(Radiographics. 2000;20:1637-1648.)
© RSNA, 2000
CT of Heart Transplant Recipients: Spectrum of Disease1
Friedrich D. Knollmann, MD ,
Manfred Hummel, MD ,
Roland Hetzer, MD, PhD and
Roland Felix, MD, PhD
1 From the Strahlenklinik, Charité, Campus Virchow-Klinikum, Augustenburger Platz 1, 13353 Berlin, Germany (F.D.K., R.F.); and the Department of Cardiothoracic and Vascular Surgery, German Heart Institute Berlin, Germany (M.H., R.H.). Presented as a scientific exhibit at the 1999 RSNA scientific assembly. Received March 27, 2000; revision requested May 5 and received June 2; accepted June 26. Address correspondence to F.D.K. (e-mail: friedrich.knollmann@charite.de).
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Abstract
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The emergence of heart transplantation as the ultimate treatment for end-stage heart failure has been accompanied by new diagnostic challenges. Computed tomography (CT) has emerged as an important diagnostic tool in the evaluation of heart transplant recipients because many infectious, ischemic-hemorrhagic, and neoplastic complications are amenable to early detection with this modality. In the early postoperative period, CT is mostly indicated in the evaluation of infectious complications or cerebral symptoms. Later, CT is mostly performed for staging of infectious or neoplastic disease. Infectious complications include mediastinitis, soft-tissue inflammation, abscess formation, cerebral infarction, and aspergillosis. Complications related to ischemia or hemorrhage include allograft rejection and coronary allograft vasculopathy, the latter being the leading long-term cause of death in heart transplant recipients. CT is also indicated in malignant disease (eg, lymphoma, visceral carcinoma, skin tumors), which is the second most important long-term cause of death. Moreover, CT is helpful in identifying disease caused by immunosuppressive therapy (eg, leukoencephalopathy, osteoporosis, thoracic lipomatosis). CT has proved superior to both ultrasound and magnetic resonance imaging in the evaluation of heart transplant recipients. It has become the diagnostic modality of choice for many transplant-related complications and may help improve postoperative treatment of affected patients.
Index Terms: Aspergillosis, 60.2056 • Brain, diseases, 10.8722 • Coronary vessels, diseases, 54.459, 54.754 • Grafts, 51.459, 54.459 • Heart, transplantation, 51.459 • Lipoma and lipomatosis, 60.319 • Lymphoma, **.342 • Osteoporosis, 30.56, 40.56
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Introduction
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Heart transplantation has emerged as the ultimate treatment option in end-stage heart disease in many cases and is now widely recognized as standard practice (1). Still, perioperative mortality, the need for long-term immunosuppressive therapy, and the recurrence of heart disease represent important limitations. The imaging findings in heart transplant recipients are similar to those encountered with any major surgical procedure involving the thorax; however, there are also some unique issues pertaining to this patient group that deserve special attention (2). From a prognostic viewpoint, the most important diagnostic considerations include infectious complications, allograft disease, and neoplastic disease. The time course of different complications varies greatly depending on the cause of the complication. According to the widely accepted nomenclature of the International Society for Heart and Lung Transplantation, early disease is defined as that which occurs less than 1 year after surgery (3). During the 1st postoperative year, graft failure and infectious disease are the leading causes of death (Fig 1). The distribution of various causes of death at our institution was largely the same as that reported by the International Society of Heart and Lung Transplantation in over 48,000 heart transplant recipients at over 300 institutions worldwide (3). In the late postoperative period, coronary artery disease of the cardiac graft (cardiac allograft vasculopathy) and neoplastic disease are the leading causes of death (Fig 2). Computed tomography (CT) has emerged as an important diagnostic tool in heart transplant recipients because many infectious, ischemic, or neoplastic complications are amenable to early detection with this modality.
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Figure 1. Graph illustrates the distribution of causes of death in heart transplant recipients within 1 year after surgery at the German Heart Institute Berlin between 1986 and 1999.
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Figure 2. Graph illustrates the distribution of causes of death in heart transplant recipients more than 1 year after surgery at the German Heart Institute Berlin between 1986 and 1999.
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In this article, we report on 13 years' experience with CT in heart transplant recipients at the German Heart Institute Berlin, where over 1,300 patients underwent heart transplantation between 1986 and 1999. During this time, 505 CT studies were performed in 432 patients (Fig 3). In the early postoperative period, CT was indicated primarily in the evaluation of infectious complications or cerebral symptoms. Later, CT was mostly performed for staging of infectious or neoplastic disease.
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Infectious Complications
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The prevalence and distribution of pathogens following heart transplantation as well as their CT appearance are not significantly different from those found with other solid organ transplantation procedures (4).
The overall sensitivity of CT in detecting lung disease after solid organ transplantation has been reported as 70%—96%, with a specificity of 30%—70% (4). Other investigators have demonstrated that CT greatly improves the differential diagnosis of lung disease in immunocompromised patients by providing a correct diagnosis among the first three choices in 70% of cases, as opposed to 53% with chest radiography (5). Bacteria are the most common pathogens in early posttransplantation infectious disease (6) and often manifest as bacterial pneumonia or lead to abscess formation with cavitation (Fig 4). The CT appearance of such processes may be very similar to that of pulmonary aspergillosis (Fig 5) (7).
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Figure 4a. Lung abscess with cavitation. CT scans obtained with mediastinal windowing (a) and lung windowing (b) demonstrate a lung abscess with cavitation caused by both Klebsiella pneumoniae and Legionella species.
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Figure 4b. Lung abscess with cavitation. CT scans obtained with mediastinal windowing (a) and lung windowing (b) demonstrate a lung abscess with cavitation caused by both Klebsiella pneumoniae and Legionella species.
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Figure 5a. Pulmonary aspergillosis. CT scans obtained with mediastinal windowing (a) and lung windowing (b) demonstrate isolated pulmonary aspergillosis with an upper lobe predilection and cavitation.
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Figure 5b. Pulmonary aspergillosis. CT scans obtained with mediastinal windowing (a) and lung windowing (b) demonstrate isolated pulmonary aspergillosis with an upper lobe predilection and cavitation.
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Nocardia species is another otherwise uncommon pathogen and causes extensive soft-tissue inflammation and the formation of abscesses with contrast material—enhancing rims (Fig 6) (8). Postoperative bacterial mediastinitis typically occurs shortly after surgery.
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Figure 6. Extensive soft-tissue inflammation and abscess formation. CT scan demonstrates extensive soft-tissue inflammation and an abscess with a contrast-enhancing rim in the right thigh caused by Nocardia species.
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The CT signs of mediastinitis include mediastinal fluid collections and air inclusions as well as focal contrast enhancement (Fig 7). Early detection is important, and surgical treatment is usually mandatory. The differential diagnosis includes early postoperative retention of air, sternal dehiscence, mediastinal hematoma, and encapsulated pleural effusions.
Bacterial infectious complications of the head and neck include sinusitis, mastoiditis, and intracranial abscess formation (Fig 8). Differentiation between intracranial abscess formation and cerebrovascular disease can be very difficult if only unenhanced CT is used.
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Figure 8a. Intracranial abscess formation. Unenhanced (a) and contrast-enhanced (b) CT scans demonstrate the delayed appearance of ringlike contrast enhancement, which suggested bacterial brain abscesses. This finding was confirmed at surgery.
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Figure 8b. Intracranial abscess formation. Unenhanced (a) and contrast-enhanced (b) CT scans demonstrate the delayed appearance of ringlike contrast enhancement, which suggested bacterial brain abscesses. This finding was confirmed at surgery.
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Rim enhancement may also occur as the result of cerebral infarction, which is particularly common in transplant recipients who have been supported with a mechanical assist device while awaiting transplantation (Fig 9). The differentiation of cerebral infarction from abscess formation is based on the extent of contrast enhancement, which is more prominent in the latter; the location of the process with respect to cerebral artery territories; the number of lesions and their distribution; and clinical history. Laboratory test results, including spinal fluid analysis and the course of neurologic deficits, also provide important clues.
Although many patients have elevated pancreatic enzyme levels after heart transplantation, necrotizing pancreatitis is found in only a fraction of cases (Fig 10).
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Figure 10. Necrotizing pancreatitis in a 54-year-old man. CT scan of the upper abdomen demonstrates signs of necrotizing pancreatitis including peripancreatic fluid accumulation and pancreatic edema.
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Aspergillus infection constitutes one of the most important infectious complications of heart transplantation (9). Aspergillus infection commonly manifests as isolated pulmonary nodular disease with an upper lobe predilection and cavitation (Fig 5). The differential diagnosis includes pulmonary metastasis, bronchial carcinoma, tuberculosis, areas of pulmonary infarction, focal pulmonary hemorrhage after lung biopsy, and other fungal infections.
Invasive aspergillosis causes nodular infiltration with a ground-glass-attenuation rim but without cavitation. Immunosuppressive therapy renders heart transplant recipients particularly vulnerable to this pattern of Aspergillus infection (Fig 11). In patients with a recent history of pulmonary aspergillosis and new-onset severe neurologic deficit, cerebral aspergillosis should be considered. At contrast-enhanced CT, cerebral aspergillosis manifests as bifrontal hypoattenuating cerebral defects with rim enhancement (Fig 12a, 12b). On unenhanced scans, it may be difficult to differentiate this disease entity from immunosuppressive druginduced toxic leukoencephalopathy.
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Figure 12a. Cerebral aspergillosis with intralesional hemorrhage in a 55-year-old woman who presented with severe neurologic deficit. (a, b) Unenhanced (a) and contrast-enhanced (b) CT scans demonstrate the delayed appearance of bifrontal hypoattenuating cerebral defects with rim enhancement due to cerebral aspergillosis. (c) CT scan obtained 9 days later while the patient was undergoing fungistatic therapy reveals intralesional hemorrhage with intense contrast enhancement. Intracranial aspergillosis was confirmed at autopsy.
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Figure 12b. Cerebral aspergillosis with intralesional hemorrhage in a 55-year-old woman who presented with severe neurologic deficit. (a, b) Unenhanced (a) and contrast-enhanced (b) CT scans demonstrate the delayed appearance of bifrontal hypoattenuating cerebral defects with rim enhancement due to cerebral aspergillosis. (c) CT scan obtained 9 days later while the patient was undergoing fungistatic therapy reveals intralesional hemorrhage with intense contrast enhancement. Intracranial aspergillosis was confirmed at autopsy.
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Figure 12c. Cerebral aspergillosis with intralesional hemorrhage in a 55-year-old woman who presented with severe neurologic deficit. (a, b) Unenhanced (a) and contrast-enhanced (b) CT scans demonstrate the delayed appearance of bifrontal hypoattenuating cerebral defects with rim enhancement due to cerebral aspergillosis. (c) CT scan obtained 9 days later while the patient was undergoing fungistatic therapy reveals intralesional hemorrhage with intense contrast enhancement. Intracranial aspergillosis was confirmed at autopsy.
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Another possible course of disease is intralesional hemorrhage, which generally indicates a poor prognosis (Fig 12c). A similar appearance may be caused by hemorrhagic brain infarction and cerebral metastasis.
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Allograft Rejection
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Although graft rejection is usually not diagnosed at CT, rejection of the aortic graft component may cause aortic dehiscence (10). This pathologic condition manifests as severe periaortic hematoma, usually in later postoperative years (Fig 13).
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Figure 13. Allograft rejection in a patient who had undergone heart transplantation several years earlier. CT scan shows an aortic pseudoaneurysm (arrow) and aortic dehiscence caused by allograft rejection.
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Two patients in our series had aortic pseudoaneurysms due to graft rejection. Both patients underwent surgical revision and had a favorable outcome.
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Coronary Allograft Vasculopathy
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Coronary allograft vasculopathy is the leading long-term cause of death in heart transplant recipients. A recent study showed that electron beam CT can be used to quantitate coronary artery calcifications as an indicator of allograft vasculopathy. In that study, significant coronary artery calcifications were present in all patients with more than 50% coronary artery stenosis (Figs 14, 15), and the total calcium score correlated well with the degree of intimal proliferation at intracoronary ultrasonography (US) (11). Other investigators have found a similar accuracy for electron beam CT in excluding coronary stenosis, with a negative predictive value of up to 97% (12). Thus, calcium scoring with electron beam CT can be used to assess allograft coronary heart disease after heart transplantation. It has also been demonstrated that the presence of coronary artery calcifications in heart transplant recipients correlates well with the future occurrence of coronary events (13).
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Figure 14. Coronary allograft vasculopathy in a 54-year-old man with a total calcium score of 73 and 75% stenosis of the first diagonal branch at angiography. Electron beam CT scan demonstrates significant calcification of the proximal left anterior descending artery (arrow).
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Figure 15. Graph illustrates the correlation between coronary artery calcium load and obstructive disease in 50 heart transplant recipients seen at the German Heart Institute Berlin between 1997 and 1999.
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Neoplastic Disease
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The second most important long-term cause of mortality in heart transplant recipients is malignant disease, which represents another major indication for CT. In our experience, lymphoma, visceral carcinoma, and skin tumors are the most common neoplasms found in heart transplant recipients (Fig 16). This distribution is compatible with patterns reported at other centers, and a similar distribution of solid organ cancers has also been observed after bone marrow transplantation (14). Today, these neoplasms are considered to be the result of long-term immunosuppressive therapy (15).
Unlike with nonimmunosuppressed patients, lymphomas are often found in extramedullary locations in solid organ transplant recipients who are undergoing immunosuppressive therapy and may manifest as thoracic or abdominal tumors, sometimes being limited to a single site. Lymphomas often affect the abdomen, manifesting as intestinal obstruction (Fig 17a, 17b), hepatic masses (Fig 17c), or nodal enlargement. In such cases, a complete staging CT study is performed to define the exact extent of disease, including mediastinal and pulmonary manifestations (Fig 18). The differential diagnosis includes metastasis, hepatocellular carcinoma, benign hepatic tumors, benign reactive lymphadenopathy, and tuberculosis. The differential diagnosis of bowel wall thickening also includes bacterial enteritis, other inflammatory bowel diseases, and intestinal ischemia. Aortic anastomotic pseudoaneurysms (Fig 13) and mediastinal lymphoma may be indistinguishable on chest radiographs. CT has been described as a more comprehensive diagnostic choice than US in the evaluation of posttransplantation lymphoproliferative disorders (Fig 19) (16) and can be used in heart transplant recipients without the restrictions imposed on MR imaging by metallic implants. Bacterial abscess formation remains an important consideration in the differential diagnosis (Fig 20), and CT-guided biopsy may be required to resolve that issue.
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Figure 17a. Lymphoma in a 37-year-old man. (a) Upper gastrointestinal radiograph reveals severe jejunal obstruction due to lymphoma (arrow). Note also the presence of a cardiac pacemaker device in the upper abdomen, which also serves to record an intramyocardial electrocardiogram. The electrocardiogram is transmitted to the transplant center via telephone on a daily basis for early detection of rejection. This procedure has made routine myocardial biopsy obsolete at our center but usually obviates the use of magnetic resonance (MR) imaging in heart transplant recipients. (b) CT scan helps confirm severe intestinal obstruction due to wall thickening (arrow). The lesion was surgically confirmed as an intestinal lymphoma. (c) CT scan shows multiple hepatic areas of hypoattenuation (arrow) that also proved to be due to lymphoma.
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Figure 17b. Lymphoma in a 37-year-old man. (a) Upper gastrointestinal radiograph reveals severe jejunal obstruction due to lymphoma (arrow). Note also the presence of a cardiac pacemaker device in the upper abdomen, which also serves to record an intramyocardial electrocardiogram. The electrocardiogram is transmitted to the transplant center via telephone on a daily basis for early detection of rejection. This procedure has made routine myocardial biopsy obsolete at our center but usually obviates the use of magnetic resonance (MR) imaging in heart transplant recipients. (b) CT scan helps confirm severe intestinal obstruction due to wall thickening (arrow). The lesion was surgically confirmed as an intestinal lymphoma. (c) CT scan shows multiple hepatic areas of hypoattenuation (arrow) that also proved to be due to lymphoma.
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Figure 17c. Lymphoma in a 37-year-old man. (a) Upper gastrointestinal radiograph reveals severe jejunal obstruction due to lymphoma (arrow). Note also the presence of a cardiac pacemaker device in the upper abdomen, which also serves to record an intramyocardial electrocardiogram. The electrocardiogram is transmitted to the transplant center via telephone on a daily basis for early detection of rejection. This procedure has made routine myocardial biopsy obsolete at our center but usually obviates the use of magnetic resonance (MR) imaging in heart transplant recipients. (b) CT scan helps confirm severe intestinal obstruction due to wall thickening (arrow). The lesion was surgically confirmed as an intestinal lymphoma. (c) CT scan shows multiple hepatic areas of hypoattenuation (arrow) that also proved to be due to lymphoma.
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Figure 20. Pararenal bacterial abscess. CT scan shows a pararenal bacterial abscess, which appears similar to lymphoma and is therefore an important consideration in the differential diagnosis for lymphoma.
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The relatively high prevalence of B-cell non-Hodgkin lymphoma explains why such lesions occur at many different sites (Fig 21).
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Figure 21. B-cell non-Hodgkin lymphoma. CT scan obtained at the level of the hyoid bone shows a lateral cervical lymphoma with no spinal involvement (arrow). The mass is inferior to the left sternocleidoid muscle and displaces the left jugular vein laterally.
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Skin malignancies are surprisingly common after heart transplantation. Although many instances are detected with clinical examination and confirmed with excision, CT may help define the exact extent of malignant infiltration and the status of the lymph nodes, exclude distant metastasis, and narrow the differential diagnosis, specifically because non-Hodgkin lymphoma is a frequent consideration (Fig 22).
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Figure 22. Skin malignancy. CT scan demonstrates a left retroauricular mass (arrow) with local lymph node involvement. The mass proved to be due to squamous cell carcinoma. Treatment consisted of excision of the entire outer ear and neck dissection.
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Leukoencephalopathy due to Cyclosporine or FK-506 Toxicity
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Long-term immunosuppressive therapy with either cyclosporine or FK-506 (tacrolimus) has greatly improved the survival of heart transplant recipients. Both drugs can cause toxic leukoencephalopathy if plasma levels exceed the therapeutic level. Because both drugs have rather complicated pharmacokinetics, toxicity may occur even with meticulous monitoring. CT features consist of bilateral white matter areas of hypoattenuation. FK-506 toxicity demonstrates a pattern that is indistinguishable from cyclosporine-induced leukoencephalopathy (Fig 23), which is important to recognize because prompt dose reduction may completely resolve neurologic symptoms. A similar appearance with bilateral periventricular areas of hypoattenuation may be caused by internal hydrocephalus (Fig 24). Differentiation from cyclosporine-induced leukoencephalopathy is made on the basis of earlier CT findings and clinical history. In this setting, a review of the cyclosporine regimen and current cyclosporine plasma levels is important in differentiating these two entities. In addition, a trial of reduced cyclosporine dosage under strict plasma level surveillance may be indicated. Ophthalmoscopy is the standard procedure for excluding papilledema.
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Figures 23. FK-506induced leukoencephalopathy in a 66-year-old man. Cranial CT scan shows white matter disease (arrow) caused by FK-506 toxicity with an appearance that is indistinguishable from that of cyclosporine-induced leukoencephalopathy.
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Figure 24. Internal hydrocephalus in a 61-year-old woman. Cranial CT scan reveals bilateral periventricular areas of hypoattenuation caused by internal hydrocephalus (arrow) with an appearance similar to that of cyclosporine-induced toxicity. Differentiation from cyclosporine-induced leukoencephalopathy was made on the basis of earlier CT findings and clinical history.
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Long-term immunosuppressive steroid therapy in patients with a long history of advanced cardiac disease commonly causes osteoporosis. Vertebral fractures are therefore an important consideration in new-onset low back pain that occurs late after heart transplantation (Fig 25). Bone metastases and intervertebral diskitis are other important considerations in cases of nontraumatic vertebral fracture.
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Figure 25a. Fractures due to osteoporosis. (a) Axial CT scan demonstrates a vertebral body fracture (arrow). (b) Sagittal two-dimensional reconstructed image demonstrates an anterior vertebral fracture (arrow).
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Figure 25b. Fractures due to osteoporosis. (a) Axial CT scan demonstrates a vertebral body fracture (arrow). (b) Sagittal two-dimensional reconstructed image demonstrates an anterior vertebral fracture (arrow).
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Thoracic Lipomatosis
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Thoracic lipomatosis resulting from immunosuppressive therapy was a common finding at visual analysis in our series (Fig 26). Long-term immunosuppressive therapy has been shown to cause hyperlipidemia in heart transplant recipients (17), and lipid-lowering drug therapy has been established as a remedy for transplant vasculopathy in affected patients with hyperlipidemia (18). Although patients with more than 50% coronary artery stenosis displayed a different distribution of fat-tobody area ratios than did patients without stenosis, this association was not statistically significant (P = .7) (Figs 27, 28).
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Figure 27. Bar graph illustrates thoracic fat distribution in 98 heart transplant recipients without significant coronary stenosis. The graph displays the frequency distribution of the ratio of transsectional fat density area to transsectional total body area at the level of the carina. Bell curve represents normal distribution.
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Figure 28. Bar graph illustrates thoracic fat distribution in 16 heart transplant recipients with more than 50% coronary artery stenosis. The graph displays the frequency distribution of the ratio of transsectional fat density area to transsectional total body area at the level of the carina. Bell curve represents normal distribution.
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Thoracic lipomatosis is a side effect of immunosuppressive therapy and is easily recognized at CT. However, it remains a common cause of thoracic masses at routine chest radiography, making further work-up necessary to exclude malignant disease.
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Conclusions
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With the emergence of heart transplantation as the ultimate treatment for end-stage heart failure, new diagnostic challenges have arisen. CT helps detect infectious, hemorrhagic, and cerebral complications in the early postoperative phase and allows accurate assessment of infectious, neoplastic, and allograft coronary disease in later postoperative years. CT is now the diagnostic modality of choice for many transplant-related complications because it allows accurate assessment of some of the most daunting sequelae and may thus help improve patient treatment after heart transplantation.
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Footnotes
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**. indicates multiple body systems. 
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References
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Abstract
Introduction
