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1 All authors: Department of Radiology, Oita Medical University, Idaigaoka 1-1, Hasama-machi, Oita 879-5593, Japan.
Received May 2, 2003;
accepted after revision September 4, 2003.
Address correspondence to F. Okada.
Abstract
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MATERIALS AND METHODS. We retrospectively reviewed CT scans of the lung in 87 patients with adult T-cell leukemia or lymphoma who had undergone chest CT between January 1996 and March 2002 at two institutions. The CT scans were interpreted by two chest radiologists working in consensus. Parenchymal abnormalities (ground-glass attenuation, consolidation, nodules, thickening of bronchovascular bundles, interlobular septal thickening, honeycombing, crazy-paving appearance, and bronchiectasis) were evaluated, as were enlarged lymph nodes, pleural effusion, and pleural thickening. In 46 patients who underwent surgical biopsy or autopsy, CT–pathologic correlation was performed with the actual specimens by a pathologist and two chest radiologists.
RESULTS. On the CT scans, abnormal findings were seen in 60 patients (69.0%). CT findings consisted of ground-glass attenuation (n = 37), centrilobular nodules (n = 25), thickening of bronchovascular bundles (n = 22), and consolidation (n = 13). These abnormalities were predominantly seen in the peripheral lung parenchyma (n = 26). Pathologically, these findings corresponded with atypical lymphocyte infiltration along the interstitium and the alveolar spaces. Pleural effusion and enlarged lymph nodes were found in 22 and 27 patients, respectively.
CONCLUSION. CT findings in patients with adult T-cell leukemia or lymphoma consisted mainly of ground-glass attenuation, centrilobular nodules, and thickening of the bronchovascular bundles in the peripheral lung. These findings, although nonspecific, are considered suggestive of thoracic involvement in patients with adult T-cell leukemia or lymphoma.
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Common clinical manifestations of adult T-cell leukemia or lymphoma include lymphadenopathy characterized by sparing of the neck and mediastinum, skin infiltration, hepatosplenomegaly, bone infiltration, general malaise, and gastrointestinal symptoms. It has been reported that infiltration of leukemia cells into the lung is present in 54% of adult T-cell leukemia or lymphoma patients [6]. On chest radiographs, infiltration of the lungs by leukemia cells is characterized by diffuse infiltrate causing opacities in both lungs [7].
To our knowledge, no radiologic studies of pulmonary CT findings in patients with adult T-cell leukemia or lymphoma have been performed. Adult T-cell leukemia or lymphoma patients have a high frequency of respiratory complications related to infiltration of the lungs by leukemia cells, and these complications are often life-threatening. The purpose of this study was to assess pulmonary CT findings in patients with adult T-cell leukemia or lymphoma that may be of clinical significance.
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Adult T-cell leukemia or lymphoma was diagnosed by positive human T-lymphotrophic virus type I antibody and the presence of abnormal lymphocytes with convoluted nuclei (adult T-cell leukemia or lymphoma cells) in the peripheral blood or histologic findings compatible with a diagnosis of adult T-cell leukemia or lymphoma in biopsied tissue. In 71 of 87 patients, a diagnosis of adult T-cell leukemia or lymphoma was made before performing the CT examinations. Sixteen patients underwent CT before the diagnosis was evident. A total of 211 CT scans were obtained for these patients, and IV contrast medium was used in 72 of the procedures. Patients diagnosed with concurrent infectious disease by serologic tests and by clinical and pathologic findings were excluded from this study because these diseases can manifest CT findings such as ground-glass attenuation or consolidation.
CT examinations were performed with a HiSpeed Advantage scanner (General Electric Medical Systems, Milwaukee, WI), a HiSpeed LX/i Advantage (General Electric Medical Systems), or an X-press unit (Toshiba, Tokyo, Japan). Sixty-five patients underwent high-resolution CT with 1-mm collimation, and 22 patients underwent CT with 5- to 7-mm collimation. In 54 patients, follow-up CT scans were obtained 8 days–32 months after the initial scan. These CT scans extended from the lung apices to the costophrenic angle. With the HiSpeed Advantage unit, the scanning time of each section was 2.0 sec at 120 kVp and 150 mA; with the HiSpeed LX/i Advantage, the scanning time of each section was 2.0 sec at 140 kVp and 160 mA; and with the X-press unit, the scanning time was 2.0 sec at 140 kVp and 150 mA. All CT scans were obtained during suspended end inspiration with the patient in the supine position.
Two chest radiologists, who were aware of the underlying diagnoses, retrospectively interpreted the chest CT scans and reached their conclusion by consensus. All initial scans were evaluated. Followup CT was periodically performed on patients who underwent chemotherapy. However, the interval period for follow-up treatment was determined by the chemotherapeutic effect. An average of two sessions per week were reserved for reviewing CT scans, totaling approximately 50 sessions. The CT images were assessed with regard to each of the following radiologic patterns: ground-glass attenuation, consolidation, nodules, thickening of bronchovascular bundles, interlobular septal thickening, honeycombing, crazy-paving appearance, bronchiectasis, enlarged hilar or mediastinal lymph node or nodes (> 1 cm in diameter of the short axis), pleural effusion (unilateral or bilateral), pleural thickening, and pericardial effusion. Areas of ground-glass attenuation were defined as hazy increases in attenuation without obscuration of vascular markings. Areas of consolidation were defined as areas of increased attenuation that caused obscuration of the normal lung markings with or without air bronchograms. Parenchymal nodules were categorized according to the diameter of the short axis as follows: smaller than 3 mm, between 3 and 10 mm, or larger than 10 mm. If the nodule was identified around peripheral pulmonary arterial branches or 3–5 mm away from the pleura, interlobular septa, or pulmonary veins, it was defined as a centrilobular nodule.
The distribution of parenchymal disease was also noted. If the main lesion was located predominantly in the inner third of the lung, the disease was classified as having a central distribution. On the other hand, if the lesion was predominantly in the outer third of the lung, the disease was classified as having peripheral distribution. If the lesions showed no predominant distribution, the disease was classified as having random distribution. In addition, specific zonal predominance was classified into one of three zones; upper, lower, or random. Upper lung zone predominance was considered to be present when most abnormalities were seen at the upper level to the tracheal carina and, likewise, lower zone predominance was considered to be present when most abnormalities were seen below the upper zone.
CT–pathologic correlation was performed with the actual specimens by a pathologist and two chest radiologists in 46 patients, with autopsy specimens in six, or surgical biopsy in 45, and with both autopsy and surgical specimens in five. Autopsy and surgical lung biopsies corresponding to abnormal regions observed on the chest CT scans were performed within 14 and 10 days after the CT scans, respectively. Nine autopsies performed more than 14 days after the CT scans were excluded from this study.
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In the 45 patients with parenchymal disease, abnormal findings were seen predominantly in the peripheral lung (26/45, 57.8%). On the other hand, there were no patients with disease showing a predominantly central distribution. The predominant zonal distribution was in the lower zone in 12 patients (26.7%) and in the middle zone in four (8.9%); random distribution was observed in 28 (62.2%).
On follow-up CT (n = 54), ground-glass attenuation (n = 35) had disappeared in 14 patients, improved in 18, remained unchanged in two, and worsened in one after treatment. Thickening of bronchovascular bundles (n = 20) disappeared in seven patients, improved in 10, and remained unchanged in three. Interlobular septal thickening (n = 16) disappeared in 13 patients and improved in three. The areas of consolidation (n = 12) disappeared in five patients (Fig. 6A, 6B, 6C, 6D), improved in six, and worsened in one. Nodules (n = 13) disappeared in all patients.
There were small effusions in eight patients, moderately sized effusions in 11, and large effusions in three. Bilateral effusion was observed in 13 patients and unilateral effusion, in nine (Figs. 2, 3A, 3B, and 8A, 8B). No parenchymal abnormalities were observed in patients with pleural effusion (bilateral in five, unilateral in four). Pleural effusion disappeared in 18 patients and improved in four after chemotherapy. Mediastinal and hilar lymph node enlargement (11–82 mm) was found in 27 patients (45%) (Fig. 8A, 8B). Enlarged lymph nodes were generally found at the pretracheal, paratracheal, tracheobronchial, or subcarinal regions. No parenchymal abnormalities were observed in eight patients with lymph node enlargement. After treatment, lymph node enlargement improved in 23 patients and remained unchanged in three on follow-up CT scans. Enlarged lymph nodes were also found in both axillary regions in six patients.
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Less common CT findings included pulmonary fibrosis such as honeycombing (n = 1) and pericardial effusion (n = 4).
CT–Pathologic Correlation
In 46 patients who underwent surgical biopsy or autopsy, CT findings were
correlated with pathologic findings. The extent of centrilobular nodules
corresponded pathologically with that of atypical lymphocytic infiltration
along the respiratory bronchioles. In addition, thickening of the
bronchovascular bundles corresponded with infiltration of atypical lymphocytes
along the bronchovascular bundles (Fig.
3B).
The extent of ground-glass attenuation also corresponded with that of atypical lymphocytic infiltration into the interstitium, together with small nodular formations (Fig. 1B). The consolidation corresponded to the atypical lymphocytic infiltration in the interstitium and the alveolar spaces, as well as with mild congestive change (Fig. 6B). Furthermore, interlobular septal thickening and pleural thickening corresponded with the infiltration of numerous atypical lymphocytes into both the pleura and the interlobular septa (Fig. 8B).
In five patients, both surgical biopsy and autopsy were performed, and the histologic findings of the surgical biopsies were almost identical to those of the autopsy specimens.
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Adult T-cell leukemia or lymphoma is classified into four clinical subtypes. The first is the smoldering type, in which more than 5% of T lymphocytes are abnormal, the peripheral blood contains less than 4,000/µL of lymphocytes, and few abnormal blood chemistry profiles and adult T-cell leukemia or lymphoma infiltration are present. The second is the chronic type, in which lymphocytosis occurs (defined as T lymphocytosis > 4,000/µL), lactate dehydrogenase is less than twice the normal upper limit, and no hypercalcemia is present, with possible lymph node, liver, spleen, skin, and lung involvement. The third is the lymphoma type, in which histologically proven lymph node enlargement is present but no lymphocytosis is present (defined as < 1% abnormal T lymphocytes). The fourth is the acute type, for patients not classified into any of the above three types [10]. The relative percentage of adult T-cell leukemia or lymphoma cases for each lymphoma type is 55% for the acute type, 20% for the lymphoma type, 20% for the chronic type, and 5% for the smoldering type. The median survival time is 6.2 months for the acute type, 10.2 months for the lymphoma type, and 24.3 months for the chronic type; 62.8% of patients with the smoldering type were still alive after 4 years [10].
Adult T-cell leukemia or lymphoma has a poor prognosis due to life-threatening complications, including infections and hypercalcemia [11]. Among the infectious complications, cytomegalovirus is most frequently encountered in patients at autopsy. Pneumocystis carinii and Aspergillus and Candida organisms are also encountered as opportunistic infections [6, 8].
Patients with adult T-cell leukemia or lymphoma have a high frequency of respiratory complications, consisting of the infiltration of leukemia cells and pulmonary hemorrhage. It has been reported that 93.1% of adult T-cell leukemia or lymphoma patients (n = 29) presented with respiratory complications, such as tumor infiltration and infection, during the clinical course of the disease [8]. Sato et al. [6] reported that infiltration of the lung by leukemia cells was present in 54% of adult T-cell leukemia or lymphoma patients in an autopsy study. The infiltration of the lung by leukemia cells is characterized by diffuse infiltrate in shadows of both lungs observed on chest radiographs [7]. It was previously reported that 12 (34%) of 35 patients with adult T-cell leukemia or lymphoma had significant findings on chest radiographs; a reticulonodular pattern of disease, seen in 10 patients, was the most common finding [12].
To our knowledge, there have been no radiologic studies of pulmonary CT findings in patients with adult T-cell leukemia or lymphoma. We retrospectively reviewed pulmonary CT findings in 87 patients with adult T-cell leukemia or lymphoma. Of those patients, 60 (69.0%) showed abnormalities; the most common CT findings were ground-glass attenuation, followed by centrilobular nodules and thickening of bronchovascular bundles. The extent of ground-glass attenuation corresponded to that of atypical lymphocytic infiltration into the interstitium, with the formation of small nodules. In addition, centrilobular nodules and thickening of bronchovascular bundles corresponded to the presence of atypical lymphocytes along the bronchovascular bundles and mild fibrosis. Okura et al. [13] reported the first case of a nodular pattern of disease observed in the right mid lung on a chest radiograph, in which only a large nodular accumulation of adult T-cell leukemia or lymphoma cells was observed, without diffuse infiltration of the cells into the lung. In our study, 22% of patients had pulmonary nodules with or without air bronchograms.
Maruyama et al. [14] reported a crazy-paving appearance on high-resolution CT in various diseases such as alveolar proteinosis, P. carinii pneumonia, pulmonary hemorrhage, and drug-induced pneumonia. The crazy-pavign appearance, representing thickened interlobular septa between secondary lobules, has not been previously reported in a patient with adult T-cell leukemia or lymphoma. Here, we identified this CT finding in four patients (7%) with adult T-cell leukemia or lymphoma.
Human T-lymphotrophic virus type I–associated bronchopulmonary disorder can be staged in a variety of ways. Kimura [15] described a close relationship between diffuse panbronchiolitis, or idiopathic interstitial pneumonia, and human T-lymphotrophic virus type I. In that article, it was speculated that the accumulation of precancerous lymphoid cells in the bronchoalveolar areas would lead to diffuse panbronchiolitis or idiopathic interstitial pneumonia due to the host's response; a significant number of patients would eventually enter a stage of overt adult T-cell leukemia or lymphoma.
In our study, centrilobular nodules and mild thickening of the bronchial wall were seen in 25 and 22 patients, respectively. These CT findings were confirmed to be due to atypical and mildly atypical lymphocytic infiltration, respectively, of the respiratory bronchioles wall, as determined at surgical biopsy. However, the possibility that these CT findings were related to chronic infection or human T-lymphotrophic virus type I–associated bronchopulmonary disorder could not be completely ruled out because mildly atypical lymphocytes were present. On the other hand, CT findings of pulmonary fibrosis (i.e., honeycombing) were found in only one patient (2%). This result is probably due to the fact that patients with collagen disease or collagen-related disease were excluded from this study. Furthermore, none of the patients had significant fibrotic disease in the upper lobe, which is frequently seen in patients with chronic hypersensitivity pneumonitis, sarcoidosis, or pneumoconiosis.
Pleural effusion and thickening are commonly observed in patients with leukemia. These signs appear mainly in cases of acute lymphoblastic leukemia and have been recognized in 27% of leukemia patients at autopsy [16]. However, the CT manifestations of pleural disease caused by adult T-cell leukemia or lymphoma have not been previously described. A plaquelike pleural thickening on CT scans was seen in six patients (10%) with adult T-cell leukemia or lymphoma in our study. The biopsy specimens obtained from the lung showed numerous atypical lymphocytes infiltrating the pleura, and foamy cells were present in some of the alveoli. Pleural involvement with adult T-cell leukemia or lymphoma has a nonspecific appearance; therefore, radiologists should be aware that pleural thickening can be caused not only by infection or pulmonary congestion but also by adult T-cell leukemia or lymphoma infiltration in patients with the diagnosis of adult T-cell leukemia or lymphoma.
Generalized lymphadenopathy is a common manifestation of adult T-cell leukemia or lymphoma. Peripheral lymphadenopathy is reported in 59–100% of adult T-cell leukemia or lymphoma patients [9]; hilar, intraabdominal, paraaortic, and paracaval lymphadenopathies are seen in up to 50% of these patients. The results of the present study regarding lymphadenopathy (45%) were similar to those of previous reports.
It should be noted that there were several limitations of the present study. First, this was a retrospective study, and the CT findings were not sufficiently correlated with the pathologic findings because some patients were in poor general health. In addition, the CT scans and histologic specimens were not obtained on the same day, although the surgical biopsies were performed within 10 days after the CT scans. Second, with regard to the CT findings, the relationship between adult T-cell leukemia or lymphoma and human T-lymphotrophic virus type I–associated bronchopulmonary disorder remains unclear. Third, it is difficult to distinguish these CT findings from those associated with cytomegalovirus infection or hemorrhage in patients with adult T-cell leukemia or lymphoma who did not have the pathologic evidence required for diagnosis. Cytomegalovirus infection, which is the most common opportunistic infection in the lungs, can cause some of the common high-resolution CT patterns (i.e., ground-glass attenuation, interstitial thickening, and nodules) described in our earlier article [17]. Similarly, hemorrhage can cause nonspecific areas of ground-glass attenuation or consolidation [14, 18]. Finally, some of the CT examinations were performed several years ago, and, more important, not all the CT studies included 1-mm high-resolution images. If all patients had undergone high-resolution CT, the abnormal CT findings may have had a different frequency than that observed in our study.
In summary, the pulmonary CT findings in patients with adult T-cell leukemia or lymphoma consisted mainly of ground-glass attenuation, centrilobular nodules, thickening of bronchovascular bundles, and interlobular septal thickening in the peripheral lung. These findings corresponded pathologically with atypical lymphocytic infiltration along the interstitium and the alveolar spaces. Moreover, pleural effusion and lymph node enlargement were commonly observed among the patients. These CT findings are considered suggestive of adult T-cell leukemia or lymphoma pulmonary infiltration in patients with the diagnosis of adult T-cell leukemia or lymphoma.
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