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ORIGINAL ARTICLE
Year : 2017  |  Volume : 54  |  Issue : 1  |  Page : 271-275
 

Solitary pulmonary nodule evaluation in regions endemic for infectious diseases: Do regional variations impact the effectiveness of fluorodeoxyglucose positron emission tomography/computed tomography


1 Department of Nuclear Medicine and Molecular Imaging, Tata Memorial Centre, Mumbai, Maharashtra, India
2 Department of Surgical Oncology, Tata Memorial Centre, Mumbai, Maharashtra, India
3 Department of Radiation Oncology, Tata Memorial Centre, Mumbai, Maharashtra, India
4 Department of Medical Oncology, Tata Memorial Centre, Mumbai, Maharashtra, India
5 Department of Chest Medicine, Tata Memorial Centre, Mumbai, Maharashtra, India

Date of Web Publication1-Dec-2017

Correspondence Address:
Dr. N C Purandare
Department of Nuclear Medicine and Molecular Imaging, Tata Memorial Centre, Mumbai, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0019-509X.219563

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 » Abstract 

BACKGROUND: Fluorodeoxyglucose positron emission tomography/computed tomography (FDG-PET/CT) has become a preferred imaging modality for the evaluation of solitary pulmonary nodule (SPN), particularly in the developed world. Since FDG can concentrate in infective/inflammatory lesions, the diagnostic utility of FDG-PET can be questioned, particularly in regions endemic for infectious decisions. AIM: To evaluate the accuracy of FDG-PET/CT in evaluation of SPNs in a population endemic for infectious disease and to assess if regional variations have an impact on its effectiveness. MATERIALS AND METHODS: All patients who underwent an FDG/PET-CT with a clinico-radiological diagnosis of SPN categorized as indeterminate were included. Based on a maximum standardized uptake values (SUVmax) cut-off of 2.5, lesions were classified as benign (<2.5) or malignant (>2.5) and compared with gold standard histopathology. The diagnostic accuracy of PET-CT to detect malignancy was calculated. On the basis of final histopathology, lesions were grouped as (a) malignant nodules (b) infective/granulomatous nodules with a specific diagnosis and (c) nonspecific inflammatory nodules. The SUVmaxbetween these groups was compared using nonparametric statistical tests. RESULTS: A total of 191 patients (129 males, 62 females) with a median age of 64 years (range: 36–83) were included. Totally, 144 nodules (75.3%) were malignant and 47 were benign (24.7%). Adenocarcinoma (n = 84) was the most common malignancy. Tuberculosis (n = 16) and nonspecific infections (n = 24) were the two most common benign pathologies. There was a significant overlap in the metabolic uptake of malignant (median SUVmax-11.2, range: 3.3–34.6) and tuberculous nodules (median SUVmax-10.3, range: 2.7–22.5) with no statistically difference between their SUVmaxvalues (P = 0.43). The false-positive rate was 65.2% and the false-negative rate was 5.5%. The sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of FDG-PET/CT for detecting malignancy were 94.4%, 34.7%, 81.9%, 66.6%, and 79.5%, respectively. CONCLUSIONS: Though FDG-PET scans show a very high sensitivity for malignant nodules, it has a high false-positive rate and reduced specificity when characterizing SPNs in an infectious endemic region. Physicians must be aware of this limitation in the workup of lung nodules, and regional variations must be considered before further management decisions are taken.


Keywords: Fluorodeoxyglucose positron emission tomography, infections, solitary pulmonary nodule, tuberculosis


How to cite this article:
Purandare N C, Pramesh C S, Agarwal J P, Agrawal A, Shah S, Prabhash K, Karimundackal G, Jiwnani S, Tandon S, Rangarajan V. Solitary pulmonary nodule evaluation in regions endemic for infectious diseases: Do regional variations impact the effectiveness of fluorodeoxyglucose positron emission tomography/computed tomography. Indian J Cancer 2017;54:271-5

How to cite this URL:
Purandare N C, Pramesh C S, Agarwal J P, Agrawal A, Shah S, Prabhash K, Karimundackal G, Jiwnani S, Tandon S, Rangarajan V. Solitary pulmonary nodule evaluation in regions endemic for infectious diseases: Do regional variations impact the effectiveness of fluorodeoxyglucose positron emission tomography/computed tomography. Indian J Cancer [serial online] 2017 [cited 2020 Mar 31];54:271-5. Available from: http://www.indianjcancer.com/text.asp?2017/54/1/271/219563



 » Introduction Top


The term solitary pulmonary nodule (SPN) has been specifically defined in medical literature as “a single, spherical opacity of <3 cm diameter surrounded by normal lung parenchyma.”[1] The majority of SPNs do not produce clinical symptoms and are detected incidentally. Detection of an SPN on imaging is a cause for concern as 30–40% of them can be malignant.[2],[3] One of the challenges for the imaging specialist is to characterize SPN on the basis of its radiological appearance. Various morphological features have been described to differentiate malignant from benign nodules particularly on computed tomography (CT) scans. Owing to overlapping imaging features of benign and malignant nodules on CT scan, techniques such as dynamic contrast enhanced imaging which study the wash-in and wash-out criteria of nodules have been introduced for more reliable characterization.

Positron emission tomography (PET) using 18 fluorine fluorodeoxyglucose (18 F-FDG) is commonly used to differentiate benign from malignant pathologies. FDG-PET has been used for evaluation of SPNs due to its superior ability to predict malignancy as compared to morphologic imaging.[4],[5] The ultimate gold standard to diagnose a lung nodule remains histopathology of the tissue obtained by surgery or percutaneous biopsy. Such invasive procedures performed for the sake of obtaining tissue diagnosis have their own share of complications. However, studies have shown that imaging algorithms incorporating FDG-PET can reduce the number of unnecessary invasive diagnostic procedures and can also prove to be cost-effective.[6],[7] Due to its superior diagnostic accuracy,[8] FDG-PET has become a preferred imaging modality for evaluation of SPN, more so in the developed world. Since FDG can also concentrate in infective and inflammatory lesions, the diagnostic utility of FDG-PET can be questioned particularly in regions endemic for infectious diseases. Our study was undertaken to evaluate the diagnostic performance of FDG-PET in a region highly endemic for granulomatous and infectious diseases and to see if these regional variations affect its utility in comparison to the developed world.


 » Materials And Methods Top


Patient selection

Patients who underwent an FDG-PET/CT scan between January 2009 and December 2014 for characterization of SPNs were included in this retrospective study. On the basis of clinico-radiological criteria, all SPNs had been categorized as indeterminate by a team of multidisciplinary specialists and then referred for an FDG-PET/CT scan for further evaluation. Only patients where histopathological confirmation (reference standard) was available by either percutaneous biopsy or surgical resection were included. Clinical and demographic data were obtained from the electronic medical records, and imaging data were acquired from the hospital picture archiving and communications system. This information was entered into a prospective database and analyzed. SPNs detected in patients with a known history of malignancy were excluded owing to a very high probability of being due to malignant/metastatic disease. As per our institutional policy, ethics approval is not required for retrospective studies.

Data analysis

FDG-PET scans were interpreted by both visual and semi-quantitative methods by trained nuclear radiologists with more than 5 years' experience in reading FDG PET-CT scans. However, semi-quantitative estimation represented as the maximum standardized uptake value (SUVmax) of the nodule was used for analysis. Based on an SUVmax cut-off of 2.5, lesions were classified as benign (<2.5) or malignant (>2.5) and compared with the gold standard of histopathology. Sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and accuracy of PET to detect malignancy were calculated for the SUVmax cut-off value of 2.5. On the basis of final histopathology, lesions were grouped as (1) malignant nodules, (2) infective/granulomatous nodules with a specific diagnosis (e.g., tuberculosis [TB]), and (3) nonspecific inflammatory nodules. The SUVmax of these groups was compared using nonparametric statistical tests to ascertain the difference or overlap in their metabolic uptake characteristics.

Fluorodeoxyglucose positron emission tomography/computed tomography technique

FDG-PET/CT scans were obtained using dedicated FDG-PET/CT scanners (Discovery ST; GE Healthcare and Philips Astonish TF systems) incorporating 16 and 64 slice CT components. After checking and confirming the blood glucose levels to be <150 mg/dl, PET/CT studies were performed 60–90 min following intravenous administration of 5 MBq/kg of 18 F-FDG. Scans were obtained from the skull base to the mid-thigh in all patients. Intravenous and oral contrast was administered in all patients unless there was a specific request or clinical indication against it. The SUVmax were automatically generated according to the following equation: SUVmax(bw)= Ctis/Dinj/bw, where SUVmax(bw) is the maximum SUV normalized for the body weight, Ctis is tissue concentration expressed as megabecquerels per milliliter, Dinj is injected dose expressed as megabecquerels, and bw is bodyweight expressed as kilograms.


 » Results Top


A total of 191 patients (129 males, 62 females) with a median age of 64 years (range: 36–83) fulfilled the eligibility criteria and were considered for the study; 144 nodules (75.3%) were malignant and 47 were benign (24.7%). Adenocarcinoma (n = 84) was the most common etiology followed by squamous carcinoma (n = 30). TB (n = 16) and nonspecific inflammation (n = 24) were the two most common benign pathologies. Nodules were labeled as due to “nonspecific inflammation” when the final histopathology report showed findings such as “necrotic tissue, acute suppurative inflammation, chronic inflammatory infiltrate, and necrosis with dense lymphoplasmacytic infiltrate-negative for malignancy.” [Table 1] shows a detailed distribution of benign and malignant pathologies. Nodules ranged in size from 6 mm to 30 mm. About 80% of malignant nodules and 66% of benign nodules were >2 cm in size.
Table 1: Number and pathology of malignant and benign pulmonary nodules

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There was a significant overlap in the metabolic uptake of malignant (median SUVmax-11.2, range: 3.3–34.6) and tuberculous nodules (median SUVmax-10.3, range: 2.7–22.5) with no statistically significant difference between their SUVmax values (P = 0.43). However, nonspecific inflammatory nodules (median SUVmax3.5, range: 0–21.2) showed significantly lower metabolism as compared to tuberculous and malignant nodules (P< 0.001). The SUVmax values of various malignant and benign pathologies are summarized in [Table 2] and [Table 3], respectively. The box plot of SUVmax values of the three groups is shown in [Figure 1].
Figure 1: Box plot of maximum standardized uptake values of malignant, tuberculous, and nonspecific infective nodules. Malignant and tuberculous nodules show a significant overlap in their maximum standardized uptake values

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Table 2: Median and range of maximum standardized uptake value of malignant nodules

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Table 3: Median and range of maximum standardized uptake value of benign nodules

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There were 30 false-positive studies (benign nodules with SUVmax>2.5) and 8 false-negative studies (malignant nodules with SUVmax<2.5). The false-positive rate was 65.2% and the false-negative rate was 5.5%. TB accounted for most number of false-positive studies whereas low-grade neuroendocrine carcinoma accounted for all the false-negative studies. Causes of false-positive and false-negative studies and their SUVmax values are summarized in [Table 4]. The sensitivity, specificity, PPV, NPV, and accuracy of FDG-PET/CT for detecting malignancy were 94.4%, 34.7%, 81.9%, 66.6%, and 79.5%, respectively.
Table 4: Causes of false positive and false negative positron emission tomography studies based on standardised uptake value cut-off - 2.5

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 » Discussion Top


FDG-PET is considered to be an accurate noninvasive modality for evaluating indeterminate SPNs. Two meta-analyses performed for studies evaluating the diagnostic accuracy of FDG-PET have reported a high sensitivity (94–96%) and reasonable specificity (78–86%) to diagnose lung cancer.[8],[9] Such favorable data have strengthened the role of FDG-PET in the diagnostic work-up of SPNs over the years. Recommendations to use FDG-PET for evaluation of SPN are found in several guidelines.[10],[11] These guidelines are primarily based on data published in the developed Western world where the prevalence of infections and granulomatous conditions is significantly less compared to the developing world where these conditions are endemic. A handful of studies has been conducted in population's endemic for infectious diseases. Because of the tendency of FDG to accumulate in infective lesions,[12],[13] the number of false-positive results in these studies was much higher resulting in the fall of specificity of FDG-PET. A recent meta-analysis [14] has shown that the specificity of FDG-PET was estimated to be 16% lower in endemic populations (61%) as compared to studies performed in nonendemic regions (77%). In our study, the specificity of FDG-PET was even lower (34.7%) than described in the meta-analysis. Studies performed in North America, specifically targeting regions known to have infectious/granulomatous disease endemic to the local population also reported lower specificity ranging from 40% to 56%.[15],[16],[17],[18] Data from countries such as Japan [19] and South Africa [20] where TB is endemic showed a much lower specificity of 21% and 25% which is similar to our study (34.7%), whereas a study from China [21] reported a relatively higher specificity of 61%. Almost 90% of false-positive scans in our study were because of infective/inflammatory conditions, with TB accounting for nearly one-third (16/47) cases. All tuberculous nodules had an SUVmax value higher than 2.5 [Figure 2], the generally accepted cut-off between benign and malignant pathologies, whereas less than half of nontuberculous infective nodules showed an SUVmax value higher than 2.5 [Table 4]. Our study showed a significant overlap in the metabolic uptake of tuberculous and malignant nodules with no statistically significant difference between their median SUVmax values
Figure 2: True and false positive results. Arrows in (a) (axial computed tomography) and (b) (fusion positron emission tomography/computed tomography) show a malignant nodule (adenocarcinoma) with a maximum standardized uptake values of 6.8 (true positive). Arrows in (c) (axial computed tomography) and (d) (fusion positron emission tomography/computed tomography) show tuberculous nodules with a maximum standardized uptake values of 5.0 (false positive)

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[Table 1], [Table 2] and [Figure 1]. This emphasizes the difficulty in differentiating malignant from tuberculous nodules in regions with high prevalence of TB. Similar difficulties can arise even with nontuberculous infective lesions or with nonspecific inflammatory pathologies which can show high metabolic uptake; however, these lesions showed a definite trend of lower median SUVmax values compared to tuberculous and malignant nodules [Figure 1].

The sensitivity of FDG-PET across most studies is high, ranging from 94% to 96%.[8],[9] In contrast to specificity, there appears to be no significant variation in sensitivity between endemic and nonendemic regions.[14] The sensitivity of FDG-PET/CT in our study was 94.4%, which is comparable to the pooled sensitivity documented in a recent meta-analysis of seventy studies.[14] This ability of FDG-PET/CT to pick up most of the malignant nodules (true-positive rate) could be considered to be its strength irrespective of the endemic status.

All the false-negative scans (SUVmax<2.5) in our study were due to low grade, slowly growing tumors such as low-grade neuroendocrine carcinoma, also referred to as typical carcinoid [Table 4] and [Figure 3]. Poor FDG avidity of carcinoid tumors has been well documented in literature [22],[23] and is attributed to minimal mitotic activity within the tumor and fewer proliferating tumor cells.[24],[25] Bronchioloalveolar carcinoma (BAC) now referred to as adenocarcinoma in situ (AIS) and nodules with a small size <10 mm are also causes of false-negative PET studies.[26],[27] In our study, all the five BAC/AIS nodules showed increased metabolic uptake (>2.5) and did not contribute to the false-negative studies contrary to the assumption of poor PET sensitivity for AIS. A relatively low false-negative rate of 5.5% in our study suggests that PET will miss out very few malignant tumors. Since all the false negatives were low grade slowly growing tumors, it can be concluded that a negative PET in all probability rules out a high-grade malignancy. We have used an SUVmax threshold of 2.5 to differentiate benign from malignant nodules. This value has been traditionally used in early studies [28] as a cut-off value, and most of the subsequent literature has used it as the basis to calculate diagnostic accuracy. A few studies have suggested that the traditional criteria of using SUV cut-off of 2.5 are inappropriate and have recommended the use of other parameters such as visual analysis and ratio of tracer uptake in lesion to background activity for differentiating benign from malignant lesions.[29],[30],[31] However, none of the methods have been found to be entirely reliable, and the classical criteria of 2.5 SUV cut-off have stood the test of time to calculate the diagnostic accuracy in scientific work.
Figure 3: True- and false-negative results. Arrows in (a) (axial positron emission tomography) and (b) (fusion positron emission tomography/computed tomography) show a benign nodule with no perceptible fluorodeoxyglucose uptake (true negative) arrows in (c) (axial computed tomography) and (d) (fused positron emission tomography/computed tomography) show a nodule with maximum standardized uptake values of 2.1 diagnosed as low grade neuroendocrine carcinoma (false negative)

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Modifications have been made in scanning techniques to improve the sensitivity and specificity of FDG-PET in evaluation of SPNs. Dual point imaging is one such method which has been found to be useful in differentiating benign from malignant processes,[32] the rationale being progressive increase in tracer uptake in malignant lesions and a stable or decline in uptake in benign lesions. Studies evaluating the utility of dual time point imaging for SPNs have reported improved diagnostic accuracy for differentiating malignant and benign nodules.[33],[34] A study by Matthies et al. showed that a 10% increase in SUV values between initial and delayed scans increased the sensitivity from 80% to 100%.[34] However, two recent meta-analyses which evaluated 18 studies have found no additional increment in diagnostic accuracy by performing dual time point imaging owing to significant overlap of metabolic characteristics of benign and malignant nodules.[35],[36] Other authors have confirmed that dual time point imaging could not differentiate benign and malignant nodules in a TB endemic area.[20] Dual time point imaging was not a part of our study protocol, though it would have been an interesting exercise to study it in an infectious endemic population such as ours, in spite of the evidence against it.

Of the 191 nodules in our study, nearly three-quarters (75.3%) were malignant. In spite of high prevalence of infectious disease in the region, the high proportion of malignant nodules in our study can be attributed to a referral bias as the study was conducted on patients referred to a tertiary cancer hospital. This referral bias can be considered a limitation of our study, and the high percentage of malignant nodules may not be a true representation of the general population. It is very likely that this percentage would fall along with reduction in specificity if this study were to be conducted in a community-based hospital with more equitable distribution of malignant and benign pathologies. Nevertheless, the fact that all these patients were considered to be indeterminate SPNs at presentation implies that a similar distribution may well be found in community practice. Not performing dual time point imaging to further improve the diagnostic accuracy as recommended by a few researchers can be considered another weakness of the study. However, from our own initial experience of multi-point imaging and conclusions drawn from two recent meta-analyses,[35],[36] dual time point imaging is not included as a standard protocol at our institute. Availability of histopathological confirmation in all nodules and a study group drawn from an infectious endemic population are obvious strengths of our study.

Our study has shown a clear association between reduced specificity of FDG-PET and endemic lung infections. Though high sensitivity remains the strength of FDG-PET, the knowledge of reduced specificity should be kept in mind particularly in infectious endemic populations. TB can present as SPN and acts as an important confounding factor for PET examinations in addition to other nonspecific infections and inflammations. Physicians must be aware of this limitation of FDG-PET scans in the workup of lung nodules, and regional variations must be considered before further management decisions are taken.


 » Conclusion Top


Our study highlights the limitation of FDG-PET scans and its reduced effectiveness to differentiate benign from malignant SPNs in geographical regions known to be endemic for infectious diseases.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
 » References Top

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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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