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(Radiology. 2000;217:647-656.)
© RSNA, 2000

Review

Pulmonary Infections in Immunocompromised Hosts: The Importance of Correlating the Conventional Radiologic Appearance with the Clinical Setting1

Yu Whan Oh, MD, Eric L. Effmann, MD and J. David Godwin, MD

1 From the Department of Diagnostic Radiology, Korea University College of Medicine, Seoul, South Korea (Y.W.O.); the Department of Radiology, Children’s Hospital and Medical Center, Seattle, Wash (E.L.E.); and the Department of Radiology, University of Washington Medical Center, Box 357115, Seattle, WA 98195-7115 (J.D.G.). Received July 20, 1998; revision requested November 2; final revision received November 1, 1999; accepted November 10. Address correspondence to J.D.G. (e-mail: godwin@u.washington.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 ENVIRONMENTAL EXPOSURE
 UNDERLYING IMMUNE DEFECT
 DURATION AND SEVERITY OF...
 RADIOLOGIC APPEARANCE
 REFERENCES
 
The lung is one of the most frequently involved organs in a variety of complications in the immunocompromised host. Among the pulmonary complications that occur in this kind of patient, infection is the most common and is associated with high morbidity and mortality. Although chest radiography and computed tomography (CT) are essential diagnostic tools, radiologists often have difficulty in establishing the correct diagnosis on the basis of radiologic findings alone. The reasons are that the immunocompromised host is potentially susceptible to infection from many different microorganisms and that radiologic findings are seldom specific for the detection of a particular pathogen. Experience has shown that a particular clinical setting predisposes patients to infection by particular pathogens. The setting comprises (a) the specific epidemiologic or environmental exposure, (b) the type of underlying immune defect, (c) the duration and severity of immune compromise, and (d) the progression rate and pattern of the radiologic abnormality. Correlating the radiologic appearance with the clinical setting can expedite diagnosis and appropriate therapy. In this review, the authors describe the clinical settings that are helpful in choosing the radiologic approach to treatment of the immunocompromised host who presents with suspected pulmonary infection.

Index terms: Acquired immunodeficiency syndrome (AIDS), 60.2518 • Immunity • Lung, CT, 60.12111, 60.12112, 60.12118 • Lung, diseases, 60.20, 60.21, 60.23, 60.25, 60.27 • Lung, infection, 60.20


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
ENVIRONMENTAL EXPOSURE
 UNDERLYING IMMUNE DEFECT
 DURATION AND SEVERITY OF...
 RADIOLOGIC APPEARANCE
 REFERENCES
 
The term "immunocompromised host" describes a patient who is at increased risk for life-threatening infection as a consequence of a congenital or acquired abnormality of the immune system (1). During the past few decades, the population of immunocompromised hosts has expanded enormously (2,3), reflecting the increased use of immunosuppressive agents for the treatment of tumors and collagen vascular disease and for the prevention of rejection in organ transplant recipients. In addition, acquired immunodeficiency syndrome (AIDS) has resulted in the existence of many immunocompromised patients.

The lung is one of the most frequently involved organs in a variety of complications in the immunocompromised host (4,5). Among the pulmonary complications that occur in this kind of patient, infection is the most common: It accounts for about 75% of pulmonary complications and is associated with high morbidity and mortality (6). Rapid and accurate diagnosis of pulmonary disease is important, not only because of the high morbidity and mortality associated with infection but also because of the frequent complications associated with the drugs used to treat the infection (7,8).

The chest radiograph is an essential diagnostic tool. Both the pattern of the abnormality and its rate of progression on serial images help in the diagnosis (9–12). However, radiography alone is seldom adequate, because its findings are seldom specific for the detection of a particular pathogen. It is necessary to go beyond the radiologic findings and incorporate knowledge of which pathogens are likely to afflict a patient in a particular clinical setting (13). The setting comprises the specific epidemiologic or environmental exposure, the type of underlying immune defect, and the duration and severity of immunocompromise.

Although radiologic findings of different kinds of pneumonia in immunocompromised patients have been described (14–22), few articles in the radiologic literature have, to our knowledge, emphasized the clinical setting in conjunction with the radiologic manifestations (23,24). In this review, we discuss the clinical settings that can be combined with radiologic findings to facilitate a more prompt and accurate diagnosis of pulmonary infection in the immunocompromised patient.


   ENVIRONMENTAL EXPOSURE
TOP
 ABSTRACT
 INTRODUCTION
 ENVIRONMENTAL EXPOSURE
UNDERLYING IMMUNE DEFECT
 DURATION AND SEVERITY OF...
 RADIOLOGIC APPEARANCE
 REFERENCES
 
Infection depends on the interaction between the host’s vulnerabilities and the organisms to which he or she is exposed. The important environmental and epidemiologic factors include community exposure, travel, history of previous infection, drug therapy (ie, cytotoxic or immunosuppressive agents), splenectomy, and nosocomial exposure (8,10).

Exposure and History of Infection
A history of tuberculosis, a positive tuberculin skin test, or residence in an endemic area raises the suspicion of primary or reactivated tuberculosis. Similarly, travel or residence in regions where histoplasmosis, coccidioidomycosis, or strongyloidiasis is endemic will suggest these as diagnostic possibilities. Patients with AIDS may contract certain fungal infections, such as histoplasmosis and coccidioidomycosis, outside endemic areas. Even in nonendemic areas, these fungal infections may represent reactivation of latent infection. History of infection is important, because pulmonary infection caused by organisms such as Mycobacterium tuberculosis, Pneumocystis carinii, Toxoplasma gondii, and varicella-zoster virus is more often due to reactivation than to new infection. However, many or most cases of primary tuberculosis and essentially all cases of primary infection with P carinii go unrecognized in immunocompetent persons. Thus, it may be difficult to obtain a history of antecedent infection in a patient who has subsequently become immunocompromised. Finally, the occurrence of one opportunistic infection may signal susceptibility to other specific opportunistic infections (25). For instance, a patient with AIDS who has had P carinii pneumonia is at increased risk for infection with Mycobacterium avium-intracellulare (Fig 1) and cytomegalovirus and is at slightly increased risk for systemic mycosis.



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  		Figure 1a. P carinii pneumonia and subsequent atypical mycobacterial infection in a 31-year-old man with AIDS. (a) Frontal chest radiograph shows slight reticular abnormality (arrows) in the lower part of both lungs. P carinii was identified at bronchoalveolar lavage. (b) Frontal chest radiograph obtained 2 months after successful treatment for P carinii pneumonia shows multiple, ill-defined nodules (arrows) throughout the lungs. M avium-intracellulare was recovered at needle aspiration.

 


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  		Figure 1b. P carinii pneumonia and subsequent atypical mycobacterial infection in a 31-year-old man with AIDS. (a) Frontal chest radiograph shows slight reticular abnormality (arrows) in the lower part of both lungs. P carinii was identified at bronchoalveolar lavage. (b) Frontal chest radiograph obtained 2 months after successful treatment for P carinii pneumonia shows multiple, ill-defined nodules (arrows) throughout the lungs. M avium-intracellulare was recovered at needle aspiration.

 
Drug Therapy Predisposing to Infection
Most cytotoxic drugs used for treatment of malignancy or autoimmune disease cause neutropenia and monocytopenia. They can also cause mucositis of the gut, which can cause gram-negative enteric bacteria to invade the intestinal wall and enter the circulation (12). Thus, cytotoxic drugs leave the patient vulnerable to the same infections that complicate neutropenia. Corticosteroids, which are widely used for immunosuppression, have qualitative and quantitative effects on immune cells (26). They depress the number of circulating lymphocytes and monocytes and inhibit phagocytosis and the activity of lymphocytes, especially T cells. Thus, corticosteroids increase susceptibility to infections associated with defects in cell-mediated immunity and phagocytosis (Fig 2).



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  		Figure 2. Infection with Nocardia species in a 42-year-old man who was treated with high-dose corticosteroids for Crohn disease. Frontal chest radiograph shows nodular opacities (arrows) in both lungs.

 
Nosocomial Exposure
Hospitalized immunocompromised patients are at risk for nosocomial pneumonias, half of which are caused by anaerobic gram-negative bacilli, including Pseudomonas aeruginosa, Enterobacter species, Klebsiella species, Escherichia coli, and Acinetobacter species (27). Oropharyngeal colonization followed by aspiration into the lower airway is a major pathway for lung infection with these bacteria. Colonization of the oropharynx is promoted by endotracheal intubation, use of antibiotics, acute immunosuppressive therapy, and reduced gastric acidity (from antacid or H2 blocker use) (Fig 3). Low acidity allows bacteria to proliferate in the stomach; from there they colonize the oropharynx and get aspirated into the lungs. When immunocompromised patients have painful ulcers (from herpes simplex virus or Candida species infection) in the oral cavity, pharynx, or esophagus, they are particularly prone to aspiration of infectious secretions (28).



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  		Figure 3. Nosocomial pneumonia in a 15-year-old boy with Wiskott-Aldrich syndrome who required mechanical ventilation. Frontal chest radiograph shows patchy consolidation (arrow) in the right lower lobe and atelectasis (*) in the left lower lobe behind the heart. Bronchoscopy recovered P aeruginosa.

 
Moisture on hospital appliances and in ventilating ducts can provide a medium for Legionella species and other gram-negative bacteria that cause pneumonia. Patients who are on mechanical ventilators are particularly vulnerable (14). Indwelling intravenous catheters increase the risk of septicemia (Fig 4) (7,12). Catheter infection with S aureus, P aeruginosa, or Candida species can lead to septic pulmonary embolism, as can intravenous drug abuse. The incidence of pneumonia caused by some organisms varies among institutions, even when patient populations appear to be identical in terms of underlying diseases and therapy (29).



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  		Figure 4a. Septic pulmonary emboli in a 30-year-old man with AIDS who had an indwelling central venous catheter. (a) Frontal chest radiograph shows multiple nodular opacities (arrows) and right pleural effusion. (b) Transverse CT scan through the carina obtained 2 days later demonstrates bilateral peripheral nodules and cavities. Note the feeding vessels (arrows) leading to cavitary nodules. Blood and sputum cultures revealed Staphylococcus aureus.

 


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  		Figure 4b. Septic pulmonary emboli in a 30-year-old man with AIDS who had an indwelling central venous catheter. (a) Frontal chest radiograph shows multiple nodular opacities (arrows) and right pleural effusion. (b) Transverse CT scan through the carina obtained 2 days later demonstrates bilateral peripheral nodules and cavities. Note the feeding vessels (arrows) leading to cavitary nodules. Blood and sputum cultures revealed Staphylococcus aureus.

 

   UNDERLYING IMMUNE DEFECT
TOP
 ABSTRACT
 INTRODUCTION
 ENVIRONMENTAL EXPOSURE
 UNDERLYING IMMUNE DEFECT
DURATION AND SEVERITY OF...
 RADIOLOGIC APPEARANCE
 REFERENCES
 
There are five principal kinds of immune defects: phagocytosis defects, humoral or antibody (B-cell) immunity defects, complement system defects, cell-mediated (T-cell) immunity defects, and defects caused by splenectomy or hyposplenism. Specific defects are associated with specific kinds of infection (Table 1) (30). Many immunocompromised patients have multiple immune defects, which are reflective of not only the underlying disease but also the immunosuppressive or cytotoxic therapy.


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  		TABLE 1. Immunologic Defects, Predisposing Factors, and Pulmonary Infections
 
Defects in Phagocytes
Mononuclear cells—that is, monocytes and macrophages—and neutrophils are phagocytes that defend the body against bacteria and fungi. To be effective, these cells must migrate to the site of infection, engulf and kill the microorganisms, and eliminate cellular debris. In addition, mononuclear phagocytes produce regulators and present antigens to lymphocytes and thereby help to initiate and coordinate the immune response.

The most frequent quantitative defect of phagocytosis is neutropenia (<1,000 cells x109/L), which typically occurs in patients with acute leukemia or bone marrow failure or in patients who are undergoing chemotherapy for malignancy. Thus, febrile neutropenia or pneumonia is a common clinical problem. The usual pathogens in this setting are staphylococci, aerobic gram-negative bacilli, and certain fungi, especially Candida and Aspergillus species (Fig 5) (31).



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  		Figure 5a. Aspergillus fumigatus infection in a 24-year-old man who had severe neutropenia secondary to chemotherapy for acute myelogenous leukemia. (a) Frontal chest radiograph shows ill-defined focal opacity (arrows) in the upper lobe of the right lung. (b) Transverse thin-section CT scan through the hila demonstrates a nodule (arrow) in the upper lobe of the right lung with a surrounding halo of ground-glass opacity.

 


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  		Figure 5b. Aspergillus fumigatus infection in a 24-year-old man who had severe neutropenia secondary to chemotherapy for acute myelogenous leukemia. (a) Frontal chest radiograph shows ill-defined focal opacity (arrows) in the upper lobe of the right lung. (b) Transverse thin-section CT scan through the hila demonstrates a nodule (arrow) in the upper lobe of the right lung with a surrounding halo of ground-glass opacity.

 
Qualitative phagocyte defects result in the same problems that occur with neutropenia: recurrent, severe, and often fatal bacterial infection. The most important primary disorder of phagocytes is chronic granulomatous disease, in which neutrophils and monocytes are unable to kill engulfed catalase-positive microorganisms. The defective phagocytes cannot generate antimicrobial oxygen metabolites. Severe recurrent infection leads to the formation of granulomata throughout the body, especially in the lungs, liver, spleen, and lymph nodes. Chronic granulomatous disease usually manifests in the 1st year of life with recurrent pneumonia, multiple abscesses, and suppurative lymphadenopathy caused by S aureus infection (Fig 6). Serious infection can also be caused by enteric gram-negative bacilli, Nocardia asteroides, and Aspergillus species (32). Job syndrome (ie, hyperimmunoglobulin E syndrome) consists of impaired neutrophil migration, an elevated serum immunoglobulin E level, and mild eosinophilia (33). The patient has multiple staphylococcal abscesses in the skin and lungs.



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  		Figure 6. Recurrent bacterial pneumonia in a 5-month-old infant with chronic granulomatous disease. Frontal chest radiograph shows patchy consolidation (black arrows) in the upper lobes of both lungs and right hilar lymphadenopathy (white arrow).

 
Antibody (B-Cell) Immunity Defects
There are three principal ways that antibodies protect the host against invading microorganisms. The first way is neutralization, which is binding of the antibody to the virus before it can enter the host cell to replicate. Neutralization also works against bacteria that reproduce within cells. The second way is opsonization, in which the antibody coats the surface of the bacterium to stimulate phagocytic cells to ingest and kill it. This is effective against extracellular bacteria—that is, bacteria that multiply outside host cells. The third way is complement activation, which enhances opsonization and can directly kill certain bacteria (34).

Patients with defective antibodies are at risk for pneumonia caused by encapsulated bacteria, which are surrounded by a capsule of polysaccharide that inhibits phagocytosis by macrophages and neutrophils. Opsonization of these bacteria with antibody or complement is necessary before phagocytes can efficiently ingest and kill them. Another infection that occurs occasionally in the setting of antibody deficiency is P carinii pneumonia.

Antibody immunodeficiency can be primary or secondary. Primary antibody deficiencies include X-linked agammaglobulinemia, common variable immunodeficiency, selective immunoglobulin A or immunoglobulin M deficiency, and hyperimmunoglobulin M immunodeficiency. These disorders are characterized by chronic or recurrent pyogenic infection, especially pneumonia, caused by encapsulated bacteria (eg, S pneumoniae, H influenzae, and S aureus) and P aeruginosa (Fig 7). Untreated or recurrent pneumonia may lead to bronchiectasis (35). Secondary antibody deficiency due to B-cell suppression can occur with multiple myeloma, Waldenstrom macroglobulinemia, or chronic lymphocytic leukemia. Secondary deficiencies leave patients susceptible to the same pathogens that can cause recurrent pneumonia in patients with primary antibody deficiencies.



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  		Figure 7. Bacterial pneumonia in a 37-year-old man with common variable immunodeficiency. Frontal chest radiograph shows consolidation and volume loss (arrows) in the lower lobe of the left lung. Sputum cultures were positive for H influenzae.

 
Complement System Defects
The complement system consists of a group of circulating proteins that have immunologic effects when they are activated. Complement activation serves first to opsonize pathogens for phagocytosis; second, to attract inflammatory cells; and third, to kill the pathogen by creating pores in its membrane (34). Because these functions are closely tied to the actions of antibodies, defects in the complement system result in recurrent infections with extracellular bacteria, including encapsulated bacteria.

Primary deficiencies of C3 or C5 predispose the host to infection by encapsulated bacteria (36). Deficiencies of the later complement components (ie, C5b, C6, C7, C8, and C9) cause vulnerability principally to Neisseria gonorrhoeae and Neisseria meningitidis. Secondary (ie, acquired) complement defects are seldom clinically important.

Defects in Cell-mediated (T-Cell) Immunity
T cells are divided into three functional classes: (a) TC (CD8) cells kill host cells infected by pathogens—notably viruses—that replicate within the cytoplasm of host cells; (b) TH1 (CD4) cells activate macrophages and thus allow them to destroy pathogens such as M tuberculosis and P carinii, which inhabit macrophage vesicles; and (c) TH2 (CD4) cells activate B cells to produce antibodies (37). Thus, T lymphocytes are critical in both humoral and cell-mediated immunity, and deficiencies can be devastating. Although patients with cell-mediated immunodeficiency may be susceptible to infections caused by bacteria, fungi, viruses, and protozoa, the predominant pathogens are intracellular (cytoplasmic or vesicular) microorganisms, including mycobacteria, Nocardia asteroides, Legionella species, C neoformans, H capsulatum, C immitis, varicella-zoster virus, herpes simplex virus, cytomegalovirus, Epstein-Barr virus, P carinii, and T gondii (14).

Cell-mediated immunodeficiency can be primary—that is, inherited—or acquired—that is, as a consequence of other disorders or therapy. The primary disorders include DiGeorge and Nezelof syndromes (38,39). Other primary disorders are abnormalities of mixed T- and B-cell immunodeficiency, including severe combined immunodeficiency disease, Wiskott-Aldrich syndrome, and ataxia-telangiectasia (39–41). Patients have severe recurrent pneumonia or sepsis caused by encapsulated bacteria or opportunistic pathogens and, unless they are properly treated, may succumb to overwhelming infection (Fig 8) (30).



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  		Figure 8. Chickenpox pneumonia in a 4-year-old child with severe combined immunodeficiency disease. Frontal chest radiograph shows multiple, ill-defined, and occasionally confluent nodules throughout the lungs.

 
Acquired cell-mediated immunodeficiency is the most common kind of immunodeficiency. It can develop in association with protein-calorie malnutrition, lymphoma, hairy-cell leukemia, or advanced age; and it can be caused by pharmacologic agents or infection with such viruses as cytomegalovirus, Epstein-Barr virus, and, notably, human immunodeficiency virus, which targets CD4 cells (42). Depletion of CD4 cells leaves the patient with AIDS, like the patient with severe combined immunodeficiency disease, prone to recurrent pneumonia from a wide variety of opportunistic pathogens, including P carinii, cytomegalovirus, M tuberculosis, atypical mycobacteria, and pyogenic bacteria (Fig 9).



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  		Figure 9a. P carinii pneumonia in a 36-year-old man with AIDS. (a) Frontal chest radiograph shows diffuse ground-glass opacity with particular concentration in the right lung. (b) Transverse thin-section CT scan of the left lung shows geographic ground-glass opacity (arrow) in both upper and lower lobes.

 


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  		Figure 9b. P carinii pneumonia in a 36-year-old man with AIDS. (a) Frontal chest radiograph shows diffuse ground-glass opacity with particular concentration in the right lung. (b) Transverse thin-section CT scan of the left lung shows geographic ground-glass opacity (arrow) in both upper and lower lobes.

 
Defects Caused by Splenectomy or Hyposplenism
The spleen is the largest single lymphoid organ in the body. It not only filters the blood, but it also produces bacteria-specific opsonizing antibodies, especially immunoglobulin M, and removes antibody-coated bacteria from the bloodstream. Therefore, patients with impaired splenic function, whether from splenectomy or functional hyposplenism, are at risk of developing overwhelming bacterial infections, particularly those caused by encapsulated bacteria, such as S pneumoniae, H influenzae, and S aureus (Fig 10) (43). These infections occur most often in young patients and patients with immunologic disorders, such as idiopathic thrombocytopenic purpura and Hodgkin disease.



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  		Figure 10. Pneumococcal pneumonia in a 5-year-old child with sickle cell anemia. Frontal chest radiograph shows consolidation (arrows) in the lower lobe of the right lung.

 

   DURATION AND SEVERITY OF IMMUNOCOMPROMISE
TOP
 ABSTRACT
 INTRODUCTION
 ENVIRONMENTAL EXPOSURE
 UNDERLYING IMMUNE DEFECT
 DURATION AND SEVERITY OF...
RADIOLOGIC APPEARANCE
 REFERENCES
 
Information about the duration of immunosuppression also is helpful in the differential diagnosis of pneumonia (7, 44,45), because there are distinct periods of susceptibility to specific pathogens after chemotherapy for cancer and after bone marrow or other transplantations (46). In a patient with cancer who has had neutropenia because of cytotoxic chemotherapy, major infection in the 1st few days after therapy is usually caused by ordinary pathogens (eg, gram-negative bacteria or S aureus). However, after 2 weeks of neutropenia, the likelihood of fungal infection, especially Aspergillus-related pneumonia, increases (Fig 11) (7,47).



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  		Figure 11a. Fungal infection in a 62-year-old woman with acute myelogenous leukemia who developed neutropenia after induction chemotherapy. After 16 days of neutropenia, the patient developed a persistent fever. (a) Frontal chest radiograph obtained 2 days after the onset of fever shows focal consolidation (arrow) in the upper lobe of the right lung. (b) Transverse CT scan obtained on the same day as a shows consolidation (arrow) in the posterior segment of the right lung upper lobe. A fumigatus was recovered at thoracoscopic biopsy.

 


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  		Figure 11b. Fungal infection in a 62-year-old woman with acute myelogenous leukemia who developed neutropenia after induction chemotherapy. After 16 days of neutropenia, the patient developed a persistent fever. (a) Frontal chest radiograph obtained 2 days after the onset of fever shows focal consolidation (arrow) in the upper lobe of the right lung. (b) Transverse CT scan obtained on the same day as a shows consolidation (arrow) in the posterior segment of the right lung upper lobe. A fumigatus was recovered at thoracoscopic biopsy.

 
In organ transplant recipients, there are three important periods (7,45). In more than 95% of infections that occur within 1 month after transplantation, the pathogenic organisms are the same as those that afflict noncompromised patients who have undergone thoracic or abdominal operations other than transplantation. Pulmonary infections during this period include aspiration pneumonia caused by oral flora or gram-negative bacilli and septic emboli caused by indwelling intravenous catheters. From 1 to 6 months after transplantation, viruses such as cytomegalovirus, Epstein-Barr virus, and herpes simplex virus are potential causes of lung infection (Fig 12). In addition, because these viruses can impair immunity, they can predispose the host to opportunistic pneumonia caused by P carinii or A fumigatus.



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  		Figure 12. Cytomegalovirus pneumonia in a 34-year-old man who was immunosuppressed because of renal transplantation 3 months earlier and developed shortness of breath and fever. Frontal chest radiograph shows multiple small, ill-defined nodules throughout the lungs.

 
Beyond 6 months after transplantation, patients can be divided into three groups with different infectious problems: The 75%–85% of patients who have adequate graft function develop infection only occasionally, and any infections tend to be those of the general (nontransplant) population; the 5%–10% of patients who have impaired graft function and require high levels of immunosuppressive therapy are at risk for opportunistic infection; and the 5%–10% of patients who have chronic viral infection may develop organ failure or malignancy (7), notably posttransplantation lymphoproliferative disorder, which is almost invariably associated with Epstein-Barr virus infection (48). Posttransplantation lymphoproliferative disorder ranges from mild polyclonal lymphoid hyperplasia to monoclonal proliferation and frank lymphoma.

Infection is more common in lung transplant recipients than in recipients of other organ transplants and is the most common cause of death of these patients. The risk factors include those related to not only the immunosuppressive therapy but also the direct exposure of the graft (the lung) to infectious agents in the atmosphere. Other factors that predispose the host to pneumonia include tissue ischemia during transplantation, which damages the mucosa and erodes its effectiveness as a barrier, impaired cough reflex, and interruption of lymphatic drainage (49). Most transplantation-related pneumonias are caused by bacteria or viruses, but some are caused by fungi or parasites. Bacterial infections, which are most often caused by gram-negative organisms or staphylococci, usually develop in the first 2 months after transplantation (50). Cytomegalovirus infection usually occurs 2–12 weeks after transplantation and may be difficult to distinguish from acute rejection. Pneumonias caused by Candida, Aspergillus, and Cryptococcus species; P carinii; and herpes simplex virus are less common.

In patients with AIDS, the frequency and causes of pneumonia reflect the CD4 cell count, which is an indicator of the severity of immunocompromise (51,52). In patients with CD4 cell counts higher than 200 cells x109/L, bacteria—namely S pneumoniae, H influenzae, S aureus, and M tuberculosis—are the typical causes of pulmonary infection, whereas in patients with CD4 cell counts lower than 200 cells x109/L, P carinii pneumonia and disseminated tuberculosis are common. In patients with very low CD4 cell counts (<100 cells x109/L), opportunistic infection is caused by cytomegalovirus, atypical mycobacteria, or fungi (Fig 13). The CD4 cell count also affects the radiologic features of tuberculosis (16,24). In the early stages of AIDS, the radiologic findings are usually those of reactivation tuberculosis, whereas in patients with advanced immunocompromise, the findings are those of primary tuberculosis.



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  		Figure 13a. P carinii pneumonia and subsequent disseminated cryptococcal infection in a 29-year-old man with AIDS. (a) Frontal chest radiograph shows diffuse low-grade opacity in both lungs. P carinii was identified at bronchoalveolar lavage, at which time the CD4 cell count was 164 cells x109/L. (b) Frontal chest radiograph obtained 1 year later shows a large nodule (black arrow) in the lower lobe of the left lung in association with a miliary pattern in both lungs. Disseminated cryptococcal infection was confirmed at bronchoscopic and transthoracic needle biopsies, at which time, the CD4 cell count was only 82 cells x109/L. Left hilar lymphadenopathy (white arrow) also had developed.

 


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  		Figure 13b. P carinii pneumonia and subsequent disseminated cryptococcal infection in a 29-year-old man with AIDS. (a) Frontal chest radiograph shows diffuse low-grade opacity in both lungs. P carinii was identified at bronchoalveolar lavage, at which time the CD4 cell count was 164 cells x109/L. (b) Frontal chest radiograph obtained 1 year later shows a large nodule (black arrow) in the lower lobe of the left lung in association with a miliary pattern in both lungs. Disseminated cryptococcal infection was confirmed at bronchoscopic and transthoracic needle biopsies, at which time, the CD4 cell count was only 82 cells x109/L. Left hilar lymphadenopathy (white arrow) also had developed.

 

   RADIOLOGIC APPEARANCE
TOP
 ABSTRACT
 INTRODUCTION
 ENVIRONMENTAL EXPOSURE
 UNDERLYING IMMUNE DEFECT
 DURATION AND SEVERITY OF...
 RADIOLOGIC APPEARANCE
REFERENCES
 
Although the radiologic appearance of pulmonary infection in an immunocompromised host is often nonspecific and variable, chest radiography has an important role in diagnosis and management (1,10,53). Detection of a new lung infection may be the reason for admission to the hospital, and follow-up radiography helps monitor the response to treatment. In addition, proper interpretation of radiographic findings can help to narrow the list of potential pathogens and determine the most appropriate diagnostic procedure, such as bronchoalveolar lavage, transbronchial biopsy, percutaneous biopsy, or open biopsy (22,28).

There are three principal patterns of infection in the immunocompromised patient: (a) localized consolidation—patchy, segmental, or lobar, (b) nodules with or without cavitation, and (c) diffuse or interstitial opacity (Table 2) (8,22,45). Localized consolidation most often reflects infection with bacteria (including Legionella pneumophila) or mycobacteria. Single or multiple nodules commonly reflect septic emboli or infection with fungi, Nocardia species, L micdadei, or mycobacteria. Cavitation of nodules or consolidation suggests invasive aspergillosis, Legionella species–related pneumonia, or septic emboli.


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  		TABLE 2. Radiologic Patterns and Rates of Progression of the Pulmonary Conditions
 
Cavitation in aspergillosis reflects angioinvasion, which leads to hemorrhagic infarction and lung necrosis. The resultant cavity may have a crescent of air between the contracted necrotic mass and the outer wall of surrounding lung tissue. This "air-crescent" sign is common with invasive aspergillosis, but it is a late manifestation that occurs when the neutrophil count has already begun to recover. The survival rate is higher for patients who develop the sign than for those who do not (54).

The diffuse pattern is typically caused by P carinii, cytomegalovirus, or varicella-zoster virus and less frequently by bacteria, mycobacteria, or fungi. Miliary dissemination is one pattern of diffuse disease. It is most commonly caused by tuberculosis or fungal infections such as histoplasmosis or cryptococcosis.

The differential diagnosis of these radiographic patterns in immunocompromised patients includes noninfectious diseases. Pulmonary infarction and lymphoma can cause consolidation; metastatic tumor, lymphoma, and posttransplantation lymphoproliferative disorder can cause nodules; and nonspecific interstitial pneumonitis, lymphocytic interstitial pneumonia, radiation or drug injury, hemorrhage, pulmonary edema, Kaposi sarcoma, and lymphangitic carcinomatosis can cause diffuse disease (8,22).

Combined with the radiographic pattern, the rate of progression of the lung abnormalities and symptoms is a clue to their cause (Table 2) (28,45). An acute process that evolves in a day may be bacterial pneumonia, pulmonary infarction, edema, or hemorrhage. A subacute or chronic process that evolves over days or weeks may be infection caused by P carinii, viruses, mycobacteria, or fungi. A chronic process that develops over weeks or months may be tumor, drug reaction, or radiation injury.

Chest radiography has limited sensitivity for the detection of early infection in immunocompromised patients, and findings are often nonspecific (55–57). Another confounding factor is that a patient with neutropenia who has pneumonia may have delayed or unusually subtle radiographic findings in the lungs, which reflects the depressed inflammatory response (28). In addition, the radiograph may be normal in 10% of patients with AIDS who have P carinii pneumonia. The radiograph may also be normal early in the course of drug-induced lung disease (11,56).

CT helps overcome some of the limitations of chest radiography. The CT features of common pulmonary infections in immunocompromised patients have been described, and the usefulness of CT, especially thin-section CT, has been demonstrated (17–22,58–63). CT is particularly useful in depicting early infection in immunocompromised patients. In febrile neutropenia, thin-section CT may depict 20% more pneumonias and demonstrate pneumonia about 5 days earlier than do chest radiographs (64). Thus, the use of thin-section CT might be considered in all cases of febrile neutropenia with negative chest radiographs. Proposed roles for thin-section CT in immunocompromised patients include (a) demonstrating abnormalities in patients with clinically suspected pulmonary disease but normal or questionable radiographic findings, (b) providing greater confidence in the diagnosis in patients with nonspecific radiographic findings, and (c) determining the optimal type and site of biopsy (57).

As described earlier, there are relatively specific CT findings with certain infections in immunocompromised patients, so a confident diagnosis is possible in some clinical settings. Such infections include septic emboli, tuberculosis, invasive aspergillosis, and P carinii pneumonia. Septic emboli are characterized by multiple cavitating nodules with visible feeding vessels, and they usually occur in patients who are intravenous drug abusers or who have an indwelling intravenous catheter (Fig 4) (57,58). CT also depicts the characteristic appearance of tuberculous lymphadenopathy—low attenuation in the centers and enhancement of the margins (Fig 14) (56,65). Lymphadenopathy from cryptococcosis or histoplasmosis also can have low attenuation in the centers at CT, but lymphadenopathy from Kaposi sarcoma or lymphoma usually does not (66). Although the halo sign can be found with other conditions, such as candidiasis, cytomegalovirus, and Kaposi sarcoma, a nodule or mass surrounded by ground-glass opacity (the halo sign) strongly suggests invasive aspergillosis when it occurs in a patient with neutropenia who is receiving cytotoxic therapy and broad-spectrum antibiotics (Fig 5) (18,67). In a patient with AIDS who has hypoxia, the presence of ground-glass opacity in a perihilar or geographic distribution at CT is highly suggestive of P carinii pneumonia (Fig 9) (56,61).



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  		Figure 14. Tuberculous mediastinal lymphadenitis in a 34-year-old man with AIDS. Transverse CT scan shows right paratracheal lymphadenopathy (arrows) with characteristic low attenuation in the center and enhancement of the rim.

 
Bronchiectasis occurs in some patients with congenital or acquired immune defects, including AIDS, and is the result of chronic or recurrent infection (35,68,69). The predisposing factor is usually antibody immunodeficiency, which creates vulnerability to encapsulated bacteria (Fig 15) (69,70). Similarly, in patients with AIDS, bronchiectasis is most commonly caused by bacteria (71). Thus, the detection of bronchiectasis in an immunocompromised patient suggests a susceptibility to bacterial infection and may indicate the need for prophylactic antibiotics, postural drainage, or surgical resection (69). Thin-section CT is the standard diagnostic examination for bronchiectasis.



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  		Figure 15a. Bronchiectasis in a 21-year-old man with X-linked agammaglobulinemia. (a) Frontal and (b) lateral chest radiographs show diffuse cystic bronchiectasis (arrows) in both lungs. This patient had undergone left lower lobectomy because of hemoptysis caused by bronchiectasis.

 


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  		Figure 15b. Bronchiectasis in a 21-year-old man with X-linked agammaglobulinemia. (a) Frontal and (b) lateral chest radiographs show diffuse cystic bronchiectasis (arrows) in both lungs. This patient had undergone left lower lobectomy because of hemoptysis caused by bronchiectasis.

 
In summary, prompt and accurate diagnosis of pulmonary infection helps to reduce morbidity and mortality in the immunocompromised host. Because so many organisms can affect these patients and radiologic findings are often nonspecific for pneumonias caused by different microorganisms, radiologists often have difficulty in interpreting imaging studies. However, because specific pathogens are likely to manifest in specific clinical settings, correlating the radiologic findings with the clinical setting is very helpful in narrowing the list of potential pathogens and in increasing diagnostic confidence.


   FOOTNOTES
 
Abbreviation: AIDS = acquired immunodeficiency syndrome


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 ABSTRACT
 INTRODUCTION
 ENVIRONMENTAL EXPOSURE
 UNDERLYING IMMUNE DEFECT
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