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ORIGINAL ARTICLE

Hiatal hernias are correlated with increased severity of non-cystic fibrosis bronchiectasis MELISSA JANE MCDONNELL,1,2 MOHAMMAD AHMED,1 JEEBAN DAS,3 CHRIS WARD,2 MATSHEDISO MOKOKA,1 DAVID P. BREEN,1 ANTHONY O’REGAN,1 JOHN J. GILMARTIN,1 JOHN BRUZZI3 AND ROBERT M. RUTHERFORD1 Departments of 1Respiratory Medicine and 3Radiology, Galway University Hospitals, Galway, Ireland, and 2Institute of Cell and Molecular Biosciences, Framlington Place, Newcastle Medical School, Newcastle University, Newcastle upon Tyne, UK

ABSTRACT Background and objective: Hiatal hernias (HH) are associated with gastro-oesophageal reflux and may contribute to lung disease severity. We aimed to evaluate the prevalence of HH among stable non-cystic fibrosis bronchiectasis (NCFB) patients and determine associations with disease severity. Methods: A retrospective cross-sectional cohort study of 100 consecutive NCFB patients in our institution was performed. Data were collected on baseline variables, microbiology, lung function and radiology, according to the modified Bhalla score. Disease severity was assessed using the Bronchiectasis Severity Index (BSI) and FACED severity scores. Results: Following expert radiological review, 81 patients were deemed suitable for study inclusion (mean age (SD) 62.6 (12.4), females 55 (67.9%), body mass index (BMI) 26.9 (5.7)); 29 (35.8%) were HH positive (HH+). HH+ patients had a trend towards higher BMI (P = 0.07), and a significantly higher proportion had reflux symptoms (HH+ 62.1% vs HH− 28.8%, P < 0.01). The presence of HH+ was associated with cystic bronchiectasis (HH+ 30.1%, HH− 11.5%; P = 0.03), increased number of lobes involved (HH+ 2.62 (1.54), HH− 2.17 (1.42); P = 0.03), increased extent of bronchiectasis, (HH+ 6.2 (4.7), HH− 4.5 (3.1); P = 0.04), decreased parenchymal attenuation (HH+ 1.0 (1.8), HH− 0.2 (0.5); P = 0.03) and reduced per cent predicted forced expiratory volume in 1 s (HH+ 75.4% (24.5), HH− 90.4% (25.5); P = 0.02). There was no lobar predilection. HH+ was associated with increased disease severity scores: BSI (HH+ 4.93 (1.65), HH− 3.25 (2.13); P < 0.001) and FACED (HH+ 2.21 (1.52), HH− 1.35 (1.43); P < 0.01). Conclusions: HH+ was associated with worse disease severity in NCFB patients, characterized by decreased lung function, increased extent and severity of radiological disease, and increased composite disease severity scores. Correspondence: Melissa Jane McDonnell, Department of Respiratory Medicine, Galway University Hospitals, Galway, Ireland. Email: [email protected] Received 29 August 2014; invited to revise 5 October 2014; revised 3 January 2015; accepted 1 February 2015 ( Associate Editor: Yuanlin Song). Article first published online: 14 April 2015 © 2015 Asian Pacific Society of Respirology

SUMMARY AT A GLANCE This is the first study to evaluate the role of hiatal hernias in bronchiectasis. The presence of a hiatal hernia was associated with worse disease severity, characterized by decreased lung function, increased extent and severity of radiological disease, and increased composite disease severity scores.

Key words: bronchiectasis, hiatal hernia, prevalence, scoring system, severity. Abbreviations: ABPA, allergic bronchopulmonary aspergillosis; BAL, bronchoalveolar lavage; BMI, body mass index; BSI, Bronchiectasis Severity Index; CF, cystic fibrosis; COPD, chronic obstructive pulmonary disease; ERS, European Respiratory Society; FEV1, forced expiratory volume in 1 s; FVC, forced vital capacity; GORD, gastro-oesophageal reflux disease; HH, hiatal hernia; HH+, presence of a hiatus hernia on independent expert radiological review; HH−, absence of a hiatus hernia on independent expert radiological review; HRCT, high-resolution computed tomography; IPF, idiopathic pulmonary fibrosis; LOS, lower oesophageal sphincter; MDCT, multidetector computed tomography; NCFB, non-cystic fibrosis bronchiectasis; PFT, pulmonary function test; PPI, proton pump inhibitor.

INTRODUCTION Non-cystic fibrosis bronchiectasis (NCFB) is an umbrella term for patients suffering from repeated episodes of bronchitis and recurrent chest infections with associated structural dilatation of the airways visible on high-resolution computed tomography (HRCT). NCFB has numerous aetiologies but despite intensive investigation, up to 50% of patients have no causative factor identified.1 Gastro-oesophageal reflux disease (GORD) has been shown to be associated with disease severity in several chronic respiratory diseases, including asthma, chronic obstructive pulmonary disease (COPD), cystic fibrosis (CF), idiopathic pulmonary Respirology (2015) 20, 749–757 doi: 10.1111/resp.12522

750 fibrosis (IPF) and bronchiolitis obliterans post-lung transplantation.2–5 It has been suggested that GORD may play a role in the development and severity of NCFB. To date, there is a paucity of studies examining this relationship. Prevalence studies of reflux in bronchiectasis, utilizing questionnaire and/or 24-h oesophageal pH monitoring, have shown symptomatic and clinically silent reflux in 26–75% of patients.6 Symptomatic GORD in bronchiectasis has been associated with reduced lung function, an increased exacerbation frequency and reduced quality of life.7,8 The relationship between hiatal hernias (HH) and GORD has been extensively investigated over the past few decades. HH occurs when part of the stomach protrudes into the thoracic cavity through the oesophageal hiatus of the diaphragm due to disruption of the anti-reflux barrier at the gastrooesophageal junction. This is an anatomically complex area made up of the lower oesophageal sphincter (LOS), the crural diaphragm and the anatomical flap valve.9,10 In patients with a HH, the flap valve disrupts and the LOS moves above the crural diaphragm, causing the high-pressure zone to lose its synergistic configuration, and both the LOS and diaphragm sphincters to become appreciably weaker, compromising oesophageal acid clearance and facilitating the development of reflux.9 An increased prevalence of HH has been reported in asthma and IPF.11,12 To our knowledge, there have been no studies to date looking at the prevalence rate of HH in NFCB patients. We therefore estimated the prevalence of HH on HRCT among a well-defined cohort of NFCB patients and compared clinical indices in HH-positive (HH+) and HH-negative (HH−) patients to determine potential associations with independent and composite markers of disease severity.

METHODS Study population A retrospective observational cross-sectional cohort study of 100 consecutive patients referred for investigation of NCFB in our institution (Galway University Hospitals, Ireland) over an 18-month period (January 2011–June 2012) was performed. All suspected NCFB patients in our institution undergo a dedicated diagnostic clinical work-up including history, examination, detailed aetiological screening bloods, spirometry, bronchoscopy, bronchoalveolar lavage (BAL) and HRCT according to methodologies previously described, with screening for CF and primary ciliary dyskinesia in select patients.13 Data were collected on baseline demographics including gender, age at diagnosis, body mass index (BMI), smoking status, medical comorbidities (determined by the Charlson Comorbidity Index), GORD symptoms and proton pump inhibitor (PPI) treatment, aetiology of NCFB, Medical Research Council Dyspnoea score, number of exacerbations and hospitalizations over the prior year, baseline microbiological status on BAL, baseline pulmonary function and baseline radiological involvement. Ethical approval Respirology (2015) 20, 749–757

MJ McDonnell et al.

was granted by our local Research Ethics Committee. Individual patient consent was not required as this was a retrospective research study based on routine diagnostic investigations and bronchiectasis work up.

Diagnosis of bronchiectasis The diagnosis of NCFB was defined as patients with daily mucopurulent sputum production plus dilated and thickened airways on HRCT.1 Aetiology was defined according to methodologies previously described; a diagnosis of idiopathic bronchiectasis was made if all aetiological screening tests were negative, and no associations with other known diseases were found.13 CT images were acquired on a 64-slice multidetector CT scanner (Somatom Sensation Cardiac 64, Siemens, Erlangen, Germany). Inspiratory spiral and expiratory sequential scans were performed at an initial collimation of 5 mm, and reconstructed at 1.0-mm thin slices at section intervals of 10 mm. Scanning parameters included a kVp of 120 (doseadjusted), 40 mAs (care-dose), rotation time of 0.5 s and a pitch of 1.4. Intravenous contrast media was not administered, and scans were performed with patients positioned supine. All scans were reported by radiologists with expertise in HRCT imaging at the time of scanning. Subsequent independent review for confirmation and scoring of disease severity according to the modified Bhalla score, validated for use in NCFB, was performed by an expert thoracic radiologist (J.B.).14 The extent of bronchiectasis, severity of bronchial dilatation, bronchial wall thickness, presence of mucus plugging in large and small airways, and decrease in parenchymal attenuation were scored for each lobe, with the lingula considered a separate lobe, making a total of six lobes (Table 1). Total lung scores for each abnormality were defined as the mean score from all lobes for each HRCT feature. The proportion of cystic versus varicose or cylindrical bronchiectasis was recorded along with the total number of lobes involved. Lobar predominance was assessed by calculating the mean scores for all HRCT features per lobe. A combined HRCT total score for all HRCT features across all lobes was subsequently derived from summing the individual scores. Evaluation of the presence of a HH The presence of HH was determined by evaluation of the oesophageal junction in relation to the diaphragm using recognized anatomical definitions.15 Where ‘present’, each HH was classified according to gastric fundus size as small (5 cm). ‘Absent’ HH was graded as 0. Pulmonary function tests Pulmonary function tests (PFT) were performed using a Sensormedics V-Max 22 device (CareFusion GmbH, Hoechberg, Germany) allowing calculation of forced expiratory volume in 1 s (FEV1), forced vital capacity (FVC) and FEV1/FVC ratio. Values were expressed as percentage predicted for age, gender, height and ethnicity employing standard European © 2015 Asian Pacific Society of Respirology

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Hiatal hernias in bronchiectasis Table 1 Modified Bhalla high-resolution tomography (HRCT) scoring system HRCT abnormality Presence and extent of bronchiectasis

Grade

Interpretation

0 1

3 0 1

No disease Bronchiectasis affecting one or part of one bronchopulmonary segment (localized) Bronchiectasis in more than one bronchopulmonary segment (extensive) Generalized cystic bronchiectasis Normal 100–200% arterial diameter 200–300% arterial diameter >300% arterial diameter Normal 100% arterial diameter None Present

0 1

None Present

0 1 2

Normal ≤50% lobar volume >50% lobar volume

2

3 Bronchial dilatation relative to adjacent pulmonary artery

0 1 2

Bronchial wall thickness relative to adjacent pulmonary artery

Presence of mucus plugging within the large airways Presence of mucus plugging within the centrilobular bronchiole Extent of decreased attenuation

computed

3 0 1 2

Respiratory Society (ERS)/American Thoracic Society reference ranges.16 All PFT were carried out by pulmonary physiologists trained according to the recommendations of the ERS.17

Relationship between HH and disease severity To analyse the relationship between HH and disease severity, statistical comparisons of known individual clinical markers of severity between HH+ and HH− patients were performed. Factors that have been shown to be associated with disease severity in individual studies include extent of overall bronchiectasis and bronchial wall hypertrophy on HRCT, chronic colonization by Pseudomonas aeruginosa, exacerbation frequency and high concentrations of proinflammatory markers in sputum or serum.18–20 Two composite severity scores for bronchiectasis have recently been developed: the Bronchiectasis Severity Index (BSI) and the FACED scoring system, both of which can be utilized to determine a potential relationship between the presence of HH and disease severity.21,22 Statistical analysis Statistics were computed using SPSS Version 21 for Windows (SPSS, Chicago, IL, USA) for Windows plat© 2015 Asian Pacific Society of Respirology

Figure 1 Axial computed tomography (CT) images of the lower thorax in (a) lung and (b) mediastinal soft tissue windows demonstrate mild cylindrical bronchiectasis and peribronchial wall thickening (arrows) in association with a large hiatal hernia (asterix).

form and Graph Pad Prism Version 5 (Graph Pad Software, Inc. San Diego, CA, USA). Mean and standard deviation were used for continuous parametric data, median and interquartile range for continuous nonparametric data, and frequencies and percentages for categorical data. Patients were divided into HH-positive (HH+) and HH-negative (HH−) groups. Subgroup analyses were performed using the chisquare test or unpaired t-test depending on data distribution. Chi-square test was used for clinical characteristics including gender, cystic versus cylindrical disease and microbial colonization. Group mean spirometric values and age were normally distributed and compared using the unpaired t-test. HRCT scores (total and by section) were not normally distributed. Group means were compared by the Mann–Whitney U-test. A P-value

Hiatal hernias are correlated with increased severity of non-cystic fibrosis bronchiectasis.

Hiatal hernias (HH) are associated with gastro-oesophageal reflux and may contribute to lung disease severity. We aimed to evaluate the prevalence of ...
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