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Cystic Fibrosis: Usefulness of Thoracic CT in the Examination of Patients before Lung Transplantation¹

¹ From the Departments of Radiology (E.M.M., H.P.M., J.J.E, P.C.G.), Medicine (S.M.P., V.F.T.), Pathology (T.A.S.), and Surgery (R.D.D.), Duke University Medical Center, Box 3808, Erwin Rd, Durham, NC 27710. From the 1998 RSNA scientific assembly. Received July 14, 1998; revision requested September 10; final revision received December 9; accepted March 29, 1999. Address reprint requests to H.P.M. (e-mail: mcada003@mc.duke.edu).

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To evaluate the usefulness of thoracic computed tomography (CT) in the pre–lung transplantation examination of patients with cystic fibrosis (CF).

MATERIALS AND METHODS: Fifty-six patients (age range, 12–42 years) with CF were evaluated for possible lung transplantation from 1991 to 1997. Twenty-six of these patients underwent bilateral lung transplantation, 19 were awaiting transplantation at the time of the study, seven died before transplantation, and four were excluded for psychosocial concerns. Preoperative chest radiographic and CT findings were reviewed and correlated with clinical, operative, and pathology records.

RESULTS: In seven patients, discrete, 1–2-cm pulmonary nodules were detected at CT. Five of these patients underwent transplantation; the nodules were found to be mucous impactions. No malignancy was found in any of the patients who underwent transplantation. Pretransplantation sputum cultures grew Aspergillus fumigatus in seven patients, none of whom had radiologic findings suggestive of Aspergillus infection. Radiographic or CT findings were suggestive of mycetoma in five cases, but no such tumors were found at transplantation. The accuracies of chest radiography and CT for the detection of pleural disease in 48 hemithoraces were 81% (n = 39) and 69% (n = 33), respectively. The radiologic findings of pleural thickening did not influence the surgical approach in any patient.

CONCLUSION: Thoracic CT has little utility in the routine pre–lung transplantation examination of patients with CF.

Index terms: Computed tomography (CT), utilization, 60.12111, 60.12118 • Fibrosis, cystic, 60.252 • Pleura, diseases, 66.252

	Introduction

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In the past decade, lung transplantation has emerged as a feasible therapy for patients with end-stage lung disease (1,2). Single lung transplantation is most frequently performed for nonsuppurative lung diseases such as emphysema, pulmonary hypertension, and interstitial fibrosis. Bilateral sequential lung transplantation is most commonly performed for suppurative lung diseases such as cystic fibrosis (CF) and bronchiectasis (3). CF is now the third most common indication for lung transplantation after emphysema and idiopathic pulmonary fibrosis (4).

In most transplantation centers, thoracic computed tomography (CT) is an integral part of the preoperative examination of patients who are being considered for lung transplantation (5). The primary role of CT in this setting is for the detection of previously unsuspected lung malignancies (6). CT is also useful in patients who are being considered for single-lung transplantation, because findings such as asymmetric pleural or parenchymal disease can affect decisions regarding which lung to transplant (6).

CT is commonly recommended and performed as part of the pre–lung transplantation examination of patients with CF (3,5,7). However, the value of pretransplantation CT in patients with CF is unclear. Because these patients are young, they are unlikely to have unsuspected lung malignancy. Furthermore, because patients with CF have chronic bilateral pulmonary infection, single lung transplantation is not feasible, and these patients are always treated with bilateral sequential lung transplantation. Thus, determining which lung or pleural space is more severely affected is not as important as it is in patients who are being considered for single-lung transplantation. Nevertheless, CT is commonly recommended and performed as part of the pre–lung transplantation examination of patients with CF (3,5,7). We performed a retrospective review of findings in all patients with CF who were referred to our center for possible lung transplantation to determine whether CT altered the clinical or surgical treatment of these patients.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Sixty-one patients with CF who were referred to our institution during a 6-year period (September 1991 to December 1997) for possible lung transplantation were included. All patients underwent chest radiography, chest CT, and quantitative perfusion scintigraphy as part of their standard pre–lung transplantation examination (Table 1). Five patients underwent chest CT at an outside institution; because these studies were unavailable at the time of our review, these patients were excluded from the study. The remaining 56 patients (30 male, 26 female; mean age, 26 years; age range, 12–42 years) formed our study group.

The severity of bronchiectasis was graded as mild if the luminal diameter was slightly greater than the diameter of the adjacent blood vessel, moderate if the luminal diameter was two to three times the vessel diameter, and severe if the luminal diameter was more than three times the vessel diameter (7). The CT findings were recorded as diagnostic of mycetoma when a gravity-dependent mass was seen within a cavity. The findings were recorded as suspicious for mycetoma when a crescent of air around a non–gravity-dependant mass was seen or when linear opacities were seen crisscrossing a cavity, bulla, or cyst. Mediastinal lymphadenopathy was recorded when one or more lymph nodes with a short-axis dimension of greater than 1.0 cm was seen.

Multiple chest radiographs were obtained in all patients. For our evaluation, we chose to review the radiograph obtained closest to the time of CT (range, 0–91 days; mean, 10 days; median, 2 days). These radiographs were randomized and jointly reviewed by the same radiologists who reviewed the CT studies, and the findings were recorded by consensus. The readers were blinded to patient names, CT and perfusion scintigraphic results, decisions regarding transplantation, surgical results, and histopathologic findings. There was a 2–3-week interval between the review of chest radiographs and the review of CT scans obtained in the same patient. Chest radiographs were evaluated by using the same criteria used to evaluate the CT studies.

After the reviews of the chest radiographs and CT scans were complete, the patients' medical records were searched for perioperative complications, pre- and postoperative sputum or bronchoalveolar lavage culture results, and operative and histopathologic findings. The surgical notes were reviewed specifically for comments regarding intraoperative blood loss (ie, expected, greater than expected, or less than expected) and the presence or absence of pleural adhesions. All explanted lung specimens were evaluated grossly and microscopically at the time of transplantation for evidence of acute infection, bronchiectasis, mycetoma, or malignancy. Deflated lung specimens were palpated for nodules, which, if found, were sectioned and examined microscopically. An experienced pulmonary pathologist (T.A.S.) reviewed all of the available pathologic material at the time of our study. The Fisher exact test for group comparisons was performed by using SAS V6.12 software (Statistical Analysis Software Institute, Cary, NC).

	RESULTS

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Clinical Course
Twenty-six of the 56 patients included in the study underwent lung transplantation, 19 were awaiting transplantation at the time this article was written, seven died before transplantation, and four were excluded from being considered for transplantation because of substance abuse or depression. No patient was excluded on the basis of radiologic findings. All 26 patients who underwent transplantation underwent bilateral sequential lung transplantation. The mean time between pretransplantation evaluation and surgery was 12.9 months. At histopathologic examination, all of the explanted lungs showed typical findings of end-stage CF, including severe bronchiectasis, mucous plugging, extensive suppuration, and fibrosis.

Radiographic and CT Findings
Pleural disease.—Of the 26 patients who underwent lung transplantation, two underwent pleurodesis for recurrent pneumothorax after their pretransplantation radiologic examination but before transplantation. Therefore, correlation of the radiographic, CT, and operative findings of pleural thickening was performed in 48 hemithoraces of the remaining 24 patients. Pleural thickening was seen on the chest radiographs in 17 (35%) of the 48 hemithoraces and on the chest CT scans in nine (19%). Compared with the operative reports, the chest radiographic findings correctly predicted the presence or absence of pleural disease in 39 (81%) of the 48 hemithoraces, and the CT findings correctly predicted the presence or absence of pleural disease in 33 (69%). The sensitivity and specificity for the detection of pleural disease with CT were 38% and 100%, respectively, compared with 67% and 96%, respectively, with chest radiography (Table 2). This difference was not statistically significant according to the results of the Fisher exact test.

Parenchymal and airway disease.—Pulmonary consolidation was seen on the chest radiographs obtained in 11 (20%) of 56 patients and on the chest CT scans obtained in 24 (43%) of them (Fig 1). At CT, the consolidation involved the right lung in 12 patients, the left lung in four patients, and both lungs in eight patients. None of these patients had symptoms of acute infection at the time of the examination. The sputum samples obtained in all 56 patients were positive for either Pseudomonas or Burkholderiella species.

View larger version (117K): [in this window] [in a new window]   Figure 1a. Atypical mycobacterial infection in a 22-year-old woman with cystic fibrosis. (a) Axial chest CT scan (10-mm collimation, lung window settings) shows severe bilateral bronchiectasis (arrowheads) and consolidation in the left upper lobe. (b) Axial chest CT scan (10-mm collimation, mediastinal window settings) shows multiple enlarged lymph nodes (arrows) in the prevascular space on the left side. This patient had no clinical symptoms of acute pneumonia at the time of the CT examination. At transplantation 13 months later, infection due to Mycobacterium avium-intracellulare complex was found in the left upper lobe and mediastinal lymph nodes.

View larger version (91K): [in this window] [in a new window]   Figure 1b. Atypical mycobacterial infection in a 22-year-old woman with cystic fibrosis. (a) Axial chest CT scan (10-mm collimation, lung window settings) shows severe bilateral bronchiectasis (arrowheads) and consolidation in the left upper lobe. (b) Axial chest CT scan (10-mm collimation, mediastinal window settings) shows multiple enlarged lymph nodes (arrows) in the prevascular space on the left side. This patient had no clinical symptoms of acute pneumonia at the time of the CT examination. At transplantation 13 months later, infection due to Mycobacterium avium-intracellulare complex was found in the left upper lobe and mediastinal lymph nodes.

Chest radiographs showed symmetric bronchiectasis that was graded as severe in 36 (64%), moderate in 16 (29%), and mild in four (7%) of 56 patients. CT scans showed symmetric bronchiectasis that was graded as severe in 39 (70%), moderate in 16 (29%), and mild in one (2%) of 56 patients. All of the patients who underwent transplantation had either moderate or severe symmetric bronchiectasis at chest radiography and CT.

Mycetomas.—No diagnostic findings of mycetoma were seen on any of the CT scans or chest radiographs. However, findings that were suspicious for mycetoma were seen at chest radiography in two (4%) of 56 patients and at CT in three (5%) additional patients (Fig 2). None of these five patients' sputum cultures were positive for Aspergillus infection, and at transplantation, no mycetomas were found. Seven (12%) of 56 patients, none of whom had radiologic findings that were suggestive of mycetoma, had preoperative sputum samples that were positive for Aspergillus infection.

View larger version (84K): [in this window] [in a new window]   Figure 2. Possible mycetomas in a 23-year-old man with CF. Axial chest CT scan (10-mm collimation, lung window settings) shows severe bilateral bronchiectasis. There are crescentic areas of hypoattenuation with intracavitary masses (arrowheads) in the left upper lobe; these findings raise the possibility of mycetomas. At transplantation 18 months later, no mycetoma was found. All sputum cultures for Aspergillus species were negative.

Adenopathy.—The chest radiographic findings in eight (14%), and the chest CT findings in 37 (66%) of 56 patients suggested mediastinal lymphadenopathy (Fig 1). Mediastinal lymph node sampling was performed in all 26 patients who underwent transplantation. In most cases, the histologic examination demonstrated reactive hyperplasia; necrotizing granulomatous inflammation was found in one case. The sputum culture of the necrotizing granulomatous inflammation grew M avium-intracellulare complex. The follow-up chest radiographs obtained in all patients with enlarged lymph nodes at CT showed no evidence of progressive enlargement for at least 1 year.

Additional CT findings.—Chest CT demonstrated the following additional findings in the 56 patients: prior cholecystectomy in six, renal calculi in five, fatty replacement of the pancreas in four, splenomegaly in three, cholelithiasis in two, and a nodular liver in two patients, and a fatty liver and pericardial effusion in one patient each. None of the three patients with hepatic abnormalities at CT had clinical evidence of cirrhosis; the results of preoperative liver biopsy in one of them showed hepatic steatosis only. Neither of the patients with CT evidence of gallstones underwent preoperative cholecystectomy.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Possible reasons for performing routine pre–lung transplantation CT in patients with CF include to detect asymmetric pleural or parenchymal disease that might affect decisions regarding which lung should be explanted first for transplantation or the selection of donor lungs; to detect lung nodules or adenopathy that is suggestive of malignancy; and to detect findings that are suggestive of infection (eg, aspergillosis).

The decision regarding which lung to explant first during bilateral sequential lung transplantation has not been rigorously evaluated. The procedure usually is begun on the right side because this allows easy access for cannulation of the right atrium if cardiopulmonary bypass is required (9,10). After the first native lung is removed, the patient must rely on the second native lung for oxygenation until transplantation of the first lung is complete. If the remaining native lung fails, cardiopulmonary bypass will be required to complete the operation. In general, most transplantation surgeons prefer to avoid cardiopulmonary bypass in this setting because it prolongs the operative time and increases the risk of bleeding complications and mortality (4,9,11). These concerns are especially important in patients with CF because they usually have substantial pleural or mediastinal adhesions and enlarged bronchial collateral vessels.

Theoretically, in patients with asymmetric lung destruction, the most damaged lung should be removed first to minimize hemodynamic instability and the need for cardiopulmonary bypass. Given the small number of patients with asymmetric disease who underwent transplantation in our series, we cannot confirm this hypothesis. We can conclude, however, that CT is not necessary for this determination, because we found no substantial difference between chest radiography and CT in the detection of asymmetric parenchymal disease in this group of patients with end-stage CF. Moreover, the surgeons at our institution rely more heavily on the results of quantitative perfusion scintigraphy than on the findings of chest CT or radiography for predicting asymmetric lung function, as do others (12–14). That is, they will preferentially remove the lung that is the least perfused first if the difference in perfusion between the two lungs is greater than 10%.

Asymmetric pleural disease usually is not an important factor in the decision of which lung to explant first during bilateral sequential lung transplantation. This is because most patients with CF have pleural adhesions, regardless of whether the adhesions are radiologically evident, and because both native lungs are mobilized and all pleural adhesions are lysed prior to the removal of the first native lung (9,10). In our series, CT was somewhat less sensitive than chest radiography in the detection of pleural disease when the findings of both modalities were compared with the operative findings. This was surprising because others (15) have found that CT is more sensitive for the detection of pleural disease than chest radiography. However, in the patients in our study, the most severe pleural abnormality was typically over the lung apices, which is an area that is not as well evaluated on cross-sectional imaging studies such as CT. Thus, in our experience, CT does not add substantial information regarding pleural disease compared with that provided by using chest radiography in patients with end-stage CF.

Nevertheless, in selected patients with marked asymmetric lung destruction or pleural disease, or in cases of prior lobectomy, the surgeon may find CT to be more useful than chest radiography for assessing the volume of the affected hemithorax or the degree of pleural thickening (4). This information might be helpful in selecting and sizing donor lungs and in planning the surgical approach. In our experience, this degree of asymmetry is unusual, and we believe that CT should not be used routinely for this purpose. It is important to note that no patient in our series was excluded from transplantation consideration on the basis of radiographic or CT findings of pleural disease.

Although CT demonstrated more areas of parenchymal consolidation than did chest radiography, this result was of doubtful importance, because no patient had clinical evidence of infection at the time of the pretransplantation examination, and all of the patients' sputum cultures were chronically positive for bacterial organisms. In addition, these findings had no effect on the pretransplantation evaluation, because the mean time between evaluation and transplantation was 12.9 months.

Thus, we found that the findings of CT performed before transplantation had no effect on surgical decision making in the evaluation of parenchymal and pleural disease. In addition, the CT findings had no influence on decisions regarding which patients to consider for transplantation. These decisions were based solely on clinical parameters such as rate of deterioration, oxygen dependence, and serial measurements of the forced expiratory volume in 1 second (2–4).

Radiographically occult malignancies are detected by using CT in up to 5% of patients with emphysema who are evaluated for possible lung transplantation or lung volume reduction surgery (6,16). However, in the study of Kazerooni et al (6), no occult malignancies were found in patients with Eisenmenger disease, CF, or primary pulmonary hypertension who were screened with CT. Although patients with CF have an increased risk of developing gastrointestinal malignancy, the risk of intrathoracic malignancy (eg, germ cell neoplasm, lung cancer, or lymphoma) is not increased in this population (17). In our series, CT enabled the detection of more adenopathy and pulmonary nodules than did chest radiography. In other patients, these findings might suggest occult malignancy. However, in CF patients, these findings proved to be of little clinical importance. In the group of patients who underwent transplantation in our study, the adenopathy usually was due to reactive node hyperplasia or infection, and the nodules proved to be either mucoid impactions or infections. No malignancies were found in any of the patients with CF who underwent transplantation. Thus, we concluded that CT is not likely to be useful for screening this population for malignancy and should not be performed for this reason. Obviously, however, CT should be performed when there is concern for malignancy on the basis of clinical examination or chest radiographic findings.

Aspergillus colonization is a common and potentially important complication of end-stage CF (4,18,19). In our series, the CT findings were not useful as predictors of Aspergillus colonization or infection. Mycetoma formation, which is a rare form of Aspergillus infection in patients with end-stage CF, is considered to be a contraindication to lung transplantation in some centers (4,20–22). No mycetomas were found in our series. In fact, we had five cases that were false-positive for mycetoma at chest radiography or CT. These false-positive cases probably were due to intracavitary blood clots or mucous plugs. Some of these false-positive cases might have been prevented by performing imaging with the patient in the prone position because this method is presumably more specific for the diagnosis of mycetoma. No specific radiologic features were seen in the patients whose preoperative sputum cultures were positive for aspergillosis. Thus, we were unable to determine which patients had Aspergillus colonization by using chest radiography or CT. In addition, neither chest radiography nor CT was predictive of infection with other organisms such as M avium-intracellulare complex, Pseudomonas species, or Burkholderiella species.

In our series, CT depicted several extrathoracic findings of possible importance: renal calculi, gallstones, and findings suggestive of hepatic cirrhosis. Findings of cirrhosis are particularly important because patients who have CF with substantial hepatic dysfunction generally have been excluded from consideration for lung transplantation (23). In our series, however, no patient was excluded because of hepatic disease, and these CT findings did not alter the clinical or surgical treatment of these patients.

We did not specifically evaluate the ability of CT to predict which patients required transplantation. At our institution, as at others (3–5,8,18,24), this decision was based primarily on clinical parameters and not on the severity of lung disease as judged by using chest radiography or CT. Some authors (7) have suggested that because CT is more sensitive than chest radiography for the detection of the morphologic alterations of CF, CT should be used to follow up these patients. However, there is little objective evidence suggesting that follow-up CT alters the outcome in these patients, and there are no data suggesting that CT is useful for predicting the need for and timing of lung transplantation.

Therefore, on the basis of our experience, we conclude that CT is not routinely indicated for the pre–lung transplantation examination of patients with CF. Because CT accounts for up to 10% of the cost for pretransplantation evaluation (6), its use in this setting should be discouraged.

	Footnotes

 
Abbreviation: CF = cystic fibrosis

Author contributions: Guarantors of integrity of entire study, E.M.M., H.P.M.; study concepts and design, H.P.M., E.M.M.; definition of intellectual content, H.P.M.; literature research, E.M.M., S.M.P.; clinical studies, H.P.M., E.M.M., S.M.P., J.J.E, T.A.S.; data acquisition, H.P.M., E.M.M., S.M.P., T.A.S., J.J.E.; data analysis, H.P.M., E.M.M.; manuscript preparation, H.P.M., E.M.M., P.C.G.; manuscript editing, V.F.T., R.D.D., P.C.G.; manuscript review, H.P.M., P.C.G.

	References

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This Article Abstract Figures Only Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Marom, E. M. Articles by Goodman, P. C. Search for Related Content PubMed PubMed Citation Articles by Marom, E. M. Articles by Goodman, P. C.