Marathon race performance increases the amount of particulate matter deposited in the respiratory system of runners: an incentive for “clean air marathon runs”

Minute ventilation

For the purpose of this study, we have assumed that the V_E in resting men, as well as in runners at rest would amount to 8 L min⁻¹, while the V_E obtained by an average marathon runner (marathon performance time equal to 4 h 30 min (270 min)) during a marathon race amounts to 62 L min⁻¹, i.e., ∼7–8 times higher than at rest. The V_E of the elite marathon runners (performance time 2 h (120 min)) during a marathon race was assumed to be 115 L min⁻¹, i.e., ∼14–15 times higher than at rest. Our predictions of the V_E during a marathon race for an average runner and an elite runner are in agreement with experimental data collected in various groups of marathon runners, representing a broad range of performance levels (for details, see Maron et al., 1976; Mahler, Moritz & Loke, 1982; Hausswirth, Bigard & Guezennec, 1997).

Air quality on the day of a marathon race

The measurements of the air quality were made in Kraków at the Jagiellonian University Campus by the University Measurement Station (UMS), (for details, see Nieckarz & Zoladz, 2020), located close to the green areas crossed by the marathon route (GPS location: 50.0291°N, 19.9046°E). In this paper, we used the data collected by this station on the day of an annual marathon in Kraków (“Cracovia Maraton”), i.e., on April 28th 2019. The station was equipped with digital laser dust sensor SEN0177 (DFRobot, China), which continuously measures the mass concentration of PM₁ PM_2.5,PM₁₀ in the air and the concentration of suspended particulate matter (C) in the five size categories mentioned in Table 1. The data were used as a source of information to calculate total deposition by means of Eq. (1).

The sampling rate was 30 times per minute. Then, the data were aggregated to obtain average values per minute. Finally, we analysed the average values of concentrations that had been calculated on the basis of stored 1 min data. The station made measurements with the accuracy of 15% in a wide range of data (above 100 µg m⁻³) and inaccuracy equal ±10 µg m⁻³ below 100 µg m⁻³. The accuracy of the particulate matter detector used in our station in Kraków was verified by comparing the data recorded by the UMS station with the readings obtained from reference station EDM107 that belongs to the GRIMM company (Grimm & Eatough, 2009). According to the producer of the EDM107 analyser (the GRIMM company), the measurement error of this system is ± 2 µg m⁻³.

Calculation of the total deposition

Total deposition (TD) of suspended PM in the human respiratory tract was calculated with Eq. (1), where: V is the volume of ventilated air [m³]; n is the number of a particle diameter range, DF_n is the average deposition fraction in n-th range; C_n is the concentration of PM in n-th range of diameter [m⁻³]; ρ_n – the aerosol effective density in n-th range [kg m⁻³] (see Table 2); d_n  –the average particle diameter in the n-th range [m]. (1)${\displaystyle \mathrm{TD}=\sum _{n=1}^5\mathrm{V}\cdot {\mathrm{DF}}_n\cdot {\mathrm{C}}_n\cdot {\rho }_n\cdot \frac{\pi \cdot d_n^3}{6}}$ Deposition fraction (DF) can be calculated with Eq. (2), where: C_in and C_ex are, respectively, the inhaled and exhaled concentrations of suspended particulate matter; d is a particle diameter. The DF can also be calculated by applying average values of both concentrations for n ranges to Eq. (3), where C_ex,n and C_in,n are, respectively, the inhaled and exhaled concentrations of PM in n-th range. (2)${\displaystyle \mathrm{DF}\left(d\right)=1-\frac{{\mathrm{C}}_{\mathrm{ex}}\left(d\right)}{{\mathrm{C}}_{\mathrm{in}}\left(d\right)}}$ (3)${\displaystyle {\mathrm{DF}}_n=1-\frac{{\mathrm{C}}_{\mathrm{ex},n}}{{\mathrm{C}}_{\mathrm{in},n}}}$ In this paper, size-resolved DF profiles proposed by Hussein et al. (2019) for a male at rest and a male during exercise have been used. The curves in Fig. 1 present–as a red line–a continuous function of size-resolved total DF in the respiratory tract of an adult for a male at rest (black line) and for a male during exercise (male-exercise) for the particle diameter range from 0.3 µm to 10 µm (Hussein et al., 2019).

The black and red line levels in Fig. 1 present the average values calculated for the five selected diameter rages expressed in µm: [0.3–0.5), [0.5–1.0), [1.0–2.5), [2.5–5.0), [5.0–10.0), which correspond to the ranges implemented in the measurement station (UMS) to count suspended particulate matter. The values of DF_n for the five ranges are listed in Table 1.

The quality of the air in Kraków on the day of the marathon race

As presented in Fig. 2, the quality of the air in Kraków on the day of the marathon race (28th April, 2019), as judged on the basis of the amount of the PM₁₀ in the air, fell within the 2006 WHO standard (still valid, see WHO, 2018), set at the level of 50 µg m⁻³ (WHO, 2006). It should be noticed that our measurements of the air quality in Kraków on the day of the marathon race showed a progressive decrease of PM₁₀ in the air during the race. Its values reached 30 µg m⁻³, 23 µg m⁻³, 22 µg m⁻³ and 17 µg m⁻³ in the 1st, 2nd, 3rd and 4th hour of the marathon, respectively. This is why, we have used the average PM₁₀ value amounting to 22 µg m⁻³ for some considerations made in this study. The observed progressive decline in the PM₁₀ concentration during the race could be due to traffic restrictions imposed in the town for the 4 h of the race. Nevertheless, it should be noticed that, on some days in the early months of the year (January–February 2019), several times higher amounts of PM₁₀ in the air were found in the morning / midday hours (9:00–13: 30), with the pick of 124 µg m⁻³ on 21st January, 2019. Moreover, it seems to be worth mentioning that on certain occasions in previous years (30 January 2017), even higher daily values of PM₁₀ concentrations, reaching 696 µg m⁻³, have been recorded in the centre of Kraków (close the main traffic artery) (for a review, see Nieckarz & Zoladz, 2020).

Deposition of suspended particulate matter at rest

Figures 3A and 3B presents levels of deposition of PM₁, PM_2.5, PM₁₀ in the respiratory tract of runners at rest (both average and elite runners, assuming that their V_E at rest is 8 L min⁻¹), expressed in µg h⁻¹ (Fig. 3A) and in µg 24 h⁻¹ (Fig. 3B).

Deposition of suspended particulate matter during a marathon race

Figures 3B and 3E present the values of deposition of PM₁, PM_2.5, PM₁₀ in the respiratory tract in an elite and an average marathon runner during the race, expressed in µg h⁻¹ (Fig. 3B) and in µg per marathon race (Fig. 3E).

Daily deposition of suspended particulate matter on the day of the marathon race

We also calculated the total deposition of varied fractions of PM₁, PM_2.5, PM₁₀ in the respiratory tract in elite and in average runners on the day (24 h) of the marathon, while taking into consideration their deposition during the race and in the remaining time of the 24 h period, when runners were at rest (see Figs. 3C and 3F).

Impact of air quality on PM deposition in the respiratory tract during marathon race

Figure 4A prensents the results of calculations of depositions of the PM₁, PM_2.5, PM₁₀ in the respiratory tract of runners during two marthon races: the first one performed in relatively clean air (PM₁₀ = 22 µg m⁻³) on 28th April 2020, and the second one pefformed in more poluted air (PM₁₀ = 124 µg m⁻³), as recorded in Kraków on 21st Januray, 2020 (see Fig. 2). Note huge diffrences between these two races in the deposition rates applicable to an average runner.

Impact of air quality on daily deposition of PM in the respiratory tract in runners

As presented in Fig. 4B, the increase of air pollution showed by comparing the measurements performed on 21st January and on 28th April 2020 (see Fig. 2) had a strong impact on the daily deposition of PM₁, PM_2.5, PM₁₀ in the respiratory tract in runners. It can be seen that the levels of deposition of varied fractions of PM on 21st January 2020 are about 5.5−8.5 times greater than on the 28th April 2020 (see Fig. 4B).

The calculations of the level of deposition of varied fractions of particulate matter at rest and during a marathon run are based on real concentrations of suspended particles in the air registered during the 4 h 30 min of the marathon race and during the remaining 19 h 30 min of rest.

Comparison of the rate of PM₁₀ deposition in the respiratory tract in runners at rest and during a marathon race performed in the air with the PM₁₀= 50 µg m⁻³

As presented in Fig. 5, the increase of minute ventilation from its level at rest up to 62 L min⁻¹ in an average runner increased the rate of PM₁₀ deposition in the respiratory tract of runners from 9 to 45 µg h⁻¹. In the case of elite runners, the increase of the V_E from its level at rest (8 L min⁻¹) up to 115 L min⁻¹ during the marathon race, performed within 2 h: 00 min, resulted in an increase of the rate of PM₁₀ deposition in the respiratory tract from 9 up to 446 µg h⁻¹. As shown in Fig. 5, we estimated that performance of a marathon race by an average marathon runner breathing in the air with PM₁₀ = 50 µg m⁻³ at V_E = 62 L min⁻¹ will result in the same rate of the PM₁₀ deposition as in the case of breathing the air with PM₁₀ = 251 µg m⁻³ when at rest (V_E = 8 L min⁻¹). We have also calculated that performance of a marathon race by an elite marathon runner (2 h: 00 min) breathing in the air with PM₁₀ = 50 µg m⁻³ at V_E = 115 L min⁻¹ during the race will result in the same rate of the PM₁₀ deposition in the respiratory tract as in the case of breathing the air with PM₁₀ = 446 µg m⁻³ when at rest (V_E = 8 L min⁻¹). The values of the factors used in these calculations (DF_At rest and DF_Exercise), namely 0.37 and 0.24, respectively, represent the mass deposition fraction factors for PM₁₀ calculated on the basis of real data, presented and analysed earlier (see (4) and Fig. 5). These values are in agreement with the results of previous studies (Guo et al., 2020; Rissler et al., 2017). (4)${\displaystyle D{F}_{Atrest∕Exercise}=\frac{\mathrm{TD}}{\mathrm{M}}}$ Where: TD - total deposion of PM₁₀ calculated with Eq. (1) (using DF for male-rest and male-exercise, respectively, according to Table 1) in the volume of ventilated air (V), M - is the mass of PM₁₀ in the same volume V.

We also calculated the daily (24 h) amount of the PM₁₀ deposition in the respiratory tract in a runner at rest, while breathing the air containing 50 µg m⁻³ of PM₁₀, with the V_E of 8 L min⁻¹. In these conditions, the daily PM₁₀ deposition reached 213 µg per 24 h (see Fig. 6A). As presented in Fig. 6B, in order not to exceed the basal level of daily PM₁₀ deposition of 213 µg per 24 h, the air on the day when an elite runner runs in a marathon race should contain no more than 29.5 µg m⁻³ of PM₁₀ (see Fig. 6).

We have also evaluated the relationship between PM₁₀ content in the air and its deposition rate during the marathon race performed by an average runner as well as by an elite marathon runner (Fig. 7). As presented in Fig. 7 the deposition rate of PM₁₀ in the respiratory tract of the runners during a marathon race is linearly dependent upon the PM₁₀ content in the air. The ∼2 times greater slope in this relationship in case of an elite runner when compared the average runner (Fig. 7), indicates that a given PM₁₀ content in the air the deposition rate of PM₁₀ in the elite runner is greater than in the average runner.

PM deposition rate at rest

As presented in Figs. 3A and 3D, PM deposition rates, assessed in our study in humans at rest on 28th April 2019 (when PM₁₀ concentration in the air was 22 µg m⁻³) reached about 1, 3.63 and 4.17 µg h⁻¹ (Figs. 3A) and 24, 87 and 100 µg 24 h⁻¹ (Figs. 3D), for PM₁, PM_2.5 and PM₁₀, respectively.

Impact of running a marathon race in “clean air” on PM deposition in humans

In the present study, we have demonstrated that a marathon race performed even in relatively clean air containing only 22 µg m⁻³ of PM₁₀ dramatically increased the rate of deposition of PM₁, PM_2.5 and PM₁₀ in the respiratory tract of marathon runners during the race. So that performance of a marathon race resulted in increased rates of PM deposition in the respiratory tract of average runners, reaching up to about 5.56, 19.34, and 23.12 µg h⁻¹ for PM₁, PM_2.5 and PM₁₀, respectively (Fig. 3B). In the case of an elite marathon runner, this PM deposition rate (expressed in µg h⁻¹) was about two times higher than in the case of an average runner and reached 10, 36 and 43.0 µg h⁻¹ for PM₁, PM_2.5 and PM₁₀, respectively (Fig. 3B).

Interestingly, the deposition rate of varied PM – expressed in µg per marathon race for all studied fractions (PM₁, PM_2.5 and PM₁₀) – was systematically higher in average runners than in the elite (see Fig. 3E). It shows that a marathon race, in the case of elite runners, generates a higher pollution stress for the respiratory system expressed in µg of PM per unit of time than in the case of average runners, but the total amount of the PM deposited during the race is clearly greater in average runners than in elite marathon runners (see, Fig. 3E). The main reason for a greater rate of PM deposition rate expressed in [µg h⁻¹] found in elite runners is higher V_E during a marathon race (115 L min⁻¹ vs. 62 L min⁻¹ in elite and in average runners, respectively). In turn, greater PM deposition during a marathon run expressed in [µg h⁻¹] that was observed in average runners (as shown in Fig. 3E) is caused by greater total V_E needed for average runners to cover the marathon distance (see also Figs. 6 and 7). The required higher total V_E during a marathon race in an average runner is due to two factors: (i) poorer running economy (i.e., higher oxygen cost of running) and (ii) higher body mass, when compared to elite runners (for overview see e.g., Maron et al., 1976; Mahler, Moritz & Loke, 1982; Hausswirth, Bigard & Guezennec, 1997; Elmer, Joyner & Carter, 2017; Hoogkamer, Kram & Arellano, 2017; Joyner et al., 2020).

Impact of marathon run in varied air quality on PM deposition in humans

As shown in Figs. 3C and 3D, running the marathon distance in Kraków on the day of 28th April 2019 (see Fig. 2) almost doubled the amount of PM₁, PM_2.5 and PM₁₀ deposited in the respiratory tract of marathon runners per 24 h, when compared with a day spend at rest in the same air quality (see comparisons in Figs. 3A and 3C). This indicates that marathon race performance even in relatively clean air strongly influences the amount of PM₁, PM_2.5 and PM₁₀ deposited in the respiratory tract of humans.

As mentioned above, so far we have discussed the levels of the deposition of PM₁, PM_2.5 and PM₁₀ in the respiratory tract of runners who exercised in relatively clean air (containing “only” 22 µg m⁻³ of PM₁₀), according to measurements performed in Kraków on 28th April 2019 (see Fig. 2). It should be noticed, however, that the air quality in Kraków on some days can be much poorer than that on the day of performance of the 18th “Cracovia Maraton” race. For example, the daily PM₁₀ concentration in the air in Krakow on 21st January 2019 reached 124 µg m⁻³. It was found that the levels of deposition of PM₁, PM_2.5, PM₁₀ in the respiratory tract during the marathon race in an average runner who exercised on 21th January 2019 reached up to 115 µg, 516 µg, 730 µg, respectively, whereas on 28th April 2019 the values were 21 µg, 71 µg, 86 µg, respectively (see Fig. 4A). We also aimed at answering the question concerning the effect of running the marathon distance by elite runners in more polluted air (PM₁₀ content = 124 µg m⁻³) on PM deposition in their respiratory track. It was found out that the levels of deposition of PM₁, PM_2.5 and PM₁₀ in their respiratory tract during the marathon race on 21th January 2019 would reach 113 µg, 511 µg, 726 µg, respectively, whereas on of 28th April 2019, the values were 20 µg, 72 µg, 86 µg, respectively (see Fig. 3B). Furthermore, in the case of an elite marathon runner participating in the marathon race on 21th January 2019, with the V_E of 115 L min⁻¹ during the race, PM₁₀ deposition rate was 206 µg h⁻¹, i.e., 411 µg of PM₁₀ per marathon race. It implies that an elite marathon runner breathing the air containing 124 µg m⁻³ of PM₁₀ at the V_E = 115 L min⁻¹ during a race would experience the same PM₁₀ deposition rate as in the case of breathing very highly polluted air –containing as much as 1 156 µg m⁻³ of PM₁₀ –when at rest. Accordingly, the daily amounts of varied PM deposited on 21st January 2019 would be several times greater than on 28th April 2019. The situation is even more dramatic in the case of the worst daily air quality levels measured by us on 30th January 2017. Namely, the PM₁₀ concentration in the air in Kraków that reached 696 µg m⁻³ on that day (which is not exceptional for large cities; see, for instance, Mage et al., 1996; Marlier et al., 2016), in the case of an elite athlete who covers the marathon distance within 2 h 00 min, would result in an extremely high deposition rate of PM₁₀, reaching up to to 1,152 µg h⁻¹, i.e., 2,305 µg of the PM₁₀ per marathon race. According to this scenario, an elite marathon runner breathing the air containing up to 696 µg m⁻³ of PM₁₀ at the V_E = 115 L min⁻¹ during the race would experience the same PM₁₀ deposition rate as a runner breathing extremely polluted air–containing as much as 6 490 µg m⁻³ of PM₁₀–when at rest. So poor air quality–when the concentration of PM₁₀ in the air is at the level of 6.50 mg m⁻³–exceeds the levels of PM₁₀ concentration measured in the most polluted parts of coal mines (Kizil & Donoghue, 2002).

Impact of marathon run performed in the air containing up to 50 µg m⁻³ of PM₁₀

According to WHO air quality guidelines (WHO, 2006), the upper limit for the content of PM₁₀ in the air is 50 µg m⁻³. For this reason, we assessed the rate of PM₁₀ deposition in the respiratory tract in humans at rest, during a marathon run by an average runner as well as during a marathon run by an elite athlete, while breathing the air containing up to 50 µg m⁻³ of PM₁₀. As shown in Fig. 5, breathing the air at (V_E) equal to 8 L min⁻¹ when at rest resulted in the PM₁₀ deposition rate of ∼9 µg h⁻¹, but a marathon run by an average marathon runner with V_E = 62 L min⁻¹ increased the deposition rate up to 45 µg h⁻¹. In an elite runner, a marathon run at the V_E = 115 L min⁻¹ increased the PM₁₀ deposition rate up to 83 µg h⁻¹. Interestingly, if an elite marathon runner breathed the air containing 50 µg m⁻³ of the PM₁₀ at the V_E = 115 L min⁻¹ during the race, it would result in the same PM₁₀ deposition rate as in the case of breathing very polluted air–containing as much as 466 µg m⁻³ of PM₁₀–when at rest. This is why, in order to minimize this health risk, runners should avoid running marathon races in cities, where the air is highly polluted. We also calculated that, in order to not exceed the daily PM deposition in the respiratory tract due to breathing the air containing 50 µg m⁻³ of PM₁₀ at rest, the PM₁₀ concentration in the air on the day of a marathon race should not exceed 29.5 µg m⁻³ (see Fig. 6B). In the subsequent consideration we went a step further and calculated the maximum PM₁₀ concentration in the air on the day of a marathon run that would be required for this level of PM₁₀ deposition rate not to be exceeded in runners participating in a marathon race. According to our calculations, the concentration of PM₁₀ in the air during a marathon race that would allow one not to exceed the PM₁₀ deposition rate of 9 µg h⁻¹ should be lower than 10 µg m⁻³ in the case of an average runner, and it should be lower than 5.5 µg m⁻³ in the case of an elite runner. This seems to be the upper limit of PM₁₀ in the air for marathon runners on the day of a marathon race in a given city. Interestingly, it has also been reported that even very moderate air pollution can negatively affect marathon performance in women (Marr & Ely, 2010). The paper reports that women’s marathon performance was slower by 1.4% for every 10 µg m⁻³ of increase in PM₁₀ concentration in the air (in range of 4.5–42 µg m⁻³ of PM₁₀–see Figure 1 in Marr & Ely (2010).

Health risk related to marathon running

It is well documented that marathon running often leads to serious health problems and, in extreme situations, it ends with runner’s death (see, for instance Cohen & Ellis, 2012; Kim et al., 2012; Siegel & Noakes, 2017; Dayer & Green, 2019). It was estimated that the risk of death during marathon race is approximately 1 death per 149,968 participants, being more than twice higher in males (one per 102,503) than in females (one per 243,879) (Dayer & Green, 2019). Poor health status of (some) marathon participants one of the factors that strongly increases the risk of health complications and deaths during a marathon race (Tsiflikas et al., 2015; Herm et al., 2017; Churchill et al., 2020). Strenuous endurance training– even when performed in laboratory conditions– leads to several adaptive responses in lungs tissue mitochondria (Jarmuszkiewicz et al., 2020). This indicates that physical exercise is indeed very challenging to the lungs when performed even in clear air. Air pollution, however, is another factor, which–in our opinion–should receive more attention as a potential health threat to marathon runners. The main reason for this is the fact that running a marathon race enhances minute ventilation by about 7–8 times in the case of an average runner and by about 15 times in the case of an elite runner. This huge increase of V_E during exercise, required to maintain muscle cell energy homeostasis during strenuous exercise (for overview see Zoladz et al., 2013; Zoladz et al., 2014; Grassi, Rossiter & Zoladz, 2015; Zoladz, Grassi & Szkutnik, 2019), increases the inflow of varied PM into the respiratory tract of runners and enhances its deposition therein (see Fig. 7). This leads to an increased risk of varied diseases (see, for instance Hoek et al., 2002; Brook et al., 2010; Du et al., 2016; Jo et al., 2017), including reported acute lungs dysfunctions in marathon runners (see Tiller, 2019). Taking in to account the fact that the air quality in several large cities that organize marathon runs can be questionable (see, for instance Monforti-Ferrario et al., 2018; Dantas et al., 2020; Lal et al., 2020; Rattigan et al., 2020), runners should pay more attention to this fact when planning to participate in marathon races (see also Morici et al., 2020).

According to the considerations we have presented above, in order to minimalize the health risk of the marathon runs, we postulate introducing the concept of the “clean air marathon runs”. Based on our calculations we predict that the PM₁₀ content in the air during “clean air marathon run” should stay below 10 µg m⁻³ in the case of an average runner and it should be lower than 5.5 µg m⁻³ in the case of an elite runner. We propose that only the marathon races which fulfil this standard could constitute a prestige league of the “clean air marathon runs”.

It should be mentioned that recent studies particularly underline negative impact of ultrafine particles (UFP, diameter below 0.1 µm) in the air on various body organs (see e.g., Bevan et al., 2020; Daiber et al., 2020; Niu et al., 2020; Shkirkova et al., 2020). Unfortunately, continuous field measurements of the UFP level in the air are conducted very rarely. At this time, within the framework of our study, we were also unable to perform such measurements. This is why further studies are needed to show the impact of acute exposure to high levels of UFP (e.g., during performance of a marathon race in polluted air) on their deposition in the lungs and on the health of humans.

Summing up: our study showed that running the marathon distance even in relatively clean air drastically increases (from five to nine times) the rate of deposition of varied airborne PM in the respiratory tract of runners, compared to its level at rest. This rate during a marathon race is about 100% greater in elite runners than in average runners (see Fig. 7), but the total PM₁₀ deposition in the respiratory tract during a marathon race in average runners is by about 22% greater (203 / 166 =1.22) than in elite runners. This huge rate of deposition of varied airborne PM in the respiratory tract of runners caused by marathon runs requires more attention, in order to develop a strategy aimed at decreasing the health risk to runners. The simplest yet effective approach aimed at minimizing the level of deposition of varied airborne PM in the respiratory tract of runners consists in avoiding marathon runs in cities, where the air is highly polluted.