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.

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