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The Importance of Physical Fitness In the Performance of Adequate Cardiopulmonary Resuscitation*

Alejandro Luca, Jos F. de las Heras, Margarita Prez, Juan C. Elvira, Alfredo Carvajal, Antonio J. lvarez and Jos L. Chicharro Chest 1999;115;158-164 DOI 10.1378/chest.115.1.158 The online version of this article, along with updated information and services can be found online on the World Wide Web at: http://chestjournal.chestpubs.org/content/115/1/158.full.html

Chest is the official journal of the American College of Chest Physicians. It has been published monthly since 1935. Copyright1999by the American College of Chest Physicians, 3300 Dundee Road, Northbrook, IL 60062. All rights reserved. No part of this article or PDF may be reproduced or distributed without the prior written permission of the copyright holder. (http://chestjournal.chestpubs.org/site/misc/reprints.xhtml) ISSN:0012-3692

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clinical investigations in critical care


The Importance of Physical Fitness In the Performance of Adequate Cardiopulmonary Resuscitation*
Alejandro Luca, MD, PhD; Jose F. de las Heras, MD; Margarita Perez, MD, PhD; Juan C. Elvira, MD; Alfredo Carvajal; Antonio J. Alvarez, MD; and Jose L. Chicharro, MD, PhD

The aim of the present investigation was to evaluate the influence of the physical fitness of a cardiopulmonary resuscitation (CPR) provider on the performance of and physiologic response to CPR. To this end, comparisons were made of sedentary and physically active subjects in terms of CPR performance and physiologic variables. Two study groups were established: group P (n 14), composed of sedentary, professional CPR rescuers (mean [ SD]; age, 34 6 years; VO2max, 32.5 5.5 mL/kg/min), and group Ex (n 14), composed of physically active, nonexpe rienced subjects (age, 34 6 years; VO2max, 44.5 8.5 mL/kg/min). Each subject was required to perform an 18-min CPR session, which involved manual external cardiac compressions (ECCs) on an electronic teaching mannequin following accepted standard CPR guidelines. Subjects gas exchange parameters and heart rates (HRs) were monitored throughout the trial. Variables indicating the adequacy of the ECCs (ECC depth and the percentage of incorrect compressions and hand placements) also were determined. Overall CPR performance was similar in both groups. The indicators of ECC adequacy fell within accepted limits (ie, an ECC depth between 38 and 51 mm). However, fatigue prevented four subjects from group P from completing the trial. In contrast, the physiologic responses to CPR differed between groups. The indicators of the intensity of effort during the trial, such as HR or percentage of maximum oxygen uptake (VO2max) were higher in group P subjects than group Ex subjects, respectively (HRs at the end of the trial, 139 22 vs 115 17 beats/min, p < 0.01; percentage of VO2max after 12 min of CPR, 46.7 9.7% vs 37.2 10.4%, p < 0.05). These results suggest that a certain level of physical fitness may be beneficial to CPR providers to ensure the adequacy of chest compressions performed during relatively long periods of cardiac arrest. (CHEST 1999; 115:158 164)
Key words: cardiopulmonary resuscitation; exercise; fitness. Abbreviations: CPR cardiopulmonary resuscitation; ECC RER respiratory exchange rate; Ve minute ventilation; Vo2 Vt tidal volume external cardiac compression; HR heart rate; oxygen uptake; Vo2max maximum oxygen uptake;

T o date, the early performance of adequate chest (cardiac) compressions is a standard of care that
*From the Departamento de Ciencias Morfologicas y Fisiologa, Universidad Europea de Madrid (Drs. Luca and Perez); Servi cio Especial de Urgencias 061, Insalud, Madrid (Drs. de las Heras, Elvira, and Alvarez); and Universidad Complutense de Madrid (Dr. Chicharro); Spain. This study was partially funded by Tecnicas Medicas M.A.B. (Barcelona, Spain). Manuscript received April 7, 1998; revision accepted July 13, 1998. Correspondence to: Alejandro Luca, MD, PhD, Unidad de Investigacion, Escuela de Medicina de la Educacion Fsica y el Deporte, Facultad de Medicina, Pabellon VI, 5a Planta, Univer sidad Complutense de Madrid, 28040 Madrid, Spain
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is considered to provide the optimal outcome in cardiopulmonary arrest.1 Manual external cardiac compressions (ECCs) represent a simple and readily available cardiopulmonary resuscitation (CPR) technique that artificially produces sufficient cardiac output to maintain basal cardiac and neurologic activities until spontaneous circulation is restored by methods such as mechanical ventilation, defibrillation, or drug administration.2,3 However, despite its proven efficacy, manual ECC has disadvantages. For example, it is difficult for one person to deliver vigorous, manual ECCs for long periods, which
Clinical Investigations in Critical Care

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results in inadequate chest compressions that may be insufficient to provide the blood flow required to maintain critical organ function.4 Several authors have reported different methods to improve basic CPR (eg, variation of compression rate and abdominal binding).3,5,6 Furthermore, mechanical active compression-decompression CPR has been introduced in an attempt to improve the outcome of CPR after cardiac arrest.7 Little attention, however, has been focused on the fact that the fatigue of the CPR provider may result in inadequate compression.8 On the other hand, numerous epidemiologic surveys suggest that adequate, regular exercise can maintain or improve fitness, preserve good health, and enhance the quality of life in comparison to a more sedentary style of life.9 Moreover, a number of studies have reported a potentially beneficial relationship between regular physical activity and several indicators of productivity in physically active employees.10 Consequently, it may be hypothesized that a high level of physical fitness could improve the efficacy of CPR. Although the data with which to evaluate the energetic cost of CPR are scarce, previous research suggests that such a procedure is physiologically demanding on subjects, including well-trained professionals. Indeed, blood lactate concentrations of approximately 3.0 mmol/L and heart rates (HRs) of approximately 130 beats/min have been reported recently in experienced professional CPR rescuers after a 30-min session of standard CPR.11 The aim of the present investigation was to evaluate the influence of the CPR providers physical fitness on performance and physiologic variables during the CPR session. A comparison was made of the results obtained from two subject groups: sedentary, professional CPR rescuers; and physically active, nonexperienced subjects. Materials and Methods
Subjects Fourteen experienced, male, professional CPR rescuers (group P) from a mobile intensive care unit (Servicio Especial de Urgencias 061, Insalud, Madrid, Spain) with a mean ( SD) of 6 2 years of experience (range, 2 to 11 years), and 14 male health professionals (physicians, physical therapists, and exercise physiologists) with no previous experience in CPR (group Ex) were selected as subjects for the study. The subjects in group P were sedentary and had not performed any regular, vigorous exercise during the preceding 2 years. In contrast, group Ex subjects were physically active and had followed an exercise program (3 to 5 sessions/wk, each consisting of 20 to 60 min of continuous activity such as running, cycling, or swimming) similar to that recommended by the American College of Sports Medicine to improve and maintain cardiorespiratory fitness in healthy adults.12

The mean ( SD) age, height, and weight, respectively, of the subjects were as follows: group P, 34 6 years, 171.7 5.7 cm, and 80.4 13.3 kg; group Ex, 34 6 years, 176.3 4.7 cm, and 77.3 10.8 kg. Written informed consent was given prior to participation in the study in accordance with the institutions (Escuela de Medicina del Deporte, Universidad Complutense de Madrid, Spain) guidelines for human subjects. Group Ex subjects received a brief training course in CPR prior to the trial. Maximal Exercise Test Before the initiation of the study protocol, all subjects performed an incremental exercise test to exhaustion to determine maximum oxygen uptake (Vo2max) and ventilatory threshold (Vt) using an automated breath-by-breath system (CPX; Medical Graphics; St. Paul, MN). The exercise test was performed on a cycle ergometer (Ergoline 900; Ergo-line; Barcelona, Spain) and consisted of a ramp protocol starting at 0 W. The workload was increased by 25 W/min, and the pedal frequency was kept constant at 60 to 80 revolutions/min. All exercise tests were terminated voluntarily by the subjects or when the established test termination criteria had been met.13 Vt was determined using the criterion of an increase in both the ventilatory equivalent for oxygen and the end-tidal Po2 with no increase in the ventilatory equivalent for carbon dioxide.14 CPR Performance Each of the subjects performed a standard CPR session on an electronic CPR teaching mannequin (Ambu Man-C; Ambu International; Copenhagen, Denmark). CPR included only manual ECCs since no ventilation was provided by the subjects. ECCs were conducted according to the following accepted guidelines: (1) subjects kneeled beside the mannequin; (2) a rate of 80 to 100 compressions/min was maintained; (3) a depth of 38 to 51 mm was maintained; and (4) a compression duration of 50% of the total compression cycle or duty cycle, which includes both the phases of chest compression and passive decompression of the chest wall, was maintained.15,16 Criteria for the termination of resuscitation were defined as the subjects physical limit (physical exhaustion or pain) or 18 min of resuscitation. The mannequin was equipped with a real-time remote display that recorded the total number of compressions and the number of correct compressions. Compressions were recorded as correct if both depth and hand placement were in keeping with standard advanced cardiac life support guidelines.15 A specially designed computer program (AmbuCPR; Ambu; Glostrup, Denmark) recorded each CPR session as a graphic, semiquantitative plot of compression depth vs time. The average values of the following variables were obtained from the mannequin after 6, 12, and 18 min of CPR: compression rate (ECCs/ min); compression depth (mm); and compression adequacy, which was recorded as the percentage of complete cycles (compression duration of 50% of duty cycle) and as the percentage of incorrect hand placements. Subjects were not permitted to watch the computer monitor during performance. After completion of the test, each subject was informed about their own performance. They were instructed not to inform or share their experience with their peers. Physiologic Variables During CPR Subjects wore a mouthpiece connected to a small, lightweight (26 g) pneumotachograph (Prevent; Medical Graphics; St. Paul, MN) for the duration of the CPR session. A pneumotacograph enhances subject comfort by eliminating the need for cumberCHEST / 115 / 1 / JANUARY, 1999

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some breathing valves and hoses, and heavy headgear. Expired air was analyzed by an automated breath-by-breath system (CPX; Medical Graphics) in order to monitor gas exchange data continuously during each CPR session. Before each trial, the instruments were calibrated using a standard 3-L syringe and precision reference gases. Corrections were made for barometric pressure, ambient temperature, and humidity. HR (beats/min) was continuously monitored during the sessions as a modified 12-lead electrocardiographic tracing (EK56; Hellige; Freiburg, Germany). The 60-s average of the following physiologic parameters, monitored during the CPR session at 6, 12, and 18 min were determined: HR (beats/min); oxygen uptake (Vo2) in absolute and relative units, respectively (L/min and mL/kg/min); minute ventilation (Ve; L/min); and respiratory exchange ratio (RER). In addition, the percentage Vo2max at 6, 12 and 18 min of resuscitation was also determined. Capillary blood samples (50 L) were taken from fingertips before and immediately after the termination of each session to determine blood lactate levels (mmol/L) using an automated lactate analyzer (YSI 23 L; Yellow Springs Instruments; Yellow Springs, OH). Statistical Analysis Data were analyzed using the SPSS 7.5 for Windows statistical package (SPSS Inc.; Chicago, IL). The Kolmogorov-Smirnov test17 was used to demonstrate a Gaussian distribution of data. A Students t test for unpaired data was used to compare physiologic variables between groups during the exercise test. Blood lactate levels were compared within and between groups using a Students t test for paired and unpaired data, respectively. In addition, the following comparisons of average physiologic and performance variables during the CPR session were performed: within groups at 6, 12, and 18 min using one-way repeatedmeasures analysis of variance; and between groups at 6, 12, and 18 min using one-way analysis of variance. When a significant F ratio was found, a Newman-Keuls post hoc analysis was performed to determine where the significant differences existed. A nonparametric test (Mann-Whitney) was used for data that did not show a normal distribution. The level of significance was set at 0.05. All data are expressed as the mean ( SD).

Table 1Maximal Exercise Test*


Group Ex, n 14 Maximal values Vo2max, L/min Vo2 max, mL/kg/min Ve, L/min HR, beats/min Values at Vt Vo2, L/min Ve, L/min HR, beats/min 3.4 44.5 144.0 183 1.9 43.97 131 0.6 8.5 34.7 10 0.4 9.7 11 SD). Group P, n 14 2.6 32.5 110.8 181 1.4 34.6 123 0.4 5.5 25.2 12 0.2 5.7 11 p Value p p p 0.001 0.001 0.001 NS 0.001 0.001 NS

p p

*All values are expressed as mean ( NS no significant difference.

the statistical comparison between groups at 18 min included only 10 subjects from group P. Compression Rate: All the subjects were able to maintain an ECC rate of 80 to 100 compressions/ min, which is in agreement with accepted guidelines for standard CPR.15,16 Compression Depth: No significant differences were found within groups during the trials (p 0.05; Fig 1). Although average values were consistently lower in group Ex subjects throughout the tests (p 0.001, p 0.01, and p 0.05 at 6, 12, and 18 min, respectively), the mean values fell within standard accepted limits (38 to 51 mm) in both groups. Percentage of Incorrect Compression Cycles: No significant differences within or between groups were found (Fig 1). Percentage of Incorrect Hand Placements: No significant differences within or between groups were found (Fig 1). Physiologic Variables During CPR Lactate Levels: Lactate levels significantly increased (p 0.001) within the groups after CPR. There were no significant differences in pre-and post-CPR lactate levels between groups (Fig 2). HR: Although the average values did not change in group Ex during the trial, the average HR increased in group P (p 0.01) at 12 and 18 min during CPR with respect to values at 6 min (Fig 3). However, HR values were significantly lower in group Ex (p 0.01) at each follow-up time. Ventilation: No significant differences within or between groups were observed (Fig 3). RER: In both groups, RER values were lower
Clinical Investigations in Critical Care

Results Maximal Exercise Test Physiologic data obtained in the maximal exercise test are shown in Table 1. Subjects in group Ex showed higher maximal and Vt values than those in group P. CPR Performance CPR Duration and Subject Assessment: There was no significant difference in the duration of CPR between groups, although a tendency toward a longer duration was observed in group Ex vs group P, respectively (1,080 0 vs 979 178 s). All the subjects in group Ex were able to complete the 18-min CPR session, whereas four subjects in group P stopped the session before 18 min. Reasons for early termination were pain in the upper extremity or in the vertebral column (n 2) and dyspnea (n 2). Consequently,
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absolute or relative units (Fig 4). No significant differences were encountered between groups with the exception of higher Vo2 in group Ex than in group P at 18 min (p 0.05). Percentage of VO2max: There were no significant differences within groups (Fig 4). However, group P subjects tended to perform CPR at a higher percent age of Vo2max than group Ex subjects. This was statistically significant at 12 min (p 0.05). Discussion The main finding of this study was that, despite their lack of expertise, nonexperienced, physically fit subjects showed different physiologic responses than and comparable CPR performances to professional, sedentary subjects. The average values of CPR performance indicators such as the percentages of incorrect cycles and incorrect hand placements were similar in both groups. In addition, although ECC depth was consistently lower in group Ex at each follow-up time, the average value was still within standard accepted limits (38 to 51 mm).15,16 Furthermore, the duration of the trials tended to be longer in group Ex. In group Ex, each subject was able to complete the trial, whereas 4 of 14 experienced rescuers in group P showed signs of physical fatigue that forced them to stop ECCs before 18 min. It should be noted that in real situations a minimum of 30 min of CPR is often required.15,16 Moreover, since hypothermia confers protection against the effects of hypoxia, resuscitation efforts in hypothermic patients should be continued for much longer.16 The physiologic responses of the subjects differed considerably between groups. Group P subjects showed significantly higher HR values throughout the trial and also showed a tendency to provide compressions at a higher percentage of Vo2max. These observations suggest that physical fitness has a significant effect on the physiologic response of resuscitation providers. Physically fit individuals can provide ECCs at a lower intensity of exercise and, therefore, have a higher resistance to fatigue. Absolute Vo2 tended to be lower in group P, perhaps suggesting a greater economy of movement during the resuscitation maneuvers, which in turn may be attributed to previous experience (5 3 years). Alternatively, these findings simply may be attributed to the fact that values of Vo2max were considerably lower in group P. However, it should be kept in mind that these subjects performed ECCs at a higher per centage of Vo2max (ie, at a higher intensity of effort). Finally, blood lactate levels significantly increased in both groups after CPR, but no signifCHEST / 115 / 1 / JANUARY, 1999

Figure 1. ECC adequacy: compression depth, percentage of incorrect cycles, and percentage of incorrect hand placements. p 0.001, p 0.01, and p 0.05 for group Ex vs group P at 6, 12, and 18 min, respectively.

during the second part of the CPR session (p 0.05 for 12 and 18 min vs 6 min; Fig 3). No significant differences between groups were detected. VO2: No significant differences were found within groups during the trial whether Vo2 was expressed in

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Figure 2. Blood lactate levels. *

0.001 in both groups for pre- vs post-CPR.

icant differences were found between groups. This may be related to the fact that the majority of group Ex subjects had undergone exercise that mainly involved the lower extremities (walking, running, cycling, etc.), whereas ECC principally involves the trunk and upper body muscles. Despite the tendency of previous resuscitation research to focus on advanced life support measures, the provision of adequate ECCs is still the standard care procedure for victims of cardiac arrest.8 In this regard, the present study has evaluated the effects of aerobic training on several indicators of ECC performance (such as the rescuers time to fatigue and the adequacy of compressions) and on the physiologic responses to such activity. Although other authors have reported the physiologic responses of experienced, professional CPR rescuers (a mean Vo2max of approximately 45 mL/kg/min) to a session of standard CPR that lasted approximately 30 min, no data concerning their aerobic training was provided.11 In the present investigation, a group of physically active individuals with relatively high Vo2max values (approximately 45 mL/kg/min), in comparison with standard values for healthy adults of the same age group (30 to 39 years),18 was selected. In contrast, the Vo2max of group P subjects was moderate and was considerably lower (approximately 32 mL/kg/min) than that of group Ex subjects. This contrast permitted evaluation of the influence of physical fitness on the physiologic responses of CPR providers. The present findings are in agreement with the
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suggestions of Baubin et al11 and show the need for at least a minimum level of physical conditioning in CPR providers. Such a conclusion is supported by the fact that physically fit individuals with no previous experience in resuscitation maneuvers were as effective as sedentary, professional rescuers in performing chest compressions. The practice of ECC is a moderately intense activity that requires a certain level of physical fitness, as shown by the increase in blood lactate levels in both subject groups. Furthermore, the metabolic cost of CPR was not negligible (a Vo2 of approximately 14 mL/kg/min, or 4 metabolic equivalents, in group P) and corresponds to that of activities such as recreational cycling or swimming. These are commonly perceived as moderately intense by healthy adults.19 In addition, during situations of actual cardiac arrest, ECCs should not be interrupted at all during resuscitation since cardiac output increases cumulatively during the first compressions.20 Other authors also have suggested that there is little margin of error in the provision of adequate critical organ perfusion by ECC.2123 Furthermore, it has been reported recently that trained personnel reach a state of physical fatigue relatively rapidly, at which time the compressions probably become inadequate to ensure vital organ perfusion.8 Moreover, CPR providers might not be able to recognize their own fatigue or its effects on ECC performance.3,8 On the other hand, the limits of this investigation include the fact that CPR was performed on a mannequin under almost ideal laboratory conditions.
Clinical Investigations in Critical Care

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Figure 3. Physiologic responses during ECC: HR, Ve, and RER. * p 0.01 for 12 and 18 min vs 6 min in group P; p 0.01 for group Ex vs group P; and ** p 0.05 for 12 and 18 min vs 6 min.

Figure 4. Physiologic responses during ECC: Vo2 and effort intensity (percentage of Vo2max). group Ex vs group P at 18 min, p 0.05; and group Ex vs group P at 12 min, p 0.05.

Under real conditions (ie, during an actual arrest), rescuers probably achieve better ECC performance because chest compressions are easier to perform in human beings and there is a sense of urgency.8 In conclusion, the findings of this study suggest the possibility of including a fitness program (ie, light to moderate aerobic exercise) for CPR providers as part of their general training. On the other hand,

CPR training is not limited to paramedic personnel. In fact, in Western societies, the survival rate of victims of cardiac arrest largely depends on the intervention of trained bystanders in initiating and maintaining CPR before paramedic personnel arrive.24 The fact that nonexperienced, physically fit subjects and professional, sedentary subjects showed comparable CPR performances, despite contrasting
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physiologic responses, strengthens the notion that physical fitness can have a positive impact on resuscitation efforts.
ACKNOWLEDGMENT: The authors are grateful to Tecnicas Medicas M.A.B. (Barcelona, Spain) for provision of laboratory material and to Ana Burton for her linguistic assistance.

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References
1 National Heart Attack Alert Program Coordinating Commitee. Access to care subcommittee: Staffing and equipping EMS systems: rapid identification and treatment of acute myocardial infarction. Am J Emerg Med 1995; 13:58 66 2 Taylor GJ, Rubin R, Tucker M, et al. External cardiac compression: a randomized comparison of mechanical and manual techniques. J Am Med Assoc 1978; 240:644 646 3 Ward KR, Menegazzi JJ, Zelenak RR, et al. A comparison of chest compression between mechanical and manual CPR by monitoring end-tidal Pco2 during human cardiac arrest. Ann Emerg Med 1993; 22:669 674 4 Paradis NA, Martin GB, Rivers EP, et al. Coronary perfusion pressure and the return of spontaneous circulation in human CPR. J Am Med Assoc 1990; 263:1106 1113 5 Wik L, Naess PA, Ilebekk A, et al. Simultaneous active compression decompression and abdominal binding increase carotid blood flow additively during cardiopulmonary resuscitation (CPR) in pigs. Resuscitation 1994; 28:55 64 6 Tucker KJ, Khan J, Idris A, et al. The biphasic mechanism of blood flow during CPR: a physiologic comparison of active compression-decompression and high-impulse manual external cardiac massage. Ann Emerg Med 1994; 1994:24:895906 7 Wik L, Mauer D, Robertson C. The first European prehospital active compression-decompression (ACD) cardiopulmonary resuscitation workshop: a report and a review of ACD-CPR. Resuscitation 1995; 30:191202 8 Hightower D, Thomas SH, Stone CK, et al. Decay in quality of closed-chest compressions over time. Ann Emerg Med 1995; 26:300 303 9 Bouchard C, Shephard RJ, Stephens T. Physical activity, fitness, and health. International proceedings and consensus statement. Champaign, IL: Human Kinetics Publishers, 1994 10 Shephard RJ, Corey P, Renzland P, et al. The impact of

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changes in fitness and lifestyle upon health care utilization. Can J Public Health 1983; 74:5154 Baubin M, Schirmer M, Nogler M, et al. Rescuers work capacity and duration of cardiopulmonary resuscitation. Resuscitation 1996; 33:135139 American College of Sports Medicine (ACSM). The recommended quality and quantity of exercise for developing and maintaining fitness in healthy adults. Med Sci Sports Exerc 1990; 22:265274 American College of Sports Medicine (ACSM). Guidelines for exercise testing and prescription. 6th ed. Malvern, PA: Lea & Febiger, 1986; 9596 Davis JA. Anaerobic threshold: a review of the concept and directions for future research. Med Sci Sports Exerc 1986; 17:6 8 American Heart Association. Guidelines for cardiopulmonary resuscitation and emergency cardiac care. J Am Med Assoc 1992; 268:21712195 European Resuscitation Council. Guidelines for basic and adult life support. Resuscitation 1992; 24:103122 Afifi AA, Azen SP Statistical analysis: a computer oriented method. 2nd ed. San Diego: Academic Press, 1979; 62 63 Brooks G, Fahey TD, White TP. Exercise physiology: human bioenergetics and its applications. 2nd ed. Mountain View, CA: Mayfield Publishing Company, 1995 Ainsworth BE, Haskell WL, Leon AS, et al. Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sports Exerc 1993; 25:71 80 Myerburg RJ, Castellanos A. Cardiovascular collapse, cardiac arrest, and sudden death. In: Wilson JD, Braunwald E, Isselbacher KJ, et al, eds. Harrisons principles of internal medicine. 12th ed. New York: MacGraw-Hill, 1991; 237242 Del Guercio LRM, Coomaraswamy RP, State D. Cardiac output and other hemodynamic variables during external cardiac massage in man. N Engl J Med 1963; 269:1398 1404 MacKenzie GI, Taylor SH, McDonald Ah, et al. Hemodynamic effects of external cardiac compression. Lancet 1964; 1:13421345 Del Guercio LRM, Feins NR, Cohn JD, et al. Comparison of blood flow during external and internal cardiac massage in man. Circulation 1965; 31(suppl):I171I180 Cummins RO, Eisenberg MS. Prehospital cardiopulmonary resuscitation: is it effective? JAMA 1985; 253:2408 2412

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The Importance of Physical Fitness In the Performance of Adequate Cardiopulmonary Resuscitation * Alejandro Luca, Jos F. de las Heras, Margarita Prez, Juan C. Elvira, Alfredo Carvajal, Antonio J. lvarez and Jos L. Chicharro Chest 1999;115; 158-164 DOI 10.1378/chest.115.1.158 This information is current as of June 20, 2012
Updated Information & Services Updated Information and services can be found at: http://chestjournal.chestpubs.org/content/115/1/158.full.html Cited Bys This article has been cited by 1 HighWire-hosted articles: http://chestjournal.chestpubs.org/content/115/1/158.full.html#related-urls Permissions & Licensing Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://www.chestpubs.org/site/misc/reprints.xhtml Reprints Information about ordering reprints can be found online: http://www.chestpubs.org/site/misc/reprints.xhtml Citation Alerts Receive free e-mail alerts when new articles cite this article. To sign up, select the "Services" link to the right of the online article. Images in PowerPoint format Figures that appear in CHEST articles can be downloaded for teaching purposes in PowerPoint slide format. See any online figure for directions.

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