Übersicht – Thoraxchirurgie

What Is the Clinical Value of PET/CT in the Diagnosis of Pulmonary Nodules? Hat das PET‑CT bei der Diagnostik des Lungenrundherds eine Bedeutung?

Authors

C. Lohrmann, W. A. Weber

Affiliation

Molecular Imaging and Therapy Service, Memorial Sloan-Kettering Cancer Center, New York, New York, United States

Key words " FDG l " PET/CT l " Imaging procedures l " pulmonary nodules l

Abstract

Zusammenfassung

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The noninvasive diagnostic workup of solitary pulmonary nodules (SPNs) continues to be a challenge for radiologists and nuclear medicine physicians. Morphological evaluation is useful to differentiate between benign and malignant SPNs, but there is a considerable overlap between the benign and the malignant features, resulting in a large fraction of morphologically indeterminate SPNs. Integrated PET/CT with the glucose analogue 18F-fluorodeoxyglucose (FDG PET/CT) can simultaneously evaluate morphological characteristics, anatomic location and metabolic status of SPNs. FDG PET/CT has been shown to result in an overall improved accuracy for the detection of malignant SPNs. In addition, it is the most accurate technique for the staging of malignant SPNs. On the other hand, there are many causes for false positive or false negative FDG PET/CTs. Therefore, FDG PET/CT cannot replace histological evaluation of SPNs, but can be clinically helpful in specific subgroups of patients with SPNs. The goal of this review is to provide an overview of the literature on PET/CT imaging in SPNs and to describe several clinical scenarios for the use of FDG PET/ CT in SPNs.

Die nicht invasive Diagnostik von solitären pulmonalen Rundherden ist noch immer eine Herausforderung für Radiologen und Nuklearmediziner. Anhand von morphologischen Kriterien können manche benigne von malignen Rundherden unterschieden werden. Es verbleibt aber eine große Gruppe von Rundherden, die weder sicher benigne noch sicher maligne Charakteristika aufweisen. Die PET/CT mit dem Glukoseanalogon Fluordeoxyglukose (FDG) ermöglicht es, in einer Untersuchung die Morphologie, anatomische Lokalisation und Stoffwechselaktivität von Rundherden zu beurteilen. Eine große Zahl von klinischen Studien hat gezeigt, dass die FDG-PET/CT die nicht invasive Diagnostik von Lungenrundherden verbessert. Die FDG‑PET/CT ist auch das bildgebende Verfahren mit der höchsten diagnostischen Genauigkeit für das Staging von malignen Lungenrundherden. Es sind jedoch auch verschiedene Ursachen für falsch-positive und falsch-negative FDG‑PET/CT Befund bekannt. Die FDG‑PET/CT kann deshalb die histologische Sicherung von Lungenrundherden nicht ersetzen. In bestimmten Subgruppen von Patienten kann die FDG‑PET/CT aber klinisch relevante Informationen liefern. Ziel dieser Arbeit ist es, einen Überblick über die aktuelle Literatur zur FDG‑PET/CT beim solitären pulmonalen Rundherd zu geben und verschiedene klinische Szenarien zu beschreiben, in denen die FDG‑PET/CT klinisch eingesetzt werden kann.

Introduction

should be avoided as much as possible in patients with benign nodules [1]. Ideally, imaging should also detect metastatic disease: lymph node or systemic metastases of primary lung cancers, but also malignancies outside of the chest with a solitary pulmonary metastasis. An SPN is defined as a single, well-defined pulmonary opacity with a diameter of < 3 cm, sur-

Schlüsselwörter " FDG l " PET/CT l " Bildgebung l " Lungenrundherd l

Bibliography DOI http://dx.doi.org/ 10.1055/s-0033-1360182 Zentralbl Chir 2014; 139: 108–113 © Georg Thieme Verlag KG Stuttgart · New York · ISSN 0044‑409X Correspondence Prof. Dr. Christian Lohrmann, MD Molecular Imaging and Therapy Service Memorial Sloan-Kettering Cancer Center 1275 York Ave, Box 77 New York, NY 10065 Tel.: + 1 21 26 39 73 73 Fax: + 1 21 27 17 32 63 United States [email protected]

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Noninvasive, accurate differentiation between benign and malignant SPNs continues to be an important clinical challenge. The primary goal is to reliably identify all patients with operable lung cancer in order not to delay potentially curative surgery. At the same time invasive procedures

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vide a brief overview of the published literature and to discuss how an FDG PET/CT can be integrated in diagnostic strategies for the evaluation of SPNs.

Rationale for the Use of FDG PET/CT in SPNs

Fig. 1 a and b 56-year-old male with an 8 mm well-defined solid nodule in the right lower lobe on CT (a). PET image (b) demonstrates an intense FDG uptake of the nodule, consistent with a malignant nodule.

rounded by normal lung tissue and not associated with atelectasis or adenopathy [2, 3]. More than 150 000 SPNs are detected yearly in the United States, predominantly by incidental findings due to the increased use of multidetector computed tomography (MDCT) and low-dose chest CT screening examinations [4, 5]. Approximately 30–50% of these nodules turn out to be malignant [3–7]. According to the American Cancer Society approximately 20 % to 30 % of lung cancers will be diagnosed as an SPN [8–10] and these patients typically have the most favorable prognosis of all newly diagnosed lung cancers. Because SPNs are so common, an ideal imaging test for differentiation of benign and malignant nodules should not be too expensive and at the same time it should be highly sensitive and specific for malignant SPNs. High sensitivity is a prerequisite because lung cancer progresses quickly, and the frequency of metastatic disease is closely correlated with the size of the primary tumor. A delay in the diagnosis of a malignant SPN because of a false negative imaging test can therefore have grave consequences. Since benign SPNs are so frequent, imaging also needs to be highly specific in order to be cost-effective. Noninvasive evaluation of SPNs is performed by chest radiography, CT, magnetic resonance imaging (MRI) and positron emission tomography (PET). Morphological evaluation is helpful to differentiate pulmonary nodules, but there is a considerable overlap between benign and malignant features and a large percentage of nodules need to be classified as “indeterminate” [11]. CT has a high sensitivity for the detection and can accurately localize SPNs, but the reported specificity and overall accuracy are highly variable [12, 13]. Studies have shown promising results using different MRI sequences in evaluating the SPN, but the technology is not used for this purpose in clinical routine so far [14]. Many studies have demonstrated the potential value of using functional parameters in characterizing SPNs using PET with the glucose analogue 18F-Fluorodeoxyglucose (18F‑FDG) PET and more recently PET/CT [15–18]. The synergy of anatomic and metabolic imaging with PET/CT results, overall, in an improved accuracy in the evaluation of SPNs [19]. Overall, the use of FDG PET and PET/CT in SPNs has been extensively studied for approximately 25 years. The aim of this review is to summarize the rationale for using FDG PET/CT in SPNs, pro-

Accelerated glycolysis is part of the metabolic reprogramming of cancer cells and increasingly seen as a requirement for neoplastic transformation and progression. Overexpression of the glucose transporters, hexokinase and other enzymes involved in the uptake and metabolism of glucose are well documented in lung cancer [20]. The biological characteristics of lung cancer cells are the basis for PET imaging with the glucose analog 18F‑FDG. The first clinical PET scanners had only a limited axial field of view and required long acquisition times. A typical PET study of the chest lasted 40 min or longer. Technical improvements and specifically the development of integrated PET/CT scanners have changed this substantially. Current PET/CT scanners allow for whole-body imaging studies in 30 min or less. Thus PET can now also provide comprehensive information about N- and M-stages in patients with malignant nodules. In addition, modern PET/CT scanners typically combine PET with a state-of-the-art multidetector CT and thus allow for the acquisition of high quality CT images. Malignant SPNs typically demonstrate intense focal FDG uptake " Fig. 1 a, b), whereas FDG uptake by benign nodules is similar (l to normal lung. The degree of FDG uptake can be evaluated qualitatively or quantitatively using the standard uptake value (SUV). SUV represents the ratio of the image-derived FDG concentration in the SPN, and the (hypothetical) concentration for a homogenous distribution of FDG in the body. The higher the SUV, the higher is the glucose metabolic rate of a nodule [21]. SUVs can be measured by automated procedures and are therefore not observer dependent, in contrast to morphologic characteristics of nodules.

Overview of the Literature of FDG PET and PET/CT in SPNs !

Several meta-analyses have demonstrated that FDG PET provides a high sensitivity, specificity and accuracy for the characterization of SPNs [15, 22–24]. Gould et al. reported a sensitivity of 94.2 % and a specificity of 83.3 % in a metaanalysis of 13 studies evaluating 450 patients with nodules greater than 8 mm in diameter [15]. Wahidi et al. found a pooled sensitivity of 87 % and specificity of 83 % for FDG PET in their meta-analysis [22]. A meta-analysis published in 2008 yielded a sensitivity of 95 %, a specificity of 82 %, a positive predictive value of 91% and a negative predictive value of 90% [23]. Vansteenkiste et al. presented a meta-analysis of 12 studies with 624 patients, demonstrating a sensitivity of 96 %, specificity of 79 %, and accuracy of 91% [24]. Fletcher et al. compared PET with CT and they found that the sensitivities to aid detection of a malignant nodule were similar (91.7 % vs. 95.6 %), but the specificity of PET scans was superior to CT scans (82.3 % vs. 40.6 %) [25]. The average nodule size in this study was 16 mm. Several PET studies have pointed out that FDG PET is more specific than CT for the diagnosis of benign lesions, but that FDG PET imaging becomes less accurate with decreasing lesion size [26]. Since the introduction of integrated PET/CT, hybrid imaging has improved the capabilities to characterize SPNs compared to PET

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and CT alone. Detailed morphologic characteristics and functional information are available with PET/CT, thus enhancing diagnostic accuracy. Yi et al. conducted a retrospective analysis of 119 patients, 79 of whom had malignant SPNs, and found a sensitivity, specificity, and accuracy of 96 %, 88 %, and 93 %, respectively, with integrated PET‑CT imaging. This accuracy was higher than that of contrast-enhanced CT. The NPV of PET/CT scanning was 92% [19]. Kim et al. found a high accuracy for the detection and characterization of SPNs (sensitivity of 97 %, specificity of 85 %, accuracy of 93 %) using PET/CT [18]. The nodule size varied between 7–30 mm in that study. In this study, PET/CT performed significantly better than PET alone with respect to accuracy, sensitivity, and specificity. PET/CT was also more specific than CT alone. In a retrospective study of 100 patients the sensitivity values for CT, PET, and integrated PET‑CT scans were 82 %, 88%, and 88 %, respectively, whereas the specificity values were 66 %, 71 %, and 77 %, respectively [27]. In this study, PET/CT imaging provided a significantly better specificity than a CT or PET scan alone, and had a positive predictive value (PPV) of 72 % and a negative predictive value (NPV) of 90 %. The authors drew the conclusion that the higher specificity of PET‑CT imaging was due to the ability to discard false positive PET uptake on the basis of CT scan morphology showing benign patterns. Chang et al. pointed out that granulomatous disease has an impact on positive PET results when studies are performed in areas of endemic disease [28]. Kagna et al. reported that integrated FDG PET/low-dose CT improves the noninvasive characterization of pulmonary nodules in patients at high risk of lung cancer, mainly due to a higher specificity and accuracy [17]. FDG PET/CT has shown a lower sensitivity for the diagnosis of adenocarcinoma with a lepidic pattern, particularly for lesions pre" Fig. 2 a, b) [29]. In a study conducted by senting as pure GGNs (l Chun et al. evaluating 68 subsolid nodules, the reported sensitivity for diagnosing malignancy was 62%, whereas specificity was 80 % [30]. In that study, FDG PET paradoxically demonstrated higher SUV values in inflammatory nodules compared with malignant nodules. Similar results were found by Tsushima et al. In their study, an SUV of more than 1.5 was suggestive of a benign etiology in SPNs with subsolid components [31]. The authors concluded that when FDG PET/CT reveals a significant uptake in SPNs with non-solid components, the lesion may have potentially benign characteristics and should be followed up with serial CT scans. When FDG uptake is not observed in SPNs with nonsolid components, the findings are more suggestive of malignancy and should be resected. Because of the low FDG uptake of these tumors and the low frequency of nodal and distant metastases in lung cancers presenting as predominantly ground glass nodules, FDG PET/CT is also generally not helpful for tumor staging [32]. Other frequent reasons for false negative PET/CT studies are carcinoid tumors and mucinous adenocarcinomas [27, 28]. False positive results are generally due to infections or inflammatory conditions, such as granulomatous diseases [33]. When PET was approved in Germany as an imaging modality for the characterization of lung nodules, in particular in patients with a high perioperative risk and when an invasive diagnostic evaluation of lung nodules is not considered possible, one of the major arguments which led to this decision was the high accuracy of PET for the evaluation of SPNs [15]. The intention was to avoid unnecessary interventions in that patient group. Overall it was concluded that the benefit and medical necessity of an additional PET examination for the characterization of an SPN was sufficiently documented. The prior mentioned results in the liter-

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Fig. 2 a and b 67-year-old women with a subsolid nodule in the left upper lobe on CT (a). Fused PET/CT image (b) demonstrate only a mild FDG uptake of the nodule, but malignancy cannot be excluded.

ature over the last years not only confirm but also provide even a higher diagnostic accuracy for the evaluation of SPN, mainly due to the technological advances of the PET systems and the development of hybrid PET/CT imaging modalities. This led to an implementation of PET/CT in the daily clinical routine for the workup of SPNs.

Diagnostic CT Versus Low-Dose CT as Part of FDG PET/CT Studies in SPNs !

The CT part of a PET/CT study can be performed in various ways [34]. Generally, a CT in expiration or during shallow breathing is required for attenuation correction of the PET images. This can be performed as a low-dose CT without intravenous contrast or as a diagnostic CT with intravenous contrast for evaluation of the hilar and mediastinal structures. In addition, it is straightforward to perform a breathhold CT immediately before or after the PET/CT image. Since the CT component of the PET/CT is identical to current multidetector CTs, the quality of the diagnostic CTs can be identical to stand-alone CT scans. However, this requires a close collaboration between nuclear medicine and diagnostic radiology in order to ensure that the appropriate protocols are followed for imaging acquisition and reconstruction. For the evaluation of an indeterminate SPN in an adult patient, we favor the application of intravenous contrast material with diagnostic CT parameters in expiration, serving both as an attenuation correction and diagnostic scan. An additional low-dose chest CT of the lung in deep inspiration is obtained after the whole-body PET/CT acquisition. This approach ensures a comprehensive morphologic characterization of SPNs. Using modern dose modulation techniques, the additional radiation exposure as compared to a typical lowdose CT with a fixed tube current is modest and usually well justified by the additional information provided by CT, especially in the patient populations where PET/CT is most clinically useful (see below).

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Assessment of FDG Avidity Using FDG PET/CT in SPNs !

The best way to evaluate FDG avidity and the criteria to define a pulmonary nodule as malignant on FDG PET/CT are currently not yet standardized. One method is to conduct a semiquantitative measurement of the SUV level. Another way is to grade the FDG uptake by visual analysis. This is usually performed by using a grading system that compares the SUV of the SPN to the FDG uptake of the mediastinal blood pool. Both methods are frequently performed and provide similar results [35–37].

Radiation Exposure of FDG PET/CT !

The radiation exposure of a dedicated whole-body FDG‑PET imaging study is moderate (about 6–7 mSv) compared to an integrated whole-body diagnostic CT scan (about 7–26 mSv) [38]. A wholebody low-dose CT solely for attenuation correction and anatomic localization of PET pathologies accounts for approximately 2– 4 mSv [39]. The effective dose for a diagnostic chest CT scan is approximately 8 mSv [40].

Recommendations for the Evaluating the SPNs Using FDG PET/CT !

The American College of Chest Physicians has recently released new guidelines for the evaluation of SPNs [41]. Lesion size is an important factor for the use of FDG PET/CT in SPNs. Smaller nodules are less likely malignant, but small malignant nodules are also more frequently false negative on FDG PET/CT because the spatial resolution of the PET scanner is limited. The guidelines by the American College of Chest Physicians therefore distinguish between nodules that are equal or smaller and those larger than 8 mm [41]. This diameter is to some extent arbitrary because the probability of malignancy and the sensitivity of PET continuously increase with lesion size. Nevertheless, it is helpful for clinical decision making to separate SPNs in these two categories. It is also helpful to distinguish solid nodules from subsolid nodules, which are categorized as pure ground glass or partly solid on CT. Therefore algorithms for the evaluation of lesions equal or smaller than approximately 8 mm, greater than approximately 8 mm and subsolid nodules require different imaging follow-up regimens [41].

Before making the decision whether or not to use FDG PET/CT imaging, it is essential to estimate the probability that an SPN is malignant, because the pretest probability is critical when interpreting further diagnostic tests [41–43]. Several quantitative models have been developed for this purpose, which take into account patient age, history of cancer, smoking status, nodule size, morphology and location [43–48]. In nodules < 8 mm in maximum diameter the sensitivity of PET is low because the spatial resolution of PET in clinical routine is about 5–10 mm. While PET can detect lesions that are beyond " Fig. 3 a, b, c), the true concentration of its spatial resolution (l FDG in these nodules will be significantly underestimated and only highly metabolically active nodules will be positive on the PET images [49]. Therefore a negative PET scan does not reliably exclude malignancy for nodules less than 8 mm in diameter. A positive scan in patients with a solid SPN, however, indicates the need for a tissue diagnosis. If a malignancy has been diagnosed by histopathology, FDG uptake in the primary tumor has been shown to even be inversely correlated with survival [50, 51]. Solid SPNs with a low or intermediate (5–65 %) pretest probability for malignancy, a diameter of at least 8 mm and a negative PET scan can be followed by active surveillance with serial CT chest scans (3, 6, 12, and 24 months) according to the American College of Chest Physicians clinical guidelines to confirm a benign diagnosis [41]. If a solid, indeterminate nodule with a high-pretest probability of malignancy (> 65 %) is detected, PET/CT is unlikely to add relevant clinical information. A positive study will have no impact on patient management and a negative study will not allow to reliably exclude malignancy. FDG PET/CT may be, however, indicated for pretreatment staging among those patients with nodules in whom malignancy is strongly suspected. Our recommendations for a management algorithm using PET/CT in the evaluation of " Fig. 4. SPNs > 8 mm are summarized in l Subsolid nodules are classified as partly solid or pure ground glass on CT. A PET‑CT scan may be considered if the lesion is partly-solid and the diameter of the solid component is at least 8 mm in diameter. Due to the high false negative results, an FDG PET/CT scan should be interpreted with caution if the SPN is pure ground-glass or if the solid component is small. If the pretest probability of the subsolid nodule is high, the patient should proceed directly to biopsy if clinically practicable; in these cases, FDG PET/CT can be used to direct lesion biopsy and to identify which parts of the nodule are metabolically active and most likely to

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Fig. 3 a to c 57-year-old male with a history of non-small cell lung cancer and a 4-mm solid nodule in the middle lobe on CT (a). Due to the small size and the proximity to a vessel, the nodule could easily be missed on CT. PET (b) and fused PET/CT (c) images demonstrate an intense FDG uptake of the nodule, suspicious for a metastasis.

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Fig. 4 Management algorithm for the use of PET/ CT in the evaluation of SPNs > 8 mm.

yield a sufficient histopathologic result [41, 52]. However, lack of uptake on PET images should not be a reason to postpone biopsy in these patients.

Conclusion !

Integrated FDG PET/CT imaging can simultaneously show the morphologic characteristics, anatomic location, and metabolic status of SPNs and has been demonstrated to be clinically useful in indeterminate nodules of at least 8 mm in diameter with a low to moderate pretest probability of malignancy (5–65 %). A recommendation for an FDG PET/CT scan for smaller nodules should take into account that the sensitivity decreases for smaller pulmonary nodules resulting in a higher rate of false negative results. In subsolid SPNs FDG PET/CT scanning may be considered if the solid component is at least 8 mm in diameter. While these categories of SPNs are useful for clinical decision making one should keep in mind that the sensitivity of PET gradually decreases with lesion diameter and that false negative results can occur in larger nodules with specific histologic characteristics (e.g., mucinous carcinomas). Also size measurements can be variable, especially for ground glass or spiculated lesions.

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CT in the diagnosis of pulmonary nodules?

The noninvasive diagnostic workup of solitary pulmonary nodules (SPNs) continues to be a challenge for radiologists and nuclear medicine physicians. M...
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