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R E V I E W A R T I C L E

Hemoptysis in Children

G S GAUDE

From Department of Pulmonary Medicine, JN Medical College, Belgaum, Karnataka, India. Correspondence to: Dr G S Gaude, Professor and Head, Department of Pulmonary Medicine, J N Medical College, Belgaum 590 010, Karnataka, India. [email protected] Received: November, 11, 2008; Initial review: May, 8, 2009; Accepted: July 27, 2009.

Context: and are uncommon in childhood, and the frequency with which they are encountered by the pediatrician depends largely on the special interests of the center to which the child is referred. Diagnosis and management of hemoptysis in this age group requires knowledge and skill in the causes and management of this infrequently occurring potentially life-threatening condition.

Evidence acquisition: We reviewed the causes and treatment options for hemoptysis in the pediatric patient using Medline and Pubmed.

Results: A focused physical examination can lead to the diagnosis of hemoptysis in most of the cases. In children, lower and aspiration are common causes. Chest radiographs often aid in diagnosis and assist in using two complementary diagnostic procedures, fiberoptic and high-resolution computed tomography. The goals of management are threefold: cessation, aspiration prevention, and treatment of the underlying cause. Mild hemoptysis often is caused by an infection that can be managed on an outpatient basis with close monitoring. Massive hemoptysis may require additional therapeutic options such as therapeutic bronchoscopy, angiography with , and surgical intervention such as resection or revascularization.

Conclusions: Hemoptysis in the pediatric patient requires prompt and thorough evaluation and treatment. An efficient systematic evaluation is imperative in identifying the underlying etiology and aggressive management is important because of the potential severity of the problem. This clinical review highlights the various etiological factors, the diagnostic and treatment strategies of hemoptysis in children.

Key words: Children, Hemoptysis, Management, Pulmonary hemorrhage, Review.

ulmonary hemorrhage was not commonly Most important in children is to first establish described in children in the early texts, that the child is experiencing hemoptysis. Extra- although it was noted to occur. Hemoptysis pulmonary bleeding, such as those arising from the Pis defined as the expectoration of or nose, or the , may be blood-tinged from the lower respiratory tract. incorrectly attributed to hemoptysis. This is known Although common in adults, blood tinged sputum is a as pseudo-hemoptysis. As the diagnostic and rare presenting symptom in children. The diagnosis treatment strategies differ markedly, the two of pediatric hemoptysis can be challenging. Children sources must be differentiated. The blood in tend to swallow their sputum; therefore, hemoptysis hemoptysis is bright red in color and may be may go unnoticed unless the bleeding is sub- admixed with sputum and frothy. The blood in stantial(1). Coupled with this, the inability to provide hemetemesis is dark red or brown and may be mixed a complete history and to cooperate with a thorough with food particles(2). One also has to differentiate physical examination may further compound the factitious hemoptysis from real hemoptysis. Once diagnostic dilemma. Thus, hemoptysis can serve as a the distinction is made, the physician can proceed to source of significant anxiety for the patient, the uncover the underlying cause. Hemoptysis is family, and the pediatrician. classified as non-massive or massive based on the

INDIAN PEDIATRICS 245 VOLUME 47__MARCH 17, 2010 G S GAUDE HEMOPTYSIS IN CHILDREN volume of blood loss; however, there are no ETIOLOGY uniform definitions for these categories. Hemoptysis is considered massive if blood loss is The etiology of hemoptysis in children is as varied as more than 200 mL per day(3). in adults. The various causes of hemoptysis in children are summarized in Table I. Important causes Pulmonary hemorrhage may even be present in a of massive hemoptysis in children are: previously healthy infant in whom neonatal medical , pulmonary , CHD, problems have been ruled out. This pulmonary bronchial AV malformation, , hemorrhage can appear as hemoptysis or blood in , bronchial adenomas, DIC and the nose or airway with no evidence of upper tracheostomy-related. respiratory or gastrointestinal bleeding. Patients have acute respiratory distress or failure, requiring Acute lower respiratory tract infection, either in mechanical ventilation and chest radiography, and the form of or tracheobronchitis, usually demonstrate bilateral infiltrates. Centers for accounts for almost up to 40% of the cases(5). In a 10 Disease Control and Prevention (CDC) has given year retrospective study of hemoptysis in children, criteria for a confirmed case of pulmonary Coss-Bu, et al.(6) observed pneumonia to be the most frequent cause accounting for 31% of the hemorrhage in a previously healthy infant aged ≤ 1 episodes of hemoptysis in children. The presence of years of age with gestational age of ≥ 32 weeks, with no history of neonatal medical problems, and whose an infectious process (e.g. necrotizing pneumonia, conditions meets all the following three criteria(4): tuberculosis, abscess, infected bronchiectasis) leads to destruction of lung parenchyma and erosion (i) Abrupt or sudden onset of overt bleeding or of blood vessels, resulting in hemoptysis. obvious evidence of blood in the airway, have been reported as the most common etiology of including epistaxis, hemoptysis or frank blood hemoptysis in several studies in children(7,8). below the at visualization. Although tuberculosis used to be commonly implicated, few cases have been reported in pediatric (ii) Severe-appearing illness leading to acute literature(5,9). Only one study by Crocco, et al.(10) respiratory distress or respiratory failure reported high prevalence of hemoptysis in resulting in admission in PICU or NICU with intubation and mechanical ventilation. TABLE I CAUSES OF HEMOPTYSIS IN CHILDREN (iii)Diffuse unilateral or bilateral pulmonary • Infections - pneumonia, tracheobronchitis infiltrates visible on chest X-ray or CT scan of thorax, and these findings should be • Cystic fibrosis documented within 48 hours of examination of • Congenital heart diseases - ASD, VSD, complex cyanotic infant. heart diseases, tetralogy of fallot, truncus arteriosus, transposition of the great arteries Criteria for probable case of pulmonary • Tuberculosis hemorrhage in the infant include a previously • Foreign body aspiration healthy infant aged ≤ 1 year with a gestational age • Nasopharyngeal bleeding of ≥ 32 weeks, with(4): • Tracheostomy-related (i) Who has sudden onset of bleeding from the • Bronchiectasis airway, with or without respiratory distress, with • Pulmonary neoplasms or without intubation and with or without • Pulmonary hemosiderosis pulmonary infiltrates on chest X-ray or CT scan; • Factitious hemoptysis (a) Who died and had evidence of bleeding • Miscellaneous – invasive aspergillosis, pulmonary from the airway found on autopsy or arteritis, catamenial hemoptysis, hydatid cysts in postmortem. • Unknown causes

INDIAN PEDIATRICS 246 VOLUME 47__MARCH 17, 2010 G S GAUDE HEMOPTYSIS IN CHILDREN tuberculosis (80%). In countries like India where the In the Western countries, hemoptysis is relatively prevalence of tuberculosis is high, this infection common in patients with cystic fibrosis (CF), should never be neglected and should rank much especially with increased survival into adulthood, higher. Another important cause of hemoptysis in and advances in medical treatment. Approximately children is bronchiectasis, which can be unilateral or 5% of patients with CF may present with massive bilateral. The bronchiectasis occurs due the repeated hemoptysis due to bronchiectasis. In one study(2), respiratory tract infections since childhood. Chronic CF contributed to 65% of cases of pediatric bacterial endobronchial infection and hemoptysis in a 10-year retrospective study. Also the of the mucosa damage and destroy mucociliary Patients with CF also had longer hospitalization defences, and this leads to secretion stasis, which in compared to other causes of hemoptysis, reflecting turn propagates further bacterial infection, and the chronic nature and the multitude of problems increases airway inflammation and bronchial associated with CF. There is hyperplasia, tortuosity dilatation(11). The infection is usually bacterial in and dilatation of bronchial arteries due to chronic nature and consists of Streptococcus pneumonie, inflammation, and hemorrhage results from erosion Staphylococcus aureus, M. catarrhalis, klebsiella of these dilated, thin walled bronchial vessels after species, or Pseudomonas aeruginosa. Aspergillus successive pulmonary infections(5). infection of the lungs either in the form of allergic Neoplasms of the respiratory tract are rare in bronchopulmonary aspergillosis (ABPA) or invasive children, but endobronchial or pulmonary aspergilliosis can occur in children and some cases parenchymal tumors may cause significant bleeding. of hemoptysis have been reported(12). Tumors that may cause hemoptysis include Congenital heart disease can be a source of bronchial carcinoid, bronchial adenoma, endobron- profuse bleeding in a child. With the advent of chial , mediastinal teratomas, tracheal corrective cardiac surgery, the incidence of tumours, or bronchial arteriovenous malformations hemoptysis in this setting has declined in children(17). Hemoptysis is a well-recognized significantly(5). Hemoptysis in CHD occurs most complication of long-term tracheostomies. frequently with pulmonary vascular obstructive Wetmove, et al.(18) reported that significant disease, but it can also occur in conjunction with bleeding may occur in approximate 10% of the enlarged collateral bronchial circulation. Hemoptysis patients with long-term tracheostomy. Fabian and in this condition is caused by erosion of a tortuous Smitheringale(19) found tracheostomy related dilated bronchial artery into a , from rupture hemoptysis to be second most common cause of of an atherosclerotic bronchial artery plaque, or from hemoptysis (15.5%). Typically, the bleeding is localized pulmonary infarction at the described as pink or red–tinged secretions on bronchopulmonary anastomosis(13). Recently, life suctioning the tracheobronchial tree. threatening hemoptysis has been reported in a child due to aortic pseudoaneurysm, which was proved by Idiopathic pulmonary haemosiderosis is a rare the aortic biopsy showing neutrophilic infiltration of cause of diffuse alveolar hemorrhage of unknown the mucosa(14). etiology. It occurs most frequently in children, has a variable natural history with repetitive episodes of Foreign body aspiration is always considered in diffuse alveolar hemorrhage, and has been reported the differential diagnosis of pediatric hemoptysis. to have a high mortality. The recurrent episodes of The bleeding in this case results from the mechanical diffuse pulmonary hemorrhage may present as trauma to the respiratory epithelium or the ensuing hemoptysis(20). Many patients develop iron inflammatory reaction, especially to vegetable deficiency anemia secondary to deposition of matter(15). Tom, et al.(16) identified foreign bodies haemosiderin iron in the alveoli. Recently, Kabra, as the second most common cause of hemoptysis. We et al.(21) described hemoptysis in about 58% of have observed four children with hemoptysis, who children in patients with pulmonary hemosiderosis. had vegetable matter impacted in the bronchi, which Most of these patients had small and recurrent were successfully removed with bronchoscope. hemoptysis. Examination of sputum and broncho-

INDIAN PEDIATRICS 247 VOLUME 47__MARCH 17, 2010 G S GAUDE HEMOPTYSIS IN CHILDREN alveolar lavage fluid can disclose hemosiderin-laden or coughing episodes, and new onset alveolar macrophages (siderophages), and the lung wheezing. A history of chronic lung disease or CHD biopsy shows numerous siderophages in the alveoli, is also important. This is followed by thorough without any evidence of pulmonary , examination of the neck and head. Special attention nonspecific/granulomatous inflammation, or should be given to the oral cavity and nasopharynx as deposition of immunoglobulins. In some of these the potential sources of bleeding. Lung examination patients normo-complement urticarial vasculitis has may reveal localized wheezing, suggesting foreign been observed in children, and this may predispose body, or rales or decreased breath sounds, which may for the hemoptysis(22). be associated with an infectious process(5). Other causes of hemoptysis are far less common, Routine blood test with complete haemogram has such as bleeding from localized lesions in upper to be done in all the children. This is imperative airways or bleeding into the lungs as like part of a because children generally tend to swallow blood systemic disease systemic lupus erythematosis, and the amount of bleeding is likely to be Goodpasture’s syndrome, pulmonary underestimated. As an infectious etiology is thromboembolism, hydatid cyst, and even common, sputum is evaluated for bacterial, fungal duplication cyst of the stomach can cause and mycobacterial organisms. Sputum culture will hemoptysis in children(23-26). Isolated pulmonary be helpful for identifying the pathogens and arteritis can lead to massive hemoptysis in sensitivities to various . children(27). Recently, catamenial hemoptysis has Chest radiography serves as a valuable screening been described in a 12 year old child and fibreoptic technique. Unilateral air trapping with hyper- bronchoscopy revealed presence of endobronchial inflation may suggest the diagnosis of foreign body (28). aspiration(1). Focal or interstitial infiltrates may Factitious hemoptysis is considered in the help the diagnosis of infection. Other helpful differential diagnosis if no etiology is discernible findings include pulmonary nodules, hilar adeno- after a thorough evaluation, especially when the pathy, pleural effusion and cardiomegaly. In approxi- medical history or patient’s behavior is unusual(29). mately one third of children with hemoptysis, chest Covert biting of the buccal mucosa has been attributed to cause hemoptysis in these children(30). TABLE II DIFFERENTIATING FEATURES OF HEMOPTYSIS AND Psychological counseling is usually required in such children. Hemoptysis Hematemesis History DIAGNOSIS Absence of nausea and Presence of nausea and Hemoptysis in children should be evaluated vomiting vomiting systematically. The investigations begin with a Lung disease Gastric or hepatic disease detailed medical history and physical examination. possible Asphyxia unusual First, the hemoptysis has to be differentiated from After the episode, sputum is After the episode, sputum is hematemesis. Historic clues are useful for always blood tinged always clear differentiating hemoptysis from hematemesis (Table II). Patient history also can help identify the Sputum examination anatomic site of bleeding, differentiate between Frothy Rarely frothy hemoptysis and pseudohemoptysis, and narrow the Liquid or clotted appearance Coffee ground appearance differential diagnosis. Once true hemoptysis is Bright red to pink Brown to black suspected, the investigations should focus on the Laboratory Parameters . Alkaline pH Acidic pH The physician should always inquire about the Mixed with macrophages Mixed with food particles possibility of foreign baby aspiration, including and neutrophils

INDIAN PEDIATRICS 248 VOLUME 47__MARCH 17, 2010 G S GAUDE HEMOPTYSIS IN CHILDREN radiographs may be normal. High Resolution TREATMENT Computed Tomography (HRCT) can be useful in further delineation of chest radiography findings. Management of the child with hemoptysis depends Contrast studies are helpful to differentiate between on two important issues – the underlying causes and vascular structures and solid masses(2). In recent the severity of the bleeding. The three goals of years, HRCT scan of thorax has become the most therapy are: to prevent asphyxiation, stop the accurate and sensitive noninvasive diagnostic tool bleeding, and treat the primary cause. Most of the for the evaluation of bronchiectasis(31). cases are self-limited and will resolve spontaneously. Minor hemoptysis If the etiology of hemoptysis is not discovered after aforementioned workup, and if the bleeding is Minor hemoptysis is managed symptomatically, by recurrent, bronchoscopy which may be rigid or giving suppressants like dextromethorphan fibreoptic, is indicated to identify source of and oral/parental haemostatic agents like bleeding(9,10). Fibreoptic bronchoscopy can be ethymsylate or Botropase, reassurance of the patient performed with sedation and allows more detailed and parents, and the treatment of the underlying evaluation of distal bronchial tree. However, it does cause. If a specific etiology is identified, appropriate not permit effective ventilation and removal of blood therapy of the underlying disease should be initiated. clots. In contrast, rigid bronchoscope offers Pulmonary infections are treated with appropriate ventilation and helps localize site of bleeding. It is antibiotics. Cystic fibrosis exacerbations are also ideal for suctioning of clotted blood and is also managed with antibiotics and corticosteroids. more effective for removal of airway foreign Tracheostomy-related trauma is managed by bodies(32). In one study, rigid bronchoscopy was modifying the suctioning technique, using soft red performed 24 times in 18 patients for diagnostic and rubber catheters, and humidification. Pulmonary therapeutic reasons. The various findings included: tuberculosis should be treated with anti-tubercular blood, mucosal inflammation, purulence, tracheal therapy. Idiopathic pulmonary hemosiderosis is abrasions, gradation tissue and bronchial mass. The treated with prednisolone. Kabra, et al.(21) recently diagnostic yield was 61%(5). The diagnostic yield of treated children with pulmonary hemosiderosis with bronchoscopy in hemoptysis ranges from 40% to prednisolone and hydroxychloroquin followed by 100% in various studies(1,9). inhaled corticosteroids, and found favorable response in majority of the patients. Cardiac evaluation should be considered in patients with hemoptysis unexplained by pulmonary Massive hemoptysis causes, even in the absence of overt cardiac symptoms(33). Echocardiography should be In small number of cases, the child may present with performed for the evaluation of any suspected life-threatening hemorrhage (>8 mL/kg every 24 congenital cardiac disease. Pulmonary thromboem- hours or 200 mL every 24 hrs). Massive hemoptysis bolism is a rare cause of hemoptysis in children, and a can quickly progress to acute respiratory distress in a combination of diagnostic procedures must be used to child. These children require multiple procedures to identify a suspected or confirmed case of pulmonary stabilize the airways and to control blood loss(34). thromboembolism in children, including ventilation Intravenous fluids and blood products are given to perfusion studies(24). When no other cause is found prevent cardiovascular collapse from the for pulmonary hemorrhage, the presumed diagnosis exsanguination of blood. Reversal of any is idiopathic pulmonary hemosiderosis(21). In these coagulation disorder and protecting the non- patients, sputum and bronchoalveolar lavage fluid bleeding lung from aspiration by placing the can disclose haemosiderin-laden alveolar bleeding side down and selectively intubating the macrophages (siderophages). good lung, in cases of massive hemoptysis, should be undertaken(35). The use of cough suppressants Figure 1 provides an algorithm for the evaluation containing codeine has been controversial as they of hemoptysis in children. have the potential to alter the level of consciousness

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History and Physical examination ↓ ↓ ↓ Suggests gastrointestinal Suggests bleeding Suggests lower or upper airway source disorders respiratory tract source ↓ ↓ ↓ Pseudohemoptysis or Laboratory evaluation Chest X-ray hemetemesis towards suspected diagnosis ↓ ↓↓ Examine the Parenchymal Normal source disease ↓↓↓ History not suggestive of History suggestive HRCT scan LRTI of LRTI of chest ↓ Observe and consider use of antibiotics ↓ ↓ ↓ ↓↓ Cessation of bleeding Recurrence of No specific diagnosis Suggests and no recurrence bleeding suggested diagnosis ↓ ↓ ↓ Laboratory evaluation No further evaluation Bronchoscopy towards suspected diagnosis ↓ ↓ ↓ No specific diagnosis Suggests diagnosis suggested ↓ ↓ Laboratory evaluation towards Observation suspected diagnosis

FIG. 1 Algorithm for diagnosing hemoptysis in children. and hence lead to the risk of aspiration. However, The bleeding should be localized without delay. judicious use and careful titration should avoid this Although there is debate regarding timing of problem(36). The various options available for bronchoscopy, most of the authors favor early massive hemoptysis are: endoscopic balloon bronchoscopy(35). This approach is associated with occlusion of a lobe or main bronchus, topical airway the best success of identifying the bleeding site. In vasoconstrictors, use of Nd-YAG laser, CO2 laser most cases, fibreoptic bronchoscopy via an existing bronchoscopy, endoscopic tumor excision, endotracheal tube is the easiest and safest approach. transcatheter embolisation of bronchial vessels and If fibreoptic bronchoscopy fails to identify the lobectomy. The foremost objectives in management bleeding site, an experienced endoscopist can of massive hemoptysis are to protect the airways, perform rigid bronchoscopy if time permits. Rigid maintain oxygenation, stop the bleeding and bronchoscopy protects the airways and helps in maintain sufficient blood volume. This is critical localization of bleeding site. Topical because most of the deaths occur due to vasoconstrictors, such as oxymetazoline or asphyxiation, not exsanguination. The airway should (1:20000), iced 0.9% , fibrinogen- be kept patent with an endotracheal tube or rigid thrombin glues or Botropase are applied through the bronchoscope in cases of severe respiratory distress. bronchoscope to curtail the bleeding. In addition,

INDIAN PEDIATRICS 250 VOLUME 47__MARCH 17, 2010 G S GAUDE HEMOPTYSIS IN CHILDREN endoscopic tamponade can be performed by balloon anesthesia and pulmonary resection. Immediate catheter or with bronchoscopic pressure(2). Patients identification of the bleeding site by bronchoscope is with alveolar hemorrhage syndromes, blood followed by resection of the bleeding source(40). dyscrasias, or those on or antiplatelet Segmentectomy or lobectomy is preferred to therapy should receive appropriate medical therapy , as the latter carries a much higher rather than invasive interventions. mortality rate. One study(41) reported 83% survival in 65 resections performed for massive hemoptysis If the hemorrhage continues despite endoscopic in this setting. Simrali, et al.(42) recently published measures, or if the bleeding site cannot be localized, their experience with surgery for bronchiectasis in emergency arteriography is carried out(5). Selective 176 children of less than 16 years with hemoptysis. bronchial artery embolisation (BAE) is effective in They performed various procedures including the emergency management of life-threatening segmental resection, lobectomy, pneumonectomy hemoptysis(37). Bronchial arteriography identifies and bilateral resection in patients with the bleeding vessel and selective embolisation with bronchiectasis. Complete resection was performed absorbable gelatin sponge, steel or platinum coils, or in almost 94% of the cases. The patients were polyvinyl alcohol particles controls the hemorrhage. followed for a mean period of 4.3 years. Successful In one study(34), there was immediate cessation of outcome was observed in 73% of cases, while hemorrhage in 77% of the cases; while long term improved outcome was seen in another 23% of the control beyond 3 months was achieved in 45% of cases. It was observed that there was good patients. Another study(37) found bronchial improvement in the quality of life even after embolisation to be superior to medical management pneumonectomy and bilateral resection of the lungs. for resolution of life threatening bleeding. BAE is Hemoptysis could be controlled in all of these cases. effective in controlling hemoptysis in most of the It was concluded that with acceptable mortality and cases although recurrent bleeding is not uncommon. morbidity rates and high chances of cure after BAE is technically challenging and requires complete resection, surgical treatment is a successful angiographic skills that are not always available in and reliable method of treatment in childhood pediatric hospitals(38). Complications are not bronchiectasis that yield marked improvement in the uncommon and may be severe or even fatal. The quality of life(42). Chan, et al.(27) has also treated most serious complication of embolisation therapy is isolated pulmonary arteritis with lobectomy, as the neurological damage due to embolisation of the hemoptysis could not be controlled with the medical spinal arteries(5). Recently, del Gregorio, et al.(39) measures alone. Hence, surgical options have to be have reported their experience with bronchial artery considered if massive hemoptysis remains embolisation in patients with hemoptysis; about 31% uncontrolled in spite of medical therapy. of these patients were having bronchiectasis. In this study, clinically successful outcome with BAE was Figure 2 provides an algorithm for the observed in 91.1% of the cases, and repeat management of hemoptysis in children. embolisation was required in 6.7% of the cases. Recurrence of hemoptysis was observed in 22.3% of Hemoptysis in children is rare, but if occurs, it is cases, but only 10.4% of patients required repeat a frightening symptom for the parents. The patient’s embolisation. Minor complications that did not history should help determine the amount of blood require treatment were observed in 28% of cases. and differentiate between hemoptysis, pseudo- Thus, BAE is a nonsurgical treatment that is safe and hemoptysis, and hematemesis. A focused physical effective in patients with massive hemoptysis(39). examination can lead to the diagnosis in most cases. Mild hemoptysis often is caused by an infection and If bronchial artery embolisation fails to control can be managed on an outpatient basis with close hemoptysis, surgical management should be monitoring. Massive hemoptysis requires immediate considered. Massive hemoptysis carries greater than hospitalization and proper therapeutic interventions 50% mortality without surgical intervention. Surgery have to be initiated at the earliest to stop the bleeding is offered to patients who can withstand general and to prevent its recurrence.

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Hemoptysis

↓ ↓ Minor hemoptysis Massive hemoptysis → Reassurance ↓ ↓ ↓ → Cough suppressants Protect airways Prevent cardio- Treat specific → Hemostatic agents vascular collapse cause → Treat underlying cause ↓ Treat infection, if present Supportive therapy ↓ Bronchoscopy

↓ ↓ Hemorrhage Hemorrhage stopped continues ↓ ↓ Treat underlying Bronchial artery disease embolisation

↓ ↓ Hemorrhage Hemorrhage stopped continues ↓ Surgical resection

FIG. 2 Algorithm for management of hemoptysis in children.

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