Study on PET scan done in Sweden

March 9, 2011

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Adrenal Gland Cancer

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Adrenal and Hypertension

[11C]Metomidate Positron Emission Tomography of Adrenocortical Tumors in Correlation with Histopathological Findings Joakim Hennings, Örjan Lindhe, Mats Bergström, Bengt Långström, Anders Sundin and Per Hellman

Departments of Surgery (J.H., P.H.), Radiology (A.S.), and Medical Sciences (O.L.), Uppsala University Hospital and Uppsala Imanet AB (O.L., B.L., M.B.), Uppsala, Sweden

Address all correspondence and requests for reprints to: Dr. Per Hellman, Department of Surgery, University Hospital, SE-751 85 Uppsala, Sweden. E-mail: per.hellman@...

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Abstract

TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences Context: Adrenal incidentalomas are common findings necessitating extensive laboratory work-up and repetitive radiological examinations. Positron emission tomography (PET) using 11C-labeled metomidate (MTO) has previously been described as a tool for specific adrenocortical imaging.

Objective: We evaluated 212 MTO-PET examinations in 173 patients to identify its role in the management of adrenal tumors.

Design: Seventy-five histopathological examinations from 73 patients were retrospectively analyzed.

Setting: All examinations were performed at a referral center.

Patients: Patients who were operated or biopsied due to adrenal tumors had histopathological diagnoses of adrenocortical adenoma (n = 26), adrenocortical cancer (ACC; n = 13), adrenocortical hyperplasia (n = 8), pheochromocytoma (n = 6), metastasis (n = 3), and tumors of nonadrenal origin (n = 19).

Main Outcome Measures: The main outcome measures were statistical analyses and findings while scrutinizing images. The hypothesis that MTO-PET is of value in the management of adrenal tumors, especially incidentaloma, was stated before data collection.

Results: Sensitivity was 0.89 and specificity was 0.96 for MTO-PET in proving adrenocortical origin of the lesions. Pheochromocytomas, metastases to the adrenal gland, and nonadrenal masses were all MTO negative. PET measurements using standardized uptake values (SUV) in pathological adrenocortical tissue could differentiate lesions larger than 1–1.5 cm from normal adrenocortical tissue. SUV was higher in aldosterone-hypersecreting adenomas, and the SUV ratio between the tumor and the contralateral gland was significantly higher in all hormonally hypersecreting adenomas as well as in ACC.

Conclusion: MTO-PET is a specific and sensitive method for diagnosing adrenocortical tumors. MTO-PET is useful in the imaging work-up of adrenal incidentalomas and may be beneficial for the examination of patients with primary aldosteronism or ACC.

Introduction

TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences ADRENAL MASSES ARE common incidental radiological findings, approaching the 6–9% prevalence reported from larger autopsy studies (1). The term incidentaloma is accepted as an entity and has hitherto indicated a search for hormonal hypersecretion and/or signs of malignant potential either by size criteria at diagnosis or by growth at follow-up (2, 3, 4). Among the causes of adrenal enlargement, hyperplasia or adenomas secreting aldosterone yielding primary aldosteronism (PA) have recently been identified more often, because many centers have reported PA as an underdiagnosed disease (5). It has been estimated that as many as 10–20% of patients with essential hypertension may suffer from undiagnosed PA (5). Thus, the increased number of incidentally diagnosed adrenal masses combined with underestimation of the prevalence of PA lead to an increased demand for effective programs to characterize adrenal masses. These include various imaging modalities for surgically correctable disease and for follow-up after resection of adrenocortical cancer (ACC). Metomidate (MTO) labeled with 11C has previously been described as a reliable positron emission tomography (PET) tracer for 11ß-hydroxylase activity, i.e. specific for enzymes in the cytochrome P45011B family (CYP11B) expressed in the adrenal cortex, and has been demonstrated to be useful to evaluate adrenal masses and for follow-up of ACC (6, 7, 8, 9). Recent reports in a small number of patients point in the same direction (10, 11). The objective of this study was to report the results from 75 [11C]MTO-PET examinations in 73 patients and their correlation to histopathology as a primary aim as well as to identify possible links to the status of the hormonal secretion.

Subjects and Methods

TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences At Uppsala Imanet (formerly Uppsala University PET Center), 212 consecutive MTO-PET examinations were performed in 173 patients between October 1996 and December 2004. The material comprises a heterogeneous group, i.e. including primary examinations of adrenal incidentalomas or hormone-producing adrenal tumors and follow-up examinations of patients with known or presumed ACC after and/or before chemotherapy. All patients underwent computed tomography (CT) without as well as with iv contrast enhancement using clinical standard imaging protocols. A study group was defined including those where we had histopathological data. A retrospective correlation of results from the MTO-PET was performed with the histopathology of 75 specimens from 73 patients (mean ± SD: age, 55.9 ± 13.8 yr; weight, 76.2 ± 14.2 kg; 41 women). The histopathological diagnoses are listed in Table 1. In addition, of the 75 MTO-PET examinations, 55 were performed using an algorithm allowing more thorough analyses of MTO uptake and signaling (see Table 1).

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TABLE 1. Subgroup characteristics: histopathology, size, and SUV The patients were managed according to the clinical routine of their respective diagnosis. For instance, hormonally silent incidentalomas not indicated for surgery because of their small size were followed according to recommendations from the Swedish Network for Endocrine Abdominal Tumors (2).

PET Carbon-11 was produced on a Scanditronix MC-17 cyclotron (Scanditronix-Wellhöfer, Uppsala, Sweden). The synthesis of [O-methyl-11C]MTO was performed as previously described (6, 7). All 75 patients were examined in either a GE 4096 whole-body PET scanner (GE Medical Systems, Milwaukee, WI) or a Siemens ECAT HR+ (Siemens, Munich, Germany) after at least 4 h of fasting, allowing free intake of clear liquids. The GE PET camera simultaneously produced 15 contiguous 6.5-mm axial slices with an in-plane resolution of 5–6 mm, and the Siemens ECAT PET camera produced 63 contiguous 2.5-mm axial slices with an in-plane resolution of 5 mm. A recent CT examination was used as a means of positioning the tumor region in the field of view of the PET camera and for anatomical correlation of the PET images. Patients were placed supine, and a laser beam was used to position the tumor region within the field of view of the PET scanner. A 10-min transmission scan was generated with an external rotating germanium-68 pin to correct the ensuing emission scan for attenuation. After a rapid iv bolus of approximately 10 MBq/kg (mean ± SD, 700 ± 200 MBq) [11C]MTO, a 45-min dynamic examination sequence was started.

Image reconstruction and data analysis From MTO-PET in 55 patients, dynamic images were reconstructed in a 128 x 128 matrix with a pixel size of 4 x 4 mm using a 6-mm Hanning filter and correction for attenuation and scattered radiation. The radioactivity concentrations in these images were recalculated to provide images of standardized uptake values (SUV), whereby the radioactivity concentration (becquerels per cubic centimeters) was divided by the injected dose per gram of body weight. Given a tissue density of 1.0 g/cc, this calculation provides an estimate of the tissue tracer accumulation relative to a presumed even radioactivity distribution in the body as a whole, which corresponds to an SUV of 1.0.

PET measurements The radiologist investigating the images (A.S.) was blinded for the radiological data from the CT scans, but had clinical information regarding the patients, such as known ACC or whether the PET study was performed due to an incidentaloma. Regions of interest (ROIs) were drawn manually in the summation images in normal adrenal, including contralateral glands as well as adrenal tumors. In each tissue a region was drawn in the area with the highest radioactivity concentration, designated the hot spot (ROIhs), comprising four contiguous pixels (0.64–1.0 cm2). In the liver a large circular ROI was drawn. SUV in the ROIs or SUVhs in the ROIhs were calculated 15–45 min after injection (Table 1). To exclude possible hormonal influence on these PET measurements, only the contralateral adrenal gland in patients with tumors of nonadrenal origin was considered normal. MTO uptake in a normal gland is characterized by a homogenous signal without any hot spots. In the remaining patients, the nontumorous adrenal gland was designated contralateral.

A true positive MTO-PET result was defined as a MTO-positive tumor corresponding to an adrenocortical tumor at histopathological examination (Fig. 1). A cortical tumor had a heterogeneous metomidate uptake with an hs, correlating to the tumor seen on CT, as judged by qualitative criteria. A false-negative MTO-PET result was noted when the examination failed to detect a cortical tumor diagnosed on CT and verified at surgery and/or histopathological examination. Nonadrenocortical lesions at MTO-PET that were verified as such by histopathological examination, but were diagnosed as tumor lesions on CT, were considered true negative observations (Fig. 1D). These lesions were totally devoid of metomidate uptake.

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FIG. 1. MTO-PET of patients with different types of adrenal pathology. A, Patient with a large, right-sided ACC, demonstrating lack of uptake in a necrotic tumor (long arrow), but reminiscent uptake in a dorsal, still viable portion (short arrow). B, Patient with PA, demonstrating a right-sided Conn adenoma with high MTO uptake (short arrow). The normal, left-sided adrenal has a lower MTO signal (long arrow). C, Patient with hypercortisolism demonstrating a left-sided adenoma (short arrow) and a nonspecific uptake in the stomach (long arrow). D, Patient with a large pheochromocytoma and no MTO uptake. Statistical methods One-way ANOVA with Dunnett's posttest was performed using PRISM version 4.01 for Windows (GraphPad, Inc., San Diego, CA). Values are presented as the mean ± SD.

Ethical considerations The study comprises retrospective data partly included in other studies (6, 7, 9) that used informed consent and approval of the local ethics committee. Some recent MTO-PET investigations were performed in newer, not yet published, studies, also using informed consent and with approval from the local ethics committee. The hospital has also decided that PET using MTO is a routine clinical method for patients with suspected or known ACC. Therefore, some recent patients have undergone MTO-PET without ethical approval due to the clinical routine status.

Results

TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences PET results Forty-two MTO-PET examinations revealed MTO-positive tumors. The size of these lesions at the corresponding CT examination averaged 5.5 cm (range, 1–20 cm). The sensitivity of MTO-PET for proving the adrenocortical origin of a lesion was 0.89 (42 of 47 histopathologically proven adrenocortical tumors). Thus, five MTO-PET examinations proved false negative. In two of these cases, the surgical finding and histopathological diagnosis demonstrated an almost completely necrotic ACC (Fig. 1). In one of these tumors, a narrow, faintly visible brim that accumulated MTO surrounded the necrosis, whereas the other tumor was completely devoid of MTO uptake. In these two patients, no MTO-positive extraadrenal metastases helped to reveal the adrenocortical origin of the tumor. Both patients were operated on because the size of the tumors exceeded 4 cm, this being an absolute indication for surgery in our department.

The other three of the five false-negative MTO-PET examinations were related to tumor size. In two of these patients, small Conn adenomas were found at surgery (1 cm), and the third patient had a discrete area of nodular hyperplasia (1 cm). Overall, the lower size resolution limit when an SUV in an enlarged adrenal differs from the contralateral normal adrenal was approximately 1 cm. In our material, the smallest tumors were in patients with PA, which was a reason for their examination.

One false-positive result occurred in one patient, rendering a specificity of 0.96. This patient had a 20-cm lesion adjacent to the left kidney. The tumor itself was MTO negative, but a small uptake was noted in the right lower part of the abdomen near the parietal peritoneum, and a metastasis from an ACC was suspected. The adrenal tumor proved to be a leiomyosarcoma, and no pathological lymph node was found after exploration and sampling at surgery. Thus, the false-positive uptake in the lower abdomen misled the interpretation of the negative large mass, which, nevertheless, was operated upon due to its size. This patient was denoted false positive due to the misinterpretation of the PET images, although the tumor itself was negative.

Pheochromocytomas, metastases to the adrenal gland, and benign nonadrenocortical lesions were all MTO negative (Fig. 1).

PET measurements The results of PET measurements are described in Table 1. Almost completely necrotic ACC, devoid of MTO uptake, were excluded from the statistical analyses of the SUV measurements. SUVhs did not discriminate between malignant necrotic tumors and tumors with a benign cause of necrosis, e.g. fibrosis secondary to bleeding.

The mean SUVhs in Conn adenomas was significantly higher than that in normal adrenal glands (P < 0.01). There were no significant differences in SUVhs between the contralateral glands regardless of type of pathology or hormonal activity in the affected gland. However, when the quotient between the tumor and the contralateral adrenal gland was considered, this was higher for Conn adenomas, Cushing adenomas, and ACC than that of normal adrenal glands (left/right; P < 0.01, P < 0.05, and P < 0.01, respectively). The SUV in the liver was similar in all groups.

Discussion

TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences Incidentally detected adrenal tumors constitute a clinical problem because of the hitherto clinically accepted demand for work-up, including biochemical testing and follow-up imaging procedures. The number of detected lesions is escalating dramatically because of the higher resolution of today's generation of CT scanners and ultrasound equipment and the increasing number of patients who are examined by these techniques. In our hospital, most patients who are referred to undergo clinical work-up because of an incidentaloma have been diagnosed by CT.

Several incidentalomas may be characterized at CT as benign cortical adenomas based on their low attenuation values at native (not enhanced with contrast) examination, indicative of a lipid-containing tumor. Administration of iv contrast leading to enhancement of the attenuation signal also supports a cortical solid lesion. Recently, it has been shown that attenuation measurements at CT performed 10 min after contrast medium injection adds information to this characterization, because the contrast medium washout is faster in adenomas than in ACC, pheochromocytomas, and metastases (12). This technique may decrease the number of uncharacterized incidentalomas.

However, in a large proportion of patients, the incidentalomas still escape characterization by CT, and additional radiological examination by magnetic resonance imaging (MRI) is required. Using MRI signal sequences in and out of phase, a loss of signal is detected in the latter phase in a fat-containing lesion (chemical shift). Thus, even after radiological workup, including additional CT and/or MRI, up to one third of incidentalomas remain uncharacterized (9).

The large clinical problem of identifying incidentalomas that require treatment from benign hormonally silent lesions demands sensitive and reliable methods. Apparently, characterization by CT and MRI is not fully sufficient. The lack of sensitivity of CT and MRI in this respect has resulted in protocols including repetitive follow-up CT examinations during up to 18 months of surveillance to detect growing lesions that are suspect for cancer and thorough biochemical analyses for diagnosis of hormonal hypersecretion. The increased detection of PA adds to this quantitative problem, because associated adrenal tumors in such patients need to be characterized.

We have previously demonstrated that MTO is a promising and sensitive PET tracer for the imaging of adrenocortical tumors (6, 7, 9, 11). This finding has been supported by other groups, although these studies have included only a small numbers of patients (10, 11). Because of the binding of MTO to the 11ß-hydroxylase activity in the adrenal cortex, MTO-PET may divide incidentalomas into two major groups with a high specificity. MTO-positive lesions constitute the adrenocortical tumors, i.e. adrenocortical adenomas or hyperplasias and ACC, whereas the MTO-negative lesions constitute all other tumors. The present retrospective correlative study in a larger number of patients comprised a subset of 75 (of 212) patients who underwent MTO-PET, but who also underwent surgery or needle biopsy for subsequent histopathological diagnosis.

The physical resolution of the PET scanner is approximately 0.5–1.0 cm. Smaller tumors may be depicted given that the tracer accumulation is high. In our material, the smallest lesion depicted at MTO-PET measured approximately 1 cm. Therefore, discrimination between uni- or bilateral adrenal disease in cases of PA may be difficult based on size criteria only.

According to data presented in Table 1, the SUVhs may discriminate Conn adenomas from normal and contralateral adrenal glands. In contrast, the quotient between the tumor and the contralateral adrenal gland discriminated between aldosterone- as well as cortisol-hypersecreting adenomas and ACC from normal adrenal glands. The SUVhs in the contralateral adrenal in patients with hormonal hypersecretion was similar to that in patients with nonfunctioning tumors and in patients with tumors not emanating from the adrenal gland. An assumed suppression of [11C]MTO accumulation in the contralateral adrenal by hormonal hypersecretion thus could not be verified.

One may speculate that the MTO uptake correlates to the amount of expressed CYP11B enzymes, relating to the increased number of cells. In addition, the SUVhs may correlate to cellular density. These assumptions would indicate a lack of relation between hormonal activity and MTO uptake or SUVhs. In contrast, an increased enzyme expression per cell, possibly resulting in higher SUVhs, may be associated with increased hormonal secretion. This hypothesis may be supported by our finding of higher SUVhs values in aldosterone-hypersecreting adrenal glands. However, additional cellular analyses are mandatory to clarify these questions.

Indeed, in certain situations, MTO-PET may be difficult to interpret. As also previously noted in patients suffering from ACC, the lack of MTO uptake may be due to large necroses. The lack of signal could not be differentiated from necroses emanating from other causes, e.g. fibrosis secondary to bleeding. Furthermore, differentiation between a central noncortical tumor, replacing the adrenal gland, and an ACC with extended necrosis is difficult. A false-negative result is probably difficult to avoid when facing the latter, unless MTO accumulation in coexisting metastases leads to the diagnosis. In clinical practice, most ACC exceeds the generally accepted size of 3–4 cm, which indicates surgery, and/or demonstrate hormonal adrenocortical hypersecretion. However, the absence or presence of metastases at MTO-PET in these cases adds information necessary for the therapeutic decision, timing of surgery vs. chemotherapy, etc. (8, 9).

The statistical analyses in the present study allow the possibility of performing prospective suggestions of the origin of the adrenal enlargement. In an individual patient, a tumor SUVhs higher than 24.3 would be equal to a 95% risk of a cortical adenoma or an ACC. If the SUVhs is more than 32, there is a 95% risk of a Conn adenoma. A more robust figure may, instead, be the quotient between the SUVhs in a tumor and that of the contralateral adrenal gland. With a quotient more than 1.4, there is a 99.5% risk of adrenocortical tumor.

As discussed above, a considerable proportion of patients are subjected to repetitive CT and/or MRI examinations to exclude lesion growth, but the nature of the incidentaloma remains uncharacterized. However, different investigational algorithms are used in different parts of the world, where the National Institutes of Health consensus propose fewer CT scans than many European programs (13). By contrast, MTO-PET performed as the first imaging procedure in patients with incidentalomas, replacing repetitive CT and MRI, would divide the patients into two groups. One larger group would comprise patients with adrenocortical tumors in whom the future workup may be limited and concentrated on possible adrenocortical hormonal hypersecretion and follow-up according to size criteria. In contrast, a second smaller group, with varying tumor diagnoses, would require more extensive workup. With recently developed PET-CT scanners, combining both modalities in the same gantry, this characterization will be even more refined, because the uptake of MTO or its absence may be demonstrated at the same time as attenuation measurement of the tumor is performed. In addition, with the development of more stable MTO tracers, such as those labeled with 18F, the technique will become more widely available.

In conclusion, MTO-PET facilitates the diagnosis of adrenal tumors (6, 8, 9, 10, 11) and contributes to the staging of ACC, follow-up after surgical and oncological treatment, and restaging in recurrent disease (8, 9). The present results point toward an as yet not fully proven clinical role for MTO-PET in the evaluation of the increasing number of incidentalomas and PA found. Ideally, MTO-PET may in some cases also replace the invasive, and often technically difficult, adrenal venous sampling procedure, although tracers correlating to enzymatic and secretory activity, rather than mere expression, possibly enhance functional resolution. To make MTO-PET more available, an MTO analog labeled with a more long-lived positron emitter than 11C has been developed.

Acknowledgments We greatly acknowledge the staff at Uppsala Imanet AB.

Footnotes This work was supported by grants from the Amersham Fund at Uppsala University.

J.H., A.S., and P.H. have nothing to declare. Ö.L. and B.L. are employed by Uppsala Imanet AB, and M.B. was previously employed by Uppsala Imanet AB.

First Published Online January 10, 2006

Abbreviations: ACC, Adrenocortical cancer; CT, computed tomography; hs, hot spot; MRI, magnetic resonance imaging; MTO, metomidate; PA, primary aldosteronism; PET, positron emission tomography; ROI, regions of interest; SUV, standardized uptake value.

Submitted on October 14, 2005 Accepted on January 4, 2006

References

TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences

Kloos R, Gross MD, Francis I, Korobkin M, Shapiro B 1995 Incidentally discovered adrenal masses. Endocr Rev 16:460–484[Abstract/Free Full Text] Bülow B, Ahrén B 2002 Adrenal incidentaloma–experience of a standardized diagnostic programme in the Swedish prospective study. J Intern Med 252:239–246[CrossRef][Medline] Grumbach M, Biller B, Braunstein G, K, Carney J, Godley P, E, Lee J, Oertel Y, Posner M, Schlechte J, Wieand H 2003 Management of the clinically inapparent adrenal mass ("incidentaloma"). Ann Intern Med 138:424–429[Abstract/Free Full Text] Mansmann G, Lau J, Balk E, Rothberg M, Miyachi Y, Bornstein S 2004 The clinically inapparent adrenal mass: update in diagnosis and management. Endocr Rev 25:309–340[Abstract/Free Full Text] Mulatero P, Stowasser M, Loh KC, Fardella CE, Gordon RD, Mosso L, Gomez- CE, Veglio F, Young Jr WF 2004 Increased diagnosis of primary aldosteronism, including surgically correctable forms, in centers from five continents. J Clin Endocrinol Metab 89:1045–1050[Abstract/Free Full Text] Bergstrom M, Juhlin C, Bonasera TA, Sundin A, Rastad J, Akerstrom G, Langstrom B 2000 PET imaging of adrenal cortical tumors with the 11ß-hydroxylase tracer 11C-metomidate. J Nucl Med 41:275–282[Abstract/Free Full Text] Bergström M, Bonasera T, Bergström E, Backlin C, Juhlin C, Långström B 1998 In vitro and in vivo primate evaluation of carbon-11-etomidate and carbon-11-metomidate as potential tracers for PET imaging of the adrenal cortex and its tumors. J Nucl Med 39:982–989[Abstract/Free Full Text] sson B, Bergström M, Sundin A, Juhlin C, Örlefors H, Öberg K, Långström B 2002 The role of PET in localization of neuroendocrine and adrenocortical tumors. Ann NY Acad Sci 970:159–169[Medline] Khan TS, Sundin A, Juhlin C, Langstrom B, Bergstrom M, sson B 2003 11C-Metomidate PET imaging of adrenocortical cancer. Eur J Nucl Med Mol Imaging 30:403–410[Medline] Minn H, Salonen A, Friberg J, Roivainen A, Viljanen T, Långsjö J, Salmi J, Valimäki M, Nagren K, Nuutila P 2004 Imaging of adrenal incidentalomas with PET using 11C-metomidate and 18F-FDG. J Nucl Med 45:972–979[Abstract/Free Full Text] Zettinig G, Mitterhauser M, Wadsak W, Becherer A, Pirich C, Vierhapper H, Niederle B, Dudczak R, Kletter K 2004 Positron emission tomography imaging of adrenal masses: 18F-fluorodeoxyglucose and the 11ß-hydroxylase tracer 11C-metomidate. Eur J Nucl Med Mol Imaging 31:403–410[CrossRef][Medline] Szolar D, Kammerhuber F 1997 Quantitative CT evaluation of adrenal gland masses: a step forward in the differentiation between adenomas and nonadenomas? Radiology 202:517–521[Abstract/Free Full Text] 2002 NIH state-of-the-science statement on management of the clinically inapparent adrenal mass ("incidentaloma"). NIH Consens State Sci Statements 19:1–25

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[18F]FETO - a longer lived PET tracer for the measurement of 11-beta-hydroxylase activity Markus Mitterhauser, et al. JCEM Online, 8 Sep 2006 [Full text]

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