Commentary
Recurrent pneumonia . . . Not! Daniel Hughes MD FRCPC
C
ough is a common presenting symptom of children encountered in primary care. It usually arises from intercurrent viral infections and is of short duration. When cough is associated with other respiratory symptoms or signs, such as fever and tachypnea, in a generally unwell child, pneumonia is suspected. Paediatricians, paediatric respiratory physicians and infectious disease specialists are frequently asked to assess patients believed to have a diagnosis of recurrent pneumonia. Recurrent pneumonia is defined as ≥2 episodes in one year or ≥3 episodes ever, with radiographic clearing of densities between episodes (1). The initial difficulty for the consultant is often determining the basis on which a diagnosis of pneumonia was made. If there was no evidence on auscultation of bronchial breath sounds or focal crackles/crepitations, and especially when chest radiographs were not always performed to assess for evidence of airspace disease/ consolidation, the term ‘acute or recurrent lower respiratory infection’ better describes the situation (2). In some cases, the referral is triggered by the radiologists’ reports of ‘pneumonia’, while in others, the parent requests a referral due to concern regarding the repeated ‘diagnoses of pneumonia’ requiring multiple courses of antibiotics. The latter situation may be accompanied by the parent producing a computerized list of their child’s medications provided by the pharmacist. The typical referred patient is a preschool/early school-age child (two to eight years of age) with a history of recurring (not chronic) respiratory symptoms associated with fever, in which the clinical and/or radiological findings have suggested repeated episodes of ‘pneumonia’. It is not uncommon for a diagnosis of ‘pneumonia’ to have been made on purely clinical grounds (a challenge in a young child) without a chest radiograph being performed. Multiple courses of antibiotics have usually been prescribed. A more focused history may reveal that the episodes begin with coryza followed by cough, the latter persisting for as long as two to four weeks. Associated features include fever of up to 39°C to 40°C, lack of energy and loss of appetite. Chest radiographs, when performed, often reveal ‘pneumonia’ and antibiotics are usually prescribed. These episodes may recur frequently, particularly in the winter, and, when close to one another, leave the parents with the impression that their child is always sick. This pattern of illness is particularly noted in children attending nursery schools, daycares and other settings in which exposure to viral infections is common. School-age siblings may also transmit viruses. The child’s cough, initially dry, becomes wet-sounding and parents, if prompted, will report being able to feel congestion when they place their hands on the child’s chest, consistent with the ruttle reported by Elphick et al (3). Classical wheeze may or may not be heard. Atopic features in the child and/or family are occasionally noted. Between exacerbations, particularly in the summer, the child is usually asymptomatic. The wet cough and chest congestion may be apparent to the consultant when the child is examined during an exacerbation. At these times, chest radiographs
usually demonstrate retained secretions, bronchial wall thickening and, occasionally, atelectasis (often involving the right middle lobe [RML]). Lobar consolidation reflecting airspace disease is rarely observed when radiographs are reviewed by an experienced paediatric radiologist. A diagnosis of asthma may have been considered in some cases but excluded when the child failed to respond to inhaled bronchodilators and/or inhaled corticosteroids, usually administered using metered-dose inhalers. In this situation, these observations should not be interpreted as ruling out asthma. In addition to antibiotics, the medication list provided by the pharmacist often includes inhaled bronchodilators, corticosteroids and other asthma medications. An important clue to the clinical diagnosis may arise if the parent reports significant improvement in the child’s symptoms when they are treated with bronchodilators administered through wet nebulization and/or systemic steroids, usually associated with an emergency department visit. There is evidence that the most common cause of ‘recurrent pneumonia’ and ‘recurrent bronchitis’ in children is underappreciated asthma (4), and hypersecretory asthma, in which production of excess bronchial secretions is particularly prominent, may play an important role (5). This is supported by the author’s clinical experience. The radiographic opacities, interpreted incorrectly as ‘pneumonia’, result from these secretions. The difficulty in diagnosing pneumonia radiographically and the overdiagnosis of pneumonia have been well described (6,7). That true recurrent pneumonia can occur in patients with an underlying disorder, such as pulmonary aspiration, congenital cardiac defects, neuromuscular disorders, immunodeficiency, etc, is not questioned. The issue is whether otherwise healthy children are subject to recurrent pneumonia or even whether recurrent pneumonia is a complication of asthma. In a 10-year retrospective survey of almost 3000 children admitted to hospital with pneumonia, only 8% met the criteria for recurrent pneumonia (8). An underlying illness to explain the recurrences was identified in 92%. Eighteen patients had no underlying etiological diagnosis but detailed testing had not been performed. In cases in which the underlying etiology was discovered after the diagnosis of pneumonia, asthma was the most common. Similarly, in patients seen in an ambulatory setting over a fiveyear period, 70 of 2264 children (3%) attending a paediatric chest clinic in India met the criteria for recurrent pneumonia (9). An underlying cause was noted in 59 and no cause in 11, yet all of these children had bronchiectasis. Of note, asthma was identified to be the underlying cause in 10 of 59 patients. The notion that asthma in children can be complicated by recurrent pneumonia has a long history and contributes to the confusion when assessing these children. This is especially true when the RML is involved. The RML is subject to atelectasis because of the anatomy of the bronchus and the lack of collateral ventilation with other lobes. Excess mucus production in hypersecretory asthma can lead to RML atelectasis. It is well recognized
Correspondence and reprints: Dr Daniel Hughes, Pediatric Respiratory Medicine, IWK Health Centre, 5850 University Avenue, PO Box 9700, Halifax, Nova Scotia B3K 6R8. Telephone 902-470-8218, e-mail [email protected] Accepted for publication May 9, 2013 Paediatr Child Health Vol 18 No 9 November 2013
©2013 Pulsus Group Inc. All rights reserved
459
Commentary
that the most common cause of the so-called ‘right middle lobe syndrome’ is asthma. The confusion surrounding this issue dates back to the 1950s and 1960s (10,11). Kjellman (11), in his study investigating the relationship between asthma and recurrent pneumonia, noted that 14 of 125 asthmatic children fulfilled the criteria for recurrent pneumonia and, radiographically, the RML was over-represented but, unfortunately, as the author stated, no distinction was made between atelectasis and pneumonia. Probably the most illustrative study was that by Eigen et al (4), who examined 81 patients referred to their clinic with a diagnosis of persistent or recurrent pneumonia. The diagnosis was based on abnormal chest radiographs demonstrating “segmental or subsegmental densities or an increase in bronchovascular associated densities.” Twenty of 81 patients had an apparent cause for their persistent or recurrent pneumonia. Of the 61 with no obvious etiology, 30 had a history of allergy or family history of asthma, 19 had a history of wheezing and 11 had wheezing noted on physical examination. Nineteen patients with no underlying etiology underwent pulmonary function testing, and nine had airflow obstruction, with four of five demonstrating a bronchodilator response. Twelve patients were recalled for pulmonary function testing and three had airways obstruction and bronchodilator response. The nine with normal lung function underwent a methacholine challenge, and eight had positive responses. In total, 92% of the no-etiology group had evidence of airways hyperreactivity. The authors concluded that their study had “identified a group of asthmatics in whom excessive mucus production rather than bronchospasm caused the majority of symptoms and in whom the recurrent chest infiltrates originated as atelectasis from mucus plugging rather than as infectious processes”. Hypersecretory asthma does not completely fit the description of a newly discovered entity referred to as ‘persistent or protracted bacterial bronchitis’ (PBB) because the latter is described as chronic wet cough lasting longer than four weeks and resolution of cough with antibiotic treatment (12). However, there is the possibility that some patients with PBB have hypersecretory asthma. Of 81 patients with PBB, Donnelly et al (13) noted a diagnosis of asthma in 31%. The author suggested that PBB is often misdiagnosed as asthma; however, an alternative explanation is that asthma is misdiagnosed as PBB. It must be emphasized that this author is referring to children with recurring wet cough associated with viral respiratory tract infections, not chronic wet cough with or without sputum production. In the latter situation, bronchiectasis should be considered. Evidence of bronchiectasis on the chest radiograph includes persistent patchy infiltrates, dilated mucous-filled bronchi resembling fingers in a glove or dilated air-filled bronchi resembling tram tracks. Bronchiectasis may be confirmed using computed tomography of the chest. Causes of bronchiectasis include cystic fibrosis, primary ciliary dyskinesia, immunodeficiency, retained foreign body and recurrent aspiration (5). The diagnostic confusion between asthma and recurrent pneumonia has recently been discussed by Brand et al (14). The authors state that asthma is not a common underlying cause of recurrent pneumonia but the probability remains that the diagnosis of recurrent pneumonia itself is questionable. It is recommended that the consultant limit investigations to a review of previous chest radiographs, sweat testing, serum immunoglobulins and, for individuals old enough, spirometry. Young children swallow rather than expectorate and, consequently, sputum is rarely available for culture or examination (15). For children with recurrent ‘pneumonia-like’ symptoms due to underlying asthma and/or hypersecretory asthma, exacerbations typically improve with intermittent administration of salbutamol. 460
It has been the author’s experience that salbutamol delivered by wet nebulization alone is particularly beneficial. Rarely has the author encountered a child with this asthma phenotype who could be successfully managed using metered-dose inhalers, although they may exist. Oral steroids, such as prednisolone, may be required for more severe exacerbations. Following an explanation and reassurance that their otherwise healthy child has no reason to experience recurring episodes of pneumonia (including written instructions), the parents are instructed to initiate therapy at home at the onset of the child’s symptoms and continue, generally for seven to 10 days. Antibiotics are not prescribed. Children with recurrent, more severe episodes benefit from the use of daily inhaled steroids, similar to other children with asthma (16). Having had the opportunity to follow these patients for many years, it has become apparent that the recurring wet cough eventually becomes a dry one and none have developed bronchiectasis. In 30 years, the author has never observed recurrent bacterial pneumonia in an otherwise normal child, yet hardly a week passes without being referred such a child subjected to multiple chest radiographs and an abundance of antibiotics. Physicians should consider a diagnosis of hypersecretory asthma in these children and provide more appropriate and effective therapy. Educational REsouRcEs foR PaREnts: Hypersecretory Asthma – Information for Parents. Chest Clinic, IWK Health Centre (Halifax, Nova Scotia).
REfEREncEs
1. Wald E. Recurrent and nonresolving pneumonia in children. Semin Respir Infect 1993;8:46-58. 2. Shann F, Hart K, Thomas D. Acute lower respiratory tract infections in children: Possible criteria for selection of patients for antibiotic therapy and hospital admission. Bull World Health Organ 1984;62:749-53. 3. Elphick H, Ritson S, Rodgers H, et al. When a “wheeze” is not a wheeze: Acoustic analysis of breath sounds in infants. Eur Respir J 2000;16:593-7. 4. Eigen H, Laughlin J, Homrighausen J. Recurrent pneumonia in children and its relationship to bronchial hyperreactivity. Pediatrics 1982;70:698-704. 5. Phelan P, Olinsky A, Robertson C. Respiratory illness in children, 4th edn. Oxford: Blackwell Scientific Publications, 1994:146-7. 6. Kramer M, Roberts-Brauer R, Williams R. Bias and “overcall” in interpreting chest radiographs in young febrile children. Pediatrics 1992;90:11-3. 7. Davies H, Wang E, Manson D, et al. Reliability of the chest radiograph in the diagnosis of lower respiratory infections in young children. Pediatr Infect Dis J 1996;15:600-4. 8. Owayed A, Campbell D, Wang E. Underlying causes of recurrent pneumonia in children. Arch Pediatr Adolesc Med 2000;154:190-4. 9. Lodha R, Puranik M, Natchu U, et al. Recurrent pneumonia in children: Clinical profile and underlying causes. Acta Paediatr 2002;91:1170-3. 10. Ratner B. Asthma in children: Salient diagnostic problems. JAMA 1950;142:538-42. 11. Kjellman B. Bronchial asthma and recurrent pneumonia in children – clinical evaluation of 14 children. Acta Paediatrica Scand 1967;56:651-9. 12. Chang A, Redding G, Everard M. Chronic wet cough: Protracted bronchitis, chronic suppurative lung disease and bronchiectasis. Pediatr Pumonol 2008;43:519-31. 13. Donnelly D, Critchlow A, Everard M. Outcomes in children treated for persistent bacterial bronchitis. Thorax 2007;62:80-4. 14. Brand P, Hoving M, deGroot E. Evaluating the child with recurrent lower respiratory tract infections. Paediatr Respir Rev 2012;13:135-8. 15. Rogers D. Pulmonary mucus: Pediatric perspective. Pediatr Pulmonol 2003;36:178-88. 16. Kovesi T, Schuh S, Spier S, et al. Achieving control of asthma in preschoolers. CMAJ 2010;182:E172-83.
Paediatr Child Health Vol 18 No 9 November 2013
Recurrent pneumonia . . . Not! Daniel Hughes MD FRCPC
C
ough is a common presenting symptom of children encountered in primary care. It usually arises from intercurrent viral infections and is of short duration. When cough is associated with other respiratory symptoms or signs, such as fever and tachypnea, in a generally unwell child, pneumonia is suspected. Paediatricians, paediatric respiratory physicians and infectious disease specialists are frequently asked to assess patients believed to have a diagnosis of recurrent pneumonia. Recurrent pneumonia is defined as ≥2 episodes in one year or ≥3 episodes ever, with radiographic clearing of densities between episodes (1). The initial difficulty for the consultant is often determining the basis on which a diagnosis of pneumonia was made. If there was no evidence on auscultation of bronchial breath sounds or focal crackles/crepitations, and especially when chest radiographs were not always performed to assess for evidence of airspace disease/ consolidation, the term ‘acute or recurrent lower respiratory infection’ better describes the situation (2). In some cases, the referral is triggered by the radiologists’ reports of ‘pneumonia’, while in others, the parent requests a referral due to concern regarding the repeated ‘diagnoses of pneumonia’ requiring multiple courses of antibiotics. The latter situation may be accompanied by the parent producing a computerized list of their child’s medications provided by the pharmacist. The typical referred patient is a preschool/early school-age child (two to eight years of age) with a history of recurring (not chronic) respiratory symptoms associated with fever, in which the clinical and/or radiological findings have suggested repeated episodes of ‘pneumonia’. It is not uncommon for a diagnosis of ‘pneumonia’ to have been made on purely clinical grounds (a challenge in a young child) without a chest radiograph being performed. Multiple courses of antibiotics have usually been prescribed. A more focused history may reveal that the episodes begin with coryza followed by cough, the latter persisting for as long as two to four weeks. Associated features include fever of up to 39°C to 40°C, lack of energy and loss of appetite. Chest radiographs, when performed, often reveal ‘pneumonia’ and antibiotics are usually prescribed. These episodes may recur frequently, particularly in the winter, and, when close to one another, leave the parents with the impression that their child is always sick. This pattern of illness is particularly noted in children attending nursery schools, daycares and other settings in which exposure to viral infections is common. School-age siblings may also transmit viruses. The child’s cough, initially dry, becomes wet-sounding and parents, if prompted, will report being able to feel congestion when they place their hands on the child’s chest, consistent with the ruttle reported by Elphick et al (3). Classical wheeze may or may not be heard. Atopic features in the child and/or family are occasionally noted. Between exacerbations, particularly in the summer, the child is usually asymptomatic. The wet cough and chest congestion may be apparent to the consultant when the child is examined during an exacerbation. At these times, chest radiographs
usually demonstrate retained secretions, bronchial wall thickening and, occasionally, atelectasis (often involving the right middle lobe [RML]). Lobar consolidation reflecting airspace disease is rarely observed when radiographs are reviewed by an experienced paediatric radiologist. A diagnosis of asthma may have been considered in some cases but excluded when the child failed to respond to inhaled bronchodilators and/or inhaled corticosteroids, usually administered using metered-dose inhalers. In this situation, these observations should not be interpreted as ruling out asthma. In addition to antibiotics, the medication list provided by the pharmacist often includes inhaled bronchodilators, corticosteroids and other asthma medications. An important clue to the clinical diagnosis may arise if the parent reports significant improvement in the child’s symptoms when they are treated with bronchodilators administered through wet nebulization and/or systemic steroids, usually associated with an emergency department visit. There is evidence that the most common cause of ‘recurrent pneumonia’ and ‘recurrent bronchitis’ in children is underappreciated asthma (4), and hypersecretory asthma, in which production of excess bronchial secretions is particularly prominent, may play an important role (5). This is supported by the author’s clinical experience. The radiographic opacities, interpreted incorrectly as ‘pneumonia’, result from these secretions. The difficulty in diagnosing pneumonia radiographically and the overdiagnosis of pneumonia have been well described (6,7). That true recurrent pneumonia can occur in patients with an underlying disorder, such as pulmonary aspiration, congenital cardiac defects, neuromuscular disorders, immunodeficiency, etc, is not questioned. The issue is whether otherwise healthy children are subject to recurrent pneumonia or even whether recurrent pneumonia is a complication of asthma. In a 10-year retrospective survey of almost 3000 children admitted to hospital with pneumonia, only 8% met the criteria for recurrent pneumonia (8). An underlying illness to explain the recurrences was identified in 92%. Eighteen patients had no underlying etiological diagnosis but detailed testing had not been performed. In cases in which the underlying etiology was discovered after the diagnosis of pneumonia, asthma was the most common. Similarly, in patients seen in an ambulatory setting over a fiveyear period, 70 of 2264 children (3%) attending a paediatric chest clinic in India met the criteria for recurrent pneumonia (9). An underlying cause was noted in 59 and no cause in 11, yet all of these children had bronchiectasis. Of note, asthma was identified to be the underlying cause in 10 of 59 patients. The notion that asthma in children can be complicated by recurrent pneumonia has a long history and contributes to the confusion when assessing these children. This is especially true when the RML is involved. The RML is subject to atelectasis because of the anatomy of the bronchus and the lack of collateral ventilation with other lobes. Excess mucus production in hypersecretory asthma can lead to RML atelectasis. It is well recognized
Correspondence and reprints: Dr Daniel Hughes, Pediatric Respiratory Medicine, IWK Health Centre, 5850 University Avenue, PO Box 9700, Halifax, Nova Scotia B3K 6R8. Telephone 902-470-8218, e-mail [email protected] Accepted for publication May 9, 2013 Paediatr Child Health Vol 18 No 9 November 2013
©2013 Pulsus Group Inc. All rights reserved
459
Commentary
that the most common cause of the so-called ‘right middle lobe syndrome’ is asthma. The confusion surrounding this issue dates back to the 1950s and 1960s (10,11). Kjellman (11), in his study investigating the relationship between asthma and recurrent pneumonia, noted that 14 of 125 asthmatic children fulfilled the criteria for recurrent pneumonia and, radiographically, the RML was over-represented but, unfortunately, as the author stated, no distinction was made between atelectasis and pneumonia. Probably the most illustrative study was that by Eigen et al (4), who examined 81 patients referred to their clinic with a diagnosis of persistent or recurrent pneumonia. The diagnosis was based on abnormal chest radiographs demonstrating “segmental or subsegmental densities or an increase in bronchovascular associated densities.” Twenty of 81 patients had an apparent cause for their persistent or recurrent pneumonia. Of the 61 with no obvious etiology, 30 had a history of allergy or family history of asthma, 19 had a history of wheezing and 11 had wheezing noted on physical examination. Nineteen patients with no underlying etiology underwent pulmonary function testing, and nine had airflow obstruction, with four of five demonstrating a bronchodilator response. Twelve patients were recalled for pulmonary function testing and three had airways obstruction and bronchodilator response. The nine with normal lung function underwent a methacholine challenge, and eight had positive responses. In total, 92% of the no-etiology group had evidence of airways hyperreactivity. The authors concluded that their study had “identified a group of asthmatics in whom excessive mucus production rather than bronchospasm caused the majority of symptoms and in whom the recurrent chest infiltrates originated as atelectasis from mucus plugging rather than as infectious processes”. Hypersecretory asthma does not completely fit the description of a newly discovered entity referred to as ‘persistent or protracted bacterial bronchitis’ (PBB) because the latter is described as chronic wet cough lasting longer than four weeks and resolution of cough with antibiotic treatment (12). However, there is the possibility that some patients with PBB have hypersecretory asthma. Of 81 patients with PBB, Donnelly et al (13) noted a diagnosis of asthma in 31%. The author suggested that PBB is often misdiagnosed as asthma; however, an alternative explanation is that asthma is misdiagnosed as PBB. It must be emphasized that this author is referring to children with recurring wet cough associated with viral respiratory tract infections, not chronic wet cough with or without sputum production. In the latter situation, bronchiectasis should be considered. Evidence of bronchiectasis on the chest radiograph includes persistent patchy infiltrates, dilated mucous-filled bronchi resembling fingers in a glove or dilated air-filled bronchi resembling tram tracks. Bronchiectasis may be confirmed using computed tomography of the chest. Causes of bronchiectasis include cystic fibrosis, primary ciliary dyskinesia, immunodeficiency, retained foreign body and recurrent aspiration (5). The diagnostic confusion between asthma and recurrent pneumonia has recently been discussed by Brand et al (14). The authors state that asthma is not a common underlying cause of recurrent pneumonia but the probability remains that the diagnosis of recurrent pneumonia itself is questionable. It is recommended that the consultant limit investigations to a review of previous chest radiographs, sweat testing, serum immunoglobulins and, for individuals old enough, spirometry. Young children swallow rather than expectorate and, consequently, sputum is rarely available for culture or examination (15). For children with recurrent ‘pneumonia-like’ symptoms due to underlying asthma and/or hypersecretory asthma, exacerbations typically improve with intermittent administration of salbutamol. 460
It has been the author’s experience that salbutamol delivered by wet nebulization alone is particularly beneficial. Rarely has the author encountered a child with this asthma phenotype who could be successfully managed using metered-dose inhalers, although they may exist. Oral steroids, such as prednisolone, may be required for more severe exacerbations. Following an explanation and reassurance that their otherwise healthy child has no reason to experience recurring episodes of pneumonia (including written instructions), the parents are instructed to initiate therapy at home at the onset of the child’s symptoms and continue, generally for seven to 10 days. Antibiotics are not prescribed. Children with recurrent, more severe episodes benefit from the use of daily inhaled steroids, similar to other children with asthma (16). Having had the opportunity to follow these patients for many years, it has become apparent that the recurring wet cough eventually becomes a dry one and none have developed bronchiectasis. In 30 years, the author has never observed recurrent bacterial pneumonia in an otherwise normal child, yet hardly a week passes without being referred such a child subjected to multiple chest radiographs and an abundance of antibiotics. Physicians should consider a diagnosis of hypersecretory asthma in these children and provide more appropriate and effective therapy. Educational REsouRcEs foR PaREnts: Hypersecretory Asthma – Information for Parents. Chest Clinic, IWK Health Centre (Halifax, Nova Scotia).
REfEREncEs
1. Wald E. Recurrent and nonresolving pneumonia in children. Semin Respir Infect 1993;8:46-58. 2. Shann F, Hart K, Thomas D. Acute lower respiratory tract infections in children: Possible criteria for selection of patients for antibiotic therapy and hospital admission. Bull World Health Organ 1984;62:749-53. 3. Elphick H, Ritson S, Rodgers H, et al. When a “wheeze” is not a wheeze: Acoustic analysis of breath sounds in infants. Eur Respir J 2000;16:593-7. 4. Eigen H, Laughlin J, Homrighausen J. Recurrent pneumonia in children and its relationship to bronchial hyperreactivity. Pediatrics 1982;70:698-704. 5. Phelan P, Olinsky A, Robertson C. Respiratory illness in children, 4th edn. Oxford: Blackwell Scientific Publications, 1994:146-7. 6. Kramer M, Roberts-Brauer R, Williams R. Bias and “overcall” in interpreting chest radiographs in young febrile children. Pediatrics 1992;90:11-3. 7. Davies H, Wang E, Manson D, et al. Reliability of the chest radiograph in the diagnosis of lower respiratory infections in young children. Pediatr Infect Dis J 1996;15:600-4. 8. Owayed A, Campbell D, Wang E. Underlying causes of recurrent pneumonia in children. Arch Pediatr Adolesc Med 2000;154:190-4. 9. Lodha R, Puranik M, Natchu U, et al. Recurrent pneumonia in children: Clinical profile and underlying causes. Acta Paediatr 2002;91:1170-3. 10. Ratner B. Asthma in children: Salient diagnostic problems. JAMA 1950;142:538-42. 11. Kjellman B. Bronchial asthma and recurrent pneumonia in children – clinical evaluation of 14 children. Acta Paediatrica Scand 1967;56:651-9. 12. Chang A, Redding G, Everard M. Chronic wet cough: Protracted bronchitis, chronic suppurative lung disease and bronchiectasis. Pediatr Pumonol 2008;43:519-31. 13. Donnelly D, Critchlow A, Everard M. Outcomes in children treated for persistent bacterial bronchitis. Thorax 2007;62:80-4. 14. Brand P, Hoving M, deGroot E. Evaluating the child with recurrent lower respiratory tract infections. Paediatr Respir Rev 2012;13:135-8. 15. Rogers D. Pulmonary mucus: Pediatric perspective. Pediatr Pulmonol 2003;36:178-88. 16. Kovesi T, Schuh S, Spier S, et al. Achieving control of asthma in preschoolers. CMAJ 2010;182:E172-83.
Paediatr Child Health Vol 18 No 9 November 2013
