The two most common parenchymal disorders associated with IBD are organizing pneumonia and necrobiotic nodules [14]. Nonspecific interstitial lung disease (NSIP) and eosinophilic pneumonia have been described, but are most often related to drug toxicity [5].

Parenchymal lung abnormalities in IBD occur most frequently in patients with ulcerative colitis, with a discrete female predominance [14, 30]. In a review by Black et al, among 155 patients with IBD and thoracic involvement, 58% were women, and 65% had ulcerative colitis [14]. Parenchymal lung abnormalities associated with IBD typically appear several years after the onset of intestinal manifestations, and their evolution is independent from that of the latter [36].

Organizing pneumonia is the most common parenchymal lung abnormality in IBD, and occurs more frequently in patients with ulcerative colitis than in those with Crohn’s disease [14, 15, 21]. In an analysis of more than 400 patients with pulmonary manifestations of IBD, Storch et al found nine patients with organizing pneumonia, of which eight had ulcerative colitis [37]. In Crohn’s disease, non-caseating granulomatous infiltrates may be combined with organizing pneumonia [33]. Organizing pneumonia can be related to IBD or drug-induced [38].

Clinically, organizing pneumonia can present as a condition with fever, cough, dyspnea, and raised inflammatory markers. Organizing pneumonia is usually reversible with treatment without sequelae but tends to recur.

On CT, organizing pneumonia usually presents as multifocal alveolar consolidation, often accompanied by an air bronchogram [39]. Lesions preferentially have a subpleural or peribronchial distribution predominating in the lower lobes [39] (Fig. 4). These consolidations are nonspecific and mimic infectious pneumonia. The recurrence of consolidations in a different locations (migratory pattern) and the reversed halo sign are key imaging findings for the diagnosis (Fig. 5). The reversed halo sign, also known as the Atoll sign, was first described in patients with cryptogenic organizing pneumonia [40]. It is found in less than 20% of patients with IBD-related organizing pneumonia. It is characterized by a central ground-glass opacity surrounded by a crescentic or ring-shaped consolidation. Initially considered highly suggestive of organizing pneumonia, it has been described in several other inflammatory diseases (lupus, rheumatoid arthritis, granulomatosis with polyangiitis), infectious (fungal), vascular, and neoplastic diseases [41].

Various CT patterns of inflammatory bowel disease-related organizing pneumonia. A CT image in the axial plane shows bilateral consolidation with air bronchogram in a 71-year-old patient with Crohn’s disease. B CT image in the axial plane shows a pseudo-tumoral lesion (arrow) in a 36-year-old patient with Crohn’s disease. C CT image in the axial plane shows multiple consolidations with the atoll sign (arrow) in a 35-year-old patient with Crohn’s disease

Recurrent organizing pneumonia in a 28-year-old patient with Crohn’s disease. A CT image in the axial plane shows peribronchovascular consolidations in the left lower lobe consistent with organizing pneumonia. These lesions disappeared with corticosteroids. B Few months after corticosteroids withdrawal, a recurrence of organizing pneumonia was observed in other lung areas

Organizing pneumonia may also be present as a single or as multiple pulmonary nodules (focal nodular organizing pneumonia) [42]. The differential diagnoses in patients with IBD include necrobiotic and noncaseating granulomatous nodules.

Necrobiotic nodules associated with IBD were first described in 2000 by Faller et al [43]. They account for around 5% of pulmonary manifestations encountered in IBD [16, 33]. They can be observed in both Crohn’s disease and ulcerative colitis, but recent data suggest a greater prevalence in Crohn’s disease [44, 45]. In 2012, Barbosa et al reported 15 published cases of necrobiotic nodules, 10 of which were observed in patients with Crohn’s disease [45]. The majority of cases were associated with active intestinal disease [46,47,48] and observed in young patients (< 30-year-old) [46]. More rarely, true granulomatous pulmonary nodules without caseous necrosis have been reported and almost exclusively in pediatric patients with Crohn’s disease [49, 50]. In a case report by Roblin et al the patient was 13-year-old and the pulmonary granulomatous involvement preceded the digestive disease, which occurred a few weeks later [49].

Histologically, necrobiotic nodules combine sterile aggregates of neutrophils with areas of central necrosis, and are closely related to pulmonary nodules in rheumatoid arthritis and cutaneous nodules in pyoderma gangrenosum [3]. They may display a pseudo-granulomatous appearance when epithelioid histiocytes are associated with aggregates of plasma cells [51]. Differentiation between necrobiotic nodules, caseous granulomas and nodular organizing pneumonia requires histological sampling, which is often not performed as it is not necessary for patient management.

The clinical presentation of necrobiotic nodules and non-caseating granulomatous nodules is nonspecific. The most frequent symptoms are dyspnea, cough and sometimes chest pain in the case of subpleural localization; fever is less frequent compared to organizing pneumonia [41].

On imaging, necrobiotic nodules and granulomatous nodules have a similar presentation. On CT, they are solid nodules or masses generally measuring less than 3 cm, are predominantly located in subpleural areas, and may subsequently cavitate (Fig. 6) [45, 46, 52]. Due to their nonspecific appearance, there is no criterion for differentiating these two types of lesions. Granulomatous nodules may also present as consolidations, mimicking organizing pneumonia.

Necrobiotic nodule (histologically confirmed) in a 41-year-old patient with Crohn’s disease. A CT image in the axial plane reveals a right lower lobe nodule that was diagnosed during the initial Crohn’s disease flare-up and surgical resection. B HES staining of the lesion showing necrotizing granuloma. The central necrosis (*) is surrounded by epithelioid granuloma with giant cell (arrow)

Interstitial lung diseases (ILDs) are more frequently associated with ulcerative colitis than with Crohn’s disease. A recent literature review identified 31 patients with ILD, the majority of which had ulcerative colitis (22/31), and 64% were drug-induced [53]. ILDs other than organizing pneumonia that have been reported in patients with IBD include pleuroparenchymal fibroelastosis (Fig. 7), NSIP, desquamative interstitial pneumonia, eosinophilic pneumonia, and usual interstitial pneumonia [14, 53,54,55]. These ILD are less common than organizing pneumonia, which represents almost half of the cases of ILD observed in IBD patients [53].

Pleuroparenchymal fibroelastosis in a 70-year-old patient with ulcerative colitis. A CT image in the axial plane shows bilateral subpleural consolidations with bronchiolectasis. B CT image in the coronal plane shows apical distribution and volume loss in the upper lobes. The combination of these CT findings is highly suggestive of the diagnosis of pleuroparenchymal fibroelastosis, and no surgical biopsy has been performed

ILD usually occurs some months or even years after the onset of IBD. In a literature review on ILDs associated with ulcerative colitis, Xu et al found that the ILD occurred 1‑ to 15 years after the diagnosis of ulcerative colitis in 12 patients (12/14, 85%), and five of them developed ILD during IBD activity (5/12; 42%) [56].

In IBD, drug-induced pneumonias are mainly related to purine analogues (Azathioprine, 6-mercaptopurine), 5-ASA derivates (mesalazine, sulfasalazine), Methotrexate, and anti-tumor necrosis factor (TNF) alpha [53, 57, 58]. The clinical presentation is non-specific with the most frequent symptoms being dyspnea, cough and fever, however patients can be asymptomatic [53]. On imaging, drug-induced pneumonias can show different patterns, such as organizing pneumonia (Fig. 8) or nonspecific interstitial pneumonia [16, 43, 59]. The diagnosis of drug-induced pneumonia is based on (i), a similar radiological and/or histopathological pattern, (ii), exclusion of other etiologies, (iii), improvement after discontinuation of treatment and, (iv), relapse of symptoms in cases of drug rechallenge. Anti-TNF alpha used in treatment can also cause infectious complications, including tuberculosis.

Drug-induced pneumonia in an 18-year-old patient with ulcerative colitis treated with mesalamine. CT image in the axial plane images show bilateral subpleural consolidations (arrows in A and B). CT-guided transthoracic biopsy was performed and showed pathological findings compatible with mesalamine-induced lung disease

IBD are also associated with an increased risk of infectious pneumonia, even in untreated patients. In a cohort of 74,156 IBD patients and 1,482,363 controls without IBD, Kantsø et al. showed that Crohn’s disease and ulcerative colitis are associated with an increased risk of invasive pneumococcal disease before and after the diagnosis of IBD (hazard ratio, 1.99; 95% confidence interval, 1.59–2.49 for Crohn’s disease and 1.46; 95% confidence, 1.25–1.69 for ulcerative colitis). Pneumococcal vaccination is therefore recommended for all IBD patients [60].

The use of immunosuppressive agents also increases the risk of opportunistic pulmonary infection. Immunosuppressive agents used in IBD include systemic corticosteroids, anti-TNF agents, and JAK inhibitors. Biologic therapies and JAK inhibitors are associated with an increased risk of tuberculosis. For this reason, IBD patients should be screened for latent tuberculosis prior to immunosuppression [61]. Screening for latent tuberculosis is based on a combination of epidemiological risk factors, physical examination, chest X-ray and tuberculin skin test or interferon-gamma release test. Tuberculosis is not the only pulmonary infection at increased risk under immunosuppressive therapy in IBD patients. In the event of infectious pneumonia in an IBD patient undergoing immunosuppressive treatment, the presence of Legionella pneumophila should always be suspected and the patient tested [61]. Immunosuppressive drugs also increase the risk of pneumocystis, and prophylaxis should be considered for certain treatment combinations [61].

The imputability of IBD in the development of thoracic lesions is sometimes difficult to assess, particularly in smokers who may smoking-related chronic obstructive pulmonary disease. IBD may also be associated with other immune disorders, which are themselves responsible for thoracic manifestations such as common variable immunodeficiency.