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Chronic cough and inflammatory bowel disease: an under-recognised association?

James Wingfield Digby, Jenny King, Robert Lord, Jaclyn Ann Smith, Paul Marsden
Breathe 2023 19: 220262; DOI: 10.1183/20734735.0262-2022
James Wingfield Digby
1The University of Manchester, Faculty of Allergy, Immunology and Respiratory Medicine, Wythenshawe Hospital, Wythenshawe, Manchester, UK
2Manchester University NHS Foundation Trust, North West Lung Centre, Wythenshawe Hospital, Wythenshawe, Manchester, UK
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  • For correspondence: james.digby@mft.nhs.uk
Jenny King
1The University of Manchester, Faculty of Allergy, Immunology and Respiratory Medicine, Wythenshawe Hospital, Wythenshawe, Manchester, UK
2Manchester University NHS Foundation Trust, North West Lung Centre, Wythenshawe Hospital, Wythenshawe, Manchester, UK
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Robert Lord
2Manchester University NHS Foundation Trust, North West Lung Centre, Wythenshawe Hospital, Wythenshawe, Manchester, UK
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Jaclyn Ann Smith
1The University of Manchester, Faculty of Allergy, Immunology and Respiratory Medicine, Wythenshawe Hospital, Wythenshawe, Manchester, UK
2Manchester University NHS Foundation Trust, North West Lung Centre, Wythenshawe Hospital, Wythenshawe, Manchester, UK
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Paul Marsden
2Manchester University NHS Foundation Trust, North West Lung Centre, Wythenshawe Hospital, Wythenshawe, Manchester, UK
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Abstract

Respiratory complications of inflammatory bowel disease (IBD) are common and may be under-recognised. Chronic cough may present many years after a colectomy for IBD, is typically productive and can be very responsive to inhaled corticosteroids. https://bit.ly/3DrHNoy

A 51-year-old man presented with a 6-year history of chronic cough to a tertiary chronic cough clinic. The cough was productive (egg cup full of sputum daily), present day and night and associated with numerous triggers. He denied haemoptysis or breathlessness and his weight was stable. The cough was rated on a verbal cough severity scale as 9/10 in severity (where 0 is no cough and 10 is the worst possible cough), and occurred largely in bouts, which were often associated with retching and dizziness. It had worsened in severity in the 2 years prior to attending our specialist cough clinic.

His past medical history included a 15-year history of ulcerative colitis (UC), initially managed medically (combination of azathioprine and steroids), with a subsequent total colectomy (2017) and re-anastomosis (2018). He was an ex-smoker having quit in 1999, with a 5 pack-years smoking history. He worked in construction, with occasional exposure to spray paints.

He had previously been investigated for his cough between 2015 and 2019, at which point he had a normal chest radiograph, sequential blood eosinophil counts and total IgE level. His spirometry was also supranormal, with no forced expiratory volume in 1 s (FEV1) reversibility, and a normal fractional exhaled nitric oxide (FENO). He had undergone multiple treatment trials, including azithromycin, carbocisteine, nasal sprays, proton-pump inhibitors, domperidone, baclofen, metoclopramide and gabapentin. His symptoms had not improved with any of these medications. He had not previously been treated with inhaled corticosteroids.

On examination, his body mass index was 25 kg·m−2, he was not clubbed and his chest examination was unremarkable. Further investigations were arranged, including lung function (figure 1 and table 1), blood tests, a computed tomography (CT) of the thorax (figure 2) and a bronchoscopy.

FIGURE 1
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FIGURE 1

Spirometry and flow–volume loop.

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TABLE 1

Spirometry results

FIGURE 2
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FIGURE 2

High-resolution computed tomography of the thorax.

Task 1

What do the CT and spirometry investigations show?

  • a) Normal appearances of both CT thorax and spirometry

  • b) Severe airflow obstruction and emphysema

  • c) Mild airflow obstruction and cylindrical lower lobe bronchiectasis

  • d) Restrictive lung function and ground-glass opacities

Answer 1

c. This patient's lung volumes are supranormal, but the FEV1/forced vital capacity (FVC) is <0.70 suggesting mild airflow obstruction. The gas transfers are normal. The CT thorax shows mild lower lobe bronchiectasis, which is more marked on the right side. Radiologically bronchiectasis is defined by abnormally widened and thickened airways (airway diameter larger than corresponding blood vessel – “signet ring sign”) that fail to taper as they extend to the lung parenchyma [1]. There is no evidence of emphysema, ground-glass changes or cavitation.

The results of the blood tests and bronchoscopy are shown in table 2.

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TABLE 2

Blood test and bronchoscopy results

Task 2

What do the blood test and bronchoscopy results suggest?

  • a) Normal findings

  • b) Neutrophilic inflammation in the absence of infection

  • c) Eosinophilic bronchitis

  • d) Acute bacterial infection

  • e) Diffuse alveolar haemorrhage

Answer 2

b. The American Thoracic Society (ATS) reference range for normal bronchoalveolar lavage (BAL) cell differential in non-smoking adults is eosinophil count <1%, lymphocytes 10–15%, neutrophils <3%, macrophages >85% and others <5% [2].

  The BAL differential cell count is consistent with neutrophilic inflammation in the absence of an identified infection. This supports the macroscopic findings of inflamed airways and excessive purulent secretions.

  The blood tests are unremarkable aside from the mildly raised myeloperoxidase (MPO) titre on the enzyme-linked immunosorbent assay (ELISA). The perinuclear anti-neutrophil cytoplasmic antibodies pattern observed here can be associated with microscopic polyangiitis (MPA) and eosinophilic granulomatosis with polyangiitis (EGPA) [3, 4]. Neither the history nor clinical examination were in keeping with these. There was no evidence of diffuse alveolar haemorrhage at bronchoscopy. Renal function was also normal, with no evidence of microscopic proteinuria or haematuria. MPO is an enzyme stored within cytoplasmic granules of neutrophils. Described as “friend and foe”, it plays an important role in innate defence against infections, but may also be a marker (and contribute to the pathogenesis) of inflammatory conditions, such as inflammatory bowel disease (IBD), vasculitis and atherosclerosis [5, 6].

Based on our findings, and a review of the literature, we treated this patient as a case of IBD-associated airways disease and inflammatory bronchiectasis. The patient was given a 2-week course of oral prednisolone (30 mg daily), followed by high-dose inhaled corticosteroids (beclomethasone 400 μg three times a day). The response to this was excellent, with a reduction in his verbal cough severity score from 9/10 to 1/10. He was followed up with a telephone call at 6 months and reported a sustained improvement in his symptoms.

Task 3

Which of following respiratory conditions can be associated with IBD?

  • a) Bronchiectasis

  • b) ILD

  • c) Inflammation, scarring and stenosis of the central airways

  • d) Single or multiple pulmonary nodules

  • e) All of the above

Answer 3

e. These conditions are all associated with IBD and will be discussed in more detail in the Discussion section.

Discussion

IBD is common, with an estimated prevalence of 84 per 100 000 population globally [7]. There are a variety of well-documented respiratory manifestations of IBD, which can range from mild nonspecific respiratory symptoms through to severe, debilitating sequelae. The prevalence of respiratory symptoms in this group is high (25–63%) [8, 9], and even in the absence of these symptoms, lung function is diminished in up to 45% of patients [10].

The diagnosis is frequently delayed given symptoms are nonspecific, can precede the diagnosis of IBD or may manifest many years after colectomy [11]. In this case, the cough pre-dated the patient's colectomy, but continued despite definitive intervention for IBD, worsening in severity in the 2 years prior to presentation at our clinic. Interestingly, there are a number of case reports of cough manifesting for the first time after definitive treatment of IBD, occurring as early as months after surgery, to over a decade later, in both Crohn's disease and UC [12, 13].

The underlying mechanisms linking respiratory disease with IBD are not fully established, but could lie in their common embryonic pathway, with the respiratory system developing from the ventral wall of the foregut at 3–4 weeks gestation [14].

Pulmonary manifestations may occur at any location in the respiratory tract (see table 3). Airway inflammation is most common, and results in cough, often with expectoration of copious amounts of mucopurulent secretions [16]. At the severe end of the spectrum, widespread inflammation can occur, with extensive mucosal involvement of the large airways, in some cases leading to stenosis and a “cobble-stone” appearance (interestingly, similar to luminal findings seen in active bowel disease). The most common association is bronchiectasis, which has been reported in nearly 10% of patients [17]. The incidence of this is higher in females and nonsmokers [9, 18], and usually occurs in the lower lobes. Smaller airways are less commonly involved but should be considered where wheeze and breathlessness accompany cough, with case series describing both pan-bronchiolitis and granulomatous bronchiolitis [19, 20].

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TABLE 3

Respiratory manifestations of inflammatory bowel disease

The incidence of interstitial lung disease (ILD) in IBD is thought to be low, but evidence is largely limited to case reports. In a 2020 review of 31 cases of IBD-related ILD across 14 European centres, the incidence was higher in UC compared with Crohn's disease and most frequently related to medications (64.5%) [21]. In this group the most common medications causing respiratory disease were infliximab and aminosalicylates. The most commonly cited non-drug related ILD in this group was organising pneumonia and usual interstitial pneumonia, but there have also been case reports of lymphocytic interstitial pneumonia, eosinophilic pneumonia and desquamative interstitial pneumonia [22].

Studies have suggested genetic similarities between sarcoidosis and Crohn's disease, in which CD4 lymphocyte activation drives the formation of non-caseating granulomas [23]. It is therefore not surprising that both mimicry and overlap can occur with up to 10% of patients with sarcoidosis having gastrointestinal involvement [24]. A definitive link between UC and sarcoidosis is less clear, but has been reported [25].

Rarely patients can present with a serositis, which can manifest as pleuritic chest pain [26]. A higher frequency of pulmonary nodules are also observed, thought to be related to aggregation of neutrophils. These can be numerous and tend to cavitate [27].

Small vessel vasculitides, including EGPA, MPA and granulomatosis with polyangiitis (GPA), are multisystem conditions that can present with diffuse alveolar haemorrhage [28]. Affiliation with IBD is rare, with a recent retrospective of 1697 vasculitis patients reporting a co-prevalence of 0.78% between EGPA and UC and 0.71% between Crohn's disease and GPA. No cases were associated with MPA. A raised MPO antibody level is not specific for vasculitis in patients with IBD, with 62% of patients testing positive despite no evidence of vasculitis [29]. MPO antibodies do however correlate with IBD activity and treatment responses [30].

It is important to consider a broad differential diagnosis in any patient presenting with cough on the background of current or pre-existing IBD. An initial history should focus on the nature of symptoms (cough with or without sputum), dyspnoea and previous or current use of disease-modifying drugs or biologic treatments.

Treatment

Treatment of IBD-related respiratory disease depends on the site of involvement, nature and severity of symptoms. In the case presented, cough was the main symptom, which had been chronic, refractory to previous treatment and very troublesome. The response to inhaled corticosteroids was pronounced. This is in keeping with reports from case series, where either high-dose inhaled or oral corticosteroids have been used with success in IBD-related respiratory disease [9]. Expert consensus suggests longer courses of oral steroids should be reserved for patients with parenchymal disease or resistant airways disease [22]. In this case an improvement in cough was achieved with inhaled corticosteroids alone, but given the associated bronchiectasis, the patient will also be treated according to guidelines, with microbiological surveillance of sputum and chest physiotherapy for airway sputum clearance [31, 32].

Durable clinical responses have been reported, with the two most cited inhaled corticosteroids in IBD related-airways disease being beclomethasone (up to 2500 μg daily) and budesonide (up to 2000 μg daily) [16]. Nebulised steroids (budesonide 2–4 mg per day) can be used in conjunction with oral steroids in refractory cases [16]. Sequential and repeated endobronchial delivery of methylprednisolone (40–80 mg to the left or right bronchial tree) has been utilised to good effect in cases refractory to standard treatment [33].

There is paucity of data on the role of anti-tumour necrosis factor therapy in IBD-related respiratory disease, aside from isolated case reports in Crohn's disease [34]. The risks of infection with this treatment, particularly in patients with bronchiectasis, would have to be carefully be considered [35].

Treatment of IBD-ILD is not empiric and will depend on the site and severity and cause of the disease.

Conclusion

Chronic cough is a debilitating condition, which left untreated has severe physical and psychological consequences. Large airways disease and bronchiectasis should be strongly considered in patients presenting with a cough on the background of IBD (even if this is quiescent or definitively treated with a colectomy in the past). Cross-sectional imaging and bronchoscopy are of value in this group, followed by early treatment with high-dose inhaled corticosteroids, which are often highly effective. Respiratory manifestations of IBD are common, and cover the breadth of the respiratory tract, from upper airway problems to large and small airways and parenchymal disease.

Footnotes

  • Conflicts of interest: J.A. Smith reports grants or contracts from Wellcome Investigator Award, NIHR Manchester Biomedical Research Centre and Bellus Health Inc.; royalties or licenses from Vitalograph Ltd (payment to Manchester University Trust); consulting fees from Merck, Bellus Health, Shionogi, Nocion, Algernon, Trevi, AstraZeneca, Bayer, Chiesi and Boehringer Ingelheim; payment or honoraria for lectures, presentations, speakers’ bureaus, manuscript writing or educational events from Merck; a patent issued (payment to Manchester University Trust); and receipt of equipment for use by Manchester University Trust from Vitalograph Ltd. P. Marsden reports grants or contracts from Merck (investigator initiated research funding award); and lecture fees from Olympus. The remaining authors have no conflicts to declare.

  • Received November 18, 2022.
  • Accepted January 26, 2023.
  • Copyright ©ERS 2023
http://creativecommons.org/licenses/by-nc/4.0/

Breathe articles are open access and distributed under the terms of the Creative Commons Attribution Non-Commercial Licence 4.0.

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Chronic cough and inflammatory bowel disease: an under-recognised association?
James Wingfield Digby, Jenny King, Robert Lord, Jaclyn Ann Smith, Paul Marsden
Breathe Mar 2023, 19 (1) 220262; DOI: 10.1183/20734735.0262-2022

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Chronic cough and inflammatory bowel disease: an under-recognised association?
James Wingfield Digby, Jenny King, Robert Lord, Jaclyn Ann Smith, Paul Marsden
Breathe Mar 2023, 19 (1) 220262; DOI: 10.1183/20734735.0262-2022
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