key: cord-0059553-6tlhswkr
authors: Sollini, Martina; Mariani, Giuliano
title: Nuclear Medicine Imaging of Lung Infection
date: 2021-01-23
journal: Radionuclide Imaging of Infection and Inflammation
DOI: 10.1007/978-3-030-62175-9_13
sha: b5cd48783cbc3e36d597a9c0db4633bf1429586e
doc_id: 59553
cord_uid: 6tlhswkr

Acute or chronic infection of the upper or lower respiratory tract caused by microorganisms (bacteria, viruses, fungi, or parasites) causes discomfort and affects the day-to-day life of patients and can become severely complicated. The diagnosis of lung infection is generally based on clinical findings associated with the detection of parenchymal infiltrate at chest X-ray or CT scan. However, in some instances, radiological imaging alone cannot distinguish an acute exacerbation from sequela of a prior infection. Nuclear medicine imaging techniques have been extensively used in patients with lung infection, mostly for TB-associated or HIV-associated infections. Single-photon emitting agents used for identifying lung infection include (67)Ga-citrate, (111)In-oxine-leukocytes, (99m)Tc-HMPAO-leukocytes, preferably employing SPECT/CT imaging. More recently, the use of [(18)F]FDG for PET imaging (currently PET/CT) has been steadily growing and is now the preferred radionuclide imaging modality not only for identifying sites of lung infection but also for assessing the efficacy of therapy, especially in TB infection and in HIV-associated infections. PET/CT with [(18)F]FDG is also being increasingly used in patients with ventilator-associated pneumonia.

• To become familiar with the pathophysiology and clinical presentation of the most frequent and potentially severe forms of lung infection • To understand the principles of X-ray-based and radionuclide-based imaging for diagnosing/identifying sites of lung infection • To learn the role of single-photon emitting agents for imaging lung infection: 67 Ga-citrate, 111 In-oxineleukocytes, 99m Tc-HMPAO-leukocytes

• To learn the role of the positron emitting agent, [ 18 F] FDG for imaging lung infection • To learn the most common patterns of radionuclide imaging in patients with different forms of lung infection caused by Streptococcus pneumoniae [2, 3] . Symptoms, treatment, prevention, and prognosis differ depending on the cause of infection (bacterial, viral, fungal, or parasitic), the type of infection (acquired in a community environment, hospital, or nursing home), and the patient's status (immunocompetent or immunocompromised) [4] . The main signs and symptoms of lung infections are fever, shortness of breath, dry or productive coughing, fatigue (particularly in case of infection caused by Candida), production of mucus, tightness, pressure, and pain in the chest that worsens when breathing in deeply or coughing.

In case of infection with methicillin-resistant Staphylococcus aureus (MRSA), concomitant skin or urinary infection may also be present [1] . The diagnosis of lung infection is generally based on clinical findings associated with the detection of parenchymal infiltrate at chest X-ray or CT scan [5] . High-resolution CT is the imaging method of choice to evaluate diffuse lung and small airway diseases [6] , and it reliably detects infection also in the presence of an underlying chronic lung disease (such as bronchiectasis) [7, 8] . However, in some instances, radiological imaging alone cannot distinguish an acute exacerbation from sequela of a prior infection.

Cultures of both blood and sputum often identify the microorganism responsible for the infection, so that the most adequate antibiotic therapy can be planned, although falsepositive as well as false-negative findings have been reported [9] [10] [11] . When infection from Mycobacterium tuberculosis (TB) or HIV-associated infection is suspected, specific recommendations and guidelines should be followed for a correct diagnosis [12] .

Nuclear medicine imaging techniques have been extensively used in patients with lung infection, mostly for TB-associated or HIV-associated infections [13] [14] [15] [16] . Following seminal work by Levenson et al. in patients with Pneumocystis cari-nii pneumonia [17] , increased uptake of 67 Ga-citrate has been described in many conditions (besides Pneumocystis carinii pneumonia), such as abscess, TB or mycotic lesions, pneumoconiosis, and infection from cytomegalovirus, although false-negative results have been reported [16, [18] [19] [20] [21] . One of the most important non-oncologic clinical applications of 67 Ga-citrate scintigraphy of the lungs is early detection of opportunistic infection; this imaging technique enables to detect diffusely increased uptake of the radiopharmaceutical in the lung even when the chest X-ray is normal [17, 22] . In this regard, although 67 Ga-citrate scintigraphy for pulmonary diseases is hampered by several drawbacks (such as its relative lack of specificity, delay between tracer injection and imaging time, and suboptimal imaging characteristics) [23] , its sensitivity is higher than that of a chest X-ray in the detection of pulmonary TB [24] and of lung involvement from paracoccidioidomycosis [25] . In patients with TB, the intensity of pulmonary uptake of 67 Ga-citrate is directly related to the inflammation level and to the burden of Mycobacterium tuberculosis (assessed by semi-quantitation of sputum acid-fast bacillus) [26] . 67 Ga-citrate scintigraphy and high-resolution CT in sputum smear-negative patients with active TB perform equally well in the noninvasive diagnosis of TB, with high sensitivity (100% versus 93%) and specificity (83% versus 100%) [27] . Sequential 67 Ga-citrate scans are also helpful to monitor the response to treatment in patients with TB, chronic lung disease, or AIDS, in whom radiological findings can be equivocal because of the confounding effects of either chronic pulmonary fibrotic changes or poor inflammatory reaction due to immunodeficiency [28] . 67 Ga-citrate scintigraphy has also been employed to determine the most appropriate duration of treatment with different anti-TB regimens [26] . Pulmonary lesions in active TB compared to nontuberculous mycobacterial infection in acid-fast bacilli smearpositive non-HIV-infected patients have also been successfully evaluated with 67 Ga-citrate scintigraphy, demonstrating the usefulness of this technique in predicting active pulmonary TB in acid-fast bacilli smear-positive patients [29] .

Scintigraphy with autologous leukocytes labeled with either 111 In-oxine (most recently reviewed in [30] ) or 99m Tc-HMPAO [31] detects infection with high diagnostic accuracy (sensitivity up to 95% for soft tissue infections). However, there have been only a limited number of investigations on the usefulness of this imaging method for diagnosing lung infections [32] . In patients with focal pulmonary bacterial infections, scintigraphy with labeled leukocytes is more sensitive than 67 Ga-citrate scintigraphy [33] , and it is often positive before changes can even be seen on a plain chest X-ray [34] . Equivocal results have instead been reported for radiolabeled leukocyte scintigraphy in patients with bronchiectasis [32, 35] .

• Acute or chronic infection of the upper or lower respiratory tract due to microorganisms causes discomfort, affects the day-to-day life of patients, and can become severely complicated. • The diagnosis of lung infection is generally based on clinical findings associated with detection of parenchymal infiltrate at chest X-ray or CT scan. • However, in some instances, radiological imaging alone cannot distinguish an acute exacerbation from sequela of a prior infection.

It should be noted that interpretation of the images obtained with labeled leukocyte scintigraphy of the lungs can be problematic, because of interference from blood pool activity in the heart and great vessels and pulmonary blood background and because of the physiologic leukocyte margination along the walls of small pulmonary vessels early after reinfusion of labeled leukocytes. Furthermore, nonspecific inflammatory changes associated with congestive heart failure or with acute respiratory distress syndrome may mimic diffuse or focal pulmonary uptake in a similar manner as observed in patients with lung infection, making the distinction between infection and inflammation difficult [23, 36] . Nonetheless, if pulmonary accumulation of radiolabeled leukocytes is graded according to soft tissue, rib, and liver activities, specificity increases up to 100% for pulmonary and pleural infections, and a negative scan rules out pulmonary infection with high confidence [37] . Furthermore, in the current clinical practice, these methodological limitations can be largely overcome by SPECT/CT imaging.

A pathophysiologic limitation of radiolabeled leukocyte scintigraphy can be seen in lung infections where leukocyte infiltrations are less significant, as it occurs in granulomatous or nonpyogenic infections [23, 34, 38] . For similar reasons, labeled leukocyte scintigraphy is not routinely used for the characterization of TB patients since variable results (especially in the evaluation of small infectious foci) have been reported, probably due to the predominant type of cells involved (lymphocytes and macrophages, rather than granulocytes) [38] . Finally, in patients with AIDS radiolabeling of autologous leukocytes for scintigraphy can be technically unfeasible because of low white blood cell counts.

Scintigraphy with 67 Ga-citrate or with 99m Tc-HMPAOlabeled leukocytes has been used in patients with occult sepsis in intensive care units. Although 67 Ga-citrate scintigraphy reliably identified extra-site(s) of infection, it did not accurately identify ventilator-associated pneumonia [39] . Instead, 99m Tc-HMPAO-leukocyte scintigraphy demonstrated good sensitivity (95-96%) and specificity (84-91%) in detecting the occult source of sepsis [40, 41] . It should be noted, however, that in this critical clinical scenario, scintigraphy with 67 Ga-citrate or with labeled leukocytes has definite disadvantages (i.e., either amount of blood needed to harvest leukocytes for labeling or long time span between administration and scintigraphy) with respect to [ 18 F]FDG PET/CT (see further below).

Although both 201 Tl-chloride and 111 In-DTPA-octreotide have been employed to distinguish benign lung lesions (i.e., infection) from cancer, their clinical application in infection per se has been very limited [23] , except for scanty reports concerning patients with fungal infection [42] or with TB infection [43] . In TB infection, 201 Tl-chloride scintigraphy seems to perform better than 67 Ga-citrate scintigraphy (sensitivity 88% versus 83%, specificity 82% versus 60%, accu-racy 85% versus 75%) [44] . Similar results have been reported for 99m Tc(V)-DMSA, suggesting that scintigraphy with this imaging agent might perform better than 67 Ga-citrate scintigraphy for assessing the overall burden and activity of TB [45] . Good diagnostic performance in patients with pulmonary TB has been reported also for 99m Tc-sestamibi and 99m Tc-tetrofosmin, with high sensitivity (96% and 94%, respectively) and specificity (86% and 88%, respectively) [46] .

Although not specific for infection, PET imaging with [ 18 F] FDG can be particularly useful to identify site(s) and extent of infectious disease or to guide biopsy in doubtful cases [22, [47] [48] [49] [50] , even before the appearance of radiological abnormalities [51] . Different patterns of [ 18 F]FDG uptake have been reported in patients with lung infections. Bacterial, viral, fungal, or parasitic pneumonia may present with either a nodular or diffuse pattern of uptake [51] [52] [53] [54] [55] [56] [57] , while TB may appear as lung or lymphatic patterns [14, 58] , and cryptococcosis may present with a solitary pulmonary/scattered nodular or bronchopneumonic/single mass pattern [59] .

A positive [ 18 F]FDG PET scan should be interpreted with caution when evaluating pulmonary nodules, especially in patients with predisposing factors for nontuberculous mycobacterial infections [60, 61] . In non-HIV-infected patients suffering from TB, [ [63, 64] , which is also related to viral load [65] . In this regard, it has been reported that dualphase [ 18 F]FDG PET can distinguish inflammation from malignancy [64] .

[ 18 F]FDG PET/CT has a promising role also in the diagnosis and identification of other HIV-associated infections (i.e., Pneumocystis pneumonia) [66, 67] , as well as in fever of unknown origin (FUO) [68] [69] [70] . However, quite often increased [ 18 F]FDG uptake due to infection cannot be distinguished from increased uptake due to malignancy [71] .

Similarly, when evaluating bronchiectasis in HIV-positive patients, [ 18 F]FDG PET/CT did not reliably predict disease exacerbation [72] . Nonetheless, although [ 18 F]FDG PET (currently PET/CT) alone does not have a definite role in identifying the cause of abnormalities, in patients with HIV it can be useful to detect or exclude the presence of abnormal [ 18 F]FDG uptake; furthermore, combining the CT anatomic landmarks with the PET findings allows the guidance of biopsy when histopathologic diagnosis is needed and therefore impacts on patient's management and clinical decisionmaking [73] .

The use of [ 18 F]FDG PET can be helpful for assessing response to therapy in a variety of nonmalignant disorders and has therefore been proposed for evaluating the efficacy of therapy also in infectious diseases [74] , especially anti-TB therapy [15] . The role of [ 18 F]FDG PET in monitoring the efficacy of therapy has been described also for patients with invasive candidiasis [54] , cryptococcosis [59] , aspergillosis [75] , and Pneumocystis carinii pneumonia [66] .

In over 85% of the cases, nosocomial pneumonia is associated with the use of respiratory assistance procedures, such as endotracheal tubes, tracheostomy/tracheotomy, nasal masks, and nebulization treatment. Ventilator-associated pneumonia (VAP), the most common nosocomial infection in the intensive care unit [76] [77] [78] , occurs in 8-28% of patients receiving prolonged mechanical ventilation (>48 h) [79] . Also tracheostomy is associated with VAP [80] , whereas nasotracheal intubation is more frequently associated with sinusitis [81] and otitis. Infection is caused by continuous tidal movements of air during artificial respiration, which determines some sort of "milking" into the adjacent structures along the nasopharyngeal path of microorganisms that cover the endotracheal tube. When suspecting VAP, endotracheal aspirates or samples collected bronchoscopically should be obtained for microbiological culture [82] . Although sensitive, chest X-ray is typically nonspecific [83] , since lobar or subsegmental atelectasis, acute respiratory distress syndrome, alveolar hemorrhage, and/or infarction may be mistaken for pneumonia. Chest CT frequently shows pulmonary abnormalities consistent with atelectasis, pleural effusion, and infiltrates in mechanically ventilated patients. The metabolic information provided by [ 18 F]FDG PET has a definite added value in these patients; in fact, detecting increased metabolism in these lesions can be crucial in deciding whether or not the abnormalities found on the CT scan are actually sites of infection causing the symptoms and signs in patients [84] . An overall good diagnostic performance of [ 18 F]FDG PET/CT in mechanically ventilated patients with suspected lung infection has been reported, with 100% sensitivity, 79% specificity, and 91% overall accuracy; because of such extremely high sensitivity, a normal [ 18 F]FDG PET/ CT scan could reliably rule out the presence of a focal active infectious process, thus excluding the need for prolonged antibiotic therapy or drainage [84] .

The recent worldwide medical emergency associated with the pandemic caused by the Covid-19 (or SARS-CoV-2) virus has opened new opportunities for the use of [ 18 F]FDG PET/CT in patients with either asymptomatic or symptomatic infection with the virus [85] [86] [87] [88] [89] [90] [91] [92] . Although in many of the cases reported so far, detection of increased [ 18 F]FDG uptake in areas exhibiting the CT pattern of interstitial pneumonia has been purely incidental, and it can reasonably be assumed that the use of [ 18 F]FDG PET/CT will provide helpful information to monitor the course of disease-and possibly to assess the efficacy of therapy.

Finally, PET imaging with other agents other than [ 18 F] FDG, such as [ 11 C]choline and 18 F-fluoroethyltyrosine, has also been explored in patients with lung infections [93] ; in this regard, in patients with pulmonary TB and atypical lung mycobacterial infection, the uptake of [ 18 F]FDG at the infections sites has been reported to be higher than uptake of [ 11 C] choline [94] .

Acknowledgments Special thanks are due to Drs. Elena Lazzeri and Annibale Versari for providing images that have been included in this chapter. (Figs. 13.1, 13.2, and 13. 3) 

Background A 20-year-old man without previous history of illness or allergies was stabbed in the back. No signs or symptoms of TB were present. Chest X-ray and CT findings were: lung wound due to stab on the back and areas with opacification of air spaces within the lung parenchyma (in the left inferior lobe) associated with pleural effusion (bleeding) and left hilar and mediastinal lymphadenopathy. Passive atelectasis.

Lung neoplasm and granulomatous/infectious process.

[ 18 F]FDG 3.7 MBq/kg.

PET/CT protocol acquisition: scan was performed for 60-120 min p.i. Acquisition of the scan included: (1) scout view (120 kV, 10 mA) in order to define the limits of body to explore, (2) whole-body CT scan (from skull base to proximal femur: 140 kV, 80 mA), and (3) craniocaudal whole-body PET (2D, 3-5 min/field of view, FOV). Images were reconstructed with soft tissue and lung filters using iterative OSEM, with and without attenuation correction using the low-dose transmission CT scan (Figs. 13.13, 13.14, and 13.15).

The conclusion of these findings is based on analyzing the characteristics of the morphometabolic changes, considering the young age of the patient. PET without CT cannot distinguish between tuberculosis and lung neoplasm, but CT findings of the hybrid PET/CT acquisition support the diagnosis of tuberculosis. The cutaneous purified protein derivative (PPD) test was positive (18 mm), and sputum smears were positive for Mycobacterium tuberculosis. The patient was treated with tuberculostatics. 

An 80-year-old man previously submitted to axillobifemoral vascular prosthesis presented with fever and cough. Abnormalities in the chest X-ray and CT: opacity in the superior lobe of the right lung of equivocal interpretation. Bronchoscopy with bronchoalveolar washing was inconclusive. Due to persistence of fever associated with suspected vascular periprosthetic infection, [ 18 F]FDG PET/CT was performed (Fig. 13.16 ). Since the PET/CT findings were inconclusive, 99m Tc-HMPAO-leukocyte scintigraphy was performed (Figs. 13.17, 13.18 and 13.19 ). 99m Tc-HMPAOleukocyte scintigraphy ruled out ongoing active infection. 

Lung neoplasm and infectious process.

[ 18 F]FDG, 3.7 MBq/kg; 99m Tc-HMPAO-leukocytes, 640 MBq.

PET/CT acquisition protocol: the scan was performed at 60-120 min p.i. Acquisition of the scan included: (1) scout view (120 kV, 10 mA) in order to define the limits of the body to explore, (2) whole-body CT scan (from skull base to proximal femur: 140 kV, 80 mA), and (3) whole-body PET (3D, 3 min/FOV). 99m Tc-HMPAO-leukocyte scintigraphy: whole-body scan was performed 30 min p.i. Planar anterior and posterior acquisitions of the chest were acquired at 30 min, 4 h, and 24 h p.i. and SPECT/CT imaging of the abdomen was acquired 3 h, whereas SPECT/CT imaging of the chest was acquired at 24 h.

This clinical case highlights the different specificity of [ 18 F] FDG PET/CT and of scintigraphy with radiolabeled leukocytes. [ 18 F]FDG allows the identification of inflammatory processes as well as infection; radiolabeled leukocytes allow the identification of only neutrophil-mediated processes, which are present in the majority of infections. 

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Rhinovirus infections in the upper airway

Epidemiology and risk of pulmonary disease

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Imaging techniques in the examination of the distal airways: asthma and COPD

Airflow obstruction in bronchiectasis: correlations between computed tomography features and pulmonary function test

Imaging of pulmonary infection

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Introducing the new BTS guideline: management of non-tuberculous mycobacterial pulmonary disease (NTM-PD)

British Thoracic Society guidelines for the management of non-tuberculous mycobacterial pulmonary disease (NTM-PD)

Geneva: World Health Organization

The role of nuclear medicine in the investigation of patients with AIDS

Monitoring response to therapy

Past and future of Ga-citrate for infection and inflammation imaging

Abnormal pulmonary gallium accumulation in P. carinii pneumonia

67 Ga lung scan: an aid in the differential diagnosis of pulmonary embolism and pneumonitis

The use of gallium-67 in pulmonary disorders

Gallium-67 citrate imaging studies of the lung

Gallium and infection

Molecular imaging of pulmonary inflammation and infection

Gallium and other agents in diseases of the lung

Gallium scanning in the 'new' tuberculosis

The role of gallium-67 scan in defining the extent of disease in an endemic deep mycosis, paracoccidioidomycosis: a predominantly multifocal disease

Monitoring treatment responses in patients with pulmonary TB using serial lung gallium-67 scintigraphy

The role of 67 gallium scintigraphy and high resolution computed tomography as predictors of disease activity in sputum smear-negative tuberculosis

The value of gallium-67 scanning in pulmonary tuberculosis

The role of gallium-67 scintigraphy in comparing inflammatory activity between tuberculous and nontuberculous mycobacterial pulmonary diseases

111 Indium white blood cell scan (indium leukocyte imaging, indium-111 scan)

The utility of [ 99m Tc]HMPAO-leukocytes for imaging infection

99m Tc-HMPAO labeled white blood cell scintigraphy in the diagnosis and monitoring of response of the therapy in patients with active bronchiectasis

Pulmonary applications of nuclear medicine

Imaging of intrathoracic disease with indium-111-labeled leukocytes

Indium-111-labeled granulocyte accumulation in respiratory tract of patients with bronchiectasis

Detection of abnormalities in febrile AIDS patients with In-111-labeled leukocyte and Ga-67 scintigraphy

Diagnostic value of lung uptake of indium-111 oxine-labeled white blood cells

Detection of subacute infectious foci with indium-111-labeled autologous leukocytes and indium-111-labeled human nonspecific immunoglobulin G: a prospective comparative study

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Influenza-like infection can result in diffuse fluorodeoxyglucose uptake in the lungs

Patterns of pulmonary tuberculosis on FDG-PET/CT

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Two cases with solitary pulmonary nodule due to nontuberculous mycobacterial infection showing intense 18 F-fluorodeoxyglucose uptake on positron emission tomography scan

Impact of FDG PET on the management of TBC treatment: a pilot study

Malignant solid tumor, HIV infection and tuberculosis in children: an unholy triad

Demonstrations of AIDS-associated malignancies and infections at FDG PET-CT

Positron emission tomography in patients suffering from HIV-1 infection

FDG-PET imaging in pneumocystis carinii pneumonia

Pneumocystis carinii pneumonia on F-18 FDG PET

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Fever of unknown origin: the value of FDG-PET/CT

The value of 18 F-FDG-PET/CT in identifying the cause of fever of unknown origin (FUO) and inflammation of unknown origin (IUO): data from a prospective study

PET/CT scanning with a high HIV/ AIDS prevalence

Positron emission tomography in the prediction of inflammation in children with human immunodeficiency virus related bronchiectasis

FDG PET/CT in patients with HIV

Clinical utility of FDG PET and PET/CT in non-malignant thoracic disorders

Successful treatment of invasive aspergillosis in chronic granulomatous disease by bone marrow transplantation, granulocyte colony-stimulating factormobilized granulocytes, and liposomal amphotericin-B

Ventilator-associated pneumonia in the ICU

Ventilator associated pneumonia in children

Ventilator-associated pneumonia: new definitions

Risk factors for ICU-acquired pneumonia

Predisposing factors for nosocomial pneumonia in patients receiving mechanical ventilation and requiring tracheotomy

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Clinical diagnosis of ventilator associated pneumonia revisited: comparative validation using immediate post-mortem lung biopsies

The radiologic diagnosis of autopsy-proven ventilator-associated pneumonia

F-18-fluorodeoxyglucose positron emission tomography combined with CT in critically ill patients with suspected infection

18 F-FDG PET/CT findings of COVID-19: a series of four highly suspected cases

FDG PET/CT of COVID-19

18 F-FDG PET/CT and COVID-19

The potential added value of FDG PET/CT for COVID-19 pneumonia

18 F-FDG uptake in asymptomatic SARS-CoV-2 (COVID-19) patient, referred to PET/ CT for non-small cells lung cancer restaging

Incidental findings suggestive of Covid-19 in asymptomatic patients undergoing nuclear medicine procedures in a high prevalence region

Nuclear medicine in SARS-CoV-2 pandemia: 18 F-FDG-PET/CT to visualize COVID-19

FDG-PET/CT findings highly suspicious for COVID-19 in an Italian case series of asymptomatic patients

A multicenter clinical trial on the diagnostic value of dual-tracer PET/CT in pulmonary lesions using 3′-deoxy-3′-18 F-fluorothymidine and 18 F-FDG

Uptake rates of 18 F-fluorodeoxyglucose and 11 C-choline in lung cancer and pulmonary tuberculosis: a positron emission tomography study