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Article |

Cardiac Function in Pediatric Septic Shock Survivors FREE

Hendrika Knoester, MD; Jeanine J. Sol, MD; Pascal Ramsodit, MD; Irene M. Kuipers, MD, PhD; Sally-Ann B. Clur, MBBCh, MSc, FCP(SA)Paed; Albert P. Bos, MD, PhD
[+] Author Affiliations

Author Affiliations: Pediatric Intensive Care Unit (Drs Knoester, Sol, Ramsodit, and Bos) and Pediatric Cardiology Department (Drs Kuipers and Clur), Emma Children's Hospital, Academic Medical Centre, Amsterdam, the Netherlands. Dr Ramsodit is now with the Twenteborg Hospital, Almelo, the Netherlands.


Arch Pediatr Adolesc Med. 2008;162(12):1164-1168. doi:10.1001/archpedi.162.12.1164.
Text Size: A A A
Published online

Objective  To evaluate the long-term effects of septic shock on cardiac function in children treated with inotropic and/or vasoconstrictive agents for 24 hours or longer.

Design  Cohort study.

Setting  Tertiary pediatric intensive care unit and outpatient follow-up clinic.

Participants  One hundred eight of 144 eligible children who were admitted to our tertiary pediatric intensive care unit with septic shock from 1995 through 2005 and were alive in 2006 were invited to participate and visit our outpatient follow-up clinic. Fifty-two healthy controls were included.

Main Exposure  Septic shock survival.

Outcome Measures  History, physical examination, electrocardiogram during rest and exercise, 24-hour electrocardiography registration, and left and right ventricular function.

Results  No children had abnormalities when histories were taken or during physical examination that were attributable to cardiac dysfunction. Six children (6%) had cardiac abnormalities: polymorphic premature ventricular contractions during exercise and 24-hour electrocardiography registration (2 patients), decreased left ventricular function (2 patients), decreased left ventricular function and polymorphic premature ventricular contractions (1 patient), and decreased right ventricular function (1 patient).

Conclusions  In this small and diverse group of pediatric septic shock survivors, we found an excellent recovery of cardiac performance in most patients. In a limited number of patients, we found rhythm disturbances and decreased ventricular function. We believe that, against the background of aging, long-term cardiac follow-up of these patients is important.

Sepsis is one of the leading causes of death in children. Mortality ranges from 4% to 20%.1 Septic shock is characterized by myocardial dysfunction, loss of vascular tone, and capillary leak leading to diminished organ perfusion and the development of multiple organ system failure. Myocardial dysfunction—caused by hypoperfusion, myocardial cell death, and/or cardiodepressant circulating substances, such as tumor necrosis factor α, IL-1 (interleukin 1), and nitric oxide—is a key factor in the development of circulatory failure during septic shock.24 Treatment includes adequate fluid resuscitation and the administration of inotropic and/or vasoconstrictive agents.5,6

Mortality due to septic shock has decreased owing to advances in pediatric intensive care practices, such as improved use of inotropic and vasoconstrictive agents and early goal-directed fluid therapy.68 Follow-up studies of children with septic shock have mainly focused on mortality and short-term morbidity.911 Particularly in children, long-term follow-up studies may be important against the background of the development and maturation of organs. Consider, for example, respiratory distress syndrome of the prematurely born infant (idiopathic respiratory distress syndrome) and acute lung injury in older children. Both have long-term pulmonary consequences. The primary insult occurs when the lung is exposed to a damaging process (idiopathic respiratory distress syndrome or acute lung injury); the secondary insult is caused by mechanical ventilation.12,13 In children treated with inotropic and/or vasoconstrictive agents because of septic shock, the primary insult on the myocardium may be the septic shock and the secondary insult may be treatment with these agents. This may result in permanent damage to the developing heart. The aim of this study was to evaluate the late (>6 months after pediatric intensive care unit [PICU] discharge) effects of septic shock on cardiac function in children and to analyze risk factors for cardiac abnormalities.

The study was performed in the PICU of the Emma Children's Hospital/Academic Medical Center Amsterdam. This is a tertiary multidisciplinary PICU with 14 beds serving the greater Amsterdam area.

PARTICIPANTS

Patients were included if they had been admitted to the PICU for septic shock between 1995 and 2005, had received inotropic and/or vasoconstrictive agents for 24 hours or longer (dopamine, dobutamine, epinephrine, and/or norepinephrine), were alive in 2006, and had been followed up for longer than 6 months after PICU discharge. Exclusion criteria were preexisting cardiac disorders and serious psychomotor retardation. The hospital's institutional review board approved the study protocol, and written consent was obtained for all included patients and/or their parents.

STUDY DESIGN

Cardiac function was evaluated in our outpatient follow-up clinic by patient history, physical examination, and electrocardiogram (ECG) recorded during rest. Electrocardiogram recording during exercise was performed when the child was older than 7 years at follow-up. Twenty-four-hour ECG recording and echocardiography were performed as well.

A structured checklist was used for history taking and the physical examination. Special attention was paid to syncope, chest pain, skipped beats and heart palpitations, peripheral pulsations, liver size, edema, and heart murmurs. Exercise testing was performed in children aged 7 years and older, as summarized in the Bruce protocol (younger children cannot perform this test owing to their size and lack of adequate concentration).14

Echocardiography was performed to evaluate systolic function of the left and right ventricles. Systolic function of the left ventricle was determined by measuring left ventricular end-diastolic diameter (LVEDD) and shortening fraction. Shortening fraction is the percentage of change in the left ventricular cavity dimension during systole ([(LVEDD − left ventricular end-systolic dimension)/LVEDD] × 100). In many studies, left ventricular function is measured by the ejection fraction. In normally shaped left ventricles, shortening fraction and ejection fraction are comparable. We chose to report shortening fraction. In pediatric literature, normal values for systolic function of the left ventricle differ from shortening fraction by more than 28% or more than 30%.1518 Systolic function of the right ventricle was determined by measuring tricuspid annular plane systolic excursion (TAPSE). There are no known reference data in the pediatric literature for TAPSE. As in adult literature, a TAPSE longer than 15.0 mm is considered normal.19 We also studied systolic cardiac function in a control group of 52 healthy children with a benign murmur. Echocardiography was performed to exclude cardiac abnormalities. Diastolic function of the left ventricle was evaluated as well and will be published separately.

During septic shock, sedation was administered when the patient needed artificial ventilation, according to our sedation protocol (morphine and midazolam). Patient characteristics at PICU admission were obtained from medical records and the patient data management system. In our PICU, it was not standard procedure to perform echocardiography to evaluate systolic function of the left ventricle or to perform an ECG during PICU admission. Echocardiography was performed when the pediatric-intensivist on duty wanted additional information on cardiac function or if one was clinically indicated. Electrocardiogram recordings were performed only when rhythm disturbances were suspected. Echocardiography to evaluate systolic function of the right ventricle was not performed.

STATISTICAL ANALYSIS

Data analysis was performed using SPSS (SPSS Inc, Chicago, Illinois). Mann-Whitney and χ2 tests were done to compare participants with nonparticipants and the control group with the patient group with regard to patient characteristics. The worst shortening fraction during admission was compared with shortening fraction at follow-up using paired t tests. Shortening fraction less than 30% and less than 28% during PICU admission and at follow-up were compared by using the Fisher exact test. A significance level of P < .05 was used in all tests.

To analyze risk factors for cardiac abnormalities, patients with cardiac abnormalities (rhythm disturbances, decreased left ventricular function, and/or decreased right ventricular function) were clustered because of the small number of patients. Mann-Whitney and χ2 tests were used to compare characteristics of patients with and without cardiac abnormalities, such as sex, age at PICU admission, age at follow-up, follow-up time, risk of mortality (Pediatric Index of Mortality 2), length of ventilation, and length of PICU stay. Furthermore, nonparametric correlations were performed to test the association between cardiac abnormalities and the use of different inotropic and/or vasoconstrictive agents, and the dosage and duration of treatment with these agents. A significance level of P < .001 was used in these tests to compensate for multiple testing.

One hundred forty-four patients who were admitted to our PICU for septic shock from 1995 through 2005 and survived fulfilled the inclusion criteria. Eleven patients refused to participate and 25 patients could not be located. One hundred eight of 144 eligible patients (75%) were evaluated. No statistically significant differences were found between participants and nonparticipants, except for sex (Table 1). The age of PICU patients ranged from newborns (with a birth weight >2 kg) to 18 years. Median follow-up time was 6.3 years (range, 0.8-12.7 years).

Table Graphic Jump LocationTable 1. Characteristics of Study Participants and Nonparticipants

The exercise test was performed in 87 of 108 patients (81%) aged 7 years or older. Twenty-four-hour ECG recording was successfully performed in 86 of 108 patients (80%). Evaluations of systolic function of the left and right ventricles were successfully performed in 105 of 108 patients (97%) and 86 of 108 patients (80%), respectively.

Medical history and physical examination revealed no abnormalities in all but 1 patient (1%). This patient complained of dyspnea while at rest and had a limited exercise capacity due to respiratory obstruction caused by an, until then, unknown tracheal stenosis, which was probably due to intubation. All patients had normal ECG results at rest and a good exercise capacity. Episodes of premature ventricular contractions (PVCs) were seen in 7 of 87 patients (8%) during and after exercise (3 patients [3.5%] had monomorphic PVCs during exercise, 3 patients (3.5%) had monomorphic PVCs during rest after exercise, and 1 patient (1%) had a series of polymorphic PVCs during exercise). In 3 of the aforementioned patients (3.5%), episodes of PVCs were seen on the 24-hour ECG recording (polymorphic PVCs in 2 and monomorphic PVCs in 1). One patient (1%) had a sinus arrest of 2.6 seconds (Table 2).

Table Graphic Jump LocationTable 2. Cardiac Abnormalities in Pediatric Septic Shock Survivors at Follow-Up

The median shortening fraction at follow-up in 105 patients was 35.9% (range, 25.0%-47.2%); 13 of 105 children (12%) had a shortening fraction of less than 30%, and 3 of 105 children (3%) had a shortening fraction of less than 28%. One of the children (1%) with a shortening fraction of less than 28% had reduced left ventricular function (shortening fraction of 25%) with paradoxical movement of the intraventricular septum and a series of PVCs during exercise. This patient had a shortening fraction of 25% at PICU discharge. He is an active athlete and has no complaints (Table 2). All the other children had normal wall motion of the left ventricle.

The median TAPSE at follow-up in 86 patients was 20.7 mm (range, 13.5-32.3 mm); 1 of 86 children (1%) had a TAPSE shorter than 15 mm. No other abnormalities at echocardiography were found (Table 2).

In 65 of 108 patients (60%), we compared shortening fraction measured during PICU admission and at follow-up (Table 3). During admission, the worst median shortening fraction was 27.0% (range, 14.3%-48.9%); at follow-up, the median shortening fraction was 36.2% (range, 25.0%-47.2%). A statistical difference was found between worst median shortening fraction during admission and median shortening fraction at follow-up. During admission, 36 of these 65 children (55%) had a worst shortening fraction of less than 30%; 34 (52%) of them had a worst shortening fraction of less than 28%. At follow-up, 6 of these 65 children (9%) had a shortening fraction of less than 30% and 2 children (3%) had a shortening fraction of less than 28% (Table 3). The children with a shortening fraction of less than 30% and those with a shortening fraction of less than 28% during admission were compared with children with a shortening fraction of less than 30% and those with a shortening fraction of less than 28%, respectively, at follow-up by Fisher exact test. No association was found (Table 3).

Table Graphic Jump LocationTable 3. Longitudinal Systolic Function During PICU Admission and at Follow-up in 65 of 108 Patients

The control group of 52 healthy children consisted of 22 girls and 30 boys with a median age of 5.9 years (range, 0.8-17.3 years). The median shortening fraction was 36.2% (range, 28.1%-44.9%), and the median TAPSE was 19.9 mm (range, 16.1-31.0 mm). The median age of the control group was significantly less than that of the patient group (Table 4).

Table Graphic Jump LocationTable 4. Shortening Fraction and TAPSE in Patients and 52 Healthy Children

Cardiac abnormalities were detected in 6 patients (shortening fraction <28% in 2, shortening fraction <28% and polymorphic PVCs in 1, TAPSE <15 mm in 1, and polymorphic PVCs in 2). No statistically significant differences were found between children with and without cardiac abnormalities with respect to sex, age at PICU admission, age at follow-up, follow-up time, risk of mortality (Pediatric Index of Mortality 2), length of ventilation, and length of PICU stay. No correlations were found between cardiac abnormalities and inotropic and/or vasoconstrictive agents used or duration of treatment with or dosage of these agents (Table 5).

Table Graphic Jump LocationTable 5. Characteristics of Inotropic and Vasoconstrictive Treatment of 108 Patients and Correlation Between Cardiac Abnormalities and Inotropic and Vasoconstrictive Treatment in 6 Patients

In this study of 108 pediatric septic shock survivors, 6 children had cardiac abnormalities consisting of PVCs during exercise with 24-hour ECG registration (2 patients), decreased left ventricular function (2 patients), decreased left ventricular function and PVCs (1 patient), and decreased right ventricular function (1 patient). Surprisingly, only 1 patient had abnormalities according to medical history and physical examination. These complaints were caused by tracheal injury due to the endotracheal tube and not cardiac dysfunction.

The rhythm disturbances found in this study are difficult to interpret. Because ECG recording at PICU admission was not standard procedure, we could not compare our findings with ECG data in the acute phase. Studies of healthy ambulatory children have documented various rhythm disturbances with a range of incidences. Monomorphic PVCs are benign; polymorphic PVCs may form a risk for ventricular tachycardia and sudden cardiac death.2024 Only 3 children had polymorphic PVC. The incidence of rhythm disturbances in our study is probably not higher than that found in the normal population. Literature on incidences and clinical relevance of rhythm disturbances in healthy children is scarce. Additional studies in pediatric septic shock survivors and healthy control groups have to be done. Our findings, however, are reassuring and suggest excellent recovery after septic shock with inotropic and/or vasoconstrictive support.

Septicemia is associated with acute myocardial failure. In adult studies, myocardial function during septic shock is evaluated predominantly with echocardiography. In these studies, reduced ejection fraction was found in 40% to 50% of patients with septic shock. Right heart dilation and decreased right ventricular function have also been described in the acute phase. The decrease in left ventricular function was reversible with full recovery of cardiac function in 7 to 10 days.25,26 Theoretically, it is conceivable that myocardial damage due to the inflammatory response, cell death, and apoptosis with remodeling does not repair completely and leads to impaired myocardial function.27,28 Furthermore, shock combined with inotropic and/or vasoconstrictive agents may cause cardiovascular damage.4,2931 It is conceivable that children are even more at risk for tissue damage because of their still-developing organ systems.3234 In our study, left and right ventricular function was normal in almost all patients (only 3 patients had shortening fraction <28% and 1 patient with TAPSE <15 mm). The implications for future cardiac function in children with decreased function are unknown and need further research. Because correlations with possible risk factors were not found, the data do not support our hypothesis. However, analysis of risk factors is only possible to formulate hypotheses for future studies owing to the small number of children with abnormalities. We believe that against the background of aging, long-term cardiac follow-up of septic shock survivors and a healthy control group is important.

A number of limitations to this study should be taken into account. First, the response rate of our study was 75%. Although other follow-up studies in the PICU have had similar response rates, this could have biased our results. Second, the number of studied children is small; owing to differences in age at PICU admission and follow-up and in follow-up times, strong conclusions are difficult. Follow-up times varied between 0.8 and 12.7 years; evaluation of late effects is not possible 0.8 years after discharge and thus our results may have been biased by including patients with the shortest follow-up times. As damaging effects of septic shock may only be seen much later in life, our follow-up time may have been too short. Third, we only had a healthy control group for cardiac function. The median age of this control group was significantly younger than the median age of the study patients. The prevalences of rhythm disturbances and decreased right ventricular function in healthy children are not well documented in the literature. The median TAPSE in our healthy controls was 19.9 mm (range, 16-31 mm). The cutoff for a normal TAPSE of 15 mm in children was possibly too low. Fourth, because this is a retrospective cohort study, it was not possible to analyze fluid at the same time echocardiography was performed. It was also not possible to evaluate the effect of other cardiodepressant medication possibly given in the acute phase. Fifth, the risk factor analysis is statistically questionable because of the small number of children with abnormalities. A prospective study with an adequate control group is necessary to analyze risk factors for cardiac damage.

In this small and diverse group of pediatric septic shock survivors, we found excellent recovery of cardiac performance in most patients. In a limited number of children, we found rhythm disturbances and decreased left ventricular function. We believe that long-term cardiac follow-up in these patients is important.

Correspondence: Hendrika Knoester, MD, Pediatric Intensive Care Unit, Emma Children's Hospital, Academic Medical Centre, Meibergdreef 9, 1105 AZ Amsterdam, the Netherlands (h.knoester@amc.uva.nl).

Accepted for Publication: May 8, 2008.

Author Contributions:Study concept and design: Knoester, Sol, Ramsodit, Kuipers, and Bos. Acquisition of data: Knoester, Sol, Ramsodit, and Kuipers. Analysis and interpretation of data: Knoester, Sol, Ramsodit, Kuipers, Clur, and Bos. Drafting of the manuscript: Knoester, Sol, Ramsodit, and Kuipers. Critical revision of the manuscript for important intellectual content: Knoester, Sol, Ramsodit, Kuipers, Clur, and Bos. Statistical analysis: Knoester, Sol, and Ramsodit. Administrative, technical, and material support: Knoester, Sol, Ramsodit, and Kuipers. Study supervision: Knoester, Kuipers, Clur, and Bos.

Financial Disclosure: None reported.

Additional Information: Both Drs Knoester and Sol served as first authors of this article.

Odetola  FOGebremariam  AFreed  GL Patient and hospital correlates of clinical outcomes and resource utilization in severe pediatric sepsis. Pediatrics 2007;119 (3) 487- 494
PubMed Link to Article
Binck  BWTsen  MFIslas  M  et al.  Bone marrow-derived cells contribute to contractile dysfunction in endotoxic shock. Am J Physiol Heart Circ Physiol 2005;288 (2) H577- H583
PubMed Link to Article
Kumar  AKrieger  ASymeoneides  SKumar  AParrillo  JE Myocardial dysfunction in septic shock, part II: role of cytokines and nitric oxide. J Cardiothorac Vasc Anesth 2001;15 (4) 485- 511
PubMed Link to Article
Rudiger  ASinger  M Mechanisms of sepsis-induced cardiac dysfunction. Crit Care Med 2007;35 (6) 1599- 1608
PubMed Link to Article
Beale  RJHollenberg  SMVincent  JLParrillo  JE Vasopressor and inotropic support in septic shock: an evidence-based review Crit Care Med 2004;32 (11) ((suppl)) S455- S465
PubMed Link to Article
Dellinger  RPCarlet  JMMasur  H  et al.  Surviving Sepsis Campaign guidelines for management of severe sepsis and septic shock [errata in Crit Care Med. 2004;32(6):1448, correction of dosage error in text; Crit Care Med. 2004;32(10):2169-2170]. Crit Care Med 2004;32 (3) 858- 873
PubMed Link to Article
Leclerc  FLeteurtre  SDuhamel  A  et al.  Cumulative influence of organ dysfunctions and septic state on mortality of critically ill children. Am J Respir Crit Care Med 2005;171 (4) 348- 353
PubMed Link to Article
Maat  MBuysse  CMEmonts  M  et al.  Improved survival of children with sepsis and purpura: effects of age, gender, and era. Crit Care 2007;11 (5) R112
PubMed Link to Article
Goldacre  MJRoberts  SEYeates  D Case fatality rates for meningococcal disease in an English population, 1963-98: database study. BMJ 2003;327 (7415) 596- 597
PubMed Link to Article
Judge  DNadel  SVergnaud  SGarralda  ME Psychiatric adjustment following meningococcal disease treated on a PICU. Intensive Care Med 2002;28 (5) 648- 650
PubMed Link to Article
Plötz  FBvan Vught  HUiterwaal  CSRiedijk  Mvan der Ent  CK Exercise-induced oxygen desaturation as a late complication of meningococcal septic shock syndrome. JAMA 2001;285 (3) 293- 294
PubMed Link to Article
Schibler  A Physiological consequences of early-life insult. Paediatr Respir Rev 2006;7 (2) 103- 109
PubMed Link to Article
Baraldi  EFilippone  M Chronic lung disease after premature birth. N Engl J Med 2007;357 (19) 1946- 1955
PubMed Link to Article
Morris  CKMyers  JFroelicher  VFKawaguchi  TUeshima  KHideg  A Nomogram based on metabolic equivalents and age for assessing aerobic exercise capacity in men. J Am Coll Cardiol 1993;22 (1) 175- 182
PubMed Link to Article
Colan  SDParness  IASpevak  PJSanders  SP Developmental modulation of myocardial mechanics: age- and growth-related alterations in afterload and contractility. J Am Coll Cardiol 1992;19 (3) 619- 629
PubMed Link to Article
Hagmolen of ten Have  WWiegman  Avan den Hoek  GJVreede  WBDerkx  HH Life-threatening heart failure in meningococcal septic shock in children: non-invasive measurement of cardiac parameters is of important prognostic value. Eur J Pediatr 2000;159 (4) 277- 282
PubMed Link to Article
Rowland  DGGutgesell  HP Noninvasive assessment of myocardial contractility, preload, and afterload in healthy newborn infants. Am J Cardiol 1995;75 (12) 818- 821
PubMed Link to Article
Park  MK Pediatric Cardiology for Practitioners. 5th ed. Philadelphia, PA Mosby Elsevier2008;
Kaul  STei  CHopkins  JMShah  PM Assessment of right ventricular function using two-dimensional echocardiography. Am Heart J 1984;107 (3) 526- 531
PubMed Link to Article
Bjelakovic  BVukomanovic  GVukomanovic  V  et al.  Heart rate variability in children with idiopathic ventricular tachycardia. Clin Auton Res 2007;17 (3) 153- 159
PubMed Link to Article
Chiu  SNWang  JKWu  MH  et al.  Cardiac conduction disturbance detected in a pediatric population. J Pediatr 2008;152 (1) 85- 89
PubMed Link to Article
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PubMed Link to Article
Parker  MMShelhamer  JHBacharach  SL  et al.  Profound but reversible myocardial depression in patients with septic shock. Ann Intern Med 1984;100 (4) 483- 490
PubMed Link to Article
Parker  MMMcCarthy  KEOgnibene  FPParrillo  JE Right ventricular dysfunction and dilatation, similar to left ventricular changes, characterize the cardiac depression of septic shock in humans. Chest 1990;97 (1) 126- 131
PubMed Link to Article
Jugdutt  BI Ventricular remodeling after infarction and the extracellular collagen matrix: when is enough enough? Circulation 2003;108 (11) 1395- 1403
PubMed Link to Article
Kumar  AKumar  AParrillo  JE Reversible myocardial dysfunction: an ubiquitous phenomenon in the critically ill? Crit Care Med 2002;30 (6) 1392- 1393
PubMed Link to Article
Pathan  NFaust  SNLevin  M Pathophysiology of meningococcal meningitis and septicaemia. Arch Dis Child 2003;88 (7) 601- 607
PubMed Link to Article
Singal  PKDhillon  KSBeamish  REKapur  NDhalla  NS Myocardial cell damage and cardiovascular changes due to i.v. infusion of adrenochrome in rats. Br J Exp Pathol 1982;63 (2) 167- 176
PubMed
Song  DLMei  SPDong  YHSpapen  H Influence of catecholamines on myocardium in experimental septic shock. Zhongguo Wei Zhong Bing Ji Jiu Yi Xue 2003;15 (11) 675- 679
PubMed
Martin  HHu  JGennser  GNorman  M Impaired endothelial function and increased carotid stiffness in 9-year-old children with low birthweight. Circulation 2000;102 (22) 2739- 2744
PubMed Link to Article
Norman  MMartin  H Preterm birth attenuates association between low birth weight and endothelial dysfunction. Circulation 2003;108 (8) 996- 1001
PubMed Link to Article
Thorburn  KBaines  PThomson  AHart  CA Mortality in severe meningococcal disease. Arch Dis Child 2001;85 (5) 382- 385
PubMed Link to Article

Figures

Tables

Table Graphic Jump LocationTable 1. Characteristics of Study Participants and Nonparticipants
Table Graphic Jump LocationTable 2. Cardiac Abnormalities in Pediatric Septic Shock Survivors at Follow-Up
Table Graphic Jump LocationTable 3. Longitudinal Systolic Function During PICU Admission and at Follow-up in 65 of 108 Patients
Table Graphic Jump LocationTable 4. Shortening Fraction and TAPSE in Patients and 52 Healthy Children
Table Graphic Jump LocationTable 5. Characteristics of Inotropic and Vasoconstrictive Treatment of 108 Patients and Correlation Between Cardiac Abnormalities and Inotropic and Vasoconstrictive Treatment in 6 Patients

References

Odetola  FOGebremariam  AFreed  GL Patient and hospital correlates of clinical outcomes and resource utilization in severe pediatric sepsis. Pediatrics 2007;119 (3) 487- 494
PubMed Link to Article
Binck  BWTsen  MFIslas  M  et al.  Bone marrow-derived cells contribute to contractile dysfunction in endotoxic shock. Am J Physiol Heart Circ Physiol 2005;288 (2) H577- H583
PubMed Link to Article
Kumar  AKrieger  ASymeoneides  SKumar  AParrillo  JE Myocardial dysfunction in septic shock, part II: role of cytokines and nitric oxide. J Cardiothorac Vasc Anesth 2001;15 (4) 485- 511
PubMed Link to Article
Rudiger  ASinger  M Mechanisms of sepsis-induced cardiac dysfunction. Crit Care Med 2007;35 (6) 1599- 1608
PubMed Link to Article
Beale  RJHollenberg  SMVincent  JLParrillo  JE Vasopressor and inotropic support in septic shock: an evidence-based review Crit Care Med 2004;32 (11) ((suppl)) S455- S465
PubMed Link to Article
Dellinger  RPCarlet  JMMasur  H  et al.  Surviving Sepsis Campaign guidelines for management of severe sepsis and septic shock [errata in Crit Care Med. 2004;32(6):1448, correction of dosage error in text; Crit Care Med. 2004;32(10):2169-2170]. Crit Care Med 2004;32 (3) 858- 873
PubMed Link to Article
Leclerc  FLeteurtre  SDuhamel  A  et al.  Cumulative influence of organ dysfunctions and septic state on mortality of critically ill children. Am J Respir Crit Care Med 2005;171 (4) 348- 353
PubMed Link to Article
Maat  MBuysse  CMEmonts  M  et al.  Improved survival of children with sepsis and purpura: effects of age, gender, and era. Crit Care 2007;11 (5) R112
PubMed Link to Article
Goldacre  MJRoberts  SEYeates  D Case fatality rates for meningococcal disease in an English population, 1963-98: database study. BMJ 2003;327 (7415) 596- 597
PubMed Link to Article
Judge  DNadel  SVergnaud  SGarralda  ME Psychiatric adjustment following meningococcal disease treated on a PICU. Intensive Care Med 2002;28 (5) 648- 650
PubMed Link to Article
Plötz  FBvan Vught  HUiterwaal  CSRiedijk  Mvan der Ent  CK Exercise-induced oxygen desaturation as a late complication of meningococcal septic shock syndrome. JAMA 2001;285 (3) 293- 294
PubMed Link to Article
Schibler  A Physiological consequences of early-life insult. Paediatr Respir Rev 2006;7 (2) 103- 109
PubMed Link to Article
Baraldi  EFilippone  M Chronic lung disease after premature birth. N Engl J Med 2007;357 (19) 1946- 1955
PubMed Link to Article
Morris  CKMyers  JFroelicher  VFKawaguchi  TUeshima  KHideg  A Nomogram based on metabolic equivalents and age for assessing aerobic exercise capacity in men. J Am Coll Cardiol 1993;22 (1) 175- 182
PubMed Link to Article
Colan  SDParness  IASpevak  PJSanders  SP Developmental modulation of myocardial mechanics: age- and growth-related alterations in afterload and contractility. J Am Coll Cardiol 1992;19 (3) 619- 629
PubMed Link to Article
Hagmolen of ten Have  WWiegman  Avan den Hoek  GJVreede  WBDerkx  HH Life-threatening heart failure in meningococcal septic shock in children: non-invasive measurement of cardiac parameters is of important prognostic value. Eur J Pediatr 2000;159 (4) 277- 282
PubMed Link to Article
Rowland  DGGutgesell  HP Noninvasive assessment of myocardial contractility, preload, and afterload in healthy newborn infants. Am J Cardiol 1995;75 (12) 818- 821
PubMed Link to Article
Park  MK Pediatric Cardiology for Practitioners. 5th ed. Philadelphia, PA Mosby Elsevier2008;
Kaul  STei  CHopkins  JMShah  PM Assessment of right ventricular function using two-dimensional echocardiography. Am Heart J 1984;107 (3) 526- 531
PubMed Link to Article
Bjelakovic  BVukomanovic  GVukomanovic  V  et al.  Heart rate variability in children with idiopathic ventricular tachycardia. Clin Auton Res 2007;17 (3) 153- 159
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Chiu  SNWang  JKWu  MH  et al.  Cardiac conduction disturbance detected in a pediatric population. J Pediatr 2008;152 (1) 85- 89
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