Acute Reduction in Spirometry Values After Prolonged Exercise Among Recreational Runners

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BACKGROUND: Prolonged endurance running may acutely reduce spirometric lung values. This study examined changes in spirometry before and immediately after prolonged endurance exercise (running and/or walking). Specifically, we examined potential
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  Acute Reduction in Spirometry Values After Prolonged ExerciseAmong Recreational Runners Gerald S Zavorsky, Ralph D Zimmerman, Derek G Shendell, and Lynda T Goodfellow BACKGROUND: Prolonged endurance running may acutely reduce spirometric lung values. Thisstudy examined changes in spirometry before and immediately after prolonged endurance exercise(running and/or walking). Specifically, we examined potential factors that predict the presence of at least a 10% postexercise reduction in FEV 1 . METHODS: After institutional review board ap-proval, recruitment occurred at a pre-race exposition, where informed consent was obtained.Pre-and post-race spirometry measurements were taken from 79 study subjects who competed ina half-marathon (  n  66) or a marathon (  n  13). Spirometry was performed 1–2 days before themarathon or half-marathon and 25 min after finish the race. RESULTS: We identified a subgroupof 23 subjects with a postexercise decrease in FEV 1  of  > 10%. In this subgroup, the mean post-racevalues for FEV 1 , FVC, and peak expiratory flow were 19–24% lower than the pre-race values. Inthe 56 subjects with a change in FEV 1  of  < 10%, the mean post-race changes in spirometry valueswere not  > 6%. There was no difference between the 2 groups in sex distribution or betweensubjects who completed the half-marathon or the full marathon. For every 1-y increase in age, thelikelihood of developing a postexercise reduction in FEV 1  of at least 10% decreased by nearly 10%(R 2   0.15,  P    .003). CONCLUSIONS: Exercise-induced bronchoconstriction (EIB) is the mostprobable explanation for the reduction in post-race FEV 1 . Prolonged endurance exercise reducedspirometric lung function by  20% in those with EIB. Age was the only predictor for EIB, and EIBdid not affect the finish times among recreational runners and/or walkers.  Key words: distancerunning; lung function; pulmonary; walking; exercise-induced bronchoconstriction; bronchospasm. [Respir Care 2019;64(1):26–33. © 2019 Daedalus Enterprises] Introduction Prolonged endurance running may acutely affect lungfunction in adults. After extended exercise (a marathon,ultra-marathon races [running], or triathlons that last sev-eral hours), pulmonary diffusing capacity, 1-3 FEV 1 , 4-6 FVC, 1,4-13 and maximum inspiratory pressures and/or sus-tained inspiratory mouth pressures 4,8,14,15 have been shownto be acutely reduced. Prolonged exercise could reduceFEV 1  and FVC, particularly in cold weather, due to waterloss from the epithelium, which leads to constriction of theairways, 12 that is, exercise-induced bronchoconstriction(EIB). The FVC and FEV 1  could also be reduced for otherreasons: bronchial epithelial damage, 16 environmental pol- Drs Zavorsky, Zimmerman, and Goodfellow are affiliated with the De-partmentofRespiratoryTherapy,GeorgiaStateUniversity,Atlanta,Geor-gia. Dr. Shendell is affiliated with the Department of Environmental andOccupational Health, School of Public Health, Rutgers University, Pis-cataway, New Jersey, the New Jersey Safe Schools Program, School of Public Health, Rutgers University, Piscataway, New Jersey, and the Ex-posure Measurement and Assessment Division, Environmental and Oc-cupational Health Sciences Institute, Rutgers Biomedical and Health Sci-ences, Piscataway, New Jersey.Financial support provided by a Georgia State University Research Initiationgrant and the Institute of Public Health at Georgia State University.The authors have disclosed no conflicts of interest.Presented as an abstract at the American College of Sports MedicineAnnual Conference, in Minneapolis, Minnesota, May 29–June 2, 2018.Correspondence: Gerald S Zavorsky, Department of Respiratory Therapy,Georgia State University, Urban Life Building, Room 1229, 140 DecaturStreet SE, Atlanta, GA, 30302. E-mail: gerryzavorsky@gmail.com.DOI: 10.4187/respcare.05881 26 R ESPIRATORY  C ARE  •  J ANUARY  2019 V OL  64 N O  1  lutants, 17,18 allergies, respiratory muscle fatigue (as deter-mined by a reduction in maximum voluntary ventilationor maximum inspiratory pressures 4,5,8,14,15 ), and/or pooreffort and/or poor technique. 19 Pulmonary edema, whichaffects diffusing capacity, could also result from intenseexercise. 1,20 Significant reductions in FEV 1  or FVC have been shownto be unaltered after prolonged exercise due to either asmall sample size (ie,  n  4) 15 or a learning effect beforeand after exercise. The airways may also dilate from pro-longedexercise,whichcausesanimprovementinFVC. 21,22 Another possibility is that there may be no actual acutechange in lung function after prolonged exercise. 13,22 As such, the purpose of this study was 3-fold. First, wewanted to determine whether spirometric variables werealtered due to prolonged exercise. Second, if there weresignificant changes in FEV 1  before and after exercise, whatwere the predictive factors? Third, if the subjects demon-strated a reduction in postexercise FEV 1  by at least 10%,was it associated with endurance running performance? Toanswer these questions, we examined changes in spiromet-ric lung function in a cohort of recreational joggers andwalkers before and immediately after the 2008 ING (In-ternationale Nederlanden Groep) Georgia half-marathonand marathon. Methods This study was initially approved by the institutionalreview board of Georgia State University in 2007 (insti-tutional review board H07344). In 2015, institutional re-view board permission was obtained to allow the leadauthor to work on the data for publication (institutionalreview board H16190).Subjects were invited to take part in this study throughrecruitment at the marathon exposition 1–2 d before theevent. Subjects were chosen based on their interest andwillingness to take a short survey and sign a consent form.After voluntarily signing a consent form, anthropometricdata were collected in a private area (ie, height and weightwere measured). Then, by using a portable spirometer, MirSpirolab III (Medical International Research, Rome, Italy),spirometry was performed with each participant by usingthe recommended guidelines published by the joint Amer-ican Thoracic Society/European Respiratory Society task force 23 ; then, 1–2 d later, the same individuals performedspirometry again immediately after the race according tothese guidelines.The interpretation of abnormal spirometric lung func-tion was determined as any value below the lower limit of the normal range, that is, below the fifth percentile for age,sex, height, and ethnicity. 24 The reference equations usedto assess whether spirometry was normal for each subjectwas based on the Global Lung Function Initiative equa-tions for FVC, FEV 1,  and FEV 1 :FVC. 25 For peak expira-toryflows,referenceequationsfromHankinsonetal 26 wereused.We identified a subgroup of subjects with a decrease inFEV 1  of    10% within 30-min post-race compared withpre-race based on the laboratory challenge test criterionfor EIB, defined as a transient narrowing of the lowerairway after exercise in the presence or absence of clini-cally recognized asthma. 27,28 Specifically, a decrease inFEV 1  of 10.0 to 24.9% was deemed mild EIB, a decreasein FEV 1  between 25.0 and 49.9% was deemed moderateEIB, and a decrease in FEV 1  of   50% was deemed severeEIB. 28 Statistical Analyses A 2-tailed independent  t   test was used to examine meandifferences in age, weight, height, and body mass indexbetween the men and women, and for sex differences inspirometric function between the pre-race and the post-race. To examine the mean changes in spirometric func-tion between the pre-race and the post-race, a 2-tailedpaired  t   test was used for the men and then separatelyagain for the women. If any of the variables listed were notnormally distributed, then a 2-tailed Wilcoxon signed-rank test was used to examine the mean changes or differences.As an added analysis, the pre-race percentages of pre-dicted FEV 1 , FVC, FEV 1 :FVC, and peak expiratory flowwere compared with the post-race values by using a paired QUICK LOOKCurrent knowledge Acute changes in lung function triggered by exercisehave been studied as early as the 1920s. Some studiesindicate prolonged exercise reduces spirometric lungfunction, whereas other studies did not report such re-duction. What this paper contributes to our knowledge Four percent of the study subjects had a mild obstruc-tivepatternasdefinedbyanFEV 1 :FVCbelowthelowerlimit normal pre-race. The decrease in FEV 1  by at least10% postexercise in 30% of the subjects was mostlyrepresentative of exercise-induced bronchoconstriction.The only predictor of exercise-induced bronchospasmwas younger age. The presence or absence of exercise-induced bronchospasm was not associated with time tocompletion of the half-marathon or marathon distance,which may be due to the lack of fast finishers in thesample. S PIROMETRY  A FTER  P ROLONGED  E XERCISE R ESPIRATORY  C ARE  •  J ANUARY  2019 V OL  64 N O  1 27  t   test. In this analysis, the percentage of predicted valuescontrolled for age, height, sex, and ethnicity. As well,2-tailed paired  t   tests were used to compare the percentageof predicted spirometry values pre-race in subjects whocompleted the full study (pre- and post-race, group 1) withthe subjects who only completed the pre-race spirometry(group 2). If any of the variables were not normally dis-tributed, then the Mann-Whitney U test was used to com-pare the means between the groups.Forward selection (conditional) binary logistic regres-sion was conducted to determine which independent vari-ables (the event distance, finish time, sex, age, and bodymass index) were predictors of obtaining a postexercisereduction in FEV 1  of at least 10% (yes or no) from exer-cise. Furthermore, a stepwise multiple linear regressionwas used to determine which factors were associated withfinish times. The event distance, sex, age, and body massindex, and whether the subjects had a postexercise reduc-tion in FEV 1  by at least 10% or not (ie, EIB) were used aspotential predictors in the model.The sample size was calculated based on the change inFEV 1  pre- and post-marathon from Maron et al. 7 Betweenpre- and post-marathon, based on a 110-mL reduction inFEV 1 7 and a correlation of 0.5 in FEV 1 , the effect size wascalculated to be 0.54 (G*Power 3.1.9.2, Universita¨t, Kiel,Germany). With an alpha error probability of .05 and astatistical power set at .80, at least 30 subjects would beneeded ( t   test family, the difference between 2 dependentmeans, G*Power 3.1.9.2). Results During the race on March 30, 2008, it was rainy andcool; the mean temperature was 47°F (8°C [range, 6–10°C43–50°F]), the mean relative humidity was 88% (range,76–100%), and the dew point was 41°F (5°C). Overall,2,226 runners and walkers finished the marathon, and8,646 runners and walkers completed the half-marathon. Atotal of 294 participants signed a consent form and com-pleted pre-race spirometry, but only 79 completed bothpre-test and post-test spirometry to constitute the subjects forthis study (group 1). The anthropometric characteristics of these recreational 79 runners are presented in Table 1.There were no differences in the pre-race percentages of predicted spirometry values between the 79 study subjectswho completed both pre- and post-race testing (group 1)and the 215 participants who only completed pre-race test-ing (group 2) (Table 2). Based on the Global Lung Func-tion Initiative reference equations, 25 3 recreational runners(4%) in group 1 who had complete pre- and post-racespirometry data displayed mild obstruction with the pre-race FEV 1 :FVC being below the lower limit of a normalrange, and the FEV 1  of   70% predicted. The subjects ingroup 2 showed a similar pattern.The proportion of female and male finishers in this studycompared with the total number of finishers in the half-marathon (44% men and 56% women) and in the fullmarathon (66% men and 34% women) was similar. Wewere not able to make a comparison of the age distributionbetween the marathon finishers in this study ( n  13) andthe total number of finishers in the marathon (2,226) dueto an insufficient sample size. Of the 79 finishers whocompleted the full study (group 1), 73% were white (92%),3 were Asian (4%), and 3 were African-American (4%).Sixty-sixstudysubjectsfinishedthehalf-marathon:27men,with times that ranged from 92.3 to 209.2 min (mean  SD,131.3  26.0 min); and 39 women, with times that rangedfrom 103.1 to 231.5 min (mean  SD, 145.9  29.8 min).Nine men and 4 women finished the full marathon, withtimes that ranged from 210.8 to 256.3 min (mean    SD, Table 1. Baseline Measurements in the 79 Subjects Who Completed Both Pre- and Post-Race TestingMeasurement Men ( n  36) Women ( n  43) Total (  N   79)Age, mean  SD (range), y 36  9 (22–57) 38  12 (17–59) 37  11 (17–59)Weight, mean  SD (range), kg 79.4  10.2 (58.7–101.6) 63.4  12.3 (47.0–99.4)* 70.8  11.5 (47.0–101.6)Height, mean  SD (range), cm 177  8 (155–191) 164  7 (152–178)* 170  10 (152–191)Body mass index, mean  SD (range), kg/m 2 25.3  3.3 (20.8–36.7) 23.4  3.9 (17.4–36.2)* 24.3  2.6 (17.4–36.7) * Indicates a significant difference among the female subjects relative to the male subjects ( P  .05). Table 2. Comparison of Spirometric Values Pre-Race in the 79Subjects Who Completed Both Pre- and Post-Race Testing(Group 1) With the 215 Subjects Who Only CompletedPre-Race Testing (Group 2)Characteristic Group 1( n  79)Group 2( n  215) P, 2-tailedAge, mean  SD, y 37  11 40  12Men, % 46 52FEV 1 , mean  SD, % predicted 97  17 92  17 .07FVC, mean  SD, % predicted 96  17 92  16 .10FEV 1 :FVC, mean  SD,% predicted101  7 100  9 .39 Because the data were not normally distributed, a Mann-Whitney U test was used to comparethe different groups. S PIROMETRY  A FTER  P ROLONGED  E XERCISE 28 R ESPIRATORY  C ARE  •  J ANUARY  2019 V OL  64 N O  1  232.4  16.6 min), and from 220.3 to 288.9 min (mean  SD, 248.8  31.2 min), respectively. Based on a walk-to-run transition at  128 m/min (7.7 km/h or 4.8 miles/h), 29 12 individuals (18%) in this study predominantly walkedthe half-marathon. None of the 13 marathon finishersaveraged a walking pace. Seventy-six study subjectswere classified as “slow” finishers because the ratio of the sex and age-matched world record time for the eventdivided by their finish time was   0.60, whereas theother 3 subjects were classified as “local class” runners(0.60:0.69). 30,31 There were differences in spirometric lung function be-tween pre- and post-race. Spirometry was measured 25  7 min post-race, and there were differences compared withpre-race values. There were parallel reductions in FEV 1 and FVC from pre- to post-race by   10% (r    0.88, P    .001). The peak expiratory flow decreased by   8%in   30% of the subjects (23/79), with no change inFEV 1 :FVC. Men and women had similar changes in spi-rometric parameters from pre- to post-race. There was nodifference in the proportion of men versus women, with adrop in FEV 1  by  10% post-race (men, 12 of 36 subjects[33%]; women, 11 of 43 subjects [26%]; a difference of 7%, chi-square test    0.46,  P    .50). Twenty-three sub- jects (32  8 y old) had a post-race FEV 1  change that meta widely used criterion for EIB, and, of these, 7 men and4womenhadapostexercisechangeof   25%,whichwouldbe considered moderate EIB. However, when these 23subjects were compared with a subgroup of individualswith a postexercise FEV 1  that changed by  10% ( n  56;40  11 y of age), significant differences in the changes inspirometric function were observed (Table 3). In the sub-group without a post-race decrease in FEV 1  by at least10%, the mean changes in spirometric parameters variedby no more than 6%. In the subgroup with a post-racechange in FEV 1  by at least 10%, there were decreases inFEV 1 , FVC, and peak expiratory flow by  20%.To control for age, height, sex, and ethnicity, the per-cent of predicted values were compared between the pre-and post-race and were stratified by subgroups (Table 4).This finding indicated that there were no clinically mean-ingful changes (even though there were statistically sig-nificant changes) in the percent of predicted FEV 1 , FVC,and FEV 1 :FVC between pre-and post-race in the subgroupof individuals with a postexercise decrease in FEV 1  by  10%. The mean percent of predicted change in any spi-rometric variable was only as high as 5%. However, in thesubgroupofindividualswithapostexercisechangeinFEV 1 by at least 10%, there was a mean decrease in the percentof predicted FEV 1  and FVC, and the peak expiratory flowby 18 to 26% (Table 4).Binary logistic regression analysis ( n    79) indicatedthat age was the best predictor of a likelihood of obtaininga decrease in FEV 1  of    10% postexercise. The modelindicated that, for every 1-y increase in age, the likelihoodof having a postexercise decrease in FEV 1  by 10% or morewas reduced by 7% (95% CI 2–12%,   2 log likeli-hood  86.7, Nagelkerke R 2  0.15,  P  .003). The eventdistance, sex, finish time, and body mass index did notsignificantly add to the model, so these were not includedin the final model.Multiple linear regression analysis ( n    78) indicatedthat the distance run, age, body mass index, and sexpredicted time to completion. Approximately 65% of the variance in the model was accounted for by the distanceof the race (event), whereas age, body mass index, andsex accounted for 7, 5, and 5% of the model, respec-tively (total adjusted R 2  0.82,  P  .001). Whether the Table 3. Pre- and Post-Race Spirometry Values Subdivided by Decreases in  FEV 1   10% and  10%Spirometry Value Pre-Race,mean  SDPost-Race,mean  SDChange, Post-Race  Pre-Race,mean  SD (bootstrapped 95% CI) Change, %  FEV 1   10% ( n  56)*†FEV 1 , L 3.28  0.76 3.18  0.76   0.10  0.16 (  0.14 to  0.06)‡   3FVC, L 3.96  0.95 3.74  0.94   0.22  0.30 (  0.31 to  0.14)‡   6FEV 1 :FVC 0.83  0.05 0.85  0.07   0.02  0.05 (0.01–0.04)‡   2PEF, L/s 6.90  2.23 6.77  2.19   0.13  1.34 (  6.49 to 0.21)   2  FEV 1   10% ( n  23)§  FEV 1 , L 4.05  1.02 3.07  0.68   0.97  0.57 (  1.20 to  0.75)‡   24FVC, L 4.89  1.31 3.82  0.93   1.07  0.87 (  1.43 to  0.73)‡   22FEV 1 :FVC 0.83  0.05 0.81  0.09   0.02  0.08 (  0.05 to 0.01)   2PEF, L/s 8.16  3.03 6.61  2.12   1.55  1.94 (  2.36 to  0.01)‡   19 * These subjects had a decrease in FEV 1  from pre-to post-race by  10%.† Mean  SD half-marathon time, 141.3  31.5 min ( n  47); mean  SD marathon time, 231.9  17.0 min ( n  9).‡ Indicates a significant difference between pre-and post-race ( P  .05).§ These subjects had an FEV 1  that decreased by   10% from pre-to post-race; the numbers for men and women are combined.   Mean  SD half-marathon time, 136.6  22.5 min ( n  19); mean  SD marathon time, 250.1  29.7 min ( n  4).PEF  peak expiratory flow S PIROMETRY  A FTER  P ROLONGED  E XERCISE R ESPIRATORY  C ARE  •  J ANUARY  2019 V OL  64 N O  1 29  subjects had a postexercise decrease in FEV 1  of    10%did not affect the model, so this was omitted. The modelwas as follows:Finish time (min)    106.9    (event)    0.86    (age inyears)    3.6    (body mass index in kg/m 2 )    22.86   (sex)    5.3; adjusted R 2   0.82, standard error of theestimate (SEE)  19.8 min,  P  .001, in which, for sex,0    male, 1    female; and for the event, 0    half-mar-athon, 1    marathon;  n    78. The standardized residualfor one participant exceeded 3.0 SD units, and, thus, thisparticipant was removed from the final model, which left78 subjects in the model.Because adding the event distance (marathon or half-marathon) may dilute the contribution of other, more in-teresting factors, another multiple linear regression wasperformed on just the half-marathon subjects. Approxi-mately 50% of this model was accounted for by body massindex (22%), sex (19%), and age (11%), not whether thesubjects had a postexercise decrease in FEV 1  of    10%.The model was as follows:Half-marathon finish time (min)  3.65  (body massindex in kg/m 2 )    20.83    (sex)    0.86    (age inyears)    5.19; adjusted R 2   0.49, standard error of theestimate (SEE)    20.0 min,    .001, in which, for sex,0  male, 1  female. The standardized residual for oneparticipant exceeded 3.0 SD units and thus that participantwas removed from the model, which left 65 subjects in themodel. Discussion When considering the first research question of whetherprolonged exercise affects spirometric variables, post-racespirometric function had only minor decrements in mostsubjects, but a subgroup of 29% (23/79) had a decrease inFEV 1  of   10%, which met a universal criterion for EIB.This subgroup showed a parallel reduction in the meanFVC along with FEV 1 , which can result from bronchoc-onstriction and associated small airway closure but couldalso reflect reduced inspired volume caused by weakness,fatigue, or reduced motivation.Mild interstitial pulmonary edema triggered by exercisecould also have caused parallel reductions in FEV 1  and FVC.Mildinterstitialpulmonaryedematriggeredbymarathonrun-ning exercise occurs in a majority of subjects 1,20 ; however,severe pulmonary edema triggered by exercise is rare. 32 Forpulmonary edema to occur, the exercise should be exhaustiveand at near-maximum effort. 33 As mentioned previously,nearly 20% of the subjects walked, and most subjects wereslow finishers. It is unlikely that the present study subjectswere of sufficient fitness to stress the pulmonary system tothe extent that moderate-to-severe pulmonary edema wouldoccur. Thus, pulmonary edema was unlikely.Cold temperature can trigger a postexercise reduction inFEV 1 . Reductions in FEV 1  due to cold air are from thereduced water content of the air, rather than the lowtemperature. 34 The inhaled water content from the am-bient conditions of the race was 15% lower than in anindoor exercise laboratory. (The race conditions were47°F (8°C) and  88% humidity, thus the inhaled watercontent would be   6.2 g of water per kg of air [7.4g/m 3 ], which is 15% lower than in an exercise labora-tory, at 68°F (20°C) and 50% humidity [7.3 g/kg or 8.7g/m 3 ] [https://www.lenntech.com/calculators/humidity/ relative-humidity.htm]  Accessed June 12, 2018 ). There- Table 4. Pre- and Post-Race Percent Predicted Spirometry Values Subdivided by Decreases in  FEV 1   10% or  10%Spirometry Value Pre-Race, mean  SD Post-Race, mean  SD Change, Post-Race  Pre-race(bootstrapped 95% CI)*  FEV 1   10% ( n  56)†‡FEV 1 , % predicted 92  12 90  12   3 (  4 to  2)§FVC, % predicted 91  11 86  14   5 (  7 to  3)§FEV 1 :FVC, % predicted 101  7 104  9   3 (1–4)§PEF, % predicted 83  23 82  20   2 (  7 to 4)  FEV 1   10% ( n  23)   ¶FEV 1 , % predicted 109  21 83  15   26 (  32 to  20)§FVC, % predicted 109  22 85  17   24 (  31 to  16)§FEV 1 :FVC, % predicted 100  6 97  11   2 (  6 to 1)PEF, % predicted 95  28 78  25   18 (  24 to  11)§ * Numbers are rounded for simplicity.† These subjects had a decrease in FEV 1  from pre-to post-race by  10%.‡ Mean  half-marathon time, 141.3  31.5 min ( n  47); mean  marathon time, 231.9  17.0 min ( n  9).§ Indicates a significant difference between pre- and post-race ( P  .05).   These subjects had an FEV 1  that decreased by   10% from pre-to post-race. ¶ Mean  half-marathon time, 136.6  22.5 min ( n  19); mean  marathon time, 250.1  29.7 min ( n  4).PEF  peak expiratory flow S PIROMETRY  A FTER  P ROLONGED  E XERCISE 30 R ESPIRATORY  C ARE  •  J ANUARY  2019 V OL  64 N O  1
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