Respiration 2005;72:233–238

Non-Cystic-Fibrosis Bronchiectasis in Children: A Persisting Problem in Developing Countries

Karadag B.a · Karakoc F.a · Ersu R.a · Kut A.b · Bakac S.a · Dagli E.a
aDivision of Pediatric Pulmonology, Marmara University, and bDivision of Pediatric Pulmonology, SSK Göztepe Training Hospital, Istanbul, Turkey
email Corresponding Author


 goto top of outline Key Words

  • Children
  • Bronchiectasis
  • Management

 goto top of outline Abstract

Background: Non-cystic-fibrosis (non-CF) bronchiectasis in childhood is still one of the most common causes of childhood morbidity in developing countries. The management of these patients remains problematic, and there are few studies of long-term outcome. Objective: The aim of this retrospective study was to define the general characteristics, underlying causative factors and long-term follow-up results of non-CF bronchiectasis patients. Methods: One hundred and eleven consecutive children, diagnosed with non-CF bronchiectasis were included in the study. General characteristics and underlying causes were recorded from the medical records. Clinical outcomes were evaluated in terms of lung function tests, annual exacerbation rates and patient/parent perception of health status. Results: Mean age of the patients was 7.4 ± 3.7 years at presentation, and patients had been followed 4.7 ± 2.7 years on average. In 62.2% of the patients, an underlying etiology was identified, whereas postinfectious bronchiectasis was the most common (29.7%). In spite of intensive medical treatment, 23.4% of the patients required surgery. The annual lower respiratory infection rate has decreased from a mean of 6.6 ± 4.0 to 2.9 ± 2.9 during follow-up (p < 0.0001). Lung function tests were also found to be improved (mean FEV1% 63.3 ± 21.0 vs. 73.9 ± 27.9; p = 0.01; mean FVC% 68.1 ± 22.2 vs. 74.0 ± 24.8; p = 0.04). There was clinical improvement in both the surgical (73%) and medical (70.1%) groups (p > 0.05). Conclusion: In conclusion, bronchiectasis remains a disease of concern to pediatricians, particularly in developing countries. Infections are still important causes of bronchiectasis, and clinical improvement can be achieved by appropriate treatment. Although medical treatment is the mainstay of management, surgery should be considered in selected patients.

Copyright © 2005 S. Karger AG, Basel

goto top of outline Introduction

Bronchiectasis is characterized by irreversible dilation of the airways associated with frequent bacterial infections and inflammatory destruction of the bronchial and peribronchial tissue [1]. Bronchiectasis has become an uncommon entity and has thus been named an ‘orphan’ disease [2]. Although morbidity and mortality from bronchiectasis seem to be declining in Western countries, the condition is still one of the most common reasons for morbidity in developing countries.

Various factors have been identified as predisposing to the development of non-cystic-fibrosis (non-CF) bronchiectasis. Recurrent respiratory infections, immune deficiency, a retained foreign body, asthma, tuberculosis and primary ciliary dyskinesia are some of the more common risk factors. Postinfectious bronchiectasis in the normal host is becoming distinctly uncommon, and, in developed countries, most patients with the disorder have an underlying systemic illness. An underlying cause of the disease was identified in 40–63% of patients in different studies [3,4,5]. Several studies reported a higher incidence of non-CF bronchiectasis in different minority groups, which was thought to be related to low socioeconomic status [6,7,8].

The management of non-CF bronchiectasis is still problematic in developing countries. Surgery is performed in fewer cases, and there are few data about long-term results of medical and surgical treatment [in these countries 9]. In this study, we sought to ascertain the general characteristics, underlying causative factors and long-term follow-up results including medical and surgical interventions of non-CF bronchiectasis patients referred to a tertiary center.


goto top of outline Patients and Methods

One hundred and eleven consecutive children, diagnosed with non-CF bronchiectasis between 1987 and 2001 and followed up for at least 2 years were included in the study retrospectively. The diagnosis of bronchiectasis was confirmed radiologically by high-resolution computed tomography (HRCT). At clinical assessment, the following information was included: age at the onset of chronic cough/wheeze, history of childhood respiratory infections (pertussis, varicella or measles), personal and family history of atopy, housing conditions and passive exposure to smoke. Duration of symptoms, sputum production, number of lower respiratory tract infections during the previous year and history of previous hospitalizations at presentation were also recorded from the chart review. Lower respiratory tract infection was defined as increased cough and sputum production and/or any change in chest X-ray. The presence of clubbing of the fingers, chest deformities and nasal polyps was also noted on physical examination.

HRCT is the current gold standard for diagnosis of bronchiectasis [10]. All patients in the study group were diagnosed by HRCT. HRCT scans were obtained after an asymptomatic period of at least 3 months after the last exacerbation. Bronchiectasis was diagnosed if there was evidence for bronchial dilation (internal bronchial diameter greater than the diameter of the accompanying pulmonary artery) and a lack of bronchial tapering on sequential slices [11]. The bronchi were evaluated on a lobar basis (regarding the lingula as a separate lobe). Bronchiectasis was defined as localized if only one lobe was affected and diffuse if more than one lobe was found to be bronchiectatic.

Sputum cultures were obtained from all patients on their first visit and at annual intervals. Sputum samples were cultured for bacteria and mycobacterial species. Lung function tests were performed on 92 patients (82.8%) at every visit by a dry spirometer (Vitalograph, Buckingham, UK), and the best value of three acceptable maneuvers was expressed as percentage of the predicted value. Spirometry was performed according to the guidelines of the American Thoracic Society, and the same standards for spirometry were used throughout the study [12, 13]. Atopy was defined by positive skin prick testing to at least one of the common aeroallergens (including house dust mite, grass pollen, cat dander, dog hair and feathers) or specific IgE (RAST) level (>0.35 IU/l). A skin prick test was accepted as positive if the reaction to the antigen was at least 3 mm above the control. In order to evaluate the immunological status of patients, IgG, IgA, IgM, IgE, IgG subclass levels (IgG1, IgG2, IgG3, IgG4) and neutrophil function tests (NBT, opsonization, chemotaxis) were obtained from all patients. A sweat test was performed on all patients in the study group, and patients with positive sweat tests (chloride levels >60 mEq/l) were excluded from analysis. We also performed tuberculin skin tests on all patients.

In order to diagnose primary ciliary dyskinesia in patients with recurrent otitis and sinusitis, the ciliary ultrastructure was assessed by electron microscopy on nasal epithelial brushings at least 6 months after a respiratory infection. Alpha-1-antitrypsin levels were measured in order to exclude alpha-1-antitrypsin deficiency. Patients who had symptoms and signs suggestive of swallowing problems and gastroesophageal reflux were investigated by barium fluoroscopy and 24-hour pH monitoring.

Flexible bronchoscopy was performed in 30 patients with recurrent/persistent atelectasis or consolidation in order to exclude a retained foreign body and obtain bronchoalveolar lavage for microbiological evaluation.

Patients were followed at 3-month intervals. At each visit during the follow-up period, patients or parents were asked about the presence of respiratory symptoms. Annual assessment included the determination of exacerbation, spirometry, sputum cultures and HRCT scan. An exacerbation was defined as a persistent (>24 h) increase in respiratory symptoms, new opacification on chest X-rays or worsening in physical examination findings of the chest [14]. The number of exacerbations in the preceding 12 months was recorded. All patients were followed up with medical treatment modalities including prompt antibiotic use in exacerbations, bronchodilators and physiotherapy. Inhaled steroids were given to patients who had symptoms suggestive of bronchial hyperreactivity and positive bronchodilator responses. Asthma was diagnosed if a patient had symptoms suggesting bronchial hyperreactivity such as wheeze and cough and a positive response to bronchodilators. In terms of underlying etiology, as we were aware of the comorbidity of asthma and bronchiectasis, we only labeled patients who had been followed up with the diagnosis of asthma in a pediatric pulmonology outpatient clinic before the diagnosis of bronchiectasis and had shown a normal HRCT during this period. Other patients were labeled as having an unidentified etiology.

Surgical procedures, including lobectomy or pneumonectomy if required, were noted during follow-up. Clinical outcomes of the patients with bronchiectasis were evaluated subjectively as ‘well, virtually asymptomatic with occasional exacerbations, improved over baseline, no change or worse’, as used previously [15]. In order to be more objective, lung function tests (FEV1% and FVC%) and annual exacerbation rates were added to patient/parent perception of health status. Outcomes of the patients were accepted as improved if at least two of these three parameters had improved.

goto top of outline Statistical Analysis

SPSS 11.0 for Windows statistical package was used throughout the study. Continuous variables were compared by t tests and the nonparametric Wilcoxon test. Analyses of categorical variables were done by the =χ2 test. Medical and surgical treatment groups were compared using the unpaired t test. A p value <0.05 was considered statistically significant.


goto top of outline Results

Mean age of the patients was 7.4 ± 3.7 years (range 1–17.5) at presentation, and they had been symptomatic for 4.9 ± 3.7 years (range 1–14.9) on average. Males made up 50.5% of the patients. Cough was the primary presenting symptom (96.9%), followed by sputum production (80.6%), dyspnea (49%) and wheeze (46.9%). Mean age of the patients when they had their first respiratory symptoms was 2.5 ± 2.7 years. Ten percent of the patients had a history of hemoptysis. On physical examination, clubbing of the fingers was found in 40.9% and chest deformity in 14.5%. In 42.6%, parents of the patients were either first- or second-degree relatives. At least one other family member had been diagnosed with bronchiectasis in 14.7% of the patients. Mean FEV1 was 63.3 ± 22.1% of predicted; mean FVC was 67.3 ± 23.1% of predicted. Of all patients, 25.2% had atopy, with house dust mite as the most frequent allergen (63.6%) in the atopic group.

An underlying etiology was identified in 62.2% of the patients (table 1). In 29.7%, bronchiectasis was postinfectious, in which severe pneumonia (17.1%), measles (8.1%), varicella (2.7%) and tuberculosis (1.8%) were the responsible infections. Immunodeficiency was diagnosed in 15.3%, followed by primary ciliary dyskinesia, asthma and foreign body aspirations.


Table 1. Underlying etiology of non-CF bronchiectasis patients

Bronchiectatic lesions were most commonly found in the lower lobes (table 2). In 46% of the patients, only one lobe was found to be affected, most commonly the left lower lobe (29%). Bilobar involvement was detected in 28.1%, and 31.9% had multilobar involvement. In patients with diffuse bronchiectasis, bilateral involvement was detected in 46.6%, followed by unilateral left (40%) and right (13.3%) lung involvement.


Table 2. Localization of bronchiectasis in the study group

In 53.1% of the patients, no organism was isolated despite repeated cultures. In 65 patients who had microorganisms grown in sputum cultures, Hemophilus influenzae (38.5%) and Streptococcus pneumoniae (23%) were the most frequently isolated organisms, followed by Staphylococcus aureus (16.9%), Pseudomonasaeruginosa (10.8%), Moraxella catarrhalis (6.2%) and Klebsiella pneumoniae (4.6%). While only one organism was isolated in 43 patients, at least two different organisms were found in 9 patients.

After a mean follow-up period of 4.7 ± 2.7 (range 2–14) years, current mean age of the patients was 12.8 ± 4.4 (range 4–24) years. All patients received medical treatment modalities including prompt antibiotic use in exacerbations, bronchodilators and physiotherapy. Inhaled steroids were given in 78.3% of the patients. In spite of intensive medical treatment, 23.4% continued to have recurrent/persistent respiratory symptoms and required surgery after a mean duration of 14 ± 14.2 months. Although the surgery rate was 15.3% for the patients recruited to the study in the last 5 years (1996–2001), it was 38.5% for the patients recruited between 1987 and 1995. While 9 patients in the surgery group had resolution of symptoms following surgical intervention, 17 patients continued to receive medical treatment during follow-up. In both the medical and surgical groups, the annual lower respiratory infection rate was reduced from a mean of 6.6 ± 4.0 to 2.9 ± 2.9 during follow-up (p < 0.0001). Lung function also improved (mean FEV1% 63.3 ± 21.0 vs. 73.9 ± 27.9, p = 0.01; mean FVC% 68.1 ± 22.2 vs. 74.0 ± 24.8, p = 0.04), and clinical improvement was achieved in 70.9% of the patients. A comparison of the medical and surgical treatment groups at presentation and after follow-up is shown in table 3. There was no difference in clinical improvement rates between the medical (70.1%) and surgical intervention groups (73%; p = 0.77).


Table 3. Comparison of medical and surgical treatment groups


goto top of outline Discussion

Bronchiectasis remains a relatively frequent complication of lower respiratory tract infections in children from developing countries and is still a great problem in these parts of the world [16, 17]. Improved social circumstances, development of broad-spectrum antibiotics and effective treatment of bacterial pneumonia have contributed to the decreased incidence of bronchiectasis in developed countries [18]. In 1994, Nikolaizik and Warner [3 ] noted that only 1% of 4,000 children referred for an evaluation of respiratory complaints had bronchiectasis unrelated to cystic fibrosis. Underlying causes such as congenital malformations, ciliary defects or immunodeficiency were identified in 63% of the children in our study. Although the consanguinity rate in the general Turkish population is 21.2%, 42.6% of the parents of the study group were either first- or second-degree relatives [19]. The higher rate of consanguinity in our study group may suggest that hereditary factors are implicated in the development of bronchiectasis in our population.

The majority of the clinical studies reported that bronchiectasis patients had symptoms in the preschool years [18]. In our study group, although the mean age at presentation was of school age, children had been symptomatic since early childhood. The most common symptoms were cough and sputum production, which is in agreement with other reports in the literature [15, 18]. Although nearly 20% of bronchiectatic children were reported to suffer from wheezing, nearly half of the patients in our study group had wheeze as a presenting symptom [1]. Hemoptysis is a frequent symptom in adult bronchiectasis patients, but it is relatively uncommon in children [16]. Only 10% of the patients in our study group reported hemoptysis, whereas clubbing of the fingers was present in 40.9%. In other studies, finger clubbing was reported in 3–51% of the bronchiectasis patients [15, 16, 18].

Bronchiectatic lesions are most commonly found in the lower lobes, as mucociliary clearance is facilitated by gravity in the upper lobes [1, 16]. In our study group, we also found that the left lower lobe was most commonly affected, followed by the right lower lobe and the right middle lobe.

All children with bronchiectasis should be investigated for an underlying cause. Evaluation of immunodeficiency, cystic fibrosis, chronic aspirations and other predisposing factors must be considered according to the clinical picture. The importance of lung damage occurring after pneumonia, pertussis, measles or tuberculosis as a cause of bronchiectasis is difficult to estimate, but is still the most common cause in developing countries [7, 17]. In our study, 28.8% of the patients became symptomatic after infections and were not found to have any other underlying etiology. The most common form of immunodeficiency associated with bronchiectasis in our patients was deficiency of total IgG, followed by IgG2 subclass deficiency. Hill et al. [20 ] reported that 6.6% of bronchiectatic patients had low IgG subclass values. Measurements of IgG subclass levels should be performed even if total IgG levels are found to be normal. In our study, 4.5% of the patients had normal total IgG, but low IgG subclass levels. Identification of immunodeficiency in these patients is important since they may benefit from replacement therapy.

In our study group, 5 patients had situs inversus and 2 had ciliary abnormalities in repeated samples. As acute infection may affect the ciliary orientation and frequency, a ciliary biopsy had been taken at least 6 weeks after respiratory infection. We assessed the ciliary ultrastructure to diagnose primary ciliary dyskinesia. Buchdahl et al. [21 ] reported the diagnosis of primary ciliary dyskinesia on the basis of their low ciliary beat frequency in several patients whose ciliary ultrastructure was normal. Combined analysis of ciliary beat frequency, beat pattern and ultrastructure might reduce the risk of misdiagnosis and help to identify additional primary ciliary dyskinesia patients in the group with unidentified underlying etiology.

Prolonged presence of a foreign body within the airway can result in the development of bronchiectasis. Kurklu et al. [22 ] reported that 1.6% of the cases of bronchiectasis in their patient group were due to a long-retained foreign body. In a long-term follow-up of foreign body aspiration, bronchiectasis was found in 25% of the patients who were diagnosed after more than 30 days of aspiration [23]. In our study group, 3.6% of the patients developed bronchiectasis after foreign body aspiration.

Our patients received chest physiotherapy and postural drainage with bronchodilator therapy which may assist in the mobilization of endobronchial secretions. We also prescribed short-term treatment with antibiotics in order to reduce the volume and bacterial density of sputum. In some studies, this regimen was found to improve lung function and bronchial hyperreactivity [24,25,26]. Prompt and effective antibiotic use is essential in acute infectious exacerbations. Antibiotic therapy should be prescribed based on bacterial cultures and sensitivity studies [16, 18]. In our study group, patients with symptoms of bronchial hyperreactivity and positive bronchodilator response were also treated by inhaled steroids. In spite of the role of inflammation in bronchiectasis, the use of anti-inflammatory agents has not been established. Tsang et al. [ 14] reported that high-dose fluticasone was found to be effective in reducing the sputum inflammatory indices in bronchiectasis. In a recent Cochrane database review by Kolbe et al. [27], although inhaled steroids were found to have no significant effect on any of the outcomes, there was a trend towards improving FEV1, FVC and PEFR. The authors concluded that larger and longer studies including the rate of decline of lung function, exacerbation frequency, hospitalizations and health status as outcomes were needed.

Identifying and treating the underlying disease is essential to prevent the progression of bronchiectasis. The relative impact of different treatment regimens on the natural course of childhood bronchiectasis has not been well studied [28]. Surgery is increasingly less applied in the management of children with bronchiectasis due to early detection and improved medical treatment modalities [7]. Most investigators now agree that aggressive medical therapy should be carried out before surgery. However, the period of this treatment should be individualized according to the underlying disease or extent of bronchiectasis [1]. Surgical management with segmental or lobar resection is most effective when localized disease is present [29]. This is uncommon when diffuse insults such as lower respiratory tract infections precede the development of bronchiectasis [7]. In our series, 23.4% of the patients had surgical resection. Although medical treatment protocols did not differ much, decision for surgery showed some changes between 1987 and 2001. The surgical management rate was 15.3% for the patients recruited to the study in the last 5 years (1996–2001), but it was 38.5% for the patients recruited between 1987–1995. According to the classical childhood series of bronchiectasis surgery by Wilson and Decker [30], final clinical assessment of the surgical cases shows 75% to be well or much improved, 22% to be improved and 4% unchanged, while patients who were not resected remained largely unchanged (69%) or deteriorated (23%). In our study, there was no difference in clinical improvement rates between medical (70.1%) and surgical intervention groups (73%). Comparing surgery and medical treatment does not seem to be appropriate at the present time, as most of the patients will benefit from either one or the combination of these treatment modalities. In our series, one group of patients received only medical treatment since their disease was far too advanced for surgical intervention. As such, we were compelled to treat that group of patients using a more aggressive medical regimen compared with the patients with minimal and stable disease without failure to thrive or serious symptoms.

In conclusion, bronchiectasis remains a disease of concern to pediatricians, particularly in developing countries. In this study, a large group of patients with non-CF bronchiectasis is discussed. Infections still remain important causes of bronchiectasis in developing countries, and clinical improvement can be achieved by appropriate treatment. Medical treatment remains the mainstay of management of bronchiectasis. Although surgery should be considered in selected patients, medical follow-up of these patients is also necessary. It is further important to note that some patients may be too ill to tolerate surgery, and aggressive medical management in these patients may be preferable.

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 goto top of outline Author Contacts

Bulent Karadag, MD
Abdibey Cad. Altinsoy Apt. No:21/7 Ziverbey-Kadiköy
TR–34150 Istanbul (Turkey)
Tel. +90 216 3266551, Fax +90 216 3257217

 goto top of outline Article Information

Received: April 22, 2004
Accepted after revision: August 25, 2004
Number of Print Pages : 6
Number of Figures : 0, Number of Tables : 3, Number of References : 30

 goto top of outline Publication Details

Respiration (International Journal of Thoracic Medicine)

Vol. 72, No. 3, Year 2005 (Cover Date: May-June 2005)

Journal Editor: Bolliger, C.T. (Cape Town)
ISSN: 0025–7931 (print), 1423–0356 (Online)

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