ABSTRACT

Objective: To investigate the validity of field walking tests to identify exercise-induced hypoxemia and to compare cardiorespiratory responses and perceived effort between laboratory-based and field-based exercise tests in subjects with bronchiectasis. Methods: This was a cross-sectional study involving 72 non-oxygen-dependent participants (28 men; mean age = 48.3 ± 14.5 years; and mean FEV1 = 54.1 ± 23.4% of the predicted value). The participants underwent cardiopulmonary exercise testing (CPET) on a treadmill and constant work-rate exercise testing (CWRET) on the same day (1 h apart). In another visit, they underwent incremental shuttle walk testing (ISWT) and endurance shuttle walk testing (ESWT; 1 h apart). Desaturation was defined as a reduction in SpO2 ≥ 4% from rest to peak exercise. Results: CPET results were compared with ISWT results, as were CWRET results with ESWT results. There was no difference in the magnitude of desaturation between CPET and ISWT (−7.7 ± 6.3% vs. −6.6 ± 5.6%; p = 0.10) and between CWRET and ESWT (−6.8 ± 5.8% vs. −7.2 ± 6.3%; p = 0.50). The incremental tests showed an agreement in the magnitude of desaturation in the desaturation and no desaturation groups (42 and 14 participants, respectively; p < 0.01), as did the endurance tests (39 and 16 participants; p < 0.01). The magnitude of desaturation was similar among the participants who did or did not reach at least 85% of the maximum predicted HR. Conclusions: Field exercise tests showed good precision to detect desaturation. Field tests might be an alternative to laboratory tests when the clinical question is to investigate exercise-induced desaturation in subjects with bronchiectasis.

Keywords: Bronchiectasis; Oxygen; Hypoxia; Exercise test.

RESUMO

Objetivo: Investigar a validade dos testes de caminhada de campo para identificar dessaturação durante o exercício, comparando os testes de exercício laboratoriais e clínicos de campo quanto às respostas cardiorrespiratórias e percepção de esforço em indivíduos com bronquiectasia não fibrocística. Métodos: Estudo transversal com 72 participantes não dependentes de oxigênio (28 homens; média de idade: 48,3 ± 14,5 anos; média do VEF1: 54,1 ± 23,4% do previsto). Os participantes foram submetidos ao teste de exercício cardiopulmonar (TECP) incremental em esteira e ao constant work-rate exercise testing (CWRET, teste de exercício com carga constante) em esteira, com intervalo de 1 h. Em outra visita, foram submetidos ao incremental shuttle walk test (ISWT, teste de caminhada incremental) e ao endurance shuttle walk test (ESWT, teste de caminhada de resistência), com intervalo de 1 h. A definição de dessaturação foi uma redução da SpO2 ≥ 4% do repouso ao pico do exercício. Resultados: O TECP e o ISWT resultaram em dessaturação de magnitude comparável (−7,7 ± 6,3% vs. −6,6 ± 5,6%; p = 0,10), assim como o fizeram o CWRET e o ESWT (−6,8 ± 5,8% vs. −7,2 ± 6,3%; p = 0,50). Houve concordância entre o TECP e o ISWT quanto ao número de participantes que apresentaram e não apresentaram dessaturação, respectivamente (42 e 14; p < 0,01), bem como entre o CWRET e o ESWT (39 e 16; p < 0,01). A magnitude da dessaturação foi semelhante nos participantes que atingiram ≥ 85% da FC máxima prevista ou não. Conclusões: Os testes de exercício de campo apresentaram boa precisão para detectar dessaturação. Os testes de campo podem ser uma alternativa aos testes de laboratório quando o objetivo é investigar a dessaturação durante o exercício em indivíduos com bronquiectasia.

Palavras-chave: Bronquiectasia; Oxigênio; Hipóxia; Teste de esforço.

INTRODUCTION



Bronchiectasis is a chronic, progressive and debilitating disease characterized by chronic inflammation, recurrent exacerbations, and progressive loss of pulmonary function. (1) Impaired diffusion capacity and an underlying interstitial lung disease have been reported in bronchiectasis, also contributing to limited pulmonary gas exchange and oxygen desaturation during exertion.(2,3)



Exercise-induced desaturation is a common finding in chronic respiratory diseases,(4) and it has previously been demonstrated in patients with bronchiectasis.(5,6) An official systematic review of the European Respiratory Society and the American Thoracic Society(7) has highlighted the importance of quantifying oxygen desaturation in patients with chronic pulmonary diseases. This recommendation was based on the relationship between oxygen saturation and important outcomes, such as severity of the disease, prognosis, and muscle weakness.(7) In patients with bronchiectasis, poor gas exchange(8) and hypoxemia(9) are predictors of mortality. In this context, patients with exertional desaturation should be monitored more regularly than those without, in order to minimize possible negative consequences of repeated episodes of hypoxemia. Cardiopulmonary exercise testing (CPET) with pulmonary gas exchange analysis is the gold standard to assess the causes of exercise limitation,(10) but it is expensive and requires highly trained personnel. Therefore, CPET is not readily available in clinical practice, and it would not be the test of choice for detecting exertional desaturation.



In previous studies, mostly involving patients with COPD, field walking tests were found to be more sensitive in detecting the magnitude of desaturation than were cycle ergometer tests.(7) A similar finding was observed in subjects with bronchiectasis in whom the magnitude of desaturation was found to be higher during an incremental walk test, such as the incremental shuttle walk test (ISWT), than during an incremental cycle ergometer test, such as CPET.(6) This result is not completely surprising because walking and cycling are completely different activities. However, the degree of exercise-induced desaturation is quite similar between the ISWT and the endurance shuttle walk test (ESWT),(11) as well as between the ISWT and the six-minute walk test (6MWT) in subjects with COPD.(12) Recently, a study has suggested that field walking tests (6MWT, ISWT, and ESWT) can be used interchangeably for the evaluation of the level of exercise-induced desaturation in subjects with non-cystic fibrosis (NCF), because they lead to an equivalent oxygen desaturation.(13) To date, the magnitude of desaturation in similar modalities of exercise (based on walking) but in different contexts (laboratory or field) has yet to be investigated in subjects with bronchiectasis. Our hypothesis was that incremental tests-CPET on a treadmill or ISWT-and tests at a constant workload-constant work-rate exercise testing (CWRET) on a treadmill or ESWT)-would show similar desaturation results. The objective of this study was investigate the validity of the ISWT and ESWT as reliable tools in order to identify exercise-induced desaturation, comparing cardiorespiratory responses and perceived effort/fatigue between laboratory-based and field-based exercise tests in subjects with NCF bronchiectasis.



METHODS



This was a cross-sectional study involving patients with NCF bronchiectasis. The inclusion criteria were being ≥ 18 years of age, not depending on oxygen, being a nonsmoker, presenting with no other chronic lung or cardiovascular diseases, and being in a stable clinical condition (absence of changes in spirometry, dyspnea, cough, general condition, medications and doses, as well as in viscosity and color of secretions in the four weeks preceding entry into the study).(14) Patients who were unable to perform or understand how to perform the proposed tests were excluded, as were those who had decided to withdraw from the study. Bronchiectasis was diagnosed in accordance with followed the British Thoracic Society guideline for NCF bronchiectasis(14) and was confirmed by HRCT.



The study was conducted in two visits. At the first visit, spirometry was performed, BMI was calculated, and the perception of dyspnea was assessed by the modified Medical Research Council (mMRC) scale. (15) In addition, the participants were randomized to perform either CPET and CWRET or ISWT and ESWT. A bronchodilator (albuterol, 400 µg) was administered 15 minutes prior to the tests. At the second visit, seven days later, spirometry was performed again to evaluate clinical stability, and the participants performed the second set of tests . Desaturation was considered present if there was a reduction in SpO2 ≥ 4% from rest to peak exercise.(4)



Spirometry was performed using Ultima CPX (MGC Diagnostics Corporation, Saint Paul, MN, USA). Acceptability and reproducibility criteria adopted for the technical procedures were those recommended by the Brazilian guidelines for lung function testing.(16) We collected data on FVC, FEV1, and FEV1/FVC ratio expressed in absolute values and as a percentage of the predicted value for the Brazilian population.(17)



The CPET was conducted on a treadmill (Millennium Classic; Inbramed/Inbrasport, Porto Alegre, RS, Brazil), using the protocol recommended by Balke and Ware,(18) including constant speed estimated on the basis of the physical fitness of the participant (pulmonary function and baseline dyspnea assessed by the mMRC scale). Increments of one percent in the inclination were imposed every minute. Considering the period of workload increment, the test should last 8-12 min. Measurements of HR (Polar Precision Performance; Polar Electro Inc., Bethpage, NY, USA) and SpO2 (finger pulse oximeter model 9500; Nonin, Plymouth, MN, USA) were continuous during the test. Blood pressure (BP) was measured every 2 min of exercise. The Borg scale was used to rate the perception of dyspnea and leg fatigue(19) at rest and immediately after the end of the exercise.



The ISWT was performed in accordance with the original description(20) in a 10-m hallway. The test was stopped if the participant could not follow the rhythm delivered by the sound. The test was also stopped if the participant showed chest pain, intolerable dyspnea, leg cramps, staggering, diaphoresis, or a pale/ashen appearance.(7) Measurements of HR and SpO2 were continuous during the test (using the same devices described for CPET) and recorded every minute. The BP and the Borg scale scores for the perception of dyspnea and leg fatigue(19) were obtained at rest and immediately after the end of the exercise. The ISWT was performed twice (30 min apart).(7) The best walk distance was expressed in absolute value and as a percentage of the predicted value.(20)



The CWRET was performed one hour after the CPET using the same maximum speed as that used for CPET and a maximum inclination of 75%. Electrocardiogram tracing, HR, and SpO2 were continuously measured during the test. The BP was measured every 2 min of exercise. The Borg scale measured the perception of dyspnea and leg fatigue(19) at rest and immediately after the end of the exercise.



The ESWT was performed as recommended,(21) being performed one hour after the ISWT and using the same interruption criteria as in the ISWT. The ESWT speed was 85% of the peak oxygen uptake during the ISWT, as determined by the following regression equation: oxygen uptake = 4.19 + (0.025 × ISWT distance). (20,21) The HR and SpO2 were continuously measured during the test. The BP and the Borg scales for the perception of dyspnea and leg fatigue(19) were obtained at rest and immediately after the end of the exercise.



The present study was conducted in accordance with the principles of the Declaration of Helsinki, and the Research Ethics Committees of the Nove de Julho University (Reference no. 451538) and the São Paulo State University (Reference no. 0921/11) approved the study. All participants gave written informed consent.



Statistical analysis



We used the Shapiro-Wilk test to determine whether the data had normal or non-normal distribution. Data with parametric distribution were expressed as means and standard deviations, and those with nonparametric distribution (Borg and mMRC scale scores) were expressed as medians and interquartile ranges.



The baseline characteristics between the groups of the participants who did and did not desaturate were compared by the unpaired Student's t-test. Comparisons between CPET and ISWT, as well as between CWRET and ESWT were analyzed by the paired Student's t test for parametric data and by the Wilcoxon test for nonparametric data. The agreement regarding the level of desaturation between CPET and ISWT, as well as between CWRET and ESWT, were analyzed by the chi-square test and Cohen's kappa coefficient (< 0.00, no agreement; 0.00-0.20, slight agreement; 0.21-0.40, fair agreement; 0.41-0.60, moderate agreement; 0.61-0.80, substantial agreement; and 0.81-1.00, perfect agreement).(22) Accuracy, sensibility, specificity, and predictive values (and their respective 95% CIs) were also calculated. The unpaired Student's t-test was used in order to compare SpO2 between the groups of participants who reached ≥ 85% and < 85% of the maximum predicted HR in the incremental and endurance tests. Statistical significance was set at p < 0.05. All statistical analyses were performed using the SPSS Statistics software package, version 20.0 (IBM Corporation, Armonk, NY, USA). The post hoc power of the sample was calculated taking into account the chi-square test, because the basis of the present study was to investigate whether there was an association between desaturation (yes or no) and exercise tests (ISWT vs. CPET and ESWT vs. CWRET). The program G*Power, version 3.1 (Heinrich Heine University, Düsseldorf, Germany)(23) was used for this analysis.



RESULTS



A convenience sample of 92 individuals was recruited; 17 declined to participate. Therefore, 75 were included in the study. Of those, 3 were excluded (2 did not perform all tests, and 1 did not perform the tests correctly). A total of 72 individuals were therefore studied, 28 of whom were male. Most of the participants were normal-weight women with a restrictive and/or obstructive pattern on spirometry (Table 1). With regard to baseline characteristics, only pulmonary function test results differed between those who did or did not present with desaturation (Table 1).



 








A similar behavior in SpO2 was observed, minute by minute, during the incremental and constant workload tests (Figure 1). Most subjects presented with desaturation in all tests (CPET: 74%; ISWT: 65%; CWRET: 64%; and ESWT: 68%). There was no difference in the levels of desaturation between the incremental and constant work-rate walk tests (Table 2). The agreement analysis between CPET and ISWT demonstrated that, of the 72 study participants, 42 presented with desaturation in both tests, and 14 presented with no desaturation in either tests (chi-square test = 17.287; p < 0.01). Comparing CWRET and ESWT, in the sample as a whole, 45 participants presented with desaturation in both tests, and 15 presented with no desaturation in either tests (chi-square test = 16.394; p < 0.01). Retrospective power analysis for both chi-square tests was 0.99. Table 3 summarizes the agreement analysis.



 






 



 








Distance, total exercise time, HR, systolic BP, and perception of dyspnea and leg fatigue were greater in CPET than in ISWT. Similarly, HR, systolic BP, and perception of dyspnea were greater in CWRET than in ESWT (Table 2). Regardless of the test, desaturation was similar among the participants who reached at least 85% of the maximum predicted HR or not (Table 2).



 








DISCUSSION



Field-based exercise tests with similar profiles to those of laboratory-based exercise tests induce similar oxygen desaturation in subjects with bronchiectasis. Cardiorespiratory responses and perception of effort were higher in laboratory-based tests than in field-based tests. Field tests are accurate for the detection of desaturation, demanding less effort from participants than do laboratory-based tests.



Oxygen desaturation cannot commonly be predicted from data obtained at rest. Therefore, exercise testing is important to determine patients who may present with desaturation during exertion.(24) Because CPET is not readily available in clinical practice, field walking tests can be an alternative for the assessment of exercise-induced desaturation, because they have low costs and are easy to perform.(7)



Exercise-induced desaturation has previously been demonstrated in individuals with bronchiectasis.(6) In that population, the level of desaturation is higher during ISWT than during CPET performed on a cycle ergometer.(6) In addition, 21% of patients who showed desaturation during ISWT showed no desaturation during CPET.(6) Similar results have been observed in subjects with COPD.(12,25,26) This finding might have occurred because the incremental CPET was performed on a cycle ergometer. However, an incremental walk test on a treadmill also led to a significantly lower PaO2 than did an incremental cycle ergometer test in subjects with COPD.(27) Therefore, tests performed on a cycle ergometer may underestimate the real desaturation during exercise, making walk tests more sensitive for detecting desaturation.(7)



In the present study, walk tests showed comparable levels of desaturation, even when using different approaches (incremental or endurance exercise tests). One previous study has demonstrated that the level of desaturation in subjects with bronchiectasis was similar during the 6MWT, ISWT, and ESWT (−6.8 ± 6.6; −6.1 ± 6.0; and −7.0 ± 5.4, respectively) and suggested that field walking tests can be used interchangeably for the evaluation of the level of exercise-induced desaturation in those subjects.(13) The same was found in patients with COPD when ISWT was compared with ESWT(11) and 6MWT.(26)



Incremental and endurance exercise tests induced more intense cardiovascular and ventilatory responses, as well as a higher perception of dyspnea, when performed on a treadmill rather than in a corridor/hallway. This is because there are important differences in the gait mechanics between these two forms of walking.(28-31) Treadmill walking requires greater effort and higher energy expenditure to maintain lateral balance control.(29,31,32) Furthermore, most patients are not familiar with that activity.(33) However, in our study, participants were allowed to support themselves using their hands on the treadmill. When subjects walk on a treadmill with hand support, there is a considerable reduction in the demand of walking and their responses change significantly. When hand support is allowed, body balance control increases, and energy consumption and the demand to maintain balance control decreases.(29,31,32) Because hand support was allowed in the present study, exercise time increased, and, consequently, more intense cardiopulmonary responses and higher perception of dyspnea were found in the tests performed on a treadmill.



Subjects that presented with desaturation had worse lung function parameters. This is not a surprising result because exertional desaturation has been associated with lower FEV1 and worse prognosis.(33) We observed that the magnitude of desaturation was similar in the groups of participants who did and did not reach the maximum predicted HR (≥ 85% and < 85%, respectively) in the incremental and constant load walk tests. These findings suggest that the highest cardiac load occurred due to a better performance on the tests rather to a tachycardic response to hypoxemia. When healthy individuals who showed desaturation at the end of the ISWT were compared with those who showed no desaturation at the end of the test, no difference was found in cardiac stress between the groups (88.3 ± 9.3% vs. 87.6 ± 9.6% of maximum predicted HR).(34)



The present study has some limitations. Although we used a convenience sample, a post hoc power analysis indicated that our sample was sufficient to show associations between the tests being compared in relation to our main objective. Pulmonary function analysis was performed only by spirometry. We know that the evaluation of DLCO would increase sensitivity for detecting gas exchange abnormalities. However, the study was not aimed at investigating the determinants of exercise-induced desaturation. Although SpO2 was recorded every minute, a more accurate comparison of the tests regarding the time to achieve desaturation was not possible in our study.



In conclusion, the magnitude of desaturation was similar between incremental walk tests (CPET and ISWT) and constant workload walk tests (CWRET and ESWT), demonstrating that field walking tests showed good precision to detect desaturation. Cardiorespiratory responses, perceived effort, and perception of fatigue were greater in laboratory-based than in field-based exercise tests. In this context, field walking tests might be an alternative to laboratory-based tests when the objective is to investigate exercise-induced desaturation in subjects with bronchiectasis.



AUTHOR CONTRIBUTIONS



CHYO: conception and design of the study; data acquisition, analysis, and interpretation; drafting of the manuscript; and final approval of the version to be published. AJ: data analysis and interpretation; critical revision of the manuscript for important intellectual content; drafting of the manuscript; and final approval of the version to be published. AAC: conception and design of the study; data analysis; critical revision of the manuscript for important intellectual content; and final approval of the version to be published. MIZF: data analysis; critical revision of the manuscript for important intellectual content; and final approval of the version to be published. RAA and SZR: data analysis and interpretation; critical revision of the manuscript for important intellectual content; and final approval of the version to be published. RS: conception and design of the study; data analysis and interpretation; critical revision of the manuscript for important intellectual content; and final approval of the version to be published. SDC: conception and design of the study; data analysis and interpretation; drafting of the manuscript; critical revision of the manuscript for important intellectual content; and final approval of the version to be published.



REFERENCES



1. Lambrech BN, Neyt K, GeurtsvanKessel CH. Pulmonary defense mechanisms and inflammatory pathways in bronchiectasis. Eur Respir Mon. 2011;52:11-21. https://doi.org/10.1183/1025448x.10003210



2. King PT, Holdsworth SR, Freezer NJ, Villanueva E, Farmer MW, Guy P, et al. Lung diffusing capacity in adult bronchiectasis: a longitudinal study. Respir Care. 2010;55(12):1686-1692.



3. Drain M, Elborn JS. Assessment and investigation of adults with bronchiectasis. Eur Respir Mon. 2011;52:32-43. https://doi.org/10.1183/1025448x.10003410



4. Hadeli KO, Siegel EM, Sherrill DL, Beck KC, Enright PL. Predictors of oxygen desaturation during submaximal exercise in 8,000 patients. Chest. 2001;120(1):88-92. https://doi.org/10.1378/chest.120.1.88



5. Jenkins S, Čečins N. Six-minute walk test: observed adverse events and oxygen desaturation in a large cohort of patients with chronic lung disease. Intern Med J. 2011;41(5):416-422. https://doi.org/10.1111/j.1445-5994.2010.02169.x



6. de Camargo AA, Amaral TS, Rached SZ, Athanazio RA, Lanza FC, Sampaio LM, et al. Incremental shuttle walking test: a reproducible and valid test to evaluate exercise tolerance in adults with noncystic fibrosis bronchiectasis. Arch Phys Med Rehabil. 2014;95(5):892-899. https://doi.org/10.1016/j.apmr.2013.11.019



7. Singh SJ, Puhan MA, Andrianopoulos V, Hernandes NA, Mitchell KE, Hill CJ, et al. An official systematic review of the European Respiratory Society/American Thoracic Society: measurement properties of field walking tests in chronic respiratory disease. Eur Respir J. 2014;44(6):1447-1478. https://doi.org/10.1183/09031936.00150414



8. Loebinger MR, Wells AU, Hansell DM, Chinyanganya N, Devaraj A, Meister M, et al. Mortality in bronchiectasis: a long-term study assessing the factors influencing survival. Eur Respir J. 2009;34(4):843-849. https://doi.org/10.1183/09031936.00003709



9. Onen ZP, Gulbay BE, Sen E, Yildiz OA, Saryal S, Acican T, et al. Analysis of the factors related to mortality in patients with bronchiectasis. Respir Med. 2007;101(7):1390-1397. https://doi.org/10.1016/j.rmed.2007.02.002



10. Radtke T, Crook S, Kaltsakas G, Louvaris Z, Berton D, Urquhart DS, et al. ERS statement on standardisation of cardiopulmonary exercise testing in chronic lung diseases. Eur Respir Rev. 2019;28(154):180101. https://doi.org/10.1183/16000617.0101-2018



11. Sandland CJ, Morgan MD, Singh SJ. Detecting oxygen desaturation in patients with COPD: incremental versus endurance shuttle walking. Respir Med. 2008;102(8):1148-1152. https://doi.org/10.1016/j.rmed.2008.03.007



12. Turner SE, Eastwood PR, Cecins NM, Hillman DR, Jenkins SC. Physiologic responses to incremental and self-paced exercise in COPD: a comparison of three tests. Chest. 2004;126(3):766-773. https://doi.org/10.1378/chest.126.3.766



13. Corso SD, Boldorini JC, de Camargo AA, José A, Rached SZ, Athanazio RA, et al. Physiological Responses During Field Walking Tests in Adults with Bronchiectasis. Respir Care. 2020;65(5):618-624. https://doi.org/10.4187/respcare.07171



14. Pasteur MC, Bilton D, Hill AT; British Thoracic Society Bronchiectasis non-CF Guideline Group. British Thoracic Society guideline for non-CF bronchiectasis. Thorax. 2010;65 Suppl 1:i1-i58. https://doi.org/10.1136/thx.2010.136119



15. Kovelis D, Segretti NO, Probst VS, Lareau SC, Brunetto AF, Pitta F. Validation of the Modified Pulmonary Functional Status and Dyspnea Questionnaire and the Medical Research Council scale for use in Brazilian patients with chronic obstructive pulmonary disease. J Bras Pneumol. 2008;34(12):1008-1018. https://doi.org/10.1590/S1806-37132008001200005



16. Sociedade Brasileira de Pneumologia. Diretrizes para testes da função pulmonar. J Pneumol. 2002;28(Suppl 3):S44-S58.



17. Pereira CA, Sato T, Rodrigues SC. New reference values for forced spirometry in white adults in Brazil. J Bras Pneumol. 2007;33(4):397-406. https://doi.org/10.1590/S1806-37132007000400008



18. BALKE B, WARE RW. An experimental study of physical fitness of Air Force personnel. U S Armed Forces Med J. 1959;10(6):675-688. https://doi.org/10.21236/ADA036235



19. Borg GA. Psychophysical bases of perceived exertion. Med Sci Sports Exerc. 1982;14(5):377-381. https://doi.org/10.1249/00005768-198205000-00012



20. Singh SJ, Morgan MD, Scott S, Walters D, Hardman AE. Development of a shuttle walking test of disability in patients with chronic airways obstruction. Thorax. 1992;47(12):1019-1024. https://doi.org/10.1136/thx.47.12.1019



21. Revill SM, Morgan MD, Singh SJ, Williams J, Hardman AE. The endurance shuttle walk: a new field test for the assessment of endurance capacity in chronic obstructive pulmonary disease. Thorax. 1999;54(3):213-222. https://doi.org/10.1136/thx.54.3.213



22. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33(1):159-174. https://doi.org/10.2307/2529310



23. Faul F, Erdfelder E, Buchner A, Lang AG. Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods. 2009;41(4):1149-1160. https://doi.org/10.3758/BRM.41.4.1149



24. Stewart RI, Lewis CM. Arterial oxygenation and oxygen transport during exercise in patients with chronic obstructive pulmonary disease. Respiration. 1986;49(3):161-169. https://doi.org/10.1159/000194875



25. Poulain M, Durand F, Palomba B, Ceugniet F, Desplan J, Varray A. 6-minute walk testing is more sensitive than maximal incremental cycle testing for detecting oxygen desaturation in patients with COPD. Chest. 2003;123(5):1401-1407. https://doi.org/10.1378/chest.123.5.1401



26. Luxton N, Alison JA, Wu J, Mackey MG. Relationship between field walking tests and incremental cycle ergometry in COPD [published correction appears in Respirology. 2013 Oct;18(7):1158]. Respirology. 2008;13(6):856-862. https://doi.org/10.1111/j.1440-1843.2008.01355.x



27. Mahler DA, Gifford AH, Waterman LA, Ward J, Machala S, Baird JC. Mechanism of greater oxygen desaturation during walking compared with cycling in patients with COPD. Chest. 2011;140(2):351-358. https://doi.org/10.1378/chest.10-2415



28. Chang MD, Shaikh S, Chau T. Effect of treadmill walking on the stride interval dynamics of human gait. Gait Posture. 2009;30(4):431-435. https://doi.org/10.1016/j.gaitpost.2009.06.017



29. de Almeida FG, Victor EG, Rizzo JA. Hallway versus treadmill 6-minute-walk tests in patients with chronic obstructive pulmonary disease. Respir Care. 2009;54(12):1712-1716.



30. Almodhy M, Beneke R, Cardoso F, Taylor MJ, Sandercock GR. Pilot investigation of the oxygen demands and metabolic cost of incremental shuttle walking and treadmill walking in patients with cardiovascular disease. BMJ Open. 2014;4(9):e005216. https://doi.org/10.1136/bmjopen-2014-005216



31. Ortega JD, Fehlman LA, Farley CT. Effects of aging and arm swing on the metabolic cost of stability in human walking. J Biomech. 2008;41(16):3303-3308. https://doi.org/10.1016/j.jbiomech.2008.06.039



32. Umberger BR. Effects of suppressing arm swing on kinematics, kinetics, and energetics of human walking. J Biomech. 2008;41(11):2575-2580. https://doi.org/10.1016/j.jbiomech.2008.05.024



33. Holland AE, Spruit MA, Troosters T, Puhan MA, Pepin V, Saey D, et al. An official European Respiratory Society/American Thoracic Society technical standard: field walking tests in chronic respiratory disease. Eur Respir J. 2014;44(6):1428-1446. https://doi.org/10.1183/09031936.00150314



34. Seixas DM, Seixas DM, Pereira MC, Moreira MM, Paschoal IA. Oxygen desaturation in healthy subjects undergoing the incremental shuttle walk test. J Bras Pneumol. 2013;39(4):440-446. https://doi.org/10.1590/S1806-37132013000400007