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Upper Limb Exercises Using Varied Workloads and Their Association With Dynamic Hyperinflation in Patients With COPD
CHEST
Original Research COPD
Upper Limb Exercises Using Varied Workloads and Their Association With Dynamic Hyperinflation in Patients With COPD Marcelo Colucci, PT; Felipe Cortopassi, PT; Elias Porto, PT; Antonio Castro, PT; Eduardo Colucci, PT; Vinicius Carlos Iamonti, PT; Gerson Souza, PT; Oliver Nascimento, MD; and José R. Jardim, MD
Background: Increased ventilation during upper limb exercises (ULE) in patients with COPD is associated with dynamic hyperinflation (DH) and a decrease in inspiratory capacity (IC). The best level of ULE load training is still unknown. Our objective was to evaluate the dynamic hyperinflation development during ULE using three constant workloads. Methods: This was a prospective, randomized protocol involving 24 patients with severe COPD (FEV1 , 50%) performing an endurance symptom-limited arm exercise of up to 20 min in an arm cycloergometer with different workloads (50%, 65%, and 80% of the maximal load). Ventilation, metabolic, and lung function variables (static IC pre-exercise and postexercise) were measured. Results: DH was observed during exercises with 65% (20.23 L) and 80% (20.29 L) workloads (P , .0001). Total time of exercise with 80% workload (7.6 min) was shorter than with 50% (12.5 min) (P. , .0005) and with 65% (10.1 min; not significant). Oxygen consumption percent predicted (Vo2) (P , .01) was lower . with 50% workload than with 80%. Eighty percent workload showed lower work efficiency (Vo2 [mL/kg]/exercise time) than the other two workloads (P , .0001). Conclusion: Different workloads during upper limb exercises showed a direct influence over dynamic hyperinflation and the endurance exercise duration. CHEST 2010; 138(1):39–46 Abbreviations: DH 5 dynamic hyperinflation; IC 5 inspiratory capacity; MVV 5 maximal voluntary ventilation; · · Ve 5 minute ventilation; Vo2 – 5 oxygen consumption
studies have shown that simple activities Recent with upper limbs may hyperinflate patients with COPD mainly due to increased ventilation.1,2 Pulmonary hyperinflation may be a precocious phenomenon
Manuscript received December 2, 2009; revision accepted January 26, 2010. Affiliations: From the Pulmonary Rehabilitation Center (Messrs M. Colucci, Cortopassi, Porto, Castro, E. Colucci, and Iamonti, and Ms Souza), Respiratory Division (Drs Nascimento and Jardim), Universidade Federal de São Paulo/Lar Escola São Francisco; the Physiotherapy Division of São Camilo University (Mr M. Colucci), São Paulo, Brazil; the Division of Pulmonary, Critical Care and Sleep Medicine (Mr Cortopassi), St. Elizabeth’s Medical Center, Tufts University School of Medicine, Boston, MA; and the Physiotherapy Division of Adventist University (Messrs Porto and Castro), São Paulo, Brazil. Funding/Support: This study was funded in part by CAPES, CNPq, and FAPESP, Brazil. Correspondence to: José R. Jardim, MD, Rua Botucatu, 740 - 3o floor Respiratory Division (Pneumologia/Unifesp) 04023-062, São Paulo, Brazil; e-mail: [email protected] www.chestpubs.org
in patients with COPD that may impair their exercise capacity.3 Upper extremities training has been an obligatory component of rehabilitation programs4 as it has been shown that trained arms may improve the quality of activities of daily living.5 Despite the conflicting results that have been presented in the literature related to the different kinds of workloads and also the different upper limb exercise methods,2,6,7 arm cycloergometer has been considered the gold standard equipment for upper extremities training.2,4,6,7 However, upper limb exercises can be limited by dynamic hyperinflation (DH), which may be related to an individual response © 2010 American College of Chest Physicians. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (http://www.chestpubs.org/ site/misc/reprints.xhtml). DOI: 10.1378/chest.09-2878 CHEST / 138 / 1 / JULY, 2010
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of the respiratory system or due to the workload imposed during the training program. Hence, we hypothesized that patients with severe to very severe COPD may develop dynamic lung hyperinflation that is proportional to the workload during arm exercise, which could limit the patient’s training efficiency. The best workload during exercise should be the one that presents the lowest degree of pulmonary DH associated with the best training effectiveness. The aim of this study was to evaluate the metabolic and ventilatory parameters and the development of dynamic pulmonary hyperinflation during a session of upper limb exercise in an arm cycloergometer with workloads equivalent to 50%, 65%, and 80% of a maximal incremental test and understand which factors are associated to the exercise limitation. Materials and Methods Subjects In a prospective study, we evaluated 24 patients with COPD who attend the COPD Outpatient Clinic of the Federal University of São Paulo/Lar Escola São Francisco, Brazil. The study was approved by the ethics institutional committee and all patients signed an informed consent. Inclusion and Exclusion Criteria: Inclusion criteria were clinical diagnosis of severe to very severe COPD (FEV1 , 50% predicted) according to American Thoracic Society/European Respiratory Society criteria,8,9 clinical stability (no exacerbation over the previous 30 days), and no previous participation in a pulmonary rehabilitation program. Exclusion criteria were current smoker or nonsmoker of , 1 year; severe comorbidities, such as heart, orthopedic, or neurologic diseases; extreme difficulty or inability to perform the inspiratory capacity (IC) maneuver; and required oxygen supplementation because of oxygen saturation , 80% at rest or during exercise.
were measured. Spirometry was repeated 15 min after the administration of a bronchodilator (albuterol 400 mg); predicted values for FVC and FEV1 were calculated according to the third National Health and Nutrition Examination Survey.13 Severity of disease was classified according to Global Initiative for Chronic Obstructive Lung Disease stages.8,9 Inspiratory Capacity Measurement: Patients used a nasal clip and breathed through a mouthpiece connected to the circuit of the KoKo equipment, which numerically and graphically recorded tidal volume levels. When stability of the end-expiratory volume was reached, the patient was asked to take a deep breath to total lung capacity. A minimum of three maneuvers (maximum of eight) was performed, and, in order to be considered reproducible, two curves should not present a variation more than 5% or 150 mL.14-16 Inspiratory capacity was registered as the value measured between the line of the end expiratory volume and total pulmonary capacity. The higher value of two reproducible curves was considered for analysis. Pulmonary hyperinflation was considered when after the test there was a reduction in the IC of 10% and/or a reduction of . 150 mL, related to the basal value.16 Arm Exercise Tests: An arm cycloergometer was used for the tests (Siemens-Elma; Solina, Sweden). For all tests subjects were seated and the arm crank height was adjusted so that the fulcrum of the pedals was at the level of the glenohumeral joint. Each patient was familiarized with the equipment before the test. During the incremental test, workloads were increased by 2.5 W every minute until the subjects indicated that they could not continue. Subjects exercised at 50 to 60 rpm and breathed through a calibrated mask flow sensor with expired gas sampled on a breath-by-breath basis (K4b2) · so that oxygen consumption (Vo2), carbon dioxide production, min· ute ventilation (Ve), tidal volume, and respiratory rate could be determined.17 Maximal voluntary ventilation (MVV) was determined · by multiplying FEV1 by 3518 so that Ve/MVV could be determined. Heart rate and pulse oxygen saturation were obtained using a forehead probe attached to a pulse oximeter (N200; Nellcor; Hayward, CA). A modified Borg scale reading 0 (nothing at all) to 10 (maximal) was assessed to evaluate subjects’ dyspnea and rate of perceived exertion.19,20 Nutritional status was assessed by BMI dividing weight in kilograms by height in square meters. Dyspnea score was measured according to the Modified Medical Research Council index consisting of 5 points.21
Protocol At the first visit the slow vital capacity mode was performed to obtain the IC according to the method discussed by Belman et al.10 Immediately afterward, all patients performed a symptom-limited, incremental, supported arm exercise test to peak work in a cycloergometer, without the use of a bronchodilator. Expired gases were analyzed using portable equipment (K4b2; Cosmed; Rome, Italy). Immediately after the incremental test the IC was measured again. At the following three visits the patients performed a randomized symptom-limited, constant-load, supported arm exercise test limited up to 20 min11,12 with a 24-h interval. The work rate for the constant-load test was set at 50%, 65%, and 80% of the peak work rate. Immediately before and at the end of the endurance arm exercise test IC was measured. Two investigators were present in each one of the tests: The principal investigator was present in all tests; the other investigator was assigned just for one of four tests, never repeating the same patient. The test was never ended without the agreement of the two investigators. Spirometry: Three acceptable spirometric evaluations (KoKo; Occupational Health Dynamics; Birmingham, AL) were done following American Thoracic Society/European Respiratory Society recommendations. FVC, slow vital capacity, and FEV1 in liters
Data Analysis According to the variability of IC measurements from various studies10,22,23 a sample of 16 subjects with a 0.05 and b 0.20 power would be necessary. Data are shown in mean and SD. Generalized linear models were used to analyze the workload effects in metabolic and ventilatory variables. As the workload was randomized at the three visits, period (visit) and sequence effects as well as interaction with workload were evaluated. Moreover, odds ratio test was used to assess variables that may lead to DH Statistical significance was determined by P , .05.
Results The demographic and spirometric characteristics of the 24 patients are shown in Table 1. The mean maximum workload at the end of the cycloergometer incremental test was 22 6 10.4 W. The IC behavior during the three tests is shown in Figure 1. Metabolic, ventilatory, and lung function
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Table 1—Demographic and Spirometric Characteristics of the Sample Variables (N 5 24)
Subjects
Male (female), n Age, y Weight, kg BMI, kg/m2 FEV1/FVC FEV1, % predicted FEV1, L FVC, % predicted Inspiratory capacity, % predicted Modified Medical Research Council score MVV, L
17 (7) 64.8 6 8 70.5 6 13 25.5 6 4.1 0.35 6 8 35.5 6 8 1.10 6 0.33 79.1 6 12 76.8 6 18 2.7 6 0.8 41.1 6 12.5
Values given as mean 6 SD unless otherwise noted. MVV 5 maximum ventilatory capacity (FEV1 3 37.5).
variables during the incremental test and during the three different endurance tests are presented in Table 2. The associations between the endurance times during the three different workloads are presented in Figure 2. The behavior of expiratory time and respiratory frequency from the exercise rest until the isotime of the three workloads is shown in Figures · 3 and 4, respectively. The ratio between Vo2 and total exercise time in each workload (work efficiency) is shown in Figure 5. The odds ratios of the development of DH during arm exercises are shown in Table 3. Discussion To our knowledge, our study is the first one to evaluate the development of dynamic pulmonary hyperinflation caused by upper limb exercises using different workloads. Our results entitle the following considerations: (1) the workloads that patients with COPD were submitted to during endurance exercise directly influenced the decrease in the IC at the end of the exercises; (2) the time to perform the exercises was negatively influenced by the workload to which they were submitted; and (3) the decrease in the IC was a consequence of the association between a reduction · in the expiratory time and the increase in the Ve which probably increased the elastic pulmonary work and reduced muscular efficiency. The Influence of the Different Workloads on the Development of Dynamic Pulmonary Hyperinflation and Endurance Capacity An important finding of this study is the influence that the workload of the exercise had on the development of dynamic pulmonary hyperinflation. It is well determined in the literature that lower limb training must be performed at high workloads, approximately 60% to 80% of the load obtained in a maximal exercise test, close to the patient’s anaerobic threshold. It has www.chestpubs.org
been shown that these workloads may cause pulmonary hyperinflation.3,12,24,25 However, although upper limb training is considered to be an obligatory exercise in a rehabilitation program, the literature is not clear about the workload that should be used for this training. Ries et al12 used the proprioceptive neuromuscular facilitation method for upper limb training in patients with COPD but failed to describe the load the patients were submitted to. The physiologic basis for upper limb training may be the same as for that of the lower limb. In this case, high loads, close to the anaerobic threshold of the muscle groups, should be used. But the choice of a high load for upper limb training may · cause high Ve because of the metabolic demands. Martinez et al26 showed that the cycloergometer incremental upper limb exercise reaches the anaerobic threshold faster than that of a lower limb exercise. In addition, studies that evaluated pulmonary hyperinflation development during upper limb training with high load confirmed a reduction in the IC,1,2,17 but no evaluation on the influence of the different workloads was done. The intensive work done by the arm muscles during the exercise with a constant workload at 80% of the maximum showed that this workload may be excessive to commence treatment in patients with light and moderate COPD.17 Gigliotti et al2 showed that pulmonary hyperinflation with concomitant reduction in the IC reached approximately 1 L in patients with COPD when they performed arm exercises with a workload of 80% of the maximum obtained. Pulmonary hyperinflation may occur in approximately 50% of the patients doing exercises with a lower workload (50% of the maximum obtained).1 However, none of these authors studied the development of pulmonary hyperinflation in the same group of patients using varied loads to evaluate if this response was connected to the load itself or to the patient’s response. We observed that an increased proportion of patients hyperinflated as they exercised increasing loads; 41.1% of our patients presented DH with a workload of 50%, whereas 66.6% and 79.1% hyperinflated while exercising with workloads of 65% and 80%, respectively. This shows that pulmonary hyperinflation during the arm exercises is more relevant to the workload that the patient is submitted to than to the patient. The fact that the time of endurance inversely decreased when the workload was increased is a direct consequence of the workload that the patient was submitted to. The maximum time programmed for a complete set of endurances exercise was 20 min. 6 In a study that exercised the upper limbs of patients with light and moderate COPD with a workload at 80% of the maximum, the average endurance time was 7.1 min.17 This exercise time reduction involving unsupported arm exercises was also observed in patients who presented severe conditions and related CHEST / 138 / 1 / JULY, 2010
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Figure 1. Inspiratory capacity before and after the submaximum exercise with the upper limbs in different loads.
to the reduction in the IC (r 5 0.67; P 5 .0008).27 Again, these authors did not relate the endurance exercise reduction with the different workloads to which the patient was submitted. In our study the endurance time during the exercise with the workload of 50% was 12.5 min, reducing to 10.1 min with a workload of 65% and to 7.6 min with a workload of 80%, clearly demonstrating a reduction in the exercise capacity in relation to the increase in the workload.
Mechanisms That Contributed to the Development of Dynamic Pulmonary Hyperinflation and to the Reduction in the Endurance of the Upper Limbs The mechanisms through which patients with COPD develop dynamic pulmonary hyperinflation and limit their exercise capacity are usually related to: · (1) increase of the Ve, (2) reduction in the expiratory time, (3) possible increase of the elastic work, and
Table 2—Comparison Among Three Exercise Sequences With Different Workloads Variables Hyperinflated patients, No./total (%) IC rest, L DIC, L Total time, min Final Borg score, arms Final Borg score, dyspnea Inspiratory time, s Expiratory time, s TI/TTOT ratio RR, breaths/min · Vo2max, mL/min/kg · Vo2max, % predicted · Ve, L/min · Ve/MVV · Ve/Vo2 · Vo2max/total time, mL/min · Ve/total time, L/min
Incremental Test
50% Endurance Workload
65% Endurance Workload
80% Endurance Workload
P Value
19/24 (79.1) 2.15 6 0.56 0.23 6 0.21 10.1 6 4.3 7.1 6 2.8 7 6 2.8 0.78 6 0.19 1.30 6 0.28 0.40 6 0.04 30.0 6 5.6 1039.9 6 252.1 60.5 6 16.5 38.7 6 10 0.96 6 0.21 35.8 6 9.8 … …
10/24 (41.1) 2.16 6 0.48 0.10 6 0.1a 12.5 6 6 7.8 6 2.4 7.7 6 2.3 0.83 6 0.29 1.42 6 0.42 0.35 6 0.05a 28.8 6 6.0 963.4 6 208.6 56.7 6 17.7a 36.9 6 9.7 0.93 6 0.26 36.1 6 7.9 99.5 6 54.9a 3.89 6 2.95
15/24 (66.6) 2.18 6 0.57 0.24 6 0.23b 10.1 6 5.6 7.5 6 2.2 7.1 6 2.6 0.77 6 0.29 1.38 6 0.34 0.37 6 0.04 29.2 6 6.0 993.8 6 279.4 58.3 6 18.5 39.4 6 11.2 0.99 6 0.28 37.9 6 8.9 123.9 6 59.9c 5.03 6 3.17
19/24 (79.1) 2.14 6 0.53 0.29 6 0.22 7.6 6 5.1 7.3 6 2.5 7.3 6 2.4 0.79 6 0.19 1.29 6 0.29 0.38 6 0.05 29.8 6 5.9 1038.9 6 264.8 60.9 6 19.1 38.4 6 11.4 0.95 6 0.23 35.4 6 9.4 170.3 6 78.6 6.56 6 3.45
, .0014 .25 , .0001 , .0005 .34 .47 .63 .07 .01 .65 .66 , .01 .08 .21 .06 , .0001 .01
Values expressed in mean 6 SD unless otherwise noted. ANOVA 5 analysis of variance; ΔIC 5 inspiratory capacity variation; IC 5 inspiratory · · capacity; RR 5 respiratory rate; TI/TTOT 5 inspiratory time/total time; Ve 5 minute ventilation; Vo2 5 oxygen consumption. See Table 1 legend for expansion of other abbreviation. aP , .05 (ANOVA between endurance 50% vs 80%). bP , .05 (ANOVA between endurance 50% vs 65%). cP , .05 (ANOVA between endurance 65% vs 80%). 42
Original Research
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Figure 2. Comparison between the endurance times during the three different workloads.
(4) decrease of the work efficiency. Our patients, independently of the load they were exercising with, usually interrupted the exercise by the time they · achieved a Ve of approximately 39 L/min, which cor· responds to 97% of MVV. The high Ve/MVV ratio for the three workloads shows that these patients had a very low ventilatory reserve, demonstrating the low ventilatory reserve that they could dispose of, which is known as one of the factors that limit exercise in patients with chronic lung disorders. Shortening of expiratory time is one of the main reasons for patients with COPD to hyperinflate during the accomplishment of a task that requires a certain load demand.23 The association of reduced lung
elastic recoil with a shorter expiratory time will make the exhaled air volume lower than the inhaled volume leaving a residue within the lungs. This phenomenon repeats itself to the point where the sum of these residues establishes a greater functional residual capacity inducing the respiratory system to reach a new balance state. The reduction of the IC, as may be observed in Figure 1, reflects that dynamic lung hyperinflation occurred.28 The evaluation of expiratory times along the exercise session minute by minute (Fig 3) clearly demonstrates that they behave quite differently. At the isotime 4, 5, 6, and 7 min there is a clear dissociation of the curves with significant statistical differences between them: the 80% workload presents the shortest expiratory time, the 65% an intermediate value, and the 50% the lowest reduction. In addition, as seen in Figure 4 , the respiratory
Figure 3. Comparison of the expiratory time in different workloads and at the isotime.
Figure 4. Comparison of the respiratory frequency in different workload and at the isotime.
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· Figure 5. Work efficiency in the three different workloads. Vo2 5 oxygen consumption.
frequency presented the same behavior. The association of the progressive shortening of the expiratory time and the increase in the respiratory frequency most probably is the reason for the increase in the dynamic pulmonary hyperinflation as the workloads increased. DH causes breathing discomfort and shortening of endurance time. Patients usually ended the exercise when they · reached a Vo2 value very close to their maximum · upper limb Vo2, tested before the exercises. This shows an increasing O2 consumption per minute of exercise as the workload was increased. In other words, as the workload increases there is a decrease in the work efficiency, which corroborates with the reduction of the endurance time (Fig 5). IC was statically measured using a validated method. In addition to its low cost, it is reproducible,29 can be easily carried out after an exhausting exercise, and requires little cooperation from the patient. This method has been used by Belman et al10 and O’Donnell et al28 to measure the IC after lower limb exercises. Although the precise criteria for dynamic pulmonary hyperinflation requires the measurements of the total Table 3—Pulmonary Hyperinflation Odds for Workloads of 50%, 65%, and 80% of the Peak Variables DH 80% vs DH 50% DH 65% vs DH 50% DH 80% vs DH 65%
Odds Ratio
95% CI
P Value
1.9 1.5 1.2
1.1-3.1 0.85-2.6 0.87-1.8
.009 .12 .17
DH 50% 5 dynamic hyperinflation in 50% workload; DH 65% 5 dynamic hyperinflation in 65% workload; DH 80% 5 dynamic hyperinflation in 80% workload.
lung capacity, and the ratio of functional residual capacity to the total lung capacity, O’Donnell et al28 and Yan et al15 demonstrated that the changes in the IC obtained using this method reflect dynamic residual volume alterations in a reproducible and accurate way.15 In our study, the basal value of the IC did not differ during the 4 days of the procedure (data not shown), demonstrating the stability and accuracy of the method. All measurements were performed at the same time of day, thus there was no influence of the circadian cycle on pulmonary function. Cycloergometer was used in the study as it is considered a gold standard in exercises that involve upper limbs.6 The arm cycloergometer allows more control over the load the patient is submitted to, a better synchronism of the movements when turning the lever, and a standardization of the speed. The originality of this article lies in the nonexistence of cross-over trials in the researched literature that compare the behavior of dynamic pulmonary hyperinflation in the same patient with COPD exercising their upper limbs with a cycloergometer. Muscle training of the upper limbs is routinely recommended for patients with COPD. Although pulmonary rehabilitation is indicated for all patients with COPD, it is more commonly used in patients with severe and very severe forms of the disease—those who present a higher level of pulmonary hyperinflation. Higher workloads clearly lead to lower endurance time, which is clearly related to higher hyperinflation and a lesser work efficiency. Based on our study, it is believable that training using an arm cycloergometer with a low workload (50% of the maximum) can be more
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feasible for the patients. This workload has shown to be more efficient than the other loads, and the levels of · Vo2 obtained with this workload were closer to those found by Velloso et al30 in patients with COPD performing activities of daily living. There is always a concern when a cross-over trial is carried out, especially related to period and sequence effects.31 Period and sequence effects were not significant for the studied variables, except for endurance time. An interaction effect of workload and period was found (P 5 .039) where a difference between 50% and 80% was detected. This can be explained by the fact that two patients reached 20 min with 80%, and because of the small sample size, these observations increased the mean. In our point of view, this interaction occurred by chance and period and sequence effects can be omitted for the all models once they are statistically evaluated. However, there are some limitations to this study: (1) the nonexistence of a control group to compare with the data found in patients with COPD; however, each patient was his or her own control; (2) not having used a measurement that could dynamically measure the IC on line during the exercise; this has not influenced the results as our aim was to evaluate the IC variation before and after the arm exercises. We conclude that higher workloads during a set of upper limb exercises in patients with severe and very severe COPD directly influence the reduction of the IC, causing dynamic pulmonary hyperinflation. Dynamic pulmonary hyperinflation is directly related to a less efficient performance during the exercises and to a reduction in the endurance time. Acknowledgments Author contributions: Mr M. Colucci: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Mr Cortopassi: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Mr Porto: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Mr Castro: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Mr E. Colucci: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Mr Iamonti: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Ms Souza: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Dr Nascimento: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Dr Jardim: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, manuscript preparation, and guidance. www.chestpubs.org
Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.
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Original Research COPD
Upper Limb Exercises Using Varied Workloads and Their Association With Dynamic Hyperinflation in Patients With COPD Marcelo Colucci, PT; Felipe Cortopassi, PT; Elias Porto, PT; Antonio Castro, PT; Eduardo Colucci, PT; Vinicius Carlos Iamonti, PT; Gerson Souza, PT; Oliver Nascimento, MD; and José R. Jardim, MD
Background: Increased ventilation during upper limb exercises (ULE) in patients with COPD is associated with dynamic hyperinflation (DH) and a decrease in inspiratory capacity (IC). The best level of ULE load training is still unknown. Our objective was to evaluate the dynamic hyperinflation development during ULE using three constant workloads. Methods: This was a prospective, randomized protocol involving 24 patients with severe COPD (FEV1 , 50%) performing an endurance symptom-limited arm exercise of up to 20 min in an arm cycloergometer with different workloads (50%, 65%, and 80% of the maximal load). Ventilation, metabolic, and lung function variables (static IC pre-exercise and postexercise) were measured. Results: DH was observed during exercises with 65% (20.23 L) and 80% (20.29 L) workloads (P , .0001). Total time of exercise with 80% workload (7.6 min) was shorter than with 50% (12.5 min) (P. , .0005) and with 65% (10.1 min; not significant). Oxygen consumption percent predicted (Vo2) (P , .01) was lower . with 50% workload than with 80%. Eighty percent workload showed lower work efficiency (Vo2 [mL/kg]/exercise time) than the other two workloads (P , .0001). Conclusion: Different workloads during upper limb exercises showed a direct influence over dynamic hyperinflation and the endurance exercise duration. CHEST 2010; 138(1):39–46 Abbreviations: DH 5 dynamic hyperinflation; IC 5 inspiratory capacity; MVV 5 maximal voluntary ventilation; · · Ve 5 minute ventilation; Vo2 – 5 oxygen consumption
studies have shown that simple activities Recent with upper limbs may hyperinflate patients with COPD mainly due to increased ventilation.1,2 Pulmonary hyperinflation may be a precocious phenomenon
Manuscript received December 2, 2009; revision accepted January 26, 2010. Affiliations: From the Pulmonary Rehabilitation Center (Messrs M. Colucci, Cortopassi, Porto, Castro, E. Colucci, and Iamonti, and Ms Souza), Respiratory Division (Drs Nascimento and Jardim), Universidade Federal de São Paulo/Lar Escola São Francisco; the Physiotherapy Division of São Camilo University (Mr M. Colucci), São Paulo, Brazil; the Division of Pulmonary, Critical Care and Sleep Medicine (Mr Cortopassi), St. Elizabeth’s Medical Center, Tufts University School of Medicine, Boston, MA; and the Physiotherapy Division of Adventist University (Messrs Porto and Castro), São Paulo, Brazil. Funding/Support: This study was funded in part by CAPES, CNPq, and FAPESP, Brazil. Correspondence to: José R. Jardim, MD, Rua Botucatu, 740 - 3o floor Respiratory Division (Pneumologia/Unifesp) 04023-062, São Paulo, Brazil; e-mail: [email protected] www.chestpubs.org
in patients with COPD that may impair their exercise capacity.3 Upper extremities training has been an obligatory component of rehabilitation programs4 as it has been shown that trained arms may improve the quality of activities of daily living.5 Despite the conflicting results that have been presented in the literature related to the different kinds of workloads and also the different upper limb exercise methods,2,6,7 arm cycloergometer has been considered the gold standard equipment for upper extremities training.2,4,6,7 However, upper limb exercises can be limited by dynamic hyperinflation (DH), which may be related to an individual response © 2010 American College of Chest Physicians. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (http://www.chestpubs.org/ site/misc/reprints.xhtml). DOI: 10.1378/chest.09-2878 CHEST / 138 / 1 / JULY, 2010
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of the respiratory system or due to the workload imposed during the training program. Hence, we hypothesized that patients with severe to very severe COPD may develop dynamic lung hyperinflation that is proportional to the workload during arm exercise, which could limit the patient’s training efficiency. The best workload during exercise should be the one that presents the lowest degree of pulmonary DH associated with the best training effectiveness. The aim of this study was to evaluate the metabolic and ventilatory parameters and the development of dynamic pulmonary hyperinflation during a session of upper limb exercise in an arm cycloergometer with workloads equivalent to 50%, 65%, and 80% of a maximal incremental test and understand which factors are associated to the exercise limitation. Materials and Methods Subjects In a prospective study, we evaluated 24 patients with COPD who attend the COPD Outpatient Clinic of the Federal University of São Paulo/Lar Escola São Francisco, Brazil. The study was approved by the ethics institutional committee and all patients signed an informed consent. Inclusion and Exclusion Criteria: Inclusion criteria were clinical diagnosis of severe to very severe COPD (FEV1 , 50% predicted) according to American Thoracic Society/European Respiratory Society criteria,8,9 clinical stability (no exacerbation over the previous 30 days), and no previous participation in a pulmonary rehabilitation program. Exclusion criteria were current smoker or nonsmoker of , 1 year; severe comorbidities, such as heart, orthopedic, or neurologic diseases; extreme difficulty or inability to perform the inspiratory capacity (IC) maneuver; and required oxygen supplementation because of oxygen saturation , 80% at rest or during exercise.
were measured. Spirometry was repeated 15 min after the administration of a bronchodilator (albuterol 400 mg); predicted values for FVC and FEV1 were calculated according to the third National Health and Nutrition Examination Survey.13 Severity of disease was classified according to Global Initiative for Chronic Obstructive Lung Disease stages.8,9 Inspiratory Capacity Measurement: Patients used a nasal clip and breathed through a mouthpiece connected to the circuit of the KoKo equipment, which numerically and graphically recorded tidal volume levels. When stability of the end-expiratory volume was reached, the patient was asked to take a deep breath to total lung capacity. A minimum of three maneuvers (maximum of eight) was performed, and, in order to be considered reproducible, two curves should not present a variation more than 5% or 150 mL.14-16 Inspiratory capacity was registered as the value measured between the line of the end expiratory volume and total pulmonary capacity. The higher value of two reproducible curves was considered for analysis. Pulmonary hyperinflation was considered when after the test there was a reduction in the IC of 10% and/or a reduction of . 150 mL, related to the basal value.16 Arm Exercise Tests: An arm cycloergometer was used for the tests (Siemens-Elma; Solina, Sweden). For all tests subjects were seated and the arm crank height was adjusted so that the fulcrum of the pedals was at the level of the glenohumeral joint. Each patient was familiarized with the equipment before the test. During the incremental test, workloads were increased by 2.5 W every minute until the subjects indicated that they could not continue. Subjects exercised at 50 to 60 rpm and breathed through a calibrated mask flow sensor with expired gas sampled on a breath-by-breath basis (K4b2) · so that oxygen consumption (Vo2), carbon dioxide production, min· ute ventilation (Ve), tidal volume, and respiratory rate could be determined.17 Maximal voluntary ventilation (MVV) was determined · by multiplying FEV1 by 3518 so that Ve/MVV could be determined. Heart rate and pulse oxygen saturation were obtained using a forehead probe attached to a pulse oximeter (N200; Nellcor; Hayward, CA). A modified Borg scale reading 0 (nothing at all) to 10 (maximal) was assessed to evaluate subjects’ dyspnea and rate of perceived exertion.19,20 Nutritional status was assessed by BMI dividing weight in kilograms by height in square meters. Dyspnea score was measured according to the Modified Medical Research Council index consisting of 5 points.21
Protocol At the first visit the slow vital capacity mode was performed to obtain the IC according to the method discussed by Belman et al.10 Immediately afterward, all patients performed a symptom-limited, incremental, supported arm exercise test to peak work in a cycloergometer, without the use of a bronchodilator. Expired gases were analyzed using portable equipment (K4b2; Cosmed; Rome, Italy). Immediately after the incremental test the IC was measured again. At the following three visits the patients performed a randomized symptom-limited, constant-load, supported arm exercise test limited up to 20 min11,12 with a 24-h interval. The work rate for the constant-load test was set at 50%, 65%, and 80% of the peak work rate. Immediately before and at the end of the endurance arm exercise test IC was measured. Two investigators were present in each one of the tests: The principal investigator was present in all tests; the other investigator was assigned just for one of four tests, never repeating the same patient. The test was never ended without the agreement of the two investigators. Spirometry: Three acceptable spirometric evaluations (KoKo; Occupational Health Dynamics; Birmingham, AL) were done following American Thoracic Society/European Respiratory Society recommendations. FVC, slow vital capacity, and FEV1 in liters
Data Analysis According to the variability of IC measurements from various studies10,22,23 a sample of 16 subjects with a 0.05 and b 0.20 power would be necessary. Data are shown in mean and SD. Generalized linear models were used to analyze the workload effects in metabolic and ventilatory variables. As the workload was randomized at the three visits, period (visit) and sequence effects as well as interaction with workload were evaluated. Moreover, odds ratio test was used to assess variables that may lead to DH Statistical significance was determined by P , .05.
Results The demographic and spirometric characteristics of the 24 patients are shown in Table 1. The mean maximum workload at the end of the cycloergometer incremental test was 22 6 10.4 W. The IC behavior during the three tests is shown in Figure 1. Metabolic, ventilatory, and lung function
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Table 1—Demographic and Spirometric Characteristics of the Sample Variables (N 5 24)
Subjects
Male (female), n Age, y Weight, kg BMI, kg/m2 FEV1/FVC FEV1, % predicted FEV1, L FVC, % predicted Inspiratory capacity, % predicted Modified Medical Research Council score MVV, L
17 (7) 64.8 6 8 70.5 6 13 25.5 6 4.1 0.35 6 8 35.5 6 8 1.10 6 0.33 79.1 6 12 76.8 6 18 2.7 6 0.8 41.1 6 12.5
Values given as mean 6 SD unless otherwise noted. MVV 5 maximum ventilatory capacity (FEV1 3 37.5).
variables during the incremental test and during the three different endurance tests are presented in Table 2. The associations between the endurance times during the three different workloads are presented in Figure 2. The behavior of expiratory time and respiratory frequency from the exercise rest until the isotime of the three workloads is shown in Figures · 3 and 4, respectively. The ratio between Vo2 and total exercise time in each workload (work efficiency) is shown in Figure 5. The odds ratios of the development of DH during arm exercises are shown in Table 3. Discussion To our knowledge, our study is the first one to evaluate the development of dynamic pulmonary hyperinflation caused by upper limb exercises using different workloads. Our results entitle the following considerations: (1) the workloads that patients with COPD were submitted to during endurance exercise directly influenced the decrease in the IC at the end of the exercises; (2) the time to perform the exercises was negatively influenced by the workload to which they were submitted; and (3) the decrease in the IC was a consequence of the association between a reduction · in the expiratory time and the increase in the Ve which probably increased the elastic pulmonary work and reduced muscular efficiency. The Influence of the Different Workloads on the Development of Dynamic Pulmonary Hyperinflation and Endurance Capacity An important finding of this study is the influence that the workload of the exercise had on the development of dynamic pulmonary hyperinflation. It is well determined in the literature that lower limb training must be performed at high workloads, approximately 60% to 80% of the load obtained in a maximal exercise test, close to the patient’s anaerobic threshold. It has www.chestpubs.org
been shown that these workloads may cause pulmonary hyperinflation.3,12,24,25 However, although upper limb training is considered to be an obligatory exercise in a rehabilitation program, the literature is not clear about the workload that should be used for this training. Ries et al12 used the proprioceptive neuromuscular facilitation method for upper limb training in patients with COPD but failed to describe the load the patients were submitted to. The physiologic basis for upper limb training may be the same as for that of the lower limb. In this case, high loads, close to the anaerobic threshold of the muscle groups, should be used. But the choice of a high load for upper limb training may · cause high Ve because of the metabolic demands. Martinez et al26 showed that the cycloergometer incremental upper limb exercise reaches the anaerobic threshold faster than that of a lower limb exercise. In addition, studies that evaluated pulmonary hyperinflation development during upper limb training with high load confirmed a reduction in the IC,1,2,17 but no evaluation on the influence of the different workloads was done. The intensive work done by the arm muscles during the exercise with a constant workload at 80% of the maximum showed that this workload may be excessive to commence treatment in patients with light and moderate COPD.17 Gigliotti et al2 showed that pulmonary hyperinflation with concomitant reduction in the IC reached approximately 1 L in patients with COPD when they performed arm exercises with a workload of 80% of the maximum obtained. Pulmonary hyperinflation may occur in approximately 50% of the patients doing exercises with a lower workload (50% of the maximum obtained).1 However, none of these authors studied the development of pulmonary hyperinflation in the same group of patients using varied loads to evaluate if this response was connected to the load itself or to the patient’s response. We observed that an increased proportion of patients hyperinflated as they exercised increasing loads; 41.1% of our patients presented DH with a workload of 50%, whereas 66.6% and 79.1% hyperinflated while exercising with workloads of 65% and 80%, respectively. This shows that pulmonary hyperinflation during the arm exercises is more relevant to the workload that the patient is submitted to than to the patient. The fact that the time of endurance inversely decreased when the workload was increased is a direct consequence of the workload that the patient was submitted to. The maximum time programmed for a complete set of endurances exercise was 20 min. 6 In a study that exercised the upper limbs of patients with light and moderate COPD with a workload at 80% of the maximum, the average endurance time was 7.1 min.17 This exercise time reduction involving unsupported arm exercises was also observed in patients who presented severe conditions and related CHEST / 138 / 1 / JULY, 2010
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Figure 1. Inspiratory capacity before and after the submaximum exercise with the upper limbs in different loads.
to the reduction in the IC (r 5 0.67; P 5 .0008).27 Again, these authors did not relate the endurance exercise reduction with the different workloads to which the patient was submitted. In our study the endurance time during the exercise with the workload of 50% was 12.5 min, reducing to 10.1 min with a workload of 65% and to 7.6 min with a workload of 80%, clearly demonstrating a reduction in the exercise capacity in relation to the increase in the workload.
Mechanisms That Contributed to the Development of Dynamic Pulmonary Hyperinflation and to the Reduction in the Endurance of the Upper Limbs The mechanisms through which patients with COPD develop dynamic pulmonary hyperinflation and limit their exercise capacity are usually related to: · (1) increase of the Ve, (2) reduction in the expiratory time, (3) possible increase of the elastic work, and
Table 2—Comparison Among Three Exercise Sequences With Different Workloads Variables Hyperinflated patients, No./total (%) IC rest, L DIC, L Total time, min Final Borg score, arms Final Borg score, dyspnea Inspiratory time, s Expiratory time, s TI/TTOT ratio RR, breaths/min · Vo2max, mL/min/kg · Vo2max, % predicted · Ve, L/min · Ve/MVV · Ve/Vo2 · Vo2max/total time, mL/min · Ve/total time, L/min
Incremental Test
50% Endurance Workload
65% Endurance Workload
80% Endurance Workload
P Value
19/24 (79.1) 2.15 6 0.56 0.23 6 0.21 10.1 6 4.3 7.1 6 2.8 7 6 2.8 0.78 6 0.19 1.30 6 0.28 0.40 6 0.04 30.0 6 5.6 1039.9 6 252.1 60.5 6 16.5 38.7 6 10 0.96 6 0.21 35.8 6 9.8 … …
10/24 (41.1) 2.16 6 0.48 0.10 6 0.1a 12.5 6 6 7.8 6 2.4 7.7 6 2.3 0.83 6 0.29 1.42 6 0.42 0.35 6 0.05a 28.8 6 6.0 963.4 6 208.6 56.7 6 17.7a 36.9 6 9.7 0.93 6 0.26 36.1 6 7.9 99.5 6 54.9a 3.89 6 2.95
15/24 (66.6) 2.18 6 0.57 0.24 6 0.23b 10.1 6 5.6 7.5 6 2.2 7.1 6 2.6 0.77 6 0.29 1.38 6 0.34 0.37 6 0.04 29.2 6 6.0 993.8 6 279.4 58.3 6 18.5 39.4 6 11.2 0.99 6 0.28 37.9 6 8.9 123.9 6 59.9c 5.03 6 3.17
19/24 (79.1) 2.14 6 0.53 0.29 6 0.22 7.6 6 5.1 7.3 6 2.5 7.3 6 2.4 0.79 6 0.19 1.29 6 0.29 0.38 6 0.05 29.8 6 5.9 1038.9 6 264.8 60.9 6 19.1 38.4 6 11.4 0.95 6 0.23 35.4 6 9.4 170.3 6 78.6 6.56 6 3.45
, .0014 .25 , .0001 , .0005 .34 .47 .63 .07 .01 .65 .66 , .01 .08 .21 .06 , .0001 .01
Values expressed in mean 6 SD unless otherwise noted. ANOVA 5 analysis of variance; ΔIC 5 inspiratory capacity variation; IC 5 inspiratory · · capacity; RR 5 respiratory rate; TI/TTOT 5 inspiratory time/total time; Ve 5 minute ventilation; Vo2 5 oxygen consumption. See Table 1 legend for expansion of other abbreviation. aP , .05 (ANOVA between endurance 50% vs 80%). bP , .05 (ANOVA between endurance 50% vs 65%). cP , .05 (ANOVA between endurance 65% vs 80%). 42
Original Research
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Figure 2. Comparison between the endurance times during the three different workloads.
(4) decrease of the work efficiency. Our patients, independently of the load they were exercising with, usually interrupted the exercise by the time they · achieved a Ve of approximately 39 L/min, which cor· responds to 97% of MVV. The high Ve/MVV ratio for the three workloads shows that these patients had a very low ventilatory reserve, demonstrating the low ventilatory reserve that they could dispose of, which is known as one of the factors that limit exercise in patients with chronic lung disorders. Shortening of expiratory time is one of the main reasons for patients with COPD to hyperinflate during the accomplishment of a task that requires a certain load demand.23 The association of reduced lung
elastic recoil with a shorter expiratory time will make the exhaled air volume lower than the inhaled volume leaving a residue within the lungs. This phenomenon repeats itself to the point where the sum of these residues establishes a greater functional residual capacity inducing the respiratory system to reach a new balance state. The reduction of the IC, as may be observed in Figure 1, reflects that dynamic lung hyperinflation occurred.28 The evaluation of expiratory times along the exercise session minute by minute (Fig 3) clearly demonstrates that they behave quite differently. At the isotime 4, 5, 6, and 7 min there is a clear dissociation of the curves with significant statistical differences between them: the 80% workload presents the shortest expiratory time, the 65% an intermediate value, and the 50% the lowest reduction. In addition, as seen in Figure 4 , the respiratory
Figure 3. Comparison of the expiratory time in different workloads and at the isotime.
Figure 4. Comparison of the respiratory frequency in different workload and at the isotime.
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· Figure 5. Work efficiency in the three different workloads. Vo2 5 oxygen consumption.
frequency presented the same behavior. The association of the progressive shortening of the expiratory time and the increase in the respiratory frequency most probably is the reason for the increase in the dynamic pulmonary hyperinflation as the workloads increased. DH causes breathing discomfort and shortening of endurance time. Patients usually ended the exercise when they · reached a Vo2 value very close to their maximum · upper limb Vo2, tested before the exercises. This shows an increasing O2 consumption per minute of exercise as the workload was increased. In other words, as the workload increases there is a decrease in the work efficiency, which corroborates with the reduction of the endurance time (Fig 5). IC was statically measured using a validated method. In addition to its low cost, it is reproducible,29 can be easily carried out after an exhausting exercise, and requires little cooperation from the patient. This method has been used by Belman et al10 and O’Donnell et al28 to measure the IC after lower limb exercises. Although the precise criteria for dynamic pulmonary hyperinflation requires the measurements of the total Table 3—Pulmonary Hyperinflation Odds for Workloads of 50%, 65%, and 80% of the Peak Variables DH 80% vs DH 50% DH 65% vs DH 50% DH 80% vs DH 65%
Odds Ratio
95% CI
P Value
1.9 1.5 1.2
1.1-3.1 0.85-2.6 0.87-1.8
.009 .12 .17
DH 50% 5 dynamic hyperinflation in 50% workload; DH 65% 5 dynamic hyperinflation in 65% workload; DH 80% 5 dynamic hyperinflation in 80% workload.
lung capacity, and the ratio of functional residual capacity to the total lung capacity, O’Donnell et al28 and Yan et al15 demonstrated that the changes in the IC obtained using this method reflect dynamic residual volume alterations in a reproducible and accurate way.15 In our study, the basal value of the IC did not differ during the 4 days of the procedure (data not shown), demonstrating the stability and accuracy of the method. All measurements were performed at the same time of day, thus there was no influence of the circadian cycle on pulmonary function. Cycloergometer was used in the study as it is considered a gold standard in exercises that involve upper limbs.6 The arm cycloergometer allows more control over the load the patient is submitted to, a better synchronism of the movements when turning the lever, and a standardization of the speed. The originality of this article lies in the nonexistence of cross-over trials in the researched literature that compare the behavior of dynamic pulmonary hyperinflation in the same patient with COPD exercising their upper limbs with a cycloergometer. Muscle training of the upper limbs is routinely recommended for patients with COPD. Although pulmonary rehabilitation is indicated for all patients with COPD, it is more commonly used in patients with severe and very severe forms of the disease—those who present a higher level of pulmonary hyperinflation. Higher workloads clearly lead to lower endurance time, which is clearly related to higher hyperinflation and a lesser work efficiency. Based on our study, it is believable that training using an arm cycloergometer with a low workload (50% of the maximum) can be more
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feasible for the patients. This workload has shown to be more efficient than the other loads, and the levels of · Vo2 obtained with this workload were closer to those found by Velloso et al30 in patients with COPD performing activities of daily living. There is always a concern when a cross-over trial is carried out, especially related to period and sequence effects.31 Period and sequence effects were not significant for the studied variables, except for endurance time. An interaction effect of workload and period was found (P 5 .039) where a difference between 50% and 80% was detected. This can be explained by the fact that two patients reached 20 min with 80%, and because of the small sample size, these observations increased the mean. In our point of view, this interaction occurred by chance and period and sequence effects can be omitted for the all models once they are statistically evaluated. However, there are some limitations to this study: (1) the nonexistence of a control group to compare with the data found in patients with COPD; however, each patient was his or her own control; (2) not having used a measurement that could dynamically measure the IC on line during the exercise; this has not influenced the results as our aim was to evaluate the IC variation before and after the arm exercises. We conclude that higher workloads during a set of upper limb exercises in patients with severe and very severe COPD directly influence the reduction of the IC, causing dynamic pulmonary hyperinflation. Dynamic pulmonary hyperinflation is directly related to a less efficient performance during the exercises and to a reduction in the endurance time. Acknowledgments Author contributions: Mr M. Colucci: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Mr Cortopassi: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Mr Porto: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Mr Castro: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Mr E. Colucci: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Mr Iamonti: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Ms Souza: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Dr Nascimento: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, and manuscript preparation. Dr Jardim: contributed to subject recruitment, data collection, data analysis, pulmonary function evaluation, exercise testing, manuscript preparation, and guidance. www.chestpubs.org
Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.
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