C L I N I C A L F E AT U R E S

Chest Radiography in Supporting the Diagnosis of Asthma in Children With Persistent Cough

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DOI: 10.3810/pgm.2014.03.2747

Claudia Halaby, MD 1 Martin Feuerman, MS 2 Dan Barlev, MD 3 Melodi Pirzada, MD 1 Winthrop University Hospital, Pediatric Pulmonary Division; 2 Winthrop University Hospital, Office of Health Outcomes Research; 3 Winthrop University Hospital, Radiology Department, Mineola, NY 1

Abstract

Objective: To establish whether chest radiographic findings suggestive of lower airway ­obstruction (LAO) disease support the diagnosis of asthma in pediatric patients with persistent cough in an outpatient setting. Methods: 180 patient charts were reviewed. The patients were children aged 1 to 18 years referred over a 3-year period to a pediatric pulmonary subspecialty clinic for evaluation of cough lasting $ 4 weeks. Chest radiographic images obtained after the initial evaluation of 90 patients diagnosed with cough-variant asthma and 90 patients diagnosed with persistent cough from nonasthma origins were compared with radiologic findings of a control group consisting of patients with a positive tuberculin skin test and no respiratory symptoms. Increased peribronchial markings/peribronchial cuffing and hyperinflation were considered radiographically suggestive findings of LAO disease. Results: Children diagnosed with cough-variant asthma at the initial evaluation had higher rates of chest radiographic findings suggestive of LAO disease (30.00%) than children with persistent cough from other causes (17.80%) or those with a positive tuberculin skin test and no respiratory symptoms (8.16%) (overall P value = 0.0063). They also had higher rates of spirometry abnormalities suggestive of an LAO defect. Children with chest radiographic findings suggestive of LAO disease were found to be younger than those with normal chest radiographic findings (5.0 ± 2.7 years vs 8.6 ± 4.7 years; P , 0.0001). Conclusion: This study suggests that chest radiographic findings indicative of an LAO in correlation with the clinical presentation can support the diagnostic suspicion of asthma, especially in younger children unable to perform spirometry. Keywords: chest radiography; persistent cough; asthma diagnosis; asthma in children

Introduction

Correspondence: Claudia Halaby, MD, Pediatric Pulmonary Division, Winthrop University Hospital, 120 Mineola Boulevard, Suite 210, Mineola, NY 11501. Tel: 516-663-3832 Fax: 516-663-3826 E-mail: [email protected]

Cough is a common presenting problem to pediatricians.1,2 When cough persists and no obvious cause can be identified, children are usually referred to a pediatric pulmonologist for further evaluation.3 Cough-variant asthma is particularly common in children, and usually manifests with chronic cough as the principal, if not the only, symptom. Although asthma is a common cause of chronic cough in children,4 infections (lower respiratory tract infections5,6 and sinusitis),7 anatomic abnormalities, allergic rhinitis, and gastroesophageal reflux8,9 may have a similar presentation. Patient history, physical examination, chest radiography (CXR), and spirometry can provide clues to specific causes of cough,2,10 although diagnosing cough-variant asthma in children, especially those aged , 5 years presenting with persistent cough, can be challenging. The history of the illness process relies on the examiner’s ability to obtain pertinent facts, or the parents’ ability to perceive, recall, and describe their children’s symptoms. The physical examination of children with persistent cough who are suspected of having asthma often does not yield diagnostic findings.

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Halaby et al

Spirometry, an essential part of pulmonary function evaluation, is a valuable tool for assessing the presence of lower airway obstruction (LAO) and lower airway hyperreactivity, which are both abnormalities seen in children with asthma.11,12 Unfortunately, spirometry in younger children is difficult to perform, because it is influenced by the technician’s experience in administering the test to a child and the child’s ability to follow respiratory maneuvers based on the examiner’s verbal commands.13–15 Obtaining a baseline CXR is recommended in children presenting for a pulmonary evaluation with symptoms of persistent cough lasting . 3 weeks.10,16 Even when an asthma diagnosis is strongly suspected, persistent cough can be a presenting symptom of a foreign body aspiration, unrecognized congenital lung malformations, or cardiovascular abnormalities, which are conditions that can sometimes be identified based on an abnormal CXR. Radiographic findings suggestive of an LAO defect, such as increased peribronchial markings/peribronchial cuffing and bilaterally increased air volume/hyperinflation, have been described in patients who clinically present with symptoms of asthma, viral pneumonia,17 or microaspiration from gastroesophageal reflux.18 Although these findings are rare in normal children without pulmonary complaints, they are thought to correspond to an inflammatory process of the small airway walls.17 Chest radiography findings in children with acute asthma exacerbation who presented to the emergency department19 or were admitted to the hospital for status asthmaticus20,21 are well described in the literature. However, CXR findings suggestive of an LAO defect/small airway inflammation of children with persistent cough suspected of having cough-variant asthma have not been documented. Furthermore, the utility of baseline CXR in supporting the diagnosis of cough-variant asthma in children with persistent cough has not been evaluated. Chest radiography is an accessible diagnostic tool and requires minimal cooperation by the child, however, there are increasing parental concerns about radiation exposure related to radiographic testing. This raises the question of CXR utility in supporting the diagnosis of asthma in children presenting with persistent cough. This study aims to determine whether CXR findings suggestive of an LAO defect are helpful in diagnosing asthma in children presenting with persistent cough.

Methods

This study was approved by the Winthrop University Hospital Institutional Review Board. 118

Three diagnostic groups were established for comparison to determine the value of CXR findings of an LAO defect in supporting the diagnosis of asthma. The first group included children with cough-variant asthma diagnosis at the initial evaluation. The second group was children diagnosed with a cough of nonasthma origin at the initial evaluation; a group that the authors hypothesized would be less likely to have CXR findings consistent with an LAO defect. The third group was a control group intended to represent the pediatric population that did not have cough or a diagnosis of asthma but had a CXR because of a positive tuberculin skin testing. We retrospectively reviewed the charts of . 300 children aged 1 to 18 years who presented as new patients to the Pediatric Pulmonary Clinic and the Pediatric Infections Disease Clinic (part of a Pediatric Specialty Center affiliated with Winthrop University Hospital) between January 2007 and December 2009 and who, at the initial visit, had a diagnosis code of asthma, cough, or latent tuberculosis infection. Patients were included in the cough-variant asthma group if their primary complaint was persistent cough for $ 4 weeks, they had a diagnostic code of asthma (­International Classification of Diseases, 9th Revision [ICD-9] code 493.9) at the initial visit, a CXR was ordered as part of the initial evaluation, and the CXR reading was reported in the chart. The first 90 consecutive charts that met the inclusion criteria in this group were selected. Patients were included in the group with a cough of nonasthma origin if their primary complaint was persistent cough for $ 4 weeks, they had a diagnosis code of cough (ICD-9 code 786.2) at the initial visit, a CXR was performed after the initial evaluation, and the CXR reading was reported in the chart. The first 90 consecutive charts that met the inclusion criteria in this group were selected. Patients were included in the control group if they presented for evaluation of a positive tuberculin skin test (ICD-9 code 011.9, code used for latent tuberculosis infection), they had no respiratory complaints, they had a negative past medical history for asthma, a CXR was performed as part of their evaluation, and the CXR reading was reported in the chart. Forty nine charts met the inclusion criteria in this group. Information gathered from the charts included sex, age at the time of evaluation, diagnosis at the initial evaluation, reports of the initial CXRs, and results of spirometry studies (for the children who underwent spirometry evaluation). For the patients included in the group with a cough of nonasthma origin, diagnosis at follow-up visits was also recorded. Findings from the CXR reports were collected as normal or abnormal. Abnormal CXR findings were further

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CXR in Pediatric Asthma Diagnosis

categorized as either suggestive of LAO disease/asthma or important incidental findings. The following were considered CXR findings suggestive of LAO disease: increased peribronchial markings/peribronchial cuffing or bilaterally increased air volume/hyperinflation. Incidental imaging findings suggestive of foreign body aspiration, pneumonia, cardiovascular anomalies, or skeletal abnormalities were considered important. Chest radiographies of the patients included in the study were performed in the radiology department affiliated with the pediatric specialty center and in 2 other radiology centers in the vicinity. Films were available for further review only if performed in the radiology department affiliated with the specialty center. To verify the presence of important incidental CXR findings, a pediatric radiologist reviewed the 115 films available at the time the study was conducted. The reviewer radiologist’s findings were recorded and compared with the initial CXR readings. Spirometries were administered in the Pediatric Pulmonary Clinic to children able to perform the test satisfactorily (aged $ 6 years) according to the American Thoracic Society/ European Respiratory Society pulmonary function testing guidelines.12 The results were documented either as normal or, alternatively, suggestive of LAO disease (ie, forced expiratory volume in 1 second [FEV1], forced expiratory flow, midexpiratory phase [forced expiratory flow25%–75%], or FEV1/ forced vital capacity was , 80% of the predicted value for age, gender, height, and ethnicity).

Statistical Methods

Comparisons of diagnostic groups (cough of nonasthma origin, cough-variant asthma, and control) for categorical variables (eg, gender, radiographic findings [yes/no]) were performed using the Fisher exact test. Comparisons of the 3 diagnostic groups for continuous variables (eg, age) were evaluated using the Kruskal-Wallis test. Evaluating the significance of the difference in mean age based on CXR findings (+/−) was calculated using the ranksum test. A  stepwise multiple logistic regression (using P , 0.05 as a cutoff) was used to determine independent

factors ­associated with ­positive radiographic findings. All calculations were performed using SAS 9.2 for Windows. Results were considered significant when the P value was , 0.05.

Results

Subject characteristics in each group are shown in Table 1. No statistically significant difference was seen in age and gender distribution among the 3 groups; the mean age for all 3 groups was approximately 8 years. Patients diagnosed with cough-variant asthma at the initial evaluation were significantly more likely to undergo spirometry evaluation than those diagnosed with cough of nonasthma origin (70% vs 49%; P = 0.0061). Chest radiography evaluation revealed findings of LAO disease in 30.0% (n = 27) of patients diagnosed at initial evaluation with asthma and in 17.8% (n  =  16) patients diagnosed with cough of nonasthma origin. Four patients (8.2%) with positive tuberculin skin test results and no pulmonary symptoms had CXR findings consistent with an LAO defect. Table  2  shows the differences observed among the 3 groups as being statistically significant (overall P = 0.0063). Table  3 presents results of the logistic regression for CXR findings suggestive of LAO disease. The logistic regression shows that pair-wise comparisons of groups are significantly predictive of positive CXR findings as well as decreasing age. Decreasing age was predictive of CXR findings suggestive of LAO defect. Gender was not a significant predictor. The percentage of abnormal CXR findings that were not suggestive of LAO disease was higher in the group of patients diagnosed at the initial visit with persistent cough not suspected of being from asthma (Table 2), but the difference was not statistically significant (14.40% vs 5.56%; P = 0.639). Examples of these findings are lobar infiltrates, right-sided aortic arch, hilar lymphadenopathy, calcified granuloma, and skeletal abnormalities (ie, scoliosis, bifid rib). Children with persistent cough diagnosed initially with asthma were more likely to have spirometry findings

Table 1.  Baseline Characteristics of Children at Initial Evaluation Characteristic

Age, y (mean ± SD) Female sex, n Performed spirometry, n

Control (Patients With +TST and No Respiratory Diseases)

Diagnosis of Asthma at Initial Evaluation

Diagnosis of Cough of Nonasthma Origin at Initial Evaluation

n = 49

n = 90

n = 90

8.1 ± 6.2 23 (46.9%) N/A

7.9 ± 3.7 35 (38.9%) 63 (70.0%)

7.7 ± 4.5 40 (44.4%) 44 (48.9%)

Overall P Value 0.73 0.59 0.0061

Abbreviations: N/A, not applicable; SD, standard deviation; +TST, positive tuberculin skin test. © Postgraduate Medicine, Volume 126, Issue 2, March 2014, ISSN – 0032-5481, e-ISSN – 1941-9260 119 ResearchSHARE®: www.research-share.com • Permissions: [email protected] • Reprints: [email protected] Warning: No duplication rights exist for this journal. Only JTE Multimedia, LLC holds rights to this publication. Please contact the publisher directly with any queries.

Halaby et al

Table 2.  Abnormalities Suggestive of LAO Defect Characteristic

Control (Patients With +TST and No Respiratory Diseases)

Diagnosis of Asthma at Initial Evaluation

Diagnosis of Cough of Nonasthma Origin at Initial Evaluation

Overall P Value

Number of CXRs with findings suggestive of LAO disease Number of abnormal CXRs with no LAO disease findings Number of spirometric tests with findings suggestive of LAO disease

4 (8.16%)

27 (30.00%)

16 (17.80%)

, 0.01

2 (4.08%)

5 (5.56%)

13 (14.40%)

0.0639

N/A

8 (22.2%)a

1 (3.23%)b

0.0313

For the 63 spirometries performed in the asthma group, 27 were suboptimal and not used. Thus, the percentage indicated is based on a sample of 63 – 27 = 36. For the 44 spirometries performed in the cough group, 13 were suboptimal and not used. Thus, the percentage indicated is based on a sample of 44 – 13 = 31. Abbreviations: CXR, chest radiography; LAO, lower airway obstruction; N/A, not applicable; +TST, positive tuberculin skin test. a

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b

s­ uggestive of LAO than patients diagnosed with cough of nonasthma origin (22.20% vs 3.23%; P = 0.0313; Table 2). Although the present results show that CXR findings suggestive of an LAO defect were more common in children diagnosed with cough-variant asthma at the initial evaluation, Table 4 shows that younger children (mean age, 5 years) were more likely to have these findings. Children who had spirometry findings suggestive of an LAO defect were older (n = 9; mean age, 12 years). However, this result should be considered with caution because of the limited sample size. In particular, Table  4 presents the comparative mean age of children with an LAO defect on spirometry and that of children with CXR findings suggestive of LAO. Of the 115 CXRs available for review by the pediatric radiologist, 61 were from children diagnosed with asthma at the initial visit, and 28 were from children diagnosed with persistent cough of a nonasthma origin. Children who had CXRs available for review were younger (the mean age was ∼1 year lower for each study group). The independent reviewer identified the same number of important incidental findings as the radiologist who initially read the CXR. In this study cohort, only 26 (28.9%) children diagnosed with persistent cough of nonasthma origin at the initial evaluation returned for follow-up visits. Of these, 22 were subsequently diagnosed with asthma, possibly because of the persistence of their symptoms and their response to asthma medication, and 8 (36.3%) had CXR findings suggestive of an LAO defect (Table 5). Table 3.  Summary of Logistic Regression for Dependent Variable: Chest Radiographic Findings Suggestive of LAO Disease Variable

Odds Ratio

95% CI

P Value

Cough vs Control Asthma vs Control Asthma vs Cough Age

3.630 10.00 2.760 0.745

1.04–12.60 2.83–35.60 1.25–6.11 0.658–0.843

0.0425 0.0004 0.0120 , 0.0001

Abbreviation: LAO, lower airway obstruction.

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Discussion

Several studies describe the CXR findings in adults and children with asthma,19–28 and the conclusions regarding the utility of this diagnostic tool are conflicting. Most of the studies regarding CXR in patients with asthma examined the incidence of abnormal radiographic findings of asthma complications,20,21,23 such as atelectasis, pneumonia, pneumomediastinum, or pneumothorax. To the authors’ knowledge, the incidence of CXR findings suggestive of an LAO defect/small airway inflammation in children with persistent cough diagnosed with asthma has not been evaluated. This study found that the incidence of radiographic findings suggestive of an LAO defect in children with persistent cough diagnosed at initial evaluation with asthma was 30.0%. This percentage was similar to that of CXR findings of an LAO defect in children diagnosed with asthma on subsequent follow-up visits (36.3%) based on symptom persistence and response to asthma therapies. These data showed that children with CXR findings suggestive of LAO defect were younger, with a mean age of approximately 5 years. Thus, evidence of LAO on CXR in younger children may help establish a diagnosis of asthma, especially because most of these children are unable to perform spirometry. Table 4.  Age Distribution of CXR and Spirometry Findings Suggestive of LAO Diseasea Diagnosis at Initial Evaluation

Age of Patients With CXR Findings Suggestive of LAO

3.3 ± 3.9 5.9 ± 2.3 4.1 ± 2.7 Total of all groups: 5.0 ± 2.7 Control Asthma Cough

Age of Patients With Spirometry Findings Suggestive of LAO N/A 11.9 ± 3.8 12.0b

Body of tables expreses values in means ± SD when available. SD cannot be calculated because n = 1. Abbreviations: CXR, chest radiography; LAO, lower airway obstruction; N/A, not applicable. a

b

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CXR in Pediatric Asthma Diagnosis

Table 5.  Data From Follow-Up Visits of Patients With Initial Diagnosis of Cough of Nonasthma Origin Characteristic

Diagnosis of Cough at Initial Evaluation

Patients followed up, n (%) Age of patients, y (Mean [SD]) Female sex, n (%) Asthma diagnosis on follow-up, n (%) CXR findings suggestive of LAO defect in patients diagnosed with asthma on follow-up, n (%)

26 (28.9%) 7.3 (4.4) 12 (46.2%) 22 (84.6%) 8 (36.3%)

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Abbreviations: CXR, chest radiography; LAO, lower airways obstruction.

Changes in spirometry suggesting an LAO defect were observed in older children (mean age, 12 years). Because spirometry is technically challenging to perform in younger children, findings that support an asthma diagnosis can only be seen in older children, thereby supporting the conclusion that CXR findings of an LAO defect are more valuable in younger children for arriving at an asthma diagnosis. This study has some limitations. Because this is a retrospective study based on chart review, there were no preset specific diagnostic criteria for asthma at the initial evaluation or the follow-up visit. The diagnosis was established by 1 of the 3 pediatric pulmonologists in the practice. The initial diagnosis was made before a CXR was obtained. Therefore, the diagnosis was not influenced by the CXR findings. Not all CXR evaluations were performed in the same radiologic facility, and . 1 pediatric radiologist was interpreting the studies. A few of the studies were performed in 2 other radiology centers in the vicinity. Chest radiography findings were collected from the reports found in the patient chart. A pediatric radiologist reviewed the findings for the patients who had the CXR performed in the radiology department associated with the authors’ facility. The radiologist was blinded to the initial diagnosis of these patients, but was aware of the hypothesis of the study. No significant differences were seen between the reported readings and those performed by the independent reviewer in identifying CXR abnormalities that were not suggestive of an LAO defect, such as pulmonary infiltrates or chest wall or cardiovascular abnormalities. The follow-up rate for patients with persistent cough who were not diagnosed with asthma at the initial evaluation was very low (28.9%), according to the charts reviewed. The authors postulated that a contributing reason for these patients not following up may have been the resolution of their symptoms during therapies not intended to treat asthma. This hypothesis is based on the observation that 84.6% of patients who returned for the follow-up visit were sub­ sequently diagnosed with asthma and treated accordingly.

Conclusion

Results of this study suggest that CXR findings suggestive of an LAO defect can help support the diagnosis of asthma in younger children, especially those too young to perform spirometry. Because of a paucity of pediatric pulmonologists in many areas around the country, children with persistent cough do not always receive immediate referral for a subspecialist evaluation. The present findings suggest that performing a simple test such as a CXR in patients with persistent cough, especially those aged , 6 years, can rule out both infectious and anatomic lung abnormalities, and can also support a diagnosis of asthma in adjunct to the clinical presentation. Further prospective, larger studies are needed to support the association between CXR changes suggestive of an LAO defect and asthma in young children.

Acknowledgments

The authors wish to thank Dr L. Krilov and Dr C. Valsamis for their valuable input in writing the manuscript.

Conflict of Interest Statement

Melodi Pirzada, MD, is a stockholder of Lucina Advanced Care. Claudia Halaby, MD, Martin Feuerman, MS, and Dan Barlev, MD, disclose no conflicts of interest.

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Chest radiography in supporting the diagnosis of asthma in children with persistent cough.

To establish whether chest radiographic findings suggestive of lower airway obstruction (LAO) disease support the diagnosis of asthma in pediatric pat...
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