a little bit to let wetness and cold of the grass caress my warm face. “Swimming in a green waterfall of grass”, I thought. Suddenly the adrenaline started to rush through my body again and I pulled up my head and turned on my headlamp.  Looking up over the grassy slope I thought I could see solid rock that must be part of the ridge. “Not far away now”, I thought as I moved my right foot up towards what looked like a more solid tussock. Feeling the rubber of my outsole dig into the soil and fine gravel under the grass I put my weight on the foot and followed after with my body. “Just one step at a time, Peter, just one step at a time”. After another step upwards I stopped again and looked down the slope. I could not see Otto, but knew he must be close on the other side of the little spur I had crossed further below. “It might be possible here, Otto” I screamed. “It might finally be possible”.

It was the second night of Petite Trotte à Léon (PTL) and we were standing on a horrible wet grassy slope of Croix de Tousse at an altitude of around 2800 meters high over the treeline on our way up towards the crossing of Côte 2922 to Petite Vélan. I still do not know exactly how we could have ended up off route and by how much. When I looked at the GPS it one minute said that we were only 10 meters from the route, the next it said 40 – a huge difference in a terrain like this. Not able to rely on the GPS we tried for a long time to find our way on the map – which of course was not detailed enough as the elevation curves did not catch how steep parts of the slope was and we often found ourselves stuck and had to climb down again. I also still do not know exactly how steep it was –  definitively too steep as we had to climb using both feet and hands and trying to find fixing points for them so part of the slope was probably a grade 4 scrambling.

Although the climb upwards in the slippery wet grass on this crazy steep slope was one of the scariest things I have ever done in my life, it was nothing compared to when we had to descent to try to find another route upwards towards the ridge. It was here I perhaps for the first time realized that your life in the mountains might depend on your shoes. Both Otto and I had of course so called trail running shoes that according to the manufacturer should be suitable for running in the mountains. However, while my fairly new La Sportiva Bushido shoes had a fairly good grip on the wet grass, Otto’s slightly more worn shoes of another brand had what looked like almost no traction. Numerous times during our wayfinding on the less step parts of the grassy slope his feet suddenly lost their grip and flew up and he fell hard backwards. Each time I was really scared that he should break his back, a leg, or worse, hit his head or not being able to arrest the fall after touching ground and rolling down the slope. It was certainly a close call several times.  In retrospect, we should of course have tested our shoes at various conditions before the race, and steep grassy slope we learned painfully during PTL are quite common in the Alps if you are not following any normal path or trail. Paradoxically, Otto had in contrast to me actually tested his shoes in the mountains in the northern part of Sweden just before the race, but obviously not on wet grassy steep slopes, while I think I was just lucky with my shoe selection. We learned later on in the race that the solution was for Otto to put on his crampons each time we crossed wet grassy and muddy terrains, the crampons certainly do work well on other surfaces besides ice, but this night we were probably too scared and shocked to come up with this simple solution.

Not being a professional athlete and not having the possibility to test several shoes in mountain conditions I started to look at what data and research that is available about the traction of outsoles of trail running shoes. Is there any comparative data available? Any standards in how to report the traction on different surfaces? Sadly, I did not find much. Almost all major trail shoe brands, like the one Otto was wearing, are making bold claims on their webpages about how good the traction is in all sorts of terrain. Just reading some of these claims make me skeptical – how could a shoe with good grip on both dry and wet rock also be good for mud, wet grass and even wet wood? Some brands, actually for instance Otto’s again, show rather impressive research data on their webpage regarding traction. Obviously, these data did not correlate well with how the shoes actually performed out on the real mountain and it makes me question the value of research performed by the manufacturer itself when there is no independent control of the data. The same thing probably hold true for at least part of the shoe reviews posted by bloggers and others who have received the shoes for free. Furthermore, Otto’s shoes were not as new as mine, but the outer soles were still well defined. How is the traction of the shoes affected by wear – when is it time to buy new ones? If readers of this blog could point me towards solid comparative independent data on these features of trail running shoes I would be very happy, but I doubt such data exist.

What I did find was a list of recommended shoes at skyrunning races on the homepage of the International Skyrunning Federation (see figure below). In their recommendation they rate the shoes as good or very good for the various types of skyrunning disciplines. It is not described how their selection and rating of shoes were being done, but I assume it involved some kind of testing of the shoes. Of note, Otto’s brand is not among the recommended in this list and it would have been good to know if they had tested the shoes and found them not meeting the standards for inclusion or if this just means that they have not tested them. Obviously, I also found a number of trail running shoe tests in various running magazines, but while features such as weight, drop, presence of rock protection and the width of the toe box naturally are objective measures differing between shoes, traction is for almost all trail shoes tested scored high in these tests and there is in most cases difficult to differentiate the shoes from each other depending on this.  Almost no test takes into account the performance on the varying surfaces in the mountain environment such as for instance dry and wet rocks, loose talus and gravel, wet grass, mud and wet roots.
 
List from ISF of recommended shoes 2014
Looking at the scientific literature about shoe – surface traction I could not find any study of trail, mountain and sky running shoes or even normal athletic running shoes. More surprisingly, I could neither find any good studies regarding traction of climbing footwear, only one study about traction in ladders shoes (Chang et al “Available friction of ladder shoes and slip potential for climbing on a straight ladder” Ergonomics 2005; 48: 1169) and a general article about the slip-resistance of different types of rubber (Manning et al “The effect of roughness, floor polish, water, oil and ice on underfoot friction: current safety footwear solings are less slip resistant than microcellular polyurethane” Appl Ergon. 2001; 32: 185). In other sports the traction developed at the shoe – surface interface has been extensively studied as it has been shown to influence injuries. Many studies have focused on the rotational traction torque forces and friction on various surfaces as higher forces in numerous studies have been associated with higher joint loading and in particular knee and ankle injuries (see for instance Wannop et al “Footwear traction and lower extremity noncontact injury” Med Sci Sports Exerc 2013; 45:2137). There are plenty of publications about this in for instance soccer (De Clercq et al “Cutting performance wearing different studded soccer shoes on dry and wet artificial turf” Footwear Science 2014; 6: 81; Schrier et al “Shoe traction and surface compliance affect performance of soccer-related movements” Footwear Science 2014; 6: 69; Smeets et al “Torsional injuries of the lower limb: an analysis of the frictional torque between different types of football turf and the shoe outsole” Br J Sports Med 2012; 46: 1078; Severn et al “Science of synthetic turf surfaces: investigation traction behavior” J Sport Engin Technol, 2011; 225: 147), American football (Wannop et al “Footwear traction and lower extremity noncontact injury” Med Sci Sports Exerc 2013; 45: 2137; Iacovelli et al “The effect of field condition and shoe type on lower extremity injuries in American Football” Br J Sports Med 2013; 47: 789);  tennis (Clarke et al “The development of an apparatus to understand the traction developed at the shoe-surface interface in tennis” J Sport Engin Technol, 2013; 227: 149; Damm et al “The effects of surface traction characteristics on frictional demand and kinematics in tennis” Sports Biomech 2013; 12: 389) and golf (Worsfold et al “Kinetic assessment of golf shoe outer sole design features” J Sports Sci Med 2009; 8: 607; Worsfold et al “Low handicap golfers generate more torque at the shoe-natural grass interface when using a driver” J Sports Sci Med 2008; 7: 408; Worsfold et al “A comparison of golf shoe designs highlights greater ground reaction forces with shorter irons” J Sports Sci Med 2007; 6: 484).

What I did find, however, was a number of scientific studies how the gait and motor pattern is changing when running on a slippery or uneven surface (for instance Sterzing et al “Running on an unpredictable irregular surface changes lower limb biomechanics and subjective perception compared to running on a regular surface” J Foot Ankle Res 2014; 7: A80; Chang et al “Contribution of gait parameters and availability coefficient of friction to perceptions of slipperiness” Gait Posture 2014; Epub ahead of print; Voloshina et al “Biomechanics and energetics of walking on uneven terrain” J Exp Biol 2013; 216: 3963; Gates et al “Kinematic strategies for walking across a destabilizing rock surface” Gait Posture 2012; 35: 36; Cappelini et al “Motor patterns during walking on a slippery walkway” J Neurophysiol 2010; 103: 746; Fong et al “Greater toe grop and gentler heel strike are the strategies to adapt to a slippery surface” J Biomech 2008; 41: 838). Not surprisingly, it appears runners on a slippery surface lower their limb positions and increase the stiffness of the legs in order to keep the center of mass (COM) more aligned with the supporting limbs and also use a gentler heel strike and relies more on the toe grip. These gait changes require more energy and I have previously written a blog post about the positive training effects of running on snow and sand and the same thing could probably be applied to wet grass and mud.

I also found a very interesting recent article looking specifically at the footwear traction and kinematics of walking at different directions in slope terrain (Wannop et al “Footwear traction and three-dimensional kinematics of level, downhill, uphill and cross-slope walking” Gait Posture 2014; 40: 118). In this study, ten participants walked along in various directions across a 19° inclined walkway. Quite surprisingly to me, the required traction at touchdown in order to not slip was similar at different sloped levels compared to level walking and the authors speculate that the increased likelihood of heel slipping during hiking down a steep slope therefore potentially is due to the presence of loose material (rocks and dirt), rather than the overall lack of traction. Not surprising, traverse walking cross the slope required the most rapid foot-floor eversion, which the authors speculate could place the hiker at higher risk of injury with a misstep or if there was a slight slip. I think the same results probably would be achieved in running as well.

While it is interesting to know that you change your gait when running on a slippery surface or on a steep slope, and thus probably could train your ability to do so, it is clear that it is not enough and that in order to avoid a fall during a mountain and sky running you also need shoes with good traction. In the lack of good independent comparative data about the traction of various shoes I think you still have to rely on trial and error yourself or talking to other runners or, if they have a blog or have written a review, reading about their experiences. I was reassured before PTL when I saw that Jared Campbell had used La Sportiva Bushido when he won and completed Barkley Marathons earlier this year. However, I think shoe selection is something very personal and of course there are other important factors than only traction. I am very happy with my selection of shoes for PTL. Last year I was running TDG in La Sportiva Helios and, although the traction was great and they were really light and comfortable, they did not offer the required protection for the last part of the race, while the Bushido did that during PTL. Still, for a shorter mountain or skyrunning race I would probably select Helios or Salomon S-Lab Sense 3 Ultra, and for a muddy trail race I would probably choose Salomon S-Lab Fellcross 3. For training I rely much on several old Asics shoes I have in my closet when running on roads, Salomon S-Lab XT models in mixed terrain and recently more frequently also on Hoka Hoka Rapa Nui shoes. But, we are soon entering a new season with new shoes coming out from the different brands so next year the selection will probably be different. Lastly, I think disclosure is important in a blog post like this and this year I have not received any shoes for testing and have not been sponsored in any way.
 
You also have to like the look of your shoes -
after all this is what you see most of the times in the later stages of a long race
(Picture from TDG 2013)
 

18 September 2014

Testosterone and mountain ultramarathon running

This past weekend I put on my running shoes for the first time since Petite Trotte à Léon (PTL) . Despite only jogging slowly for 7 kilometers (4.3 miles) I developed a massive delayed onset muscle soreness in my quadriceps. It felt like I had lost a lot of my muscle mass in my legs, and, thinking about it and looking at my legs I think that might actually been what has happened. I probably literally consumed my own leg muscles due to the catabolic energy state I was in during and immediately after the race. This made me think more about the wasted state I have been in during the past two weeks and what hormonal changes that could lead to this. Looking at my general symptoms of tiredness, poor concentration, lack of vigor and vitality, massive night sweats, occasional hot flushes and sleep disturbance I quickly focused in on low testosterone. Other cardinal symptoms of low testosterone levels include loss of morning erection and reduced sexual desire/loss of libido. Thinking back I have at least to some extent suffered from partly these same symptoms transiently for a while after Tor des Geants (TDG) and other longer ultramarathons I have done in the past. The other day I read John Burton's great race report from Tahoe 200 and in the aftermath he appears to have suffered from some of the same symptoms as well and I have had other runners telling me similar stories.

The suspicion that ultramarathon running might cause low testosterone levels made me read more about the subject and, regretfully, it appears at least from the few studies conducted so far that longer ultramarathon running indeed can lead to testosterone deficiency and even secondary hypogonadism in males. In this post I will review the effect of ultramarathon running, in particular in mountains, on testosterone and partly also other hormones and substances in the hypothalamic-pituitary-gonadal/testicular (HPG/HPT) axis (see figure below). This will be a post focused on the effects in men, mostly as the amount of literature on the effects of training on the female reproductive system is very extensive and clearly requires a separate review.

The hypothalamic-pituitary-gonadal (HPG) axis
 
Testosterone levels following Western States Endurance Run (WSER)

The first article I stumbled upon was a recent study by Kupchak and colleagues of 12 male runners completing the 161 km (100 miles) race Western States Endurance Run (WSER) (Kupchak et al “The impact of an ultramarathon on hormonal and biochemical parameters in men” Wilderness Environ Med 2014; 25: 278-288). The 12 runners ran an average of 98.7 (81.9 -115.5) km per week before the race and had a mean finish time of 25.08 (22.53 – 27.62) hours. Quite interestingly, 8 out of 12 runners had prerace values of testosterone lower than the reference limits in their assay (< 14 nmol/L). Still the values of both testosterone and luteinizing hormone (LH) decreased even further from these low baseline values during the race and were significantly lower both immediately and one-day after the race compared to the values before the race. Also sex hormone-binding globulin (SHBG) decreased during the race, while cortisol, a hormonal marker of stress, increased significantly leading to a significant and markedly lower Testosterone : Cortisol ratio. One of the problems with the study is that the blood collection for analysis occurred at various times in association with the finishing of the race and hormones such as testosterone exhibit a clear diurnal variation. Also, the authors used an immunoassay rather than today’s golden standard mass spectrometry in measuring the levels of testosterone. Still, the magnitude of change observed was clearly well beyond what could be explained by circadian undulation and the levels were clearly indicative of testosterone deficiency.

Other studies of testosterone levels following marathon and ultramarathon races

Kupchak’s study was clearly not the first in this area as there have been a large number of studies published since the beginning of the 1980’s showing statistically significant reductions of testosterone levels in blood and saliva during a marathon or ultramarathon race compared to the pre-race levels (see table below which include some selected studies I could find).
 

Study
Distance (km)
Subj
Reference
Kupchak 2014
161 (WSER)
12
Wilderness Environ Med 2014; 25:278
Tauler 2014
104
64
Appl Physiol Nutr Metab 2014; 39: 560
Kraemer 2008
161 (in cold)
10
Br J Sports Med 2008; 42: 116
Karkoulias 2008
42.2
20
Eur J Intern Med 2008; 19: 598
Ishigaki 2005
284 (over 8 days)
13
J Phys Antl Appl Hum Sci 2005; 24: 573
Fournier 1997
110
11
Int J Sports Med 1997; 18: 252
Marinelli 1994
42.2 (high altitude)
6
Horm Res 1994; 41: 225
Dressendorfer 1991
400 (over 15 days)
19
Med Sci Sports Exerc 1991; 23: 954
Raschaka 1991
1000 (over 20 days)
42
Z Ernahrungswiss 1991; 30: 276
Pestell 1989
1000
8
Clin Exp Pharm Physiol 1989; 16: 353
Tanaka 1986
42.2
7
J Endocrin Invest 1986; 9: 97
Kuusi 1984
42.2
20
Metabolism 1984; 33: 527
Schürmeyer 1984
1100 (over 20 days)
5
Int J Androl 1984;7:276


Testosterone levels in other endurance sports

This is in contrast to shorter runs of less than one hour where there actually appears to be a rise in testosterone levels during the actual run (see for instance Tremblay et al “Influence of exercise duration on post-exercise steroid hormone responses in trained males” Eur J Appl Physiol 2005; 94: 505 and Hackney et al “Testosterone responses to intensive interval versus steady-state endurance exercise” J Endocrinol Invest 2012; 35: 947). It is, however, in line with findings of a decrease in testosterone during longer endurance races in other sports. For instance during adventure racing for over 6 days (Berg et al Scand J Med Sci Sports 2008; 18: 706), cross-country skiing for 75 km and road bicycling for 4 hours (Vasankari et al Acta Endocrinol 1993; 129: 109), an Arctic ski expedition (Bishop et al Acta Astronaut 2001; 43: 261), Ironman triathlon (Neubauer et al Eur J Appl Physiol 2008; 104: 417) and military special operations training for 5 days (Opstad et al Eur J Appl Physiol Occup Physiol 1982; 49: 343) marked decreases in testosterone have been observed. All of these studies in both running and other sports have only looked at hormonal levels and not any symptoms or behavioral changes associated with these changes, like lowered sex-drive, and there is clearly a need for studies investigating this.

Baseline levels of testosterone in runners depending on weekly mileage

There have also been a number of studies performed looking at the normal baseline testosterone levels of runners and some studies have specifically analyzed the correlation between these levels and the weekly running mileage. In an important study of 53 runners published already in 1992, MacDougall and colleagues showed a correlation between weekly running mileage and testosterone levels (MacDougall et al “Relationship among running mileage, bone density, and serum testosterone in male runners” J Appl Physiol 1992;73: 1165). De Souza and colleagues published another similar study in 1994 where they looked at baseline testosterone levels in 11 high mileage runners (108 ± 4.5 km/week), 9 moderate mileage runners (54 ± 3.7 km/week) and 10 sedentary controls of similar age (28.3 ± 1.5 years) (De Souza et al “Gonadal hormones and semen quality in male runners. A volume threshold effect of endurance training” Int J Sports Med 1994; 15: 383). Interestingly they found a dose-response effect with regards to running volume as the levels of both total testosterone and free testosterone were lower in the high mileage group compared to the other groups. This also correlated with decreased sperm quality in the high mileage group. A similar correlation was found by MacKelvie and colleagues studying 5 high mileage runners (> 95 km/week) and 7 moderate mileage runners (64-80 km/week) and comparing them to sedentary controls (MacKelvie et al “Bone mineral density and serum testosterone in chronically trained, high mileage 40-55 year old male runners” Br J Sports Med 2000; 34: 273).Comparing running with endurance training one study showed that it is only the former where low baseline values of testosterone can be found together with subclinical modifications in semen characteristics (Arce et al “Subclinical alteration in hormone and semen profile in athletes” Fertil Steril 1993; 59: 398).

These findings are in contrast to other studies, for instance by Ayers et al in Fertil Steril 1985; 43: 917, Bagatell et al in Fertil Steril 1985; 43: 917 and Cooper et al in Eur J Endocrinol. 1998; 138: 517, where no low baseline levels of at least free testosterone could be observed in runners. However, these studies did not include high mileage runners. A drawback with all of these studies is also that they are retrospective. A recent interesting prospective randomized controlled trial from Iran of 286 “habitual aerobic exercisers”, training for an average of 1.8 h per day 5 days a week before entering the study, looked at the effects of a 60-week training program where the subjects ran for 120 minutes 5 times a week at either ~60% of VO2max or ~80% of VO2max (Safarinejad et al “The effects of intensive, long-term treadmill running on reproductive hormones, hypothalamus-pitutary-testis axis, and semen quality: a randomized controlled study J Endocrinol 2009; 200: 259). In both groups there was marked decrease of testosterone levels and semen quality and these changes were observed already from 12 weeks into the study. That longer period of increase in training appears required for a decrease in testosterone is indicated in a study by Hall et al where 2 weeks of running exercise at 186% of normal training intensity was not enough to lead to any hormonal changes (Hall et al “Effects of intensified training and detraining on testicular function” Clin J Sport Med 1999; 9: 203). Also, it appears again that the training intensity needs to be quite high to lead to testosterone decrease as a prospective study of 24 marathon runners did not show changes in this hormone, despite changes in semen parameters (Jensen et al in Fertil Steril 1995; 64: 1189).

Testosterone levels following tapering and following overtraining/overreaching in runners

Quite interestingly, following cessation of the training program in the Iranian study the testosterone levels rather quickly returned to the same values, or even somewhat higher, than before the start of the training period. This is in contrast to a study by Houmard and colleagues where 10 runners were followed for 4 weeks of normal training (81 ± 5 km/week; 6 days/week) followed by a 3 week tapering period with a 70% training reduction (to 24 ± 2 km/week; 5 days/week) (Houmard et al “Testosterone, cortisol, and creatine kinase levels in male distance runners during reduced training” Int J Sports Med 1990; 11: 41). The low testosterone baseline values observed during the training period were in this study not restored by the reduction in training. I clearly think more studies are needed on the effect of tapering on testosterone and other hormonal levels. Another subject were more studies are needed is the role of testosterone and the testosterone/cortisol ratio in overtraining syndrome (OTS) / overreaching (OR). The current consensus standpoint appear to be that low testosterone levels and a low testosterone : cortisol ratio only indicates actual physiological strain and cannot be used for diagnosis of OTS / OR. While I agree with this, I still think it too early to completely rule out a role for testosterone in the development of OTS /OR and further studies are needed to see if this indeed might be the case. Also, another question I have thought about is whether fluctuations in testosterone levels that might occur after endurance racing and in tapering could influence mood (swings) and well-being, something which in numerous other studies have been shown to be influenced by testosterone. I am sorry to be repetitive when I again ask for studies of this in runners.

Testosterone levels at high altitude

Mountain ultramarathons like Petite Trotte à Léon (PTL) and Tor des Geants (TDG) are not only long in terms of kilometers and race time, but also occurs at comparatively high altitudes and are associated with a marked degree of sleep deprivation in most runners at the later parts of the race (Saugy et al “Alterations of neuromuscular function after the World's most challenging mountain ultra-marathon" PLoS One 2013; 8: e65596). Both of these factors have actually independently been associated with a decrease in testosterone levels. Studies of several expeditions to the Himalayas have revealed markedly decreases in testosterone levels coupled with changes in the sperm quality (see for instance Okumura et al High Alt Med Biol 2003; 4: 349; Benso et al Eur J Endocrinol 2007; 157: 733 and Pelliccione et al Fertil Steril 2011; 96: 28). Interestingly, a study by Mirsepasi and colleagues show a decrease in testosterone after only 30 minutes running at 70% of maximal heart rate already at an altitude of 3250 meters (Mirsepasi et al “Effect of submaximal aerobic exercise at the altitude of 3250 meters on levels of serum cortisol, testosterone and testosterone to cortisol ratio in active young men” Adv Environment Biol 2013; 7: 854).

Testosterone levels following sleep deprivation

A number of studies also show that total sleep deprivation leads to a reduction of testosterone levels (for instance Schmid et al Clin Endocrinol 2012; 77: 749 and Jauch-Chara et al PloS One 2013; 8: e54209). The production of testosterone is dependent on sleep and requires at least 3 hours of deeper so called nonrapid eye moment (NREM)  slow wave sleep (SWS), which normally occurs in the first part of a sleep episode (reviewed in Wittert “The relationship between sleep disorders and testosterone in men” Asian J Andrology 2014; 16: 262). This is interesting as at least I have had the strategy to not sleep for more than 2 hours at each occasion in both TDG and PTL and that would therefore not be enough to stimulate a normal testosterone production.

The Exercise-Hypogonadal Male Condition and the effect of running on male fertility

One of the researchers who has published perhaps most scientific papers on the subject of male reproductive dysfunction following endurance training is Anthony C. Hackney at University of North Carolina in Chapel Hill in the USA. He has coined the syndrome “Exercise-Hypogonadal Male Condition” or EHMC (reviewed in for instance Lane & Hackney “Reproductive dysfunction from the stress of exercise is not gender specific: The “Exercise-Hypogonadal Male Condition” J Endocrinol Diab 2014; 1: 4). That endurance training, and in particular ultra-endurance training, might lead to impaired fertility in males have been discussed also in other review articles, for instance by Arce and colleagues (Acre et al “Exercise and male factor infertility” Sports Med 1993; 15: 146), Brandt and colleagues (Brant et al “Male athletic activities and their effects on semen and hormonal parameters” Phys Sportsmed 2010; 38: 114), du Plessis and colleagues (du Plessis et al “Is there a link between exercise and male factor infertility?” Open Rep Sci J 2011; 3: 105) and Vaamonde and colleagues (Vaamonde DM et al “The impact of physical exercise on male fertility” in the book Male Infertility 2014; 47-60 edited by du Plessis et al). Nevertheless, there are no good controlled studies of this and further studies are clearly needed to determine whether male ultramarathon runners really have impaired fertility in general.

What are the mechanisms behind the low testosterone levels following an ultramarathon?

Today we can only speculate why prolonged endurance activities such as an ultramarathon might lead to lower testosterone levels. Testosterone is produced in the testis and it has been speculated that reduced testicular blood flow or damaging testicular heating might influence the production. Others have advocated the increase in testosterone/androgen utilization in the repair of tissues might lead to increased consumption of testosterone leading to lower blood levels. Also the stress of prolonged endurance activities might lead to an inflammatory reaction acting at various levels of the HPG-axis. The response of the body to an ultramarathon might not only be a reactive response to damaging stimulus, but also a way for the body to protect itself in the longer run and it has been speculated that one positive effect of low testosterone levels in male ultramarathon runners is that it limits development of excessive muscle mass. Also, during the actual race it might lead to mobilization of amino acids for energy consumption through gluconeogenesis, hence leading to use of the muscles for energy. I have encountered some athletes, in particular in adventure racing, advocating  muscle strength training sessions in association with the endurance race or early during the recovery phase and it would be interesting to study whether this could counteract some of these effects and actually raise the testosterone levels.

Negative effects of low testosterone levels in male ultramarathon runners

No studies have been conducted on possible negative medical effects of low testosterone levels in male ultramarathon runners besides some studies showing that, rather surprisingly, low baseline levels of testosterone appear not to be associated with a decrease in bone mineral density (BMD) (see references above to MacDougall et al 1992 and MacKelvie et al 2000). Low testosterone levels and hypogonadism in middle aged and elderly men appear quite common and have been associated with male infertility and the symptoms I mentioned in the beginning of this post (reviewed in Wu et al “Identification of late-onset hypogonadism in middle-aged and elderly men” N Engl J Med  2010; 363: 123; Basaria “Male hypogonadism” Lancet 2014; 383: 1250, Finkelstein et al “Gonadal steroids and body composition, strength and sexual function in men” N Engl J Med 2013; 369: 1011 and Hackett et al “Testosterone deficiency, cardiac health, and older men” Int J Endocrinol 2014; 143763). There are also indications that low testosterone levels might lead to increased incidence of cardiovascular diseases and even higher mortality, but in the studies conducted so far there are a number of co-founding factors such as presence of type 2 diabetes and it is difficult to say what is the hen and the egg in these studies. There is clearly a need to see study if there are any long-term health effects, if any, of low testosterone levels in trained male ultramarathon runners and it will for instance be interesting to see whether there could be a correlation between testosterone levels, weekly mileage and cardiac health in runners. In these studies it would have been interesting to see the effects of testosterone replacement therapy, which is becoming increasingly popular in hypogonadism in elderly men, but this would of course be impossible and not ethical as testosterone in all forms rightly is classified as a prohibited performance enhancing drug and is on all doping lists.

Summary

In summary, I think that it has been shown quite convincingly in a number of studies that prolonged endurance activities can lead to a decrease in testosterone levels. In longer mountain ultramarathon races also the high altitude and the sleep deprivation of the runners might further contribute to this decrease. Even though some studies indicate that runners with a high weekly training mileage have lower baseline testosterone levels than the normal aged matched population, I still think further studies are needed to determine whether ultramarathon induced hypogonadism really exists. The long-term health effects of decreased testosterone in ultramarathon runners are also not known today.