AJR 2005; 184:629-637
© American Roentgen Ray Society
High-Resolution CT and Pathologic Findings of Noninfectious Pulmonary Complications After Hematopoietic Stem Cell Transplantation
Tomás Franquet1,
Nestor L. Müller2,
Kyung Soo Lee3,
Ana Giménez1 and
Julia D. Flint4
1 Department of Radiology, Hospital de Sant Pau, Universitat Autónoma de
Barcelona, Avda Sant Antoni M. Claret 167, Barcelona 08025, Spain.
2 Department of Radiology, Vancouver Hospital and Health Sciences Center and
University of British Columbia, Vancouver, BC V5Z 1M9, Canada.
3 Department of Radiology and Center for Imaging Science, Samsung Medical
Center, Sungkyunkwan University School of Medicine 50, Ilwon-Dong, Kangnam-Ku
Seoul 135-710, Korea.
4 Department of Pathology, Vancouver Hospital and Health Sciences Center and
University of British Columbia, Vancouver, BC V5Z 1M9, Canada.
Received May 7, 2004;
accepted after revision July 22, 2004.
Address correspondence to T. Franquet
(19429tfc{at}comb.es).
Introduction
The term "hematopoietic stem cell [HSC] transplantation" has
replaced the previously used term "bone marrow transplantation" to
reflect the broader range of donor stem cell sources that are now available
[1]. HSC transplantation is
being used with increasing frequency for treatment of leukemia, aplastic
anemia, myeloma, and some forms of lymphoma and solid tumors. Although HSC
transplantation is a well-established procedure, pulmonary infection and
noninfectious pulmonary complications are common
[1–3].
Noninfectious pulmonary complications include pulmonary edema, engraftment
syndrome, alveolar hemorrhage, drug-induced lung injury, idiopathic pneumonia,
obliterative bronchiolitis, cryptogenic organizing pneumonia, pulmonary
venoocclusive disease, and posttransplantation lymphoproliferative disorder
[2]. Most noninfectious causes
of lung injury are attributed to treatment-related toxicities and are
influenced by the myeloablative conditioning regimens used before
transplantation, the degree of immunosuppression, and the interaction of the
graft with the host. Therefore these causes tend to occur within specific time
periods after transplantation.
The aim of this pictorial essay is to review the high-resolution CT and
histologic features of various noninfectious pulmonary complications following
HSC transplantation. Complications are grouped according to their time of
presentation relative to the day of bone marrow transplantation (BMT) into
early complications (
100 days of BMT) and late complications (> 100
days of BMT). Early complications can be further subdivided into those that
appear in the neutropenic phase (first 30 days of transplantation) or in the
early phase (30–100 days of transplantation). During the early phase,
the neutrophil count is normal but the cell-mediated and humoral immunity is
decreased.
Early Complications
Neutropenic Phase
Pulmonary edema.—Pulmonary edema is one of the earliest
complications after HSC transplantation. It is usually secondary to the large
volumes of fluids (infused to minimize the toxicity of conditioning regimens)
and to transfusion of blood products
[2]. The high-resolution CT
findings include enlarged pulmonary vessels, septal lines, peribronchial
cuffing, ground-glass opacities, and small pleural effusions
[4,
5]
(Fig. 1). The ground-glass
opacities tend to involve mainly the dependent lung regions.
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Fig. 1. —Pulmonary edema due to fluid overload in 28-year-old woman
after hematopoietic stem cell transplantation. High-resolution CT scan
obtained though upper lobes shows smooth septal thickening in
gravity-dependent distribution. Left interlobar fissure is also prominent due
to subpleural edema.
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Engraftment syndrome.—Engraftment syndrome is a
noninfectious pulmonary complication that represents a form of diffuse
capillary leak associated with lung injury and pulmonary edema. The syndrome
occurs most frequently after autologous HSC transplantation, being reported in
7–11% of cases [2]. It is
rarely seen after allogeneic transplantation. The median time of onset is 7
days after HSC transplantation
[2]. Clinically, because it
occurs with other noninfectious pulmonary complications, patients are febrile
and may also present with skin rashes similar to those in acute
graft-versus-host disease and hypoxia. Chest radiographic findings are
nonspecific and range from normal to bilateral air-space opacification,
diffuse vascular redistribution, and pleural effusions
(Fig. 2). On CT, engraftment
syndrome usually manifests as bilateral ground-glass opacification, air-space
consolidation distributed at the hilar or peribronchial regions, and smooth
thickening of interlobular septa
[4,
5].
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Fig. 2. —Engraftment syndrome in 46-year-old woman with non-Hodgkin's
lymphoma 3 weeks after allogeneic hematopoietic stem cell transplantation.
High-resolution CT scan shows bilateral areas of consolidation having
peribronchovascular and sub-pleural distribution. Note right pleural
effusion.
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Diffuse alveolar hemorrhage.—Diffuse alveolar hemorrhage is
a serious complication of HSC transplantation with a reported mortality rate
of approximately 70–100%
[6]. The overall incidence of
diffuse alveolar hemorrhage is higher after autologous (20%) than allogeneic
(10%) HSC transplantation. It typically occurs as a diffuse process in the
first month after transplantation, often at the time of granulocyte recovery.
Although its pathogenesis is not entirely understood, predisposing risk
factors include intensive pretransplantation chemotherapy and total body and
thoracic irradiation [2]. The
high-resolution CT findings consist of extensive bilateral ground-glass
opacities with or without superimposed intralobular linear opacities (crazy
paving pattern) [4,
5] (Fig.
3A,
3B).
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Fig. 3A. —Diffuse alveolar hemorrhage in 46-year-old woman with
non-Hodgkin's lymphoma 3 weeks after allogeneic hematopoietic stem cell
transplantation. High-resolution CT scan obtained at level of carina shows
diffuse ground-glass opacity in addition to septal thickening (crazy
paving).
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Fig. 3B. —Diffuse alveolar hemorrhage in 46-year-old woman with
non-Hodgkin's lymphoma 3 weeks after allogeneic hematopoietic stem cell
transplantation. Photomicrograph of histopathologic specimen shows that
macrophages containing hemosiderin are present within alveolar spaces
(arrows). (H and E, x100)
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Drug-induced lung injury.—Drug-induced lung disease occurs
in up to 10% of patients after autologous or allogeneic HSC transplantation. A
wide range of histologic reaction patterns can be seen, the most common being
diffuse alveolar damage, hypersensitivity reaction, nonspecific interstitial
pneumonia, and organizing pneumonia
[7]. The high-resolution CT
manifestations are nonspecific and reflect the histologic findings.
High-resolution CT findings include bilateral ground-glass attenuation, poorly
defined centrilobular nodules, peribronchial or subpleural areas of
consolidation, and irregular linear opacities
[4,
5] (Figs.
4A,
4B and
5A,
5B).
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Fig. 4A. —Vincristine sulfate–induced interstitial pneumonitis in
63-year-old man with myeloma. High-resolution CT scan obtained at level of
carina shows diffuse ground-glass attenuation in right lung and bilateral
patchy areas of consolidation.
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Fig. 4B. —Vincristine sulfate–induced interstitial pneumonitis in
63-year-old man with myeloma. Photomicrograph of histopathologic section shows
patchy expansion of interstitium by lymphocytic infiltrate, mild interstitial
fibrosis, and reactive hyperplastic type 2 pneumocytes (arrows). (H
and E, x250)
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Fig. 5A. —Carmustine-induced diffuse alveolar damage in 63-year-old man
after allogeneic hematopoietic stem cell transplantation. High-resolution CT
scan obtained though lung bases shows diffuse ground-glass opacity involving
lower lung zones.
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Fig. 5B. —Carmustine-induced diffuse alveolar damage in 63-year-old man
after allogeneic hematopoietic stem cell transplantation. Photomicrograph of
histopathologic specimen shows diffuse alveolar thickening and expansion of
interstitium by mononuclear inflammatory cells, mild interstitial fibrosis,
and reactive hyperplastic type 2 pneumocytes. (H and E, x100)
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Early Phase
Idiopathic pneumonia syndrome.—Idiopathic pneumonia syndrome
is defined as diffuse lung injury occurring after HSC transplantation in the
absence of active lower respiratory tract infection even in the presence of
nonlobar radiographic infiltrates and physiologic changes consistent with
pneumonia [8]. Thus, the
diagnosis of idiopathic pneumonia syndrome is one of exclusion, which requires
the elimination of potential infectious agents as a cause for the patient's
respiratory status. Idiopathic pneumonia is the most common cause for diffuse
radiographic abnormalities between 30 and 180 days after HSC transplantation.
Clinical symptoms include dyspnea, cough, and fever. The mortality rate of
idiopathic pneumonia syndrome remains greater than 70%, and two-thirds of all
deaths are associated with progressive respiratory failure
[8]. The histologic features of
idiopathic pneumonia syndrome range from a primarily interstitial reaction
with diffuse or focal widening of the alveolar septa and interstitial spaces
by mononuclear inflammatory cells and edema to diffuse alveolar damage with
intraalveolar hyaline membranes, edema, and hemorrhage. Other associated
patterns, such as organizing pneumonia and vascular damage, have also been
described. High-resolution CT shows air-space consolidation with a basilar
predominance (Fig. 6A,
6B), a pattern consistent with
noncardiogenic pulmonary edema
[8]. Pleural effusions may be
present.
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Fig. 6A. —Idiopathic pneumonia syndrome in 40-year-old man with acute
myelogenous leukemia 4 weeks after allogeneic hematopoietic stem cell
transplantation. High-resolution CT scan obtained at level of lower lung zones
shows bilateral patchy areas of consolidation and ground-glass
attenuation.
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Fig. 6B. —Idiopathic pneumonia syndrome in 40-year-old man with acute
myelogenous leukemia 4 weeks after allogeneic hematopoietic stem cell
transplantation. Photomicrograph of histopathologic specimen shows that
alveolar septa are thickened by edema and round cell infiltration
(arrow). Hyperplasia and desquamation of alveolar lining cells,
fibrinous exudation, and hyaline membranes (arrowheads) are seen
within alveolar spaces. (H and E, x250)
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Acute graft-versus-host disease.—Graft-versus-host disease
is an immune reaction mediated by donor T-lymphocytes that recognize the
recipient's tissue as a foreign body. It may present as acute or chronic
pulmonary complication after HSC transplantation. Acute graft-versus-host
disease develops in 20–75% of patients
[9]. The most commonly affected
tissue systems are the skin, liver, and gastrointestinal system. Pulmonary
involvement is rare. The median time of onset of respiratory symptoms is 5
months (range, 1–13 months). The reported radiologic manifestations
include mild perihilar or diffuse interstitial fibrosis, cysts, and lung
nodules (Fig. 7).
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Fig. 7. —Acute graft-versus-host disease in 34-year-old man with
cell-mediated lympholysis 5 weeks after hematopoietic stem cell
transplantation. High-resolution CT scan obtained at level of inferior
pulmonary veins shows small areas of consolidation (arrow) in
association with discrete right pleural effusion.
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Pleuropericardial effusion and hepatic venoocclusive
disease.—Pleuropericardial effusion has been reported in
approximately 16% of patients in the first weeks after receiving HSC
transplantation [9]. The most
common noninfectious cause of pleural effusion is aggressive treatment with
fluids, blood, and blood-product transfusion. The effusion is usually
bilateral or right-sided and rarely related to an identifiable infectious
source. Hepatic venoocclusive disease, an occasional complication in
allogeneic HSC transplantation recipients, is characterized by jaundice,
hepatic enlargement, right upper quadrant pain, and ascites
[9]. Pleural effusion has been
reported in up to 50% of HSC transplantation recipients with hepatic
venoocclusive disease. Patients with venoocclusive disease and pleural
effusions have either no or minimal respiratory symptoms. Hepatic
venoocclusive disease usually precedes the development of pleural effusion
(Fig. 8).
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Fig. 8. —Pleuropericardial effusion in 28-year-old woman after
hematopoietic stem cell transplantation. High-resolution CT scan with
mediastinal window setting shows presence of bilateral pleural and small
pericardial effusions.
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Pulmonary cytolytic thrombi.—A rare early pulmonary vascular
complication consisting of endothelial swelling with arteriolar, venular, and
capillary thrombi has been described after allogeneic HSC transplantation with
acute graft-versus-host disease
[10]. Active graft-versus-host
disease shortly before or at the time of pulmonary cytolytic thrombi in all
patients is indicative of the presence of alloreactive donor cells and
supports a causative association. Pathologically, it is characterized by
intravascular formation of basophilic thrombi frequently accompanied by
pulmonary infarcts [10]. The
median time of onset of pulmonary cytolytic thrombi is 2 months after
transplantation, although cases have been reported as early as 2 weeks.
Although its pathogenesis is unknown, pulmonary cytolytic thrombi may be a
manifestation of acute graft-versus-host disease. CT findings consist of
multiple pulmonary nodules (Fig.
9A,
9B,
9C). The main differential
diagnosis is with pulmonary infection, a much more common cause of pulmonary
nodules after HSC transplantation.
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Fig. 9A. —Pulmonary cytolytic thrombi in 11-year-old boy after
hematopoietic stem cell transplantation for acute lymphoblastic leukemia. CT
scan shows discrete peripheral pulmonary nodules suggestive of opportunistic
infection (arrows).
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Fig. 9B. —Pulmonary cytolytic thrombi in 11-year-old boy after
hematopoietic stem cell transplantation for acute lymphoblastic leukemia.
Photomicrograph of histopathologic specimen shows that nodules consist
primarily of hemorrhagic infarcts (asterisk). Occlusive vascular
lesions are present within, adjacent to, and away from hemorrhagic infarct
(arrowheads). (H and E, x40)
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Fig. 9C. —Pulmonary cytolytic thrombi in 11-year-old boy after
hematopoietic stem cell transplantation for acute lymphoblastic leukemia.
Photomicrograph of histopathologic specimen shows that intensely basophilic,
tenacious, amorphous material occludes lumen of vessels (arrows). Few
intact cells recognized as leukocytes (arrowheads) are also seen
(inset). (H and E, x400) (Courtesy of Gulbahce HE, Minneapolis, MN)
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Acute radiation pneumonitis.—Whole-body irradiation used for
bone marrow transplantation does not result in radiologically visible
pneumonitis. However, radiation pneumonitis is commonly seen in patients who
receive localized radiation therapy for control of mediastinal lymphoma before
transplantation. Risk factors for radiation injury include total dose
delivered, preexisting lung disease, and concurrent treatment with agents that
sensitize the lung to radiation damage. Radiation pneumonitis presents 6 weeks
to 6 months after completion of radiation therapy
[4,
5]. In patients who progress to
a clinically evident radiation pneumonitis, the radiographic findings range
from normal to mild perivascular haziness. Over time, these initial lesions
may develop into alveolar infiltrates. Clinically, patients present with fever
and leukocytosis, making radiation injury a clinical syndrome difficult to
distinguish from infection. A characteristic CT pattern consists of sharply
marginated ground-glass opacities that do not follow an anatomic border
[4,
5]
(Fig. 10).
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Fig. 10. —Acute radiation pneumonitis in 28-year-old woman after
hematopoietic stem cell transplantation. High-resolution CT scan shows
paramediastinal ground-glass attenuation with associated bronchovascular
distortion. Notice sharp border between radiated area and normal lung
parenchyma (arrows).
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Late Complications
Chronic Graft-Versus-Host Disease
Chronic graft-versus-host disease is the most common nonrelapse problem
affecting long-term survivors of allogeneic HSC transplantation. Pulmonary
complications include bronchiolitis obliterans and cryptogenic organizing
pneumonia.
Bronchiolitis Obliterans
Bronchiolitis obliterans is an obstructive pulmonary disorder that affects
the small air-ways and has been reported to occur in 2–14% of allogeneic
HSC transplantation recipients who survive more than 3 months
[9]. Presenting symptoms
include progressive dyspnea accompanied by persistent cough and expiratory
wheeze. Pulmonary function testing shows new obstructive lung defects defined
by a forced expiratory volume in 1 sec (FEV1) of less than 80% of
that predicted or a decrease of FEV1–forced vital capacity by
10% or more in less than 1 year. Obliterative bronchiolitis is associated with
high mortality rate (60%) at 3 years after HSC transplantation
[9]. Histologically, there is a
predominantly constrictive bronchiolitis with destruction and narrowing of the
bronchiolar lumen by fibrous tissue. High-resolution CT findings include areas
of decreased attenuation and vascularity (mosaic perfusion), air trapping, and
bronchial dilatation (Fig.
11A,
11B).
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Fig. 11A. —Chronic (obliterative) bronchiolitis in 48-year-old woman 5
months after allogeneic hematopoietic stem cell transplantation.
High-resolution CT scan obtained at level of lower lobes shows striking
dilatation of subsegmental airways in right lower lobe. General reduction in
lung parenchymal density is also noted.
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Fig. 11B. —Chronic (obliterative) bronchiolitis in 48-year-old woman 5
months after allogeneic hematopoietic stem cell transplantation.
Photomicrograph of histopathologic section of lung parenchyma shows moderately
severe mononuclear inflammatory cell infiltrate in peribronchiolar
interstitial tissue (arrows).
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Organizing Pneumonia
Organizing pneumonia is a well-known late manifestation of chronic
graft-versus-host disease, occurring in up to 10% of patients with stem cell
transplantation [9]. Risk
factors for cryptogenic organizing pneumonia include allogeneic HSC
transplantation and graft-versus-host disease. CT findings consist of patchy
consolidation frequently in a sub-pleural or peribronchial location,
ground-glass opacities, and, occasionally, centrilobular nodules (Fig.
12A,
12B).
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Fig. 12A. —Organizing pneumonia after hematopoietic stem cell
transplantation in 38-year-old man. High-resolution CT scan obtained at level
of lower lung zones shows bilateral patchy areas of consolidation in
predominantly peribronchial distribution.
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Fig. 12B. —Organizing pneumonia after hematopoietic stem cell
transplantation in 38-year-old man. Photomicrograph of histopathologic
specimen shows presence of fibroblastic tissue in lumina of peribronchial
alveoli (arrows). (H and E, x100)
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Posttransplantation Malignancies
Posttransplantation malignancies in HSC transplantation patients are seven
times more common than primary cancer in the general population.
Posttransplantation malignancies include solid tumors, hematologic neoplasms,
and posttransplantation lymphoproliferative disorder
[2]. Posttransplantation
lymphoproliferative disorder represents a heterogeneous group of Epstein-Barr
virus–related lymphoid tumors that occur in the setting of ineffective
T-cell function because of pharmacologic immunosuppression after solid-organ
transplantation and HSC transplantation
[2]. Posttransplantation
lymphoproliferative disorder occurs in approximately 2% of HSC transplantation
patients. The CT manifestations of posttransplantation lymphoproliferative
disorder usually consist of multiple pulmonary nodules or hilar and
mediastinal lymphadenopathy or both (Fig.
13).
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Fig. 13. —Posttransplantation lymphoproliferative disease in
54-year-old man with multiple myeloma 2 months after allogenic hematopoietic
stem cell transplantation. CT scan shows multiple enlarged axillary and
mediastinal lymph nodes.
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Radiation Fibrosis
Radiation fibrosis typically occurs 6 months or more after radiation
therapy. The high-resolution CT findings consist of a reticular pattern with
associated traction bronchiectasis limited to the radiation portal
[2,
5] (Fig.
14A,
14B).
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Fig. 14A. —Radiation fibrosis in 48-year-old man after radiation therapy
for lymphoma. Chest radiograph obtained 1 year after radiation therapy shows
bilateral fibrotic changes in paramediastinal lung zone (arrows).
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Calcification of Mediastinal Lymph Nodes and Thymic Cysts
Calcification of lymph nodes and presternal soft-tissue disease may be seen
after radiation therapy for Hodgkin's disease
[2]. Calcification of
nonenlarged nodes in Hodgkin's disease signifies a favorable response to
therapy (Fig. 15). Thymic
cysts, sometimes with a thin rim of calcification, may develop as an
inflammatory response after radiation therapy for Hodgkin's disease (Fig.
16A,
16B,
16C); occasionally they
enlarge and simulate recurrent tumor
[2].
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Fig. 15. —Mediastinal lymph node calcification in 38-year-old man after
radiation therapy for lymphoma. Close-up view of CT scan shows multiple
calcified retrosternal lymph nodes (arrows). Patient had undergone
radiation therapy for Hodgkin's disease 3 years previously.
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Fig. 16A. —Calcified thymic cyst in 30-year-old man after radiation
therapy for Hodgkin's disease. Posteroanterior (A) and lateral
(B) chest radiographs show anterior mediastinal mass with thin rim of
calcification (arrows).
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Fig. 16B. —Calcified thymic cyst in 30-year-old man after radiation
therapy for Hodgkin's disease. Posteroanterior (A) and lateral
(B) chest radiographs show anterior mediastinal mass with thin rim of
calcification (arrows).
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Summary
The diagnostic approach to noninfectious pulmonary complications in the HSC
transplantation recipient remains a challenge for several reasons: the current
increase in both the number of HSC transplantation recipients and their length
of survival, the high frequency of lung disease in these patients, and the
severity of these lung diseases. A combination of the clinical information and
high-resolution CT findings, which are sometimes characteristic of several
entities, may help the radiologist in forming a meaningful differential
diagnosis of these disorders. Familiarity with the appearance of more typical
pulmonary complications should improve diagnosis and patient care.
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Introduction
Early Complications
