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Thrombotic Microangiopathy of Pulmonary Tumors: A Vascular Cause of Tree-In-Bud Pattern on CT

¹ Department of Radiology, Hospital de Sant Pau, Universidad Autónoma de Barcelona, Avda Sant Antoni M^a Claret 167, 08025 Barcelona, Spain.
² Department of Respiratory Medicine, Hospital de Sant Pau, Universidad Autónoma de Barcelona, 08025 Barcelona, Spain.
³ Department of Pathology, Hospital de Sant Pau, Universidad Autónoma de Barcelona, 08025 Barcelona, Spain.

Received December 21, 2001; accepted after revision March 11, 2002.

 
Address correspondence to T. Franquet.

Introduction

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Pulmonary tumor embolism is commonly found at autopsy but is rarely diagnosed before death [1]. Antemortem diagnosis requires a high index of clinical suspicion and knowledge of typical radiologic findings, including peripheral wedgeshaped opacities, multifocal dilatation or beading of vessels, and enlarged central arteries on CT [2, 3]. Thrombotic microangiopathy of pulmonary tumors is a rare and distinct form of tumor embolism. This entity is characterized histopathologically by widespread fibrocellular intimal hyperplasia of small pulmonary arteries and arterioles that is induced by tumor microemboli [4]. To our knowledge, the CT findings associated with thrombotic microangiopathy of pulmonary tumors have not been previously described. We recently observed a case of pulmonary tumor thrombotic microangiopathy that manifested on thin-section CT as diffuse tree-in-bud opacities—CT findings more typically seen in cases of infectious bronchiolitis. We report our case to familiarize radiologists with this important entity and this unusual cause of the tree-in-bud pattern on thin-section CT.

Case Report

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A previously healthy 48-year-old man presented with a 5-month history of progressive dyspnea, fatigue, and dry cough. At physical examination the patient was dyspneic and hypoxemic. The lungs were clear except for a few inspiratory crackles at the left base. Hematocrit was 30.2%, and WBC was 13,500/µL with 88% neutrophils. A specimen of arterial blood showed that the partial pressure of oxygen was 52 mm Hg; the partial pressure of carbon dioxide, 30 mm Hg; and the pH, 7.51. Chest radiography showed nonspecific bilateral pulmonary opacities at the lung bases. Thin-section CT of the chest revealed bilateral and diffuse well-defined opacities that appeared as longitudinal branching structures—that is, the tree-in-bud appearance (Fig. 1A,1B,1C,1D).

View larger version (140K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —48-year-old man with thrombotic microangiopathy of pulmonary tumor induced by gastric adenocarcinoma. Magnified high-resolution CT images of both lower lobes obtained using 1-mm collimation and lung window settings show multiple centrilobular nodules and branching lines with tree-in-bud appearance (arrows).

View larger version (118K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —48-year-old man with thrombotic microangiopathy of pulmonary tumor induced by gastric adenocarcinoma. Magnified high-resolution CT images of both lower lobes obtained using 1-mm collimation and lung window settings show multiple centrilobular nodules and branching lines with tree-in-bud appearance (arrows).

View larger version (153K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —48-year-old man with thrombotic microangiopathy of pulmonary tumor induced by gastric adenocarcinoma. Photograph of cut section of lung from autopsy specimen shows normal interlobular septa (arrowheads) and pulmonary veins (PV) in periphery of secondary pulmonary lobule. Multiple branching opacities can be seen in central portion of lobule.

View larger version (164K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D. —48-year-old man with thrombotic microangiopathy of pulmonary tumor induced by gastric adenocarcinoma. Photomicrograph of histopathologic specimen shows complete arteriolar occlusion by fibrocellular intimal proliferation. Clumps of tumor cells are visible in recanalized organized lesion. (H and E, x40)

The patient was initially treated with corticosteroids and IV antibiotics for presumed infectious bronchiolitis. Despite this treatment, the patient's condition worsened dramatically over the next several days. At that time, catheterization of the pulmonary artery revealed severe pulmonary artery hypertension. The patient was scheduled for open lung biopsy on the 12th hospital day, but his clinical situation worsened dramatically and he died.

At postmortem examination, the pleural surfaces of the lungs showed grayish dilatation of the lymphatics. Microscopically, most of the arterioles were occluded by cellular intimal proliferation characterized by concentric layering of spindle-shaped cells lying in a myxoid stroma. In some arterioles, recanalization of organized thrombus containing small clumps of tumor cells was identified. Changes associated with grade III hypertensive arteriopathy (intimal fibrosis and medial hypertrophy) were occasionally noted in muscular and smaller arteries. A signet-ring cell gastric adenocarcinoma was histologically proven.

Discussion

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The lung is a frequent site of tumor embolism. In a large autopsy series of patients who had extrathoracic malignancies, intravascular tumor emboli were found in up to 26% of the cadavers [1]. Primary malignancies frequently associated with pulmonary tumor emboli are hepatoma, breast and renal carcinoma, gastric and prostate cancer, and choriocarcinoma [1]. The radiologic diagnosis of pulmonary tumor embolism is difficult because the findings are often minimal or nonspecific. These findings include peripheral wedge-shaped opacities, multifocal dilatation or beading of vessels, diffuse thickening of the interlobular septa (lymphangitic carcinomatosis), and enlarged central arteries [2, 3]. Unfortunately, the diagnosis of tumor emboli in patients with extrathoracic malignancies is not often clinically or radiologically established before death.

Although pulmonary tumor embolism is common, thrombotic microangiopathy of pulmonary tumors, a distinct form of tumor embolism, is rare. Histopathologically, pulmonary tumor thrombotic microangiopathy is characterized by widespread fibrocellular intimal hyperplasia of small pulmonary arteries (so-called carcinomatous endarteritis) induced by tumor microemboli [4]. This pattern has been observed at autopsy in only 0.9-3.3% of the cadavers who had extrathoracic malignancies [4, 5]. Diffuse vascular occlusion in patients with pulmonary tumor thrombotic microangiopathy results in increased pulmonary vascular resistance. Clinically, pulmonary tumor thrombotic microangiopathy manifests with signs and symptoms that include progressive dyspnea, cough, hypoxia, and pulmonary hypertension [5].

The tree-in-bud pattern on thin-section CT, which is characterized by small centrilobular nodules and branching linear opacities, is most often seen in patients with infectious bronchiolitis [6]. In such cases, this pattern is caused by dilatation and plugging of small airways by mucus and inflammatory material. This pattern has been previously described in only a single case of pulmonary tumor embolism [7]. In that patient, the tree-in-bud pattern was caused by filling of centrilobular arteries with tumor cells [7]. We report a second case of pulmonary tumor embolism that also caused the tree-in-bud pattern on thin-section CT. However, in our patient, the tree-in-bud pattern largely resulted from fibrocellular intimal hyperplasia in small arteries and arterioles rather than from the tumor emboli themselves.

Recently, another vascular cause of the tree-in-bud pattern on thin-section CT was described in a patient with cellulose granulomatosis [8]. In this disorder, granulomatosis results from the IV injection of cellulose or other filler material that is found in medications intended for oral use only. In that patient, the intravascular foreign material and the associated granulomatous reaction in vascular walls produced the tree-in-bud pattern. Thus, the tree-in-bud pattern on thin-section CT, although usually caused by diseases of the small airways, may also be caused by a variety of vascular abnormalities including pulmonary tumor embolism and pulmonary tumor thrombotic microangiopathy.

References

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1. Schriner RW, Ryu JH, Edwards WD. Microscopic pulmonary tumor embolism causing subacute cor pulmonale: a difficult antemortem diagnosis. Mayo Clin Proc 1991;66:143 -148[Medline]
2. Shepard JA, Moore EH, Templeton PA, McLoud TC. Pulmonary intravascular tumor emboli: dilated and beaded peripheral pulmonary arteries at CT. Radiology 1993;187:797 -801[Abstract/Free Full Text]
3. Chan CK, Hutcheon MA, Hyland RH, Smith GJ, Patterson BJ, Matthay RA. Pulmonary tumor embolism: a critical review of clinical, imaging, and hemodynamic features. J Thorac Imaging 1987;2:4 -14[Medline]
4. von Herbay A, Illes A, Waldherr R, Otto HF. Pulmonary tumor thrombotic microangiopathy with pulmonary hypertension. Cancer 1990;66:587 -592[Medline]
5. Pinckard JK, Wick MR. Tumor-related thrombotic pulmonary microangiopathy: review of pathologic findings and pathophysiologic mechanisms. Ann Diagn Pathol 2000;4:154 -157[Medline]
6. Collins J, Blankenbaker D, Stern EJ. CT patterns of bronchiolar disease: what is "tree-in-bud"? AJR 1998;171:365 -370[Free Full Text]
7. Tack D, Nollevaux M-C, Gevenois PA. Tree-in-bud pattern in neoplastic pulmonary emboli. AJR 2001;176:1421 -1422[Free Full Text]
8. Bendeck SE, Leung AN, Berry GJ, Daniel D, Ruoss SJ. Cellulose granulomatosis presenting as centrilobular nodules: CT and histologic findings. AJR 2001;177:1151 -1153[Free Full Text]

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