DOI: 10.1148/rg.226025038
(Radiographics. 2002;22:1385-1393.)
© RSNA, 2002
Pulmonary Activity on Labeled Leukocyte Images: Physiologic, Pathologic, and Imaging Correlation1
Charito Love, MD,
Patrick Opoku-Agyemang, MD,
Maria B. Tomas, MD,
Paul V. Pugliese, RT,
Kuldeep K. Bhargava, PhD and
Christopher J. Palestro, MD
1 From the Division of Nuclear Medicine, Long Island Jewish Medical Center, 270-05 76th Ave, New Hyde Park, NY 11040. Presented as an education exhibit at the 2001 RSNA scientific assembly. Received February 28, 2002; revision requested April 2; final revision received May 8; accepted May 14. Address correspondence to C.L. (e-mail: love@lij.edu).
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Abstract
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Accurate interpretation of labeled leukocyte images requires knowledge of pulmonary labeled leukocyte uptake: its prevalence and patterns and its correlation with technical, physiologic, and pathologic conditions as well as with other imaging findings. Images obtained shortly after injection of labeled cells are characterized by diffuse pulmonary activity, which decreases over time, until about 4 hours after injection when it becomes indistinguishable from background activity, remaining constant thereafter. Focal pulmonary uptake that is segmental or lobar in appearance is most often associated with bacterial pneumonia. Focal pulmonary uptake that is not segmental or lobar results from technical problems during labeling or reinfusion and is not usually associated with infection. Diffuse pulmonary uptake on images obtained more than 4 hours after reinjection of labeled cells is associated with a variety of pathologic conditions, some of the more common being opportunistic infection, radiation pneumonitis, pulmonary drug toxicity, adult respiratory distress syndrome, and sepsis. However, this pattern is almost never seen in bacterial pneumonia. When pulmonary uptake patterns are analyzed and correlated with the clinical situation, labeled leukocyte scintigraphy can provide useful information about pulmonary disease.
© RSNA, 2002
Index Terms: Lung, infection, 60.21 • Lung, radionuclide studies, 60.1216, 60.1217
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LEARNING OBJECTIVES
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After reading this article and taking the test, the reader will be able to:
- Describe the normal pulmonary uptake pattern of labeled leukocytes over the first 24 hours after injection.
- State the significance of segmental-lobar pulmonary activity on labeled leukocyte images.
- Name at least three causes of diffuse pulmonary activity on labeled leukocyte images.
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Introduction
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The role of labeled leukocyte imaging in the detection of infection has been extensively investigated and reported. However, the utility of this technique in pulmonary infection has received less attention than has its utility in other areas of the body. This is probably because the diagnosis of pneumonia can be rapidly and accurately made with radiographs and sputum cultures and because pulmonary uptake of labeled cells does not necessarily indicate the presence of infection (1–3). Accurate interpretation of images requires knowledge of pulmonary uptake of labeled leukocytes: its prevalence, patterns, and correlation with technical, physiologic, and pathologic conditions, as well as with findings at other imaging modalities such as radiography and computed tomography (CT). Such information is important in preventing technical conditions or physiologic events from being erroneously attributed to pathologic conditions and vice versa. In this article, we describe and illustrate both normal and abnormal pulmonary uptake patterns at labeled leukocyte scintigraphy. We also discuss various causes of abnormal uptake patterns, including opportunistic infection, radiation pneumonitis, pulmonary drug toxicity, sepsis, adult respiratory distress syndrome (ARDS), hemodialysis, and technical causes. Although the data and images presented in this article were obtained with indium-111–labeled mixed autologous leukocytes, they are also applicable to technetium-99m–labeled leukocyte imaging.
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Normal Pulmonary Uptake Patterns
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The normal pulmonary uptake pattern of labeled leukocytes varies with the time interval between injection of labeled cells and imaging. Immediately after injection, there is pooling of labeled leukocytes within the lungs. The labeled cells gradually leave the lungs during the first few hours after injection. Early scintigrams are characterized by diffuse pulmonary activity, which decreases over time until by about 4 hours after injection it becomes indistinguishable from background activity (Fig 1).
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Figure 1. Normal pulmonary uptake. Sequential anterior images of the chest obtained after injection of In-111-labeled autologous leukocytes demonstrate diffuse bilateral pulmonary activity that decreases in intensity over time. At 24 hours, pulmonary activity is indistinguishable from surrounding soft-tissue activity.
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This phenomenon is likely due to several factors. Normal neutrophils, which are assumed to be in a nonactivated state, "stutter" or "hop" through the lungs; that is, they spend more time in contact with the pulmonary endothelium than they do in the systemic vascular bed. One reason for this is that the mean driving pressure across the pulmonary circulation is lower than that in the systemic circulation. Cell size is another factor. Neutrophils, which are about 8 µm in diameter, must pass through the pulmonary capillaries, which have an average diameter of 5.5 µm. This movement requires cytoskeletal deformation of the cells (4). During the labeling procedure, neutrophils are activated, either partially (primed) or fully. Activated cells become stiffer due to changes in cytoskeletal assembly, are less easily deformed, and consequently pass more slowly through the pulmonary vessels. Activated neutrophils also adhere to the pulmonary capillaries for a longer period than do nonactivated neutrophils. Finally, there is evidence that the in vitro labeling procedure itself causes prolonged pulmonary transit of neutrophils, presumably as a result of cell trauma during the labeling process (4,5).
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Abnormal Pulmonary Uptake Patterns
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Some investigators have reported that labeled leukocyte imaging is neither sensitive nor specific for detecting pulmonary infection (3,6). This is true when only the presence of pulmonary activity is considered without analyzing the pattern of pulmonary uptake or considering the patient being studied. Important information can be obtained if pulmonary uptake patterns are analyzed and the study is interpreted in the context of the patient being examined.
Focal Pulmonary Uptake
Focal, or localized, pulmonary uptake of labeled leukocytes has been described in numerous pathologic conditions, although its significance has been somewhat controversial. In one series, 13 patients had localized pulmonary uptake of labeled leukocytes. All 13 patients had pneumonitis, and all had radiographic abnormalities corresponding to the scintigraphic abnormalities (7). In another series, however, focal pulmonary uptake was associated with infection in only 14 of 27 cases (52%) (1). Other causes of focal uptake in this series included atelectasis, pulmonary embolism, congestive heart failure, ARDS, and aspiration pneumonia. Recent data obtained at our own institution suggest that the significance of focal pulmonary uptake can be more precisely determined by characterizing uptake as segmental-lobar or nonsegmental. When focal uptake was classified as positive for infection without regard to pattern, the sensitivity of the study was 92% and the positive predictive value was 79%. When only focal uptake that was segmental or lobar in appearance was classified as positive, the positive predictive value rose to 92% and the sensitivity remained unchanged (Figs 2, 3) (8).
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Figure 2a. Focal pulmonary uptake in a patient with bacteremia. (a) Labeled leukocyte image shows nonsegmental uptake in the left midlung. Activity in the liver, spleen, and bone marrow is normal and represents physiologic uptake. (b) Chest radiograph shows normal findings. The patient had no respiratory symptoms. The final diagnosis was septic arthritis of the left knee. Nonsegmental pulmonary activity on labeled leukocyte images is not associated with pneumonia. (Fig 2b reprinted, with permission, from reference 8.)
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Figure 2b. Focal pulmonary uptake in a patient with bacteremia. (a) Labeled leukocyte image shows nonsegmental uptake in the left midlung. Activity in the liver, spleen, and bone marrow is normal and represents physiologic uptake. (b) Chest radiograph shows normal findings. The patient had no respiratory symptoms. The final diagnosis was septic arthritis of the left knee. Nonsegmental pulmonary activity on labeled leukocyte images is not associated with pneumonia. (Fig 2b reprinted, with permission, from reference 8.)
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Figure 3a. Focal pulmonary uptake in a woman with left lower lung pneumonia. (a) Labeled leukocyte image shows intense segmental accumulation. (b) Chest radiograph obtained the same day is unremarkable. This pattern is the exception; in patients with pneumonia, usually both the radiograph and the labeled leukocyte image are abnormal.
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Figure 3b. Focal pulmonary uptake in a woman with left lower lung pneumonia. (a) Labeled leukocyte image shows intense segmental accumulation. (b) Chest radiograph obtained the same day is unremarkable. This pattern is the exception; in patients with pneumonia, usually both the radiograph and the labeled leukocyte image are abnormal.
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The segmental-lobar pattern of pulmonary uptake has been observed, in the absence of pneumonia, in patients with cystic fibrosis. Typically, this uptake is intense, multifocal, and bilateral. This appearance is due to accumulation of labeled leukocytes in pooled secretions in bronchiectatic regions of the lungs (Fig 4) (7,9). It is important to recognize that, in patients with cystic fibrosis, pulmonary uptake of labeled leukocytes, even when intense and segmental-lobar in appearance, cannot automatically be equated with infection.
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Figure 4a. Segmental-lobar pattern of pulmonary uptake in a 15-year-old boy with cystic fibrosis but stable respiratory status. (a) Labeled leukocyte image shows intense, multifocal, bilateral pulmonary uptake. (b) Chest radiograph demonstrates diffuse fibrotic changes, large bronchiectatic cavities, and airspace infiltrates. (c) CT scan shows a honeycomb pattern with severe bronchiectatic changes. The chest radiograph and CT scan were unchanged from previous images.
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Figure 4b. Segmental-lobar pattern of pulmonary uptake in a 15-year-old boy with cystic fibrosis but stable respiratory status. (a) Labeled leukocyte image shows intense, multifocal, bilateral pulmonary uptake. (b) Chest radiograph demonstrates diffuse fibrotic changes, large bronchiectatic cavities, and airspace infiltrates. (c) CT scan shows a honeycomb pattern with severe bronchiectatic changes. The chest radiograph and CT scan were unchanged from previous images.
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Figure 4c. Segmental-lobar pattern of pulmonary uptake in a 15-year-old boy with cystic fibrosis but stable respiratory status. (a) Labeled leukocyte image shows intense, multifocal, bilateral pulmonary uptake. (b) Chest radiograph demonstrates diffuse fibrotic changes, large bronchiectatic cavities, and airspace infiltrates. (c) CT scan shows a honeycomb pattern with severe bronchiectatic changes. The chest radiograph and CT scan were unchanged from previous images.
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Although nonsegmental uptake is usually solitary, multiple bilateral small, round, nonsegmental foci of activity are occasionally encountered and should not be confused with septic emboli. This phenomenon is probably the result of clumping of the cells that occurs either during the labeling process itself or during reinfusion (1,10). Some investigators have suggested that, in patients with suspected pulmonary inflammatory disease, chest images should be obtained soon (perhaps within 1 hour) after the administration of labeled leukocytes to determine whether any cell clumps are present. Such early images may facilitate the interpretation of chest images obtained the following day (11,12).
Areas of increased opacity or attenuation on chest radiographs or CT scans are not always due to pneumonia. The presence of pulmonary edema, atelectasis, and pleural effusion or thickening can confound the diagnosis of pneumonia (13). Under these circumstances, labeled leukocyte imaging may be especially useful. In immunocompetent patients, a normal labeled leukocyte image in the setting of an abnormal chest radiograph excludes pneumonia with a high degree of certainty (Fig 5) (3,8).
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Figure 5a. Bronchiolitis obliterans in a 78-year-old patient with cough and fever. (a) Chest radiograph reveals bilateral pleural effusion with minimal infiltrates in the right upper lobe, findings that raised the possibility of pneumonia. (b) Labeled leukocyte image demonstrates normal findings. Results of lung biopsy were consistent with bronchiolitis obliterans. There was no evidence of pneumonia. In the setting of an abnormal chest radiograph, a negative labeled leukocyte image rules strongly against bacterial pneumonia.
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Figure 5b. Bronchiolitis obliterans in a 78-year-old patient with cough and fever. (a) Chest radiograph reveals bilateral pleural effusion with minimal infiltrates in the right upper lobe, findings that raised the possibility of pneumonia. (b) Labeled leukocyte image demonstrates normal findings. Results of lung biopsy were consistent with bronchiolitis obliterans. There was no evidence of pneumonia. In the setting of an abnormal chest radiograph, a negative labeled leukocyte image rules strongly against bacterial pneumonia.
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Diffuse Pulmonary Uptake
Diffuse, bilateral pulmonary uptake on images obtained more than 4 hours after reinjection of labeled cells is associated with a variety of conditions. However, it is only rarely seen in bacterial pneumonia (7,8).
Opportunistic Infection.—
Opportunistic infections such as Pneumocystis carinii pneumonia may appear as diffusely increased activity on labeled leukocyte images, and when this finding is observed in an immunocompromised individual, the possibility of opportunistic infection must be considered. Although opportunistic infections may be detected with labeled leukocyte imaging, the procedure is considerably less sensitive than gallium imaging, which is the procedure of choice for this indication (Fig 6) (14).
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Figure 6a. Opportunistic pneumonia in a patient with leukemia who was admitted to the hospital because of fevers. Findings at chest radiography and CT were negative. (a) Labeled leukocyte image is negative. (b) Gallium image shows moderately intense, diffuse pulmonary activity. The patient responded to treatment for opportunistic pneumonia. Labeled leukocyte imaging is not sensitive for detecting opportunistic pulmonary infection, and gallium imaging remains the radionuclide procedure of choice for this purpose.
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Figure 6b. Opportunistic pneumonia in a patient with leukemia who was admitted to the hospital because of fevers. Findings at chest radiography and CT were negative. (a) Labeled leukocyte image is negative. (b) Gallium image shows moderately intense, diffuse pulmonary activity. The patient responded to treatment for opportunistic pneumonia. Labeled leukocyte imaging is not sensitive for detecting opportunistic pulmonary infection, and gallium imaging remains the radionuclide procedure of choice for this purpose.
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Radiation Pneumonitis.—
Radiation therapy with a dosage greater than 30 Gy can produce a pneumonitis that is characterized by destruction of pneumocytes and alveolar and capillary walls (15). This entity manifests as diffuse pulmonary activity on labeled leukocyte images (7).
Pulmonary Drug Toxicity.—
Various medications can incite a hypersensitivity pneumonitis characterized by acute inflammation consisting of neutrophils or eosinophils. Diffuse pulmonary labeled leukocyte activity has been observed in patients treated with bleomycin, methotrexate, and paclitaxel (Taxol; Bristol-Myers Squibb, Princeton, NJ) (Fig 7) (16).
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Figure 7a. Pulmonary drug toxicity in a 57-year-old patient with rheumatoid arthritis who was undergoing treatment with methotrexate. (a) Labeled leukocyte image shows diffusely increased activity in both lungs. (b) Chest radiograph is normal.
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Figure 7b. Pulmonary drug toxicity in a 57-year-old patient with rheumatoid arthritis who was undergoing treatment with methotrexate. (a) Labeled leukocyte image shows diffusely increased activity in both lungs. (b) Chest radiograph is normal.
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Sepsis.—
The phenomenon of pulmonary leukocytic sequestration in sepsis has been the subject of much debate and research (17,18). It is believed that neutrophils are activated by various cytokines, which are released peripherally in response to an infection. These activated neutrophils tend to pool in the pulmonary circulation because it is more difficult for them to undergo the cytoskeletal deformation required to maneuver through the pulmonary circulation. In addition, the pulmonary vascular endothelial cells themselves become activated, which causes increased adherence of leukocytes to the cell walls. If the inflammatory process is arrested by the body’s regulatory defense mechanisms, exudation of inflammatory cells into the lung parenchyma is minimized and vascular damage is avoided (19). Diffuse pulmonary uptake of labeled leukocytes in patients with sepsis has recently been described (8). These patients, who were successfully treated for infection, had normal chest radiographs and no respiratory symptoms at the time of the radionuclide study. Furthermore, they did not subsequently develop respiratory complications (Fig 8). Thus, diffuse pulmonary accumulation of labeled leukocytes in patients with sepsis should not automatically be equated with infection.
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Figure 8a. Sepsis in a 65-year-old patient with a hepatic abscess. (a) Labeled leukocyte image shows diffuse lung activity. Diffuse pulmonary uptake of labeled leukocytes occurs in patients with sepsis and cannot automatically be equated with infection. (b) Chest radiograph obtained the same day shows clear lungs.
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Figure 8b. Sepsis in a 65-year-old patient with a hepatic abscess. (a) Labeled leukocyte image shows diffuse lung activity. Diffuse pulmonary uptake of labeled leukocytes occurs in patients with sepsis and cannot automatically be equated with infection. (b) Chest radiograph obtained the same day shows clear lungs.
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ARDS.—
In overwhelming sepsis, unregulated cytokine production and activated neutrophil recruitment cause increased permeability of the alveolar-capillary membrane, resulting in pulmonary edema and migration of activated leukocytes into the lung parenchyma. Activated neutrophils contain cytotoxic products that are injurious to the lung parenchyma (20). When the lung parenchyma is sufficiently damaged, the patient may exhibit signs and symptoms of pulmonary insult (ARDS). The characteristic radiographic appearance is that of patchy, bilateral alveolar infiltrates (21). Diffuse bilateral pulmonary activity is typically present on labeled leukocyte images (Fig 9) (22).
Hemodialysis.—
Diffuse pulmonary activity on labeled leukocyte images has also been described in patients undergoing hemodialysis. Complement activation after hemodialysis leads to leukocytic and vascular endothelial activation, resulting in increased pulmonary sequestration of leukocytes (23).
Technical Causes.—
Diffuse pulmonary activity can occasionally be due to technical problems (eg, incomplete separation of leukocytes from red cells and platelets) or hemolysis. The presence of concomitant blood pool activity, especially cardiac blood pool activity on 24-hour images, indicates that the pulmonary uptake is due to technical causes (Fig 10) (5,8).
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Figure 10a. Pulmonary activity related to a failure in the labeling process. (a) Labeled leukocyte image demonstrates diffuse lung uptake as well as cardiac blood pool activity. (b) Chest radiograph shows normal findings. The patient had no evidence of respiratory tract infection.
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Figure 10b. Pulmonary activity related to a failure in the labeling process. (a) Labeled leukocyte image demonstrates diffuse lung uptake as well as cardiac blood pool activity. (b) Chest radiograph shows normal findings. The patient had no evidence of respiratory tract infection.
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Conclusions
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Although it is neither presently nor likely to become a primary diagnostic method, labeled leukocyte imaging can contribute useful information about pulmonary infection. Focal pulmonary uptake, when segmental or lobar in configuration, is almost always indicative of bacterial pneumonia. In contrast, nonsegmental pulmonary uptake is usually related to technical factors and does not indicate infection. Diffuse pulmonary activity, which may be due to numerous causes, is not associated with pyogenic lung infection. Careful correlation with the patient’s history should clarify the cause in individual cases.
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Footnotes
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Abbreviation: ARDS = adult respiratory distress syndrome
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[Abstract]
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Abstract
LEARNING OBJECTIVES
