Organizing Pneumonia: a rare pulmonary manifestation of ulcerative colitis

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Organizing pneumonia: a rare pulmonary manifestation of ulcerative colitis, a case report and literature review

Running head: Ulcerative colitis with organizing pneumonia

Abstract

The inflammation associated with inflammatory bowel diseases (IBD) may extend outside the bowel to many organs, including the respiratory system. These manifestations can be difficult to diagnose because of concurrent effects of drugs or infection. We report a case of organizing pneumonia in a patient with ulcerative colitis that had been under control using mesalamine. Pneumonia was initially diagnosed on the basis of fever, physical examination and chest computed tomography. After antibiotic treatment, the right lung showed partial absorption, but the disease had progressed to the left lung. Bronchoscopy revealed no abnormalities, and analysis of bronchoalveolar lavage fluid (BALF) showed elevated proportions of lymphocytes and neutrophils and no detection of bacterium. Definitive diagnosis of organizing pneumonia was made on the basis of percutaneous lung biopsy. Mesalazine therapy was stopped, and prednisolone was administered at 48 mg per day for 1 month, after which it was tapered by 4 mg per week for 3 months. Obvious pulmonary recovery was observed. Throughout the chemotherapy, the ulcerative colitis remained stable. Corticosteroid treatment based on a definitive pathological diagnosis of pulmonary involvement can improve recovery in patients with ulcerative colitis. The risk of extra-intestinal manifestations of IBD means that routine respiratory examination is recommended for IBD patients, especially those receiving sulfasalazine or masalamine, regardless of whether they show IBD symptoms or respiratory problems.

Keywords: inflammatory bowel disease, organizing pneumonia, drug-induced lung toxicity.

Introduction

Inflammatory bowel disease (IBD) is considered as a multi-organ disease with frequent extra-intestinal manifestations. Pulmonary manifestations of IBD are rare, but when they occur, they will pose a challenge to definitive diagnosis. Previous studies have documented the occurrence of airway diseases, interstitial lung disease, organizing pneumonia, pulmonary nodules, serositis and drug-induced lung disease [1-3]. However, if pulmonary involvement occurs while IBD is under control, it is far more difficult to diagnose, primarily because the clinical manifestations are complicated by the effects of the chemotherapy, concurrent infection and other factors. The failure to definitely diagnose pulmonary involvement then makes further treatment difficult, jeopardizing the patient's prognosis.

In this report, we describe the clinical, radiographic and pathologic characteristics of a rare case of pulmonary manifestation of IBD as organizing pneumonia in a patient with ulcerative colitis controlled by mesalazine therapy.

Case report

A 62-year-old male with ulcerative colitis was admitted to hospital with fever. The initial diagnosis of ulcerative colitis had been made two years earlier on the basis of bloody, purulent stool. At the time, the patient was given oral prednisolone therapy and started on low-dose mesalazine (Etiasa, 1.5 g/day; Ethypharm, France), which the patient had been taking for one year by the time of admission. Four months before admission, the bloody mucous stool had stopped. For 7 days before admission, the patient had experienced fever with a peak temperature of 39 ºC but no chills. The patient reported no prior history of pulmonary symptoms or lung disease, no occupational exposure, no history of extraintestinal manifestations of IBD, and no recent travel.

Physical examination showed the patient’s vital signs to be stable (heart rate, 85 bpm; blood pressure, 120/60 mmHg; respiration rate, 18 bpm). He had reduced breathing sounds in the right lung without wheezing or rubs.

Laboratory data included a white blood cell count of 8.1 × 109 /L (normal, 4-10 × 109 /L), comprising 57.1% neutrophils, 30.4% lymphocytes, and 0.5% eosinophils. Microcytic hypochromic anemia was present (hemoglobin, 92 g/L; mean cell volume, 67 fL; mean corpuscular hemoglobin concentration, 303 g/L), and platelet count was 339 × 109 /L. Arterial blood gas analysis showed: PaO2, 81 mmHg; PaCO2, 37 mmHg; pH, 7.45; and oxygen saturation of 96%. Erythrocyte sedimentation rate was 98 mm/h. Computed tomography (CT) showed consolidation of the right middle and lower lobes with ipsilateral pleural effusion (Fig 1, A-B). Colonoscopy showed that the ulcerative colitis was well-controlled compared to the analysis two years ago.

These analyses on admission led to a preliminary diagnosis of community-acquired pneumonia with parapneumonic pleural effusion. The patient was administered piperacillin/tazobactam (4.5 g) intravenously every 8 hours. After two days, the patient was afebrile. Antibiotic therapy lasted for 10 days. At the end of antibiotic therapy, chest CT showed partial absorption of the right lung but new involvement of the left lung, which presented as patchy, ground-glass opacity and scattered cysts (Fig 1, C-D). Bronchoscopy did not find abnormality, and analysis of bronchoscopic alveolar lavage fluid (BALF) showed 21% lymphocytes, 12% neutrophils, and 67% macrophages, without eosinophil and no detectable microorganisms. The ratio of CD4+ to CD8+ lymphocytes in BALF was 0.61. Antinuclear antibodies in serum were negative. Transbronchial lung biopsy revealed an atelectatic alveolar tissue with scattered foamy cells as well as chronic inflammatory cell infiltration and congestion. Lung function tests revealed reduced diffusion function with mildly reduced ventilation function. Percutaneous lung biopsy and corticosteroid therapy were proposed, but the patient refused further invasive examination and therapy. Therefore the patient was discharged and observed closely.

Two weeks later, the patient reported no discomfort, but the chest CT showed no obvious absorption (Fig1, E-F). Therefore the patient was hospitalized again for percutaneous lung biopsy and further therapy. The biopsy showed lymphocytic alveolitis, non-specific alveolar reaction associated with organizing pneumonia (Fig 2), which the side effect of mesalazine could not be excluded due to the rare evidence of active IBD or other extra-intestinal manifestations. Therefore mesalazine therapy was stopped and the patient was tested by negative interferon-gamma release assay (IGRA) to exclude latent tuberculosis. Subsequently the patient was given prednisolone for 1 month at a dose of 48 mg/d. Chest CT at the end of that month showed obvious absorption of the bilateral infiltration (Fig 1, G-H). Prednisolone therapy was tapered by 4 mg/week. Over the entire course of chemotherapy, the ulcerative colitis remained stable with no stool changes or other complications.

Discussion

Respiratory manifestations of ulcerative colitis are rarely seen, but they can present in diverse forms [1-4] and can appear before IBD is diagnosed or weeks or years afterwards. This makes diagnosing IBD-associated lung disease challenging. In fact, respiratory involvement of IBD can be asymptomatic and detectable only in lung function tests or high-resolution CT [6]. Evidence suggests that more than 50% of patients with IBD show impaired pulmonary function without clinical or radiographic findings [6].

In the present case, the patient did not show any respiratory symptoms on admission or afterwards, but the CT scan showed bilateral infiltration of the lungs and progression of lung involvement. Pathological examination clearly showed organizing pneumonia of the lung. Our case report, combined with previous studies, suggest that routine respiratory examinations should be carried out on IBD patients, even on those free of IBD or respiratory symptoms.

One unanswered question about our patient is whether the respiratory involvement was an extra-intestinal manifestation of ulcerative colitis or an adverse effect of mesalazine therapy. Sulfasalazine, or its metabolite mesalamine, is commonly used to treat active IBD, and some reports have suggested an association between mesalamine and pulmonary complications, in multiple patterns such as reticular or nodular changes, interstitial infiltrates, peripheral or diffuse acinar infiltrates, pleural effusions, and rarely, pure hyperinflation as seen with bronchiolitis obliterans [7,8,9]. The elevated proportions of inflammatory cells in BALF, especially lymphocytes, in our patient suggested organizing pneumonia. Till now, scattered reports involved the organizing pneumonia induced by mesalazine but none of them presented the BALF changes. Both the transbronchial lung biopsy and percutaneous lung biopsy showed lymphocytic alveolitis. In addition, a study of lung biopsies from 8 patients with ulcerative colitis reported mononuclear cell accumulation within alveolar septa and bronchioles in most cases, and interstitial thickening and fibrosis in some cases [5]. The authors of that study concluded that the interstitial pulmonary involvement may occur in ulcerative colitis even when the patient presents no respiratory symptoms [5]. This was also the case for our patient.

Previous studies suggest that the most frequent pathological findings for pulmonary changes related to ulcerative colitis are interstitial lymphocyte infiltration, alveolar fibrinous exudates, progressive fibrosis, and bronchiolitis obliterans organizing pneumonia (BOOP); BOOP may be associated with IBD progression [3,11,12]. However, these changes may also be the result of drug-induced lung toxicity, highlighting the limitations of BALF analysis and pathology for understanding the cause of pulmonary manifestations is an important question because the answer determines the most appropriate therapy. If the pulmonary complications are an extraintestinal manifestation of IBD, the dose of mesalamine or sulfasalazine may need to be increased. If, however, the pulmonary complications are due to drug-induced toxicity, then a dose increase may be unwise. Clinicians should take several factors into account when making a "best guess" about the cause of the pulmonary complications. The history, activity and clinical presentation of a patient's IBD, especially any extraintestinal manifestations, may suggest that the pulmonary complications are related to IBD. Conversely, rapid improvement of pulmonary signs and symptoms upon withdrawal of the drug suggests that the complications are drug-induced. However, discontinuing a drug may not rapidly cause radiological improvement, even if the drug is causing the pulmonary complications, and waiting to observe a clinical response may delay appropriate treatment. Thus pathological examination may be the most effective method for narrowing the differential diagnosis or providing a definitive diagnosis.

When trying to decide on the cause of pulmonary complications, differential cell counts in BALF should be interpreted with caution. Some studies suggest that neutrophils are the predominant cell type in patients with ulcerative colitis [5], whereas eosinophils are predominant in patients with drug-induced pulmonary disease[10]. On the other hand, other studies have associated mesalamine-induced lung toxicity with increases in lymphocytes and neutrophils [10].

Most cases of pulmonary involvements of IBD are treated with corticosteroids at a dose of 1 mg/kg[8,13]. While this is usually effective at promoting absorption and recovery, it can complicate definitive diagnosis of pulmonary manifestations of IBD. Conducting longer follow-up of patients (1-3 years), would help clarify whether the initial pulmonary complications were related to IBD or to drug toxicity.

This case report highlights the possibility that latent pulmonary involvement in ulcerative colitis can arise not only out of the colitis itself, but also as an adverse effect of the drugs used to treat it, usually sulfasalazine or mesalamine, which are quite difficult to differentiate. Pulmonary involvement in IBD patients who do not have active IBD or other extraintestinal manifestations may indicate drug-induced lung disease. Corticosteroid treatment based on definitive pathological diagnosis may improve recovery from pulmonary involvement of ulcerative colitis.

Figure 1

A, B: Chest computed tomography (CT) of the patient on admission which presented as consolidation of the right middle and lower lobes with isolateral pleural effusion.

C,D: Chest CT of the patient with 10-day antibiotic therapy which presented as partial absorption of the right lung but involvement of the left lung, which presented as patchy, ground-glass opacity and scattered cysts.

Figure 4

E, F: Chest CT of the patient 24 days after the admission which presented as no obvious absorption, compared with the chest CT of two weeks ago.

G, H: Chest CT of the patient after three-month prednisolone therapy: obvious absorption of the bilateral patchy, ground-glass opacities.

Figure 2

The pathological examination of the percutaneous lung biopsy based on hematoxylin and eosin-stainning(×400): cellular and lymphocytic alveolitis, non-specific alveolar reaction associated with organizing pneumonia.

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