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Article |

Effect of Pectus Excavatum Deformity on Cardiorespiratory Fitness in Adolescent Boys FREE

Thomas Rowland, MD; Kevin Moriarty, MD; Gregory Banever, MD
[+] Author Affiliations

Author Affiliations: Divisions of Pediatric Cardiology and Pediatric Surgery, Baystate Medical Center Children’s Hospital, Springfield, Mass.


Arch Pediatr Adolesc Med. 2005;159(11):1069-1073. doi:10.1001/archpedi.159.11.1069.
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Published online

Objective  To determine the magnitude of the effects of pectus excavatum deformity on endurance fitness and cardiorespiratory functional reserve in adolescent boys.

Design  Cross-sectional comparison of cardiac and ventilatory variables at rest and during a maximal cycle exercise test.

Setting  Pediatric exercise-testing laboratory.

Participants  Twelve boys (mean ± SD age, 14.1 ± 1.8 years; age range, 11.8-18.0 years) with moderate-to-severe pectus excavatum deformity (mean ± SD Haller index, 3.95 ± 0.88) and 20 control boys (mean ± SD age, 12.5 ± 0.4 years; age range, 12.1-13.5 years) without musculoskeletal deformity.

Main Outcome Measures  Endurance fitness (physical work capacity); respiratory rate, tidal volume, and minute ventilation; and cardiac output and stroke volume by Doppler echocardiography.

Results  Patients with pectus deformity had significantly lower endurance fitness than controls (mean ± SD physical work capacity, 2.60 ± 0.28 W · kg−1 vs 3.11 ± 0.45 W · kg−1) and reduced mean ± SD values for maximal cardiac index (10.6 ± 1.6 L · min−1 vs 12.0 ± 2.2 L · min−1) and peak tidal volume (3.02 ± 0.27 mL · kg−1 · 10−2 vs 3.46 ± 0.30 mL · kg−1 · 10−2). However, considerable overlap was observed in these values between the 2 groups.

Conclusions  As a group, boys with pectus excavatum deformity have lower endurance fitness than controls, and this is associated with reduced cardiac output and tidal volume responses to exercise. However, the wide variability of these measures makes it difficult to assign pectus deformity as a cause of exercise intolerance in individual patients.

Figures in this Article

The extent to which anteroposterior chest compression imposed by a pectus excavatum deformity can limit exercise capacity remains controversial.1 Moreover, the means by which such a restriction of fitness might occur—anatomic, physiologic, or psychological—is unclear. The question has particular clinical significance because indications for surgical intervention may depend on potential risks for cardiac or ventilatory dysfunction.2 The large body of research examining this issue during the past several decades has provided no clear consensus. Early studies with few participants and anecdotal case reports suggested that a certain number of patients with moderate-to-severe pectus deformity experienced significant exercise intolerance, and in some cases this was improved by surgical intervention.3 Some subsequent studies4,5 demonstrated physiologic limitations at rest and during submaximal exercise, whereas other studies2,6 did not. These cardiorespiratory deficits were highly variable and did not always correspond to the level of exercise intolerance, and improvements were not consistently seen after surgical repair.

Cardiac limitation in patients with pectus excavatum has most commonly been documented as lower resting and submaximal exercise stroke volumes in the sitting position vs supine compared with healthy subjects.4,7 Depressed maximal breathing capacity and lung tidal volumes have been indicated as ventilatory features in some (but not all) studies of these patients as well.5,8,9 Several researchers1,10 have cautioned that these comparisons between patients with pectus deformity and healthy individuals have not always taken into account important confounding variables, such as degree of pectus deformity, degree of physical conditioning, and comparison with appropriate control subjects.

Previous exercise studies4,7 have not provided information regarding cardiac variables measured during maximal exercise testing in patients with pectus excavatum deformity compared with controls. This study was designed to assess exercise endurance capacity and markers of cardiac and ventilatory functional reserve during progressive maximal exercise testing in a group of adolescent boys with moderate-to-severe pectus excavatum deformity. Findings were compared with those of healthy boys using identical testing methods.

Eighteen adolescent boys who were being considered for surgical repair of pectus excavatum deformity underwent maximal cycle testing with measurement of cardiorespiratory variables. Of these 18 boys, 6 were considered to have failed to provide a true exhaustive exercise effort (see several paragraphs later herein), and data on the remaining 12 boys provide the basis of this study. The severity of pectus deformity was assessed using the computed tomography−derived ratio of the transverse thoracic dimension to the sternovertebral distance (the Haller index).11 The mean ± SD value was 3.95 ± 0.88 (range, 2.93-5.37).

The mean ± SD age of the patients was 14.1 ± 1.8 years (age range, 11.8-18.0 years). All the patients were in good health and had no evidence of cardiac or respiratory disease; none was taking medications that would affect cardiorespiratory fitness. Nine patients (75%) had participated on organized sports teams (basketball, hockey, or football) in the preceding 3 months, but none was involved in an aerobic training program. By questionnaire, the parents scored their child’s level of habitual physical activity on a 5-point scale from 1 (inactive—watches television, reads, or does homework after school; no extracurricular sports) to 5 (very active—participates regularly in extracurricular sports; dislikes sedentary activities). On this scale, the average score was 3.7.

Measured cardiovascular variables were compared with those of a control group of 20 healthy boys (mean ± SD age, 12.5 ± 0.4 years; age range, 12.1-13.5 years) without musculoskeletal deformity who were participants in an earlier study regarding cardiovascular fitness and run performance in children.12 The controls were selected to provide a broad range of fitness, based on school 1-mile run times. Fourteen controls (70%) had recently participated on community sports teams. On the activity questionnaire, the mean score was 3.8.

Anthropometric techniques, exercise protocol, and measurement of cardiorespiratory variables were identical in patients with pectus excavatum and controls. Height and weight were recorded using a stadiometer and a calibrated balance beam scale, respectively. Average triceps and scapular skinfold thicknesses were determined from triplicate measurements on the right side of the body to the nearest 0.1 mm using standard techniques. Mean values were summed to create a skinfold score.

Exercise was performed in an air-conditioned laboratory (20°C-22°C with moderate humidity). Participants cycled in the upright position to exhaustion, with a progressive protocol of 3-minute work stages and 25- or 50-W increments (depending on body size). Pedaling cadence was 50 rpm. A true exhaustive effort was considered to have been achieved if the boys demonstrated (1) a peak heart rate exceeding 183 beats per minute (bpm) (95% of predicted) and (2) subjective evidence of fatigue (hyperpnea, sweating, or facial flushing).13 Endurance performance was assessed using physical work capacity (PWC)—the highest workload achieved—prorated for incomplete work stages and related to body mass. Ventilatory measures (tidal volume, respiratory rate, and calculated minute ventilation) were determined using a Q-Plex Cardiopulmonary System (Quinton Instruments, Seattle, Wash), which uses a pneumotachometer in the expiratory line.

Heart rate was measured using electrocardiography. Stroke volume at rest and during exercise was estimated using standard Doppler echocardiographic techniques.14 The validity and reliability of this method have previously been reported.15,16 Ascending aortic blood flow velocity was recorded using a 2.0-MHz transducer positioned in the suprasternal notch. Area under the velocity curve across time for each beat was integrated to obtain the velocity-time integral. The mean velocity-time integral was calculated from the 3 to 10 highest and most distinct curves measured at rest, in the final minute of each work stage, and immediately before termination of exercise. This value was multiplied by the cross-sectional area of the aortic root to obtain the stroke volume. The aortic area was calculated from the greatest systolic diameter measured at the sinotubular junction as viewed from the parasternal long axis on a 2-dimensional echocardiogram with the subject seated on the treadmill just before exercise testing. Cardiac output was determined as the product of stroke volume and heart rate.

Stroke volume and cardiac output were related to body surface area (stroke index and cardiac index) based on studies by Armstrong and Welsman17 and Rowland et al.18 Minute ventilation was adjusted for height, given reports that exercise minute volume (expired) related to stature is independent of size in adolescent boys,19 and tidal volume was expressed relative to body mass, a relationship which is constant during childhood.20

Comparisons between patients with pectus excavatum and controls were made at rest, at a given absolute submaximal workload (50 W), and during maximal exercise. Mean differences were assessed using independent t tests. Relationships among severity of pectus deformity (Haller index), endurance fitness (PWC per kilogram), and resting and maximal values of tidal volume, minute ventilation, stroke index, and cardiac index were assessed using Pearson product moment correlation coefficients. Statistical significance was defined as < .05. This study was reviewed and approved by the institutional review board of the Baystate Medical Center. Informed consent and assent were obtained from parents and participants, respectively. Data are given as mean ± SD.

The 12 patients with pectus excavatum were heavier (57.6 ± 13.4 kg [range, 47.0-71.5 kg] vs 47.2 ± 10.9 kg [range, 32.6-71.9 kg]; P = .02) and taller (168 ± 12 cm [range, 146-188 cm] vs 157 ± 8 cm [range, 139-176 cm]; P = .01) than the 20 control subjects. No difference was observed between the 2 groups in body composition, with a skinfold thickness sum of 19.7 ± 7.6 mm in patients and 19.2 ± 7.0 mm in controls. As noted previously herein, the 2 groups were similar in estimated level of habitual activity and in participation in organized sports.

Maximal heart rate was 191 ± 8 bpm in patients with pectus excavatum and 195 ± 6 bpm in controls (= .17), indicating an equivalent maximal exercise effort in the 2 groups. Endurance fitness as indicated by PWC per kilogram was significantly lower in the pectus excavatum group (2.60 ± 0.28 W · kg−1) compared with controls (3.11 ± 0.45 W · kg−1; P = .001) (Figure 1). No correlation was observed between the degree of pectus deformity using the Haller index and PWC per kilogram (r = 0.18; = .37).

Place holder to copy figure label and caption
Figure 1.

Cycle endurance fitness as defined by physical work capacity (PWC) relative to body mass in 12 patients with pectus excavatum deformity and 20 control subjects. Horizontal bars indicate means.

Graphic Jump Location

Accurate estimates of stroke volume using the Doppler echocardiographic technique are contingent on the assumption of a circular aortic cross section. The aortic root diameter (related to the square root of body surface area21) was similar in patients and controls (1.79 ± 0.12 cm · m−2 and 1.76 ± 0.11 cm · m−2, respectively), suggesting no differences in aortic root cross-sectional shape (ie, no anteroposterior compression by the pectus deformity).

At rest, few differences were observed between patients with pectus excavatum and controls (Table). The stroke index was 13% higher in controls (P = .07). Resting tidal volume per kilogram was significantly diminished in patients with pectus excavatum (1.14 ± 0.22 mL · kg−1 · 10−2) compared with controls (1.35 ± 0.30 mL · kg-1 · 10−2). A moderate correlation was observed between the Haller index and resting tidal volume per kilogram (r = 0.51; P = .08). There were no group mean differences in the cardiac index or height-adjusted minute ventilation.

Table Graphic Jump LocationTable. Cardiorespiratory Variables at Rest, During Submaximal Exercise, and During Maximal Exercise in Patients With Pectus Excavatum Deformity and Control Subjects*

At a common absolute workload of 50 W, similar findings were observed (Table). The only statistically significant difference between groups was a lower tidal volume per kilogram in patients with pectus excavatum (1.75 ± 0.34 mL · kg−1 · 10−2 vs 2.06 ± 0.31 mL · kg−1 · 10−2; P = .02), but this did not affect ventilatory response because mean values of minute volume (expired) related to height were similar. The stroke index was again slightly lower in boys with pectus deformity, and their mean cardiac index was 9% lower (P = .09).

At maximal exercise, the trend for a lower stroke index in patients with pectus excavatum persisted, but the 11% difference was not significant (P = .11) (Table). Maximal stroke index (r = 0.64; P = .001) and cardiac index (r = 0.67; P = .001) correlated positively with PWC per kilogram. (The maximal exercise cardiac index was higher in control subjects than in patients with pectus deformity (12.0 ± 2.2 L · min−1 · m−2 vs 10.6 ± 1.6 L · min−1 · m−2; P = .05) (Figure 2). Tidal volume at peak exercise continued to be significantly greater in control subjects than in patients with pectus excavatum (3.46 ± 0.43 mL · kg−1 · 10−2 and 3.02 ± 0.44 mL · kg−1 · 10−2, respectively; P = .01), but no group differences were seen in maximal minute ventilation. No significant relationships were observed between the Haller index and any of the physiologic variables at peak exercise.

Place holder to copy figure label and caption
Figure 2.

Maximal exercise cardiac index estimated using Doppler echocardiography in 12 patients with pectus excavatum deformity and 20 control subjects. Horizontal bars indicate means.

Graphic Jump Location

The findings from this study are generally consistent with those of previous studies: as a group, patients with a significant pectus excavatum deformity of the chest demonstrate lower endurance fitness than controls. Even in this study of a relatively small cohort of 12 patients with pectus excavatum, mean PWC (relative to body mass) on a progressive cycling test was 16.4% lower than that of control subjects. At the same time, although statistically significant, the difference in mean values of endurance times of patients with pectus deformity and control subjects in such tests is not large, with wide intersubject variability. In fact, many individuals with pectus excavatum deformity have not only normal but even above-normal fitness levels compared with controls (Figure 1). From a clinical standpoint, concluding that any complaint of exercise intolerance in a given patient is related to their pectus deformity is problematic.

In this study, use of the Haller index as a marker of the severity of pectus deformity was not predictive of either endurance fitness or maximal cardiorespiratory variables. This finding is consistent with previous studies of the failure of severity of pectus deformity to correspond to symptoms of exercise intolerance,22 cardiorespiratory variables,4,23 or measured fitness.4,8 However, Malek et al5 found that patients with pectus excavatum deformity with a Haller index greater than 4.0 were 8 times more likely to demonstrate a low “metabolic threshold” (oxygen uptake above which a sustained increase in blood lactate concentration is observed) during exercise than those with an index of 4.0 or less.

Depressed endurance fitness in young people with pectus excavatum deformity could reflect lower levels of habitual activity or sports participation, cardiac or respiratory limitations, or the influence of some other factor independent of cardiorespiratory function. This study provides some insights into this issue.

DEPRESSED AEROBIC FITNESS FROM SEDENTARY LIFESTYLE

Patients with pectus deformity might be more reticent to engage in physical activities than their peers for psychological reasons. Moreover, the pattern of diminished stroke index and cardiac index observed in this study is consistent with that observed in healthy youths with low fitness.24 However, involvement in sports teams and physical activity level by questionnaire were similar among patients with pectus deformity and control boys in this study. Eighteen of the 21 patients with pectus excavatum studied by Malek et al5 had been performing regular aerobic activity 30 minutes to 2 hours daily an average of 3 times a week. Despite this, their average maximum oxygen consumption was 75% of predicted, and their oxygen pulse (an indicator of stroke volume) was significantly lower than reference values. This information suggests that depressed endurance fitness in youths with pectus deformity cannot be explained by lower habitual physical levels.

IMPAIRED CARDIAC FUNCTION

Previous investigations have provided a solid basis for the concept that lower cardiac stroke volume (presumably from smaller, compressed ventricles) in patients with pectus deformity is responsible for depression in maximal cardiac output, and this in turn accounts for their lower maximum oxygen consumption and endurance fitness. The present study, which measured cardiac output and stroke volume at peak exercise, supports this idea. The maximal cardiac index was significantly lower in patients with pectus excavatum, and stroke index and cardiac index values at peak exercise correlated well with endurance performance (PWC per kilogram). Thus, the diminished cardiac index was a reflection of a consistently lower stroke index during rest and exercise in these patients (although the stroke index differences from controls did not reach statistical significance).

Cardiac findings in the present study mimic those in the study by Zhao et al.4 These investigators compared submaximal stroke values (using Doppler echocardiography) at moderate exercise intensity in 13 patients with pectus excavatum (aged 10-31 years) with those in a height- and weight-matched control group. Mean stroke volumes at rest were 46 mL in patients and 50 mL in controls. During upright exercise, these values increased to 55 mL in the pectus deformity group and 65 mL in controls. During supine exercise, there were no differences in stroke volume between the 2 groups, suggesting that “upright exercise capacity in this disease is affected by reduced filling of the heart in the nonsupine position.”4(p163)

Beiser et al7 demonstrated the same postural-dependent response of stroke volume and cardiac output to submaximal exercise in 6 adults with pectus deformity during cardiac catheterization. Wynn et al10 measured cardiac output using the acetylene rebreathing technique during maximal exercise testing in 12 children with pectus excavatum deformity. Comparison of maximal cardiac values with normative data was not reported. The rate of increase in cardiac output and stroke volume with respect to oxygen consumption during exercise was similar in controls, but values were in the low range of predicted.

VENTILATORY LIMITATIONS

Previous studies have provided evidence of a variety of ventilatory deficiencies in patients with pectus deformities that might prove limiting to exercise performance. In the present study, tidal volume (adjusted for body mass) was significantly reduced at rest, during submaximal exercise, and during maximal exercise in patients with pectus deformity compared with controls. However, this did not impair minute ventilation, which was similar to that of controls at all measurements, including peak exercise.

These results are consistent with those of Haller and Loughlin,2 who found no differences in respiratory rate or minute ventilation at maximal exercise in 36 teenagers with pectus deformity. In that study, 58% of the patients had subjective complaints of exercise intolerance, but treadmill endurance time and maximum oxygen consumption were no different than those of controls. Similarly, the patients with pectus deformity studied by Malek et al5 had normal maximal exercise values for minute ventilation, respiratory rate, and tidal volume despite a maximum oxygen consumption of 75% of predicted.

Other researchers, however, have described findings that suggest a possible ventilatory limitation of exercise capacity in these patients. Borowitz et al25 found that minute ventilation at maximal exercise was only 60% of predicted in their study of 10 boys with pectus deformity. Minute ventilation was 59 ± 14 L · min−1 at maximal upright exercise in the patients reported by Zhao et al4 compared with 76 ± 23 L · min−1 in controls.

SOMETHING ELSE

As noted previously herein, cardiorespiratory physiologic measures do not always correspond to descriptions of exercise intolerance in patients with pectus excavatum deformity. This raises the possibility that other influences (peripheral skeletal muscle changes or altered psychological perceptions of exercise discomfort) might be involved. In the present study, for example, is it possible that the reduced exercise capacity and lower cardiac output are not cause-and-effect but rather expressions of another undefined factor that limits exercise performance? Although the question cannot be answered definitively, the observation that stroke volume and cardiac output were lower in boys with pectus excavatum at rest and during submaximal exercise as well as during peak exercise supports a primary role of circulatory limitations on exercise capacity in these patients.

In summary, the findings from this study add to a generally consistent picture of the effect of a significant pectus excavatum deformity on cardiorespiratory fitness in youths. As a group, patients with pectus excavatum deformity have lower endurance fitness than healthy youths, but such differences are small. There is wide variability of exercise capacity in children and adolescents with a pectus deformity, and implicating a pectus defect as being responsible for claims of exercise intolerance in a given patient is difficult. It is likely that diminished circulatory responses to exercise as a result of depressed cardiac stroke volume are the major physiologic feature that limits exercise capacity in these patients.

Correspondence: Thomas Rowland, MD, Department of Pediatrics, Baystate Medical Center, Springfield, MA 01199 (Thomas.Rowland@bhs.org).

Accepted for Publication: June 23, 2004.

Acknowledgment: We thank Donna Grzelak, RN, for her assistance with this study.

Shamberger  RC Cardiopulmonary effects of anterior chest wall deformities. Chest Surg Clin N Am 2000;10245- 252
PubMed
Haller  JALoughlin  GM Cardiorespiratory function is significantly improved following corrective surgery for severe pectus excavatum. J Cardiovasc Surg (Torino) 2000;41125- 130
PubMed
Shamberger  RCWelch  KJ Cardiopulmonary function in pectus excavatum. Surg Gynecol Obstet 1988;166383- 394
PubMed
Zhao  LFeinberg  MSGaides  MBen-Dov  I Why is exercise capacity reduced in subjects with pectus excavatum? J Pediatr 2000;136163- 167
PubMed Link to Article
Malek  MHFonkalsrud  EWCooper  CB Ventilatory and cardiovascular responses to exercise in patients with pectus excavatum. Chest 2003;124870- 882
PubMed Link to Article
Quigley  PMHaller  JAJelus  KLLoughlin  GMMarcus  CL Cardiorespiratory function before and after corrective surgery in pectus excavatum. J Pediatr 1996;128638- 643
PubMed Link to Article
Beiser  GDEpstein  SEStampfer  MGoldstein  RENoland  SPLevitsky  S Impairment of cardiac function in patients with pectus excavatum, with improvement after operative correction. N Engl J Med 1972;287267- 272
PubMed Link to Article
Sigalet  DLMontgomery  MHarder  J Cardiopulmonary effects of closed repair of pectus excavatum. J Pediatr Surg 2003;38380- 385
PubMed Link to Article
Orzalesi  MMCook  CD Pulmonary function in children with pectus excavatum. J Pediatr 1965;66898- 900
PubMed Link to Article
Wynn  SRDriscoll  DJOstrom  NK  et al.  Exercise cardiorespiratory function in adolescents with pectus excavatum: observations before and after operation. J Thorac Cardiovasc Surg 1990;9941- 47
PubMed
Haller  JAKramer  SSLietman  SA The use of CT scans in selection of patients for pectus excavatum surgery: a preliminary report. J Pediatr Surg 1987;22904- 908
PubMed Link to Article
Rowland  TKline  GGoff  DMartel  LFerrone  L One-mile run performance and cardiovascular fitness in children. Arch Pediatr Adolesc Med 1999;153845- 849
PubMed Link to Article
Rowland  TW Exercise testing. Developmental Exercise Physiology. Champaign, Ill Human Kinetics Publishers1996;35- 36
Rowland  TObert  P Doppler echocardiography for the estimation of cardiac output with exercise. Sports Med 2002;32973- 986
PubMed Link to Article
Rowland  TPopowski  B Comparison of bioimpedance and Doppler cardiac output during exercise in children [abstract]. Pediatr Exerc Sci 1996;9188- 189
Rowland  TWhatley Blum  J Cardiac dynamics during upright cycle exercise in boys. Am J Hum Biol 2000;12749- 757
PubMed Link to Article
Armstrong  NWelsman  JR Cardiovascular response to submaximal treadmill running in 11- to 13-year olds. Acta Paediatr 2002;91125- 131
PubMed Link to Article
Rowland  TGoff  DMartel  LFerrone  L Influence of cardiac functional capacity on gender differences in maximal oxygen uptake in children. Chest 2000;117629- 635
PubMed Link to Article
Rutenfranz  JAndersen  KLSeliger  V  et al.  Exercise ventilation during the growth spurt period: comparison between two European countries. Eur J Pediatr 1981;136135- 142
PubMed Link to Article
Mercier  JVarray  ARamonaxto  MMercier  BPrefaut  C Influence of anthropometric characteristics on changes in maximal exercise ventilation and breathing pattern during growth in boys. Eur J Appl Physiol 1991;63235- 241
Link to Article
Gutgesell  HPRembold  CM Growth of the human heart relative to body surface area. Am J Cardiol 1990;65662- 668
PubMed Link to Article
Peterson  RJYoung  WGGodwin  JDSabiston  DCJones  RH Noninvasive assessment of exercise cardiac function before and after pectus excavatum repair. J Thorac Cardiovasc Surg 1985;90251- 260
PubMed
Kowalewski  JBrocki  MDryjanski  TZolynski  KKoktysz  R Pectus excavatum: increase of right ventricular systolic, diastolic, and stroke volume after surgical repair. J Thorac Cardiovasc Surg 1999;11887- 93
PubMed Link to Article
Rowland  TKline  GGoff  DMartel  LFerrone  L Physiologic determinants of maximal aerobic power in healthy 12-year old boys. Pediatr Exerc Sci 1999;11317- 326
Borowitz  DCerny  FZallen  GBurke  MGross  KGlick  PL Pulmonary function and exercise response in patients with pectus excavatum after Nuss repair. J Pediatr Surg 2003;38544- 547
PubMed Link to Article

Figures

Place holder to copy figure label and caption
Figure 1.

Cycle endurance fitness as defined by physical work capacity (PWC) relative to body mass in 12 patients with pectus excavatum deformity and 20 control subjects. Horizontal bars indicate means.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Maximal exercise cardiac index estimated using Doppler echocardiography in 12 patients with pectus excavatum deformity and 20 control subjects. Horizontal bars indicate means.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable. Cardiorespiratory Variables at Rest, During Submaximal Exercise, and During Maximal Exercise in Patients With Pectus Excavatum Deformity and Control Subjects*

References

Shamberger  RC Cardiopulmonary effects of anterior chest wall deformities. Chest Surg Clin N Am 2000;10245- 252
PubMed
Haller  JALoughlin  GM Cardiorespiratory function is significantly improved following corrective surgery for severe pectus excavatum. J Cardiovasc Surg (Torino) 2000;41125- 130
PubMed
Shamberger  RCWelch  KJ Cardiopulmonary function in pectus excavatum. Surg Gynecol Obstet 1988;166383- 394
PubMed
Zhao  LFeinberg  MSGaides  MBen-Dov  I Why is exercise capacity reduced in subjects with pectus excavatum? J Pediatr 2000;136163- 167
PubMed Link to Article
Malek  MHFonkalsrud  EWCooper  CB Ventilatory and cardiovascular responses to exercise in patients with pectus excavatum. Chest 2003;124870- 882
PubMed Link to Article
Quigley  PMHaller  JAJelus  KLLoughlin  GMMarcus  CL Cardiorespiratory function before and after corrective surgery in pectus excavatum. J Pediatr 1996;128638- 643
PubMed Link to Article
Beiser  GDEpstein  SEStampfer  MGoldstein  RENoland  SPLevitsky  S Impairment of cardiac function in patients with pectus excavatum, with improvement after operative correction. N Engl J Med 1972;287267- 272
PubMed Link to Article
Sigalet  DLMontgomery  MHarder  J Cardiopulmonary effects of closed repair of pectus excavatum. J Pediatr Surg 2003;38380- 385
PubMed Link to Article
Orzalesi  MMCook  CD Pulmonary function in children with pectus excavatum. J Pediatr 1965;66898- 900
PubMed Link to Article
Wynn  SRDriscoll  DJOstrom  NK  et al.  Exercise cardiorespiratory function in adolescents with pectus excavatum: observations before and after operation. J Thorac Cardiovasc Surg 1990;9941- 47
PubMed
Haller  JAKramer  SSLietman  SA The use of CT scans in selection of patients for pectus excavatum surgery: a preliminary report. J Pediatr Surg 1987;22904- 908
PubMed Link to Article
Rowland  TKline  GGoff  DMartel  LFerrone  L One-mile run performance and cardiovascular fitness in children. Arch Pediatr Adolesc Med 1999;153845- 849
PubMed Link to Article
Rowland  TW Exercise testing. Developmental Exercise Physiology. Champaign, Ill Human Kinetics Publishers1996;35- 36
Rowland  TObert  P Doppler echocardiography for the estimation of cardiac output with exercise. Sports Med 2002;32973- 986
PubMed Link to Article
Rowland  TPopowski  B Comparison of bioimpedance and Doppler cardiac output during exercise in children [abstract]. Pediatr Exerc Sci 1996;9188- 189
Rowland  TWhatley Blum  J Cardiac dynamics during upright cycle exercise in boys. Am J Hum Biol 2000;12749- 757
PubMed Link to Article
Armstrong  NWelsman  JR Cardiovascular response to submaximal treadmill running in 11- to 13-year olds. Acta Paediatr 2002;91125- 131
PubMed Link to Article
Rowland  TGoff  DMartel  LFerrone  L Influence of cardiac functional capacity on gender differences in maximal oxygen uptake in children. Chest 2000;117629- 635
PubMed Link to Article
Rutenfranz  JAndersen  KLSeliger  V  et al.  Exercise ventilation during the growth spurt period: comparison between two European countries. Eur J Pediatr 1981;136135- 142
PubMed Link to Article
Mercier  JVarray  ARamonaxto  MMercier  BPrefaut  C Influence of anthropometric characteristics on changes in maximal exercise ventilation and breathing pattern during growth in boys. Eur J Appl Physiol 1991;63235- 241
Link to Article
Gutgesell  HPRembold  CM Growth of the human heart relative to body surface area. Am J Cardiol 1990;65662- 668
PubMed Link to Article
Peterson  RJYoung  WGGodwin  JDSabiston  DCJones  RH Noninvasive assessment of exercise cardiac function before and after pectus excavatum repair. J Thorac Cardiovasc Surg 1985;90251- 260
PubMed
Kowalewski  JBrocki  MDryjanski  TZolynski  KKoktysz  R Pectus excavatum: increase of right ventricular systolic, diastolic, and stroke volume after surgical repair. J Thorac Cardiovasc Surg 1999;11887- 93
PubMed Link to Article
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