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Tetralogy of Fallot

Tetralogy of Fallot is the most common cyanotic congenital Congenital Chorioretinitis heart disease. The disease is the confluence of 4 pathologic cardiac features: overriding aorta Aorta The main trunk of the systemic arteries. Mediastinum and Great Vessels: Anatomy, ventricular septal defect, right ventricular outflow obstruction, and right ventricular hypertrophy Hypertrophy General increase in bulk of a part or organ due to cell enlargement and accumulation of fluids and secretions, not due to tumor formation, nor to an increase in the number of cells (hyperplasia). Cellular Adaptation. The timing and severity of presentation usually depend on the degree of right ventricular outflow obstruction. Definitive diagnosis is usually established by echocardiogram Echocardiogram Transposition of the Great Vessels. Chest X-ray X-ray Penetrating electromagnetic radiation emitted when the inner orbital electrons of an atom are excited and release radiant energy. X-ray wavelengths range from 1 pm to 10 nm. Hard x-rays are the higher energy, shorter wavelength x-rays. Soft x-rays or grenz rays are less energetic and longer in wavelength. The short wavelength end of the x-ray spectrum overlaps the gamma rays wavelength range. The distinction between gamma rays and x-rays is based on their radiation source. Pulmonary Function Tests may show the classic boot-shaped heart. Definitive treatment involves surgical repair. Long-term prognosis Prognosis A prediction of the probable outcome of a disease based on a individual's condition and the usual course of the disease as seen in similar situations. Non-Hodgkin Lymphomas is good for surgically corrected disease, but cardiovascular morbidity Morbidity The proportion of patients with a particular disease during a given year per given unit of population. Measures of Health Status is common.

Last updated: Sep 22, 2022

Editorial responsibility: Stanley Oiseth, Lindsay Jones, Evelin Maza

Overview

Definition

Tetralogy of Fallot (TOF) is the most common cyanotic congenital Congenital Chorioretinitis heart disease and has the following 4 (tetra) features:

Epidemiology

Etiology

  • Deviation of the infundibular septum during fetal development results in:
  • Most cases are sporadic Sporadic Selective IgA Deficiency, but a genetic component is likely.
  • 15% have a syndromic association:
    • DiGeorge syndrome DiGeorge syndrome DiGeorge syndrome (DGS) is a condition caused by a microdeletion at location q11.2 of chromosome 22 (thus also called 22q11.2 syndrome). There is a defective development of the third and fourth pharyngeal pouches, leading to thymic and parathyroid hypoplasia (causing T-cell immunodeficiency and hypocalcemia, respectively). DiGeorge Syndrome
    • Down’s syndrome
    • Alagille syndrome Alagille Syndrome Hyperbilirubinemia of the Newborn
  • Non-genetic risk factors:
    • Rubella Rubella An acute infectious disease caused by the rubella virus. The virus enters the respiratory tract via airborne droplet and spreads to the lymphatic system. Rubella Virus infection during pregnancy Pregnancy The status during which female mammals carry their developing young (embryos or fetuses) in utero before birth, beginning from fertilization to birth. Pregnancy: Diagnosis, Physiology, and Care
    • Maternal use of alcohol
    • Maternal age > 40

Mnemonics

DROP:

PROVe:

Pathophysiology

  • VSD is large and unrestrictive.
  • Pressure in left and right ventricles is essentially equal.
  • The direction of blood flow Blood flow Blood flow refers to the movement of a certain volume of blood through the vasculature over a given unit of time (e.g., mL per minute). Vascular Resistance, Flow, and Mean Arterial Pressure depends on the degree of RVOT obstruction:
    • Acyanotic presentation:
      • RVOT resistance Resistance Physiologically, the opposition to flow of air caused by the forces of friction. As a part of pulmonary function testing, it is the ratio of driving pressure to the rate of air flow. Ventilation: Mechanics of Breathing < aortic resistance Resistance Physiologically, the opposition to flow of air caused by the forces of friction. As a part of pulmonary function testing, it is the ratio of driving pressure to the rate of air flow. Ventilation: Mechanics of Breathing
      • Left-to-right shunting
    • Cyanotic presentation:
      • RVOT resistance Resistance Physiologically, the opposition to flow of air caused by the forces of friction. As a part of pulmonary function testing, it is the ratio of driving pressure to the rate of air flow. Ventilation: Mechanics of Breathing (significant RVOT obstruction) > aortic resistance Resistance Physiologically, the opposition to flow of air caused by the forces of friction. As a part of pulmonary function testing, it is the ratio of driving pressure to the rate of air flow. Ventilation: Mechanics of Breathing
      • Right-to-left shunting
    • Shunting can fluctuate:
      • Dynamic increase in RVOT resistance Resistance Physiologically, the opposition to flow of air caused by the forces of friction. As a part of pulmonary function testing, it is the ratio of driving pressure to the rate of air flow. Ventilation: Mechanics of Breathing
      • Sudden cyanotic (“tet”) spells
  • TOF may be associated with other cardiac defects:
    • Right aortic arch Aortic arch Mediastinum and Great Vessels: Anatomy (25% of cases)
    • Abnormalities of coronary arteries Arteries Arteries are tubular collections of cells that transport oxygenated blood and nutrients from the heart to the tissues of the body. The blood passes through the arteries in order of decreasing luminal diameter, starting in the largest artery (the aorta) and ending in the small arterioles. Arteries are classified into 3 types: large elastic arteries, medium muscular arteries, and small arteries and arterioles. Arteries: Histology
    • Multiple VSDs
    • Complete atrioventricular septal defects
    • Patent ductus arteriosus Ductus arteriosus A fetal blood vessel connecting the pulmonary artery with the descending aorta. Patent Ductus Arteriosus (PDA)
Pathophysiology of tetralogy of fallot

Anatomy and physiology of tetralogy of Fallot
Left: normal heart
Right: tetralogy of Fallot

Image by Lecturio.

Clinical Presentation

Age of presentation is inversely proportional to the degree of RVOT obstruction.

Severe RVOT obstruction

  • Presents in newborns
  • Profound cyanosis Cyanosis A bluish or purplish discoloration of the skin and mucous membranes due to an increase in the amount of deoxygenated hemoglobin in the blood or a structural defect in the hemoglobin molecule. Pulmonary Examination
  • Lethargy Lethargy A general state of sluggishness, listless, or uninterested, with being tired, and having difficulty concentrating and doing simple tasks. It may be related to depression or drug addiction. Hyponatremia
  • Poor feeding

Mild-to-moderate RVOT obstruction

  • Usually within 6 weeks of birth
  • Murmur picked up on physical exam
  • Progressive increase in RVOT obstruction → cyanosis Cyanosis A bluish or purplish discoloration of the skin and mucous membranes due to an increase in the amount of deoxygenated hemoglobin in the blood or a structural defect in the hemoglobin molecule. Pulmonary Examination
  • Failure to thrive Failure to Thrive Failure to thrive (FTT), or faltering growth, describes suboptimal weight gain and growth in children. The majority of cases are due to inadequate caloric intake; however, genetic, infectious, and oncological etiologies are also common. Failure to Thrive
  • Tet spells:
    • Worsening cyanosis Cyanosis A bluish or purplish discoloration of the skin and mucous membranes due to an increase in the amount of deoxygenated hemoglobin in the blood or a structural defect in the hemoglobin molecule. Pulmonary Examination
    • Hyperpnea (rapid, shallow breaths)
    • Irritability
    • Precipitated by rapid increase in RVOT resistance Resistance Physiologically, the opposition to flow of air caused by the forces of friction. As a part of pulmonary function testing, it is the ratio of driving pressure to the rate of air flow. Ventilation: Mechanics of Breathing:
      • Pain Pain An unpleasant sensation induced by noxious stimuli which are detected by nerve endings of nociceptive neurons. Pain: Types and Pathways, crying
      • Feeding
      • Bowel movement
      • Agitation Agitation A feeling of restlessness associated with increased motor activity. This may occur as a manifestation of nervous system drug toxicity or other conditions. St. Louis Encephalitis Virus
      • Fever Fever Fever is defined as a measured body temperature of at least 38°C (100.4°F). Fever is caused by circulating endogenous and/or exogenous pyrogens that increase levels of prostaglandin E2 in the hypothalamus. Fever is commonly associated with chills, rigors, sweating, and flushing of the skin. Fever

Minimal RVOT obstruction

  • Initially asymptomatic
  • Develop pulmonary overcirculation in first 4–6 weeks
  • Heart failure Heart Failure A heterogeneous condition in which the heart is unable to pump out sufficient blood to meet the metabolic need of the body. Heart failure can be caused by structural defects, functional abnormalities (ventricular dysfunction), or a sudden overload beyond its capacity. Chronic heart failure is more common than acute heart failure which results from sudden insult to cardiac function, such as myocardial infarction. Total Anomalous Pulmonary Venous Return (TAPVR): dyspnea Dyspnea Dyspnea is the subjective sensation of breathing discomfort. Dyspnea is a normal manifestation of heavy physical or psychological exertion, but also may be caused by underlying conditions (both pulmonary and extrapulmonary). Dyspnea, tachypnea Tachypnea Increased respiratory rate. Pulmonary Examination

Diagnosis

Physical examination

Imaging

  • Chest X ray:
  • Echocardiogram Echocardiogram Transposition of the Great Vessels:
    • Main confirmatory test
    • Can also be used for prenatal diagnosis
    • Evaluates:
      • Location and number of VSDs
      • Anatomy and severity of RVOT obstruction
      • Aortic arch Aortic arch Mediastinum and Great Vessels: Anatomy anatomy
      • Coronary arteries Arteries Arteries are tubular collections of cells that transport oxygenated blood and nutrients from the heart to the tissues of the body. The blood passes through the arteries in order of decreasing luminal diameter, starting in the largest artery (the aorta) and ending in the small arterioles. Arteries are classified into 3 types: large elastic arteries, medium muscular arteries, and small arteries and arterioles. Arteries: Histology
      • Associated anomalies

Other tests

  • Electrocardiogram Electrocardiogram An electrocardiogram (ECG) is a graphic representation of the electrical activity of the heart plotted against time. Adhesive electrodes are affixed to the skin surface allowing measurement of cardiac impulses from many angles. The ECG provides 3-dimensional information about the conduction system of the heart, the myocardium, and other cardiac structures. Electrocardiogram (ECG) ( ECG ECG An electrocardiogram (ECG) is a graphic representation of the electrical activity of the heart plotted against time. Adhesive electrodes are affixed to the skin surface allowing measurement of cardiac impulses from many angles. The ECG provides 3-dimensional information about the conduction system of the heart, the myocardium, and other cardiac structures. Electrocardiogram (ECG); signs of right ventricular hypertrophy Hypertrophy General increase in bulk of a part or organ due to cell enlargement and accumulation of fluids and secretions, not due to tumor formation, nor to an increase in the number of cells (hyperplasia). Cellular Adaptation):
  • Cardiac catheterization Cardiac Catheterization Procedures in which placement of cardiac catheters is performed for therapeutic or diagnostic procedures. Cardiac Surgery:
    • To further delineate anatomy in addition to echocardiogram Echocardiogram Transposition of the Great Vessels
    • Will show equal systemic left and right ventricular pressures
    • Normal or low pulmonary artery Pulmonary artery The short wide vessel arising from the conus arteriosus of the right ventricle and conveying unaerated blood to the lungs. Lungs: Anatomy pressures
    • Can be therapeutic: balloon valvuloplasty of the pulmonary valve Pulmonary valve A valve situated at the entrance to the pulmonary trunk from the right ventricle. Heart: Anatomy

Management

Medical management

  • Neonates with severe form: intravenous prostaglandins Prostaglandins A group of compounds derived from unsaturated 20-carbon fatty acids, primarily arachidonic acid, via the cyclooxygenase pathway. They are extremely potent mediators of a diverse group of physiological processes. Eicosanoids to maintain ductus arteriosus Ductus arteriosus A fetal blood vessel connecting the pulmonary artery with the descending aorta. Patent Ductus Arteriosus (PDA) patency
  • Tet spells:
    • The rationale is to increase pulmonary blood flow Blood flow Blood flow refers to the movement of a certain volume of blood through the vasculature over a given unit of time (e.g., mL per minute). Vascular Resistance, Flow, and Mean Arterial Pressure.
    • Knee-chest position (squat for older children): increases systemic vascular resistance Resistance Physiologically, the opposition to flow of air caused by the forces of friction. As a part of pulmonary function testing, it is the ratio of driving pressure to the rate of air flow. Ventilation: Mechanics of Breathing
    • Oxygen: vasodilator for pulmonary artery Pulmonary artery The short wide vessel arising from the conus arteriosus of the right ventricle and conveying unaerated blood to the lungs. Lungs: Anatomy
    • IV fluids IV fluids Intravenous fluids are one of the most common interventions administered in medicine to approximate physiologic bodily fluids. Intravenous fluids are divided into 2 categories: crystalloid and colloid solutions. Intravenous fluids have a wide variety of indications, including intravascular volume expansion, electrolyte manipulation, and maintenance fluids. Intravenous Fluids: improves right atrium filling volume
    • Morphine Morphine The principal alkaloid in opium and the prototype opiate analgesic and narcotic. Morphine has widespread effects in the central nervous system and on smooth muscle. Opioid Analgesics: mechanism unclear
    • Beta-blockers Beta-blockers Drugs that bind to but do not activate beta-adrenergic receptors thereby blocking the actions of beta-adrenergic agonists. Adrenergic beta-antagonists are used for treatment of hypertension, cardiac arrhythmias, angina pectoris, glaucoma, migraine headaches, and anxiety. Class 2 Antiarrhythmic Drugs (Beta Blockers): RVOT relaxation
    • Phenylephrine Phenylephrine An alpha-1 adrenergic agonist used as a mydriatic, nasal decongestant, and cardiotonic agent. Sympathomimetic Drugs: increases systemic afterload Afterload Afterload is the resistance in the aorta that prevents blood from leaving the heart. Afterload represents the pressure the LV needs to overcome to eject blood into the aorta. Cardiac Mechanics
  • Heart failure Heart Failure A heterogeneous condition in which the heart is unable to pump out sufficient blood to meet the metabolic need of the body. Heart failure can be caused by structural defects, functional abnormalities (ventricular dysfunction), or a sudden overload beyond its capacity. Chronic heart failure is more common than acute heart failure which results from sudden insult to cardiac function, such as myocardial infarction. Total Anomalous Pulmonary Venous Return (TAPVR):
    • Digoxin Digoxin A cardiotonic glycoside obtained mainly from digitalis lanata; it consists of three sugars and the aglycone digoxigenin. Digoxin has positive inotropic and negative chronotropic activity. It is used to control ventricular rate in atrial fibrillation and in the management of congestive heart failure with atrial fibrillation. Its use in congestive heart failure and sinus rhythm is less certain. The margin between toxic and therapeutic doses is small. Cardiac Glycosides
    • Loop diuretics Diuretics Agents that promote the excretion of urine through their effects on kidney function. Heart Failure and Angina Medication
    • ACE inhibitors ACE inhibitors Truncus Arteriosus and ARBs ARBs Agents that antagonize angiotensin receptors. Many drugs in this class specifically target the angiotensin type 1 receptor. Heart Failure and Angina Medication should not be used.
  • All cases: prophylactic antibiotics to prevent endocarditis Endocarditis Endocarditis is an inflammatory disease involving the inner lining (endometrium) of the heart, most commonly affecting the cardiac valves. Both infectious and noninfectious etiologies lead to vegetations on the valve leaflets. Patients may present with nonspecific symptoms such as fever and fatigue. Endocarditis until surgical repair

Surgical repair

Definitive:

  • Always required for normal functioning/lifespan
  • Preferred initial approach when feasible
  • Usually performed within the first 6 months of life
  • Procedure involves:
    • Repair of VSD
    • Enlargement of RVOT
    • Preservation of functional pulmonic valve if possible

Palliative:

Prognosis Prognosis A prediction of the probable outcome of a disease based on a individual’s condition and the usual course of the disease as seen in similar situations. Non-Hodgkin Lymphomas

  • Untreated: 
  • Repaired TOF patients Patients Individuals participating in the health care system for the purpose of receiving therapeutic, diagnostic, or preventive procedures. Clinician–Patient Relationship may have a normal life expectancy Life expectancy Based on known statistical data, the number of years which any person of a given age may reasonably expected to live. Population Pyramids.
  • High cardiovascular morbidity Morbidity The proportion of patients with a particular disease during a given year per given unit of population. Measures of Health Status; yearly monitoring required
  • Higher morbidity Morbidity The proportion of patients with a particular disease during a given year per given unit of population. Measures of Health Status with residual neurodevelopmental delay, even in treated infants
  • Post-surgical complications are frequent:
    • Recurrence of RVOT requiring reoperation
    • Pulmonary valve Pulmonary valve A valve situated at the entrance to the pulmonary trunk from the right ventricle. Heart: Anatomy insufficiency post-repair of the stenosis Stenosis Hypoplastic Left Heart Syndrome (HLHS)
    • Arrhythmias that may cause sudden cardiac death Sudden cardiac death Cardiac arrest is the sudden, complete cessation of cardiac output with hemodynamic collapse. Patients present as pulseless, unresponsive, and apneic. Rhythms associated with cardiac arrest are ventricular fibrillation/tachycardia, asystole, or pulseless electrical activity. Cardiac Arrest
    • Higher risk for bacterial endocarditis Bacterial endocarditis Inflammation of the endocardium caused by bacteria that entered the bloodstream. The strains of bacteria vary with predisposing factors, such as congenital heart defects; heart valve diseases; heart valve prosthesis implantation; or intravenous drug use. Endocarditis

Differential Diagnosis

  • Tricuspid atresia Atresia Hypoplastic Left Heart Syndrome (HLHS): congenital Congenital Chorioretinitis heart disease characterized by the lack of development of the tricuspid valve Tricuspid valve The valve consisting of three cusps situated between the right atrium and right ventricle of the heart. Heart: Anatomy. Presents with cyanosis Cyanosis A bluish or purplish discoloration of the skin and mucous membranes due to an increase in the amount of deoxygenated hemoglobin in the blood or a structural defect in the hemoglobin molecule. Pulmonary Examination, labored breathing, hypoxic spells. Holosystolic murmur Holosystolic Murmur Tricuspid Valve Atresia (TVA) and single S2 S2 Heart Sounds are present on exam. Diagnosis is made by echocardiogram Echocardiogram Transposition of the Great Vessels and ECG ECG An electrocardiogram (ECG) is a graphic representation of the electrical activity of the heart plotted against time. Adhesive electrodes are affixed to the skin surface allowing measurement of cardiac impulses from many angles. The ECG provides 3-dimensional information about the conduction system of the heart, the myocardium, and other cardiac structures. Electrocardiogram (ECG).
  • Transposition of the great vessels Transposition of the Great Vessels Transposition of the great vessels (TGV) is a cyanotic congenital heart disease characterized by “switching” of the great arteries. There are 2 presentations: the dextro (D)- and levo (L)-looped forms. The L-looped form is rare and congenitally corrected, as the ventricles are also switched. Transposition of the Great Vessels: congenital Congenital Chorioretinitis heart defect characterized by the switching of the great vessels so that the aorta Aorta The main trunk of the systemic arteries. Mediastinum and Great Vessels: Anatomy originates from the right ventricle and the pulmonary artery Pulmonary artery The short wide vessel arising from the conus arteriosus of the right ventricle and conveying unaerated blood to the lungs. Lungs: Anatomy from the left. Presents with cyanosis Cyanosis A bluish or purplish discoloration of the skin and mucous membranes due to an increase in the amount of deoxygenated hemoglobin in the blood or a structural defect in the hemoglobin molecule. Pulmonary Examination, tachypnea Tachypnea Increased respiratory rate. Pulmonary Examination, heart failure Heart Failure A heterogeneous condition in which the heart is unable to pump out sufficient blood to meet the metabolic need of the body. Heart failure can be caused by structural defects, functional abnormalities (ventricular dysfunction), or a sudden overload beyond its capacity. Chronic heart failure is more common than acute heart failure which results from sudden insult to cardiac function, such as myocardial infarction. Total Anomalous Pulmonary Venous Return (TAPVR), and hypoxemia Hypoxemia Neonatal Respiratory Distress Syndrome unresponsive to supplemental oxygen Supplemental Oxygen Respiratory Failure.
  • Truncus arteriosus Truncus arteriosus Truncus arteriosus (TA) is a congenital heart defect characterized by the persistence of a common cardiac arterial trunk tract that fails to divide into the pulmonary artery and aorta during embryonic development. Truncus arteriosus is a rare congenital malformation with a high mortality rate within the 1st 5 weeks of life if not managed promptly. Truncus Arteriosus: emergence of the aorta Aorta The main trunk of the systemic arteries. Mediastinum and Great Vessels: Anatomy and pulmonary artery Pulmonary artery The short wide vessel arising from the conus arteriosus of the right ventricle and conveying unaerated blood to the lungs. Lungs: Anatomy from a common trunk overriding a VSD. Symptomatic from the 1st days of life, including cyanosis Cyanosis A bluish or purplish discoloration of the skin and mucous membranes due to an increase in the amount of deoxygenated hemoglobin in the blood or a structural defect in the hemoglobin molecule. Pulmonary Examination, respiratory distress, heart failure Heart Failure A heterogeneous condition in which the heart is unable to pump out sufficient blood to meet the metabolic need of the body. Heart failure can be caused by structural defects, functional abnormalities (ventricular dysfunction), or a sudden overload beyond its capacity. Chronic heart failure is more common than acute heart failure which results from sudden insult to cardiac function, such as myocardial infarction. Total Anomalous Pulmonary Venous Return (TAPVR), poor feeding, and excessive sweating. Diagnosed by echocardiogram Echocardiogram Transposition of the Great Vessels.
  • Total anomalous pulmonary venous return: rare congenital Congenital Chorioretinitis cardiopathy in which pulmonary veins Pulmonary veins The veins that return the oxygenated blood from the lungs to the left atrium of the heart. Lungs: Anatomy drain to sites other than the left atrium. Presents with cyanosis Cyanosis A bluish or purplish discoloration of the skin and mucous membranes due to an increase in the amount of deoxygenated hemoglobin in the blood or a structural defect in the hemoglobin molecule. Pulmonary Examination from birth, heart failure Heart Failure A heterogeneous condition in which the heart is unable to pump out sufficient blood to meet the metabolic need of the body. Heart failure can be caused by structural defects, functional abnormalities (ventricular dysfunction), or a sudden overload beyond its capacity. Chronic heart failure is more common than acute heart failure which results from sudden insult to cardiac function, such as myocardial infarction. Total Anomalous Pulmonary Venous Return (TAPVR), and respiratory distress. Characterized by wide-split S2 S2 Heart Sounds.
  • Ebstein anomaly: congenital Congenital Chorioretinitis heart defect in which there is downward displacement Displacement The process by which an emotional or behavioral response that is appropriate for one situation appears in another situation for which it is inappropriate. Defense Mechanisms of the tricuspid valve Tricuspid valve The valve consisting of three cusps situated between the right atrium and right ventricle of the heart. Heart: Anatomy leaflets causing RVOT obstruction. Presents with cyanosis Cyanosis A bluish or purplish discoloration of the skin and mucous membranes due to an increase in the amount of deoxygenated hemoglobin in the blood or a structural defect in the hemoglobin molecule. Pulmonary Examination, arrhythmias, and failure to thrive Failure to Thrive Failure to thrive (FTT), or faltering growth, describes suboptimal weight gain and growth in children. The majority of cases are due to inadequate caloric intake; however, genetic, infectious, and oncological etiologies are also common. Failure to Thrive. Diagnosed by echocardiogram Echocardiogram Transposition of the Great Vessels.

References

  1. Doyle T., Kavanaugh-McHue A., Fish F.A. (2019). Management and Outcome of tetralogy of Fallot. Retrieved December 19, 2020, from https://www.uptodate.com/contents/management-and-outcome-of-tetralogy-of-fallot?search=tetralogy%20of%20fallot&source=search_result&selectedTitle=2~111&usage_type=default&display_rank=2
  2. Doyle T., Kavanaugh-McHue A. (2018). Pathophysiology, clinical features, and diagnosis of tetralogy of Fallot. Retrieved December 18, 2020, from https://www.uptodate.com/contents/pathophysiology-clinical-features-and-diagnosis-of-tetralogy-of-fallot?search=tetralogy%20of%20fallot&source=search_result&selectedTitle=1~102&usage_type=default&display_rank=1
  3. Kliegman R. M., St Geme, Joseph W., Blum, N. J., Shah, Samir S., Tasker, Robert C., & Wilson, Karen M. (2020). Cyanotic congenital heart disease: Lesions associated with decreased pulmonary blood flow. In R. M. Kliegman, J. W. St Geme, N. J. Blum, Shah, Samir S., Tasker, Robert C., & Wilson, Karen M. (Eds.). Nelson textbook of pediatrics (pp. 239-2407.e1). https://www.clinicalkey.es/#!/content/3-s2.0-B9780323529501004570

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