Multicenter Study

. 2020 Sep;8(9):773-781.

doi: 10.1016/S2213-8587(20)30218-7. Epub 2020 Jul 23.

Urine steroid metabolomics for the differential diagnosis of adrenal incidentalomas in the EURINE-ACT study: a prospective test validation study

Irina Bancos¹, Angela E Taylor², Vasileios Chortis³, Alice J Sitch⁴, Carl Jenkinson², Caroline J Davidge-Pitts⁵, Katharina Lang³, Stylianos Tsagarakis⁶, Magdalena Macech⁷, Anna Riester⁸, Timo Deutschbein⁹, Ivana D Pupovac¹⁰, Tina Kienitz¹¹, Alessandro Prete³, Thomas G Papathomas², Lorna C Gilligan¹², Cristian Bancos⁵, Giuseppe Reimondo¹³, Magalie Haissaguerre¹⁴, Ljiljana Marina¹⁵, Marianne A Grytaas¹⁶, Ahmed Sajwani¹⁷, Katharina Langton¹⁸, Hannah E Ivison¹², Cedric H L Shackleton¹⁹, Dana Erickson⁵, Miriam Asia²⁰, Sotiria Palimeri⁶, Agnieszka Kondracka⁷, Ariadni Spyroglou⁸, Cristina L Ronchi²¹, Bojana Simunov¹⁰, Danae A Delivanis⁵, Robert P Sutcliffe²², Ioanna Tsirou⁶, Tomasz Bednarczuk⁷, Martin Reincke⁸, Stephanie Burger-Stritt⁹, Richard A Feelders²³, Letizia Canu²⁴, Harm R Haak²⁵, Graeme Eisenhofer¹⁸, M Conall Dennedy¹⁷, Grethe A Ueland¹⁶, Miomira Ivovic¹⁵, Antoine Tabarin¹⁴, Massimo Terzolo¹³, Marcus Quinkler¹¹, Darko Kastelan¹⁰, Martin Fassnacht²⁶, Felix Beuschlein²⁷, Urszula Ambroziak⁷, Dimitra A Vassiliadi⁶, Michael W O'Reilly³, William F Young Jr⁵, Michael Biehl²⁸, Jonathan J Deeks⁴, Wiebke Arlt²⁹; ENSAT EURINE-ACT Investigators

Collaborators, Affiliations

Collaborators

ENSAT EURINE-ACT Investigators:
Stephan Glöckner, Richard O Sinnott, Anthony Stell, Maria C Fragoso, Darko Kastelan, Ivana D Pupovac, Bojana Simunov, Sarah Cazenave, Magalie Haissaguerre, Antoine Tabarin, Jérôme Bertherat, Rossella Libé, Tina Kienitz, Marcus Quinkler, Katharina Langton, Graeme Eisenhofer, Felix Beuschlein, Christina Brugger, Martin Reincke, Anna Riester, Ariadni Spyroglou, Stephanie Burger-Stritt, Timo Deutschbein, Martin Fassnacht, Stefanie Hahner, Matthias Kroiss, Cristina L Ronchi, Sotiria Palimeri, Stylianos Tsagarakis, Ioanna Tsirou, Dimitra A Vassiliadi, Vittoria Basile, Elisa Ingargiola, Giuseppe Reimondo, Massimo Terzolo, Letizia Canu, Massimo Mannelli, Hester Ettaieb, Harm R Haak, Thomas M Kerkhofs, Michael Biehl, Richard A Feelders, Johannes Hofland, Leo J Hofland, Marianne A Grytaas, Eystein S Husebye, Grethe A Ueland, Urszula Ambroziak, Tomasz Bednarczuk, Agnieszka Kondracka, Magdalena Macech, Malgorzata Zawierucha, Isabel Paiva, M Conall Dennedy, Ahmed Sajwani, Mark Sherlock, Rachel K Crowley, Miomira Ivovic, Ljiljana Marina, Jonathan J Deeks, Alice J Sitch, Wiebke Arlt, Irina Bancos, Vasileios Chortis, Lorna C Giligan, Beverly A Hughes, Katharina Lang, Hannah E Ivison, Carl Jenkinson, Konstantinos Manolopoulos, Donna M O'Neil, Michael W O'Reilly, Thomas G Papathomas, Alessandro Prete, Cedric H L Shackleton, Angela E Taylor, Miriam Asia, Robert P Sutcliffe, Peter Guest, Kassiani Skordilis, Cristian Bancos, Alice Chang, Caroline J Davidge-Pitts, Danae A Delivanis, Dana Erickson, Neena Natt, Todd B Nippoldt, Melinda Thomas, William F Young Jr

Affiliations

¹ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; Division of Endocrinology, Diabetes, Metabolism and Nutrition, Mayo Clinic, Rochester, MN, USA.
² Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK.
³ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK; Department of Endocrinology, Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK.
⁴ Institute of Applied Health Research, University of Birmingham, Birmingham, UK; NIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust and University of Birmingham, Birmingham, UK.
⁵ Division of Endocrinology, Diabetes, Metabolism and Nutrition, Mayo Clinic, Rochester, MN, USA.
⁶ Department of Endocrinology, Diabetes and Metabolism, Evangelismos Hospital, Athens, Greece.
⁷ Department of Internal Medicine and Endocrinology, Medical University of Warsaw, Warsaw, Poland.
⁸ Medizinische Klinik and Poliklinik IV, Klinikum der Universität, Ludwig-Maximilians-Universität München, Munich, Germany.
⁹ Division of Endocrinology and Diabetes, Department of Internal Medicine I, University Hospital Würzburg, University of Würzburg, Würzburg, Germany.
¹⁰ Department of Endocrinology, University Hospital Centre Zagreb, Zagreb, Croatia.
¹¹ Endocrinology in Charlottenburg, Berlin, Germany.
¹² Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK.
¹³ Department of Clinical and Biological Sciences, San Luigi Hospital, University of Turin, Turin, Italy.
¹⁴ Department of Endocrinology, Hôpital Haut Lévêque, CHU de Bordeaux, Pessac, France.
¹⁵ Department for Obesity, Reproductive and Metabolic Disorders, Clinic for Endocrinology, Diabetes and Metabolic Diseases, Clinical Centre of Serbia, Faculty of Medicine, University of Belgrade, Belgrade, Serbia.
¹⁶ Department of Clinical Science, University of Bergen, Bergen, Norway; Department of Medicine, Haukeland University Hospital, Bergen, Norway.
¹⁷ School of Medicine, National University of Ireland Galway, Galway, Ireland.
¹⁸ Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Carl Gustav Carus, Technical University, Dresden, Germany.
¹⁹ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; UCSF Benioff Children's Hospital Oakland Research Institute, Oakland, CA, USA.
²⁰ Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK; Department of Endocrinology, Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK.
²¹ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK; Department of Endocrinology, Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK; Division of Endocrinology and Diabetes, Department of Internal Medicine I, University Hospital Würzburg, University of Würzburg, Würzburg, Germany.
²² Department of Hepato-Pancreato-Biliary and Liver Transplant Surgery, Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK.
²³ Department of Internal Medicine, Division of Endocrinology, Erasmus University Medical Centre, Rotterdam, Netherlands.
²⁴ Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence, Italy.
²⁵ Department of Internal Medicine, Maxima Medisch Centrum, Eindhoven, Netherlands; Department of Health Services Research and CAPHRI School for Public Health and Primary Care, Maastricht University, Maastricht, Netherlands.
²⁶ Division of Endocrinology and Diabetes, Department of Internal Medicine I, University Hospital Würzburg, University of Würzburg, Würzburg, Germany; Comprehensive Cancer Center Mainfranken, University Hospital Würzburg, University of Würzburg, Würzburg, Germany; Central Laboratory, University Hospital Würzburg, University of Würzburg, Würzburg, Germany.
²⁷ Medizinische Klinik and Poliklinik IV, Klinikum der Universität, Ludwig-Maximilians-Universität München, Munich, Germany; Klinik für Endokrinologie, Diabetologie und Klinische Ernährung, Universitätsspital Zürich, Zurich, Switzerland.
²⁸ Bernoulli Institute for Mathematics, Computer Science and Artificial Intelligence, University of Groningen, Groningen, Netherlands.
²⁹ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK; Department of Endocrinology, Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK; NIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust and University of Birmingham, Birmingham, UK. Electronic address: w.arlt@bham.ac.uk.

PMID: 32711725
PMCID: PMC7447976
DOI: 10.1016/S2213-8587(20)30218-7

Multicenter Study

Urine steroid metabolomics for the differential diagnosis of adrenal incidentalomas in the EURINE-ACT study: a prospective test validation study

Irina Bancos et al. Lancet Diabetes Endocrinol. 2020 Sep.

. 2020 Sep;8(9):773-781.

doi: 10.1016/S2213-8587(20)30218-7. Epub 2020 Jul 23.

Authors

Collaborators

ENSAT EURINE-ACT Investigators:
Stephan Glöckner, Richard O Sinnott, Anthony Stell, Maria C Fragoso, Darko Kastelan, Ivana D Pupovac, Bojana Simunov, Sarah Cazenave, Magalie Haissaguerre, Antoine Tabarin, Jérôme Bertherat, Rossella Libé, Tina Kienitz, Marcus Quinkler, Katharina Langton, Graeme Eisenhofer, Felix Beuschlein, Christina Brugger, Martin Reincke, Anna Riester, Ariadni Spyroglou, Stephanie Burger-Stritt, Timo Deutschbein, Martin Fassnacht, Stefanie Hahner, Matthias Kroiss, Cristina L Ronchi, Sotiria Palimeri, Stylianos Tsagarakis, Ioanna Tsirou, Dimitra A Vassiliadi, Vittoria Basile, Elisa Ingargiola, Giuseppe Reimondo, Massimo Terzolo, Letizia Canu, Massimo Mannelli, Hester Ettaieb, Harm R Haak, Thomas M Kerkhofs, Michael Biehl, Richard A Feelders, Johannes Hofland, Leo J Hofland, Marianne A Grytaas, Eystein S Husebye, Grethe A Ueland, Urszula Ambroziak, Tomasz Bednarczuk, Agnieszka Kondracka, Magdalena Macech, Malgorzata Zawierucha, Isabel Paiva, M Conall Dennedy, Ahmed Sajwani, Mark Sherlock, Rachel K Crowley, Miomira Ivovic, Ljiljana Marina, Jonathan J Deeks, Alice J Sitch, Wiebke Arlt, Irina Bancos, Vasileios Chortis, Lorna C Giligan, Beverly A Hughes, Katharina Lang, Hannah E Ivison, Carl Jenkinson, Konstantinos Manolopoulos, Donna M O'Neil, Michael W O'Reilly, Thomas G Papathomas, Alessandro Prete, Cedric H L Shackleton, Angela E Taylor, Miriam Asia, Robert P Sutcliffe, Peter Guest, Kassiani Skordilis, Cristian Bancos, Alice Chang, Caroline J Davidge-Pitts, Danae A Delivanis, Dana Erickson, Neena Natt, Todd B Nippoldt, Melinda Thomas, William F Young Jr

Affiliations

¹ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; Division of Endocrinology, Diabetes, Metabolism and Nutrition, Mayo Clinic, Rochester, MN, USA.
² Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK.
³ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK; Department of Endocrinology, Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK.
⁴ Institute of Applied Health Research, University of Birmingham, Birmingham, UK; NIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust and University of Birmingham, Birmingham, UK.
⁵ Division of Endocrinology, Diabetes, Metabolism and Nutrition, Mayo Clinic, Rochester, MN, USA.
⁶ Department of Endocrinology, Diabetes and Metabolism, Evangelismos Hospital, Athens, Greece.
⁷ Department of Internal Medicine and Endocrinology, Medical University of Warsaw, Warsaw, Poland.
⁸ Medizinische Klinik and Poliklinik IV, Klinikum der Universität, Ludwig-Maximilians-Universität München, Munich, Germany.
⁹ Division of Endocrinology and Diabetes, Department of Internal Medicine I, University Hospital Würzburg, University of Würzburg, Würzburg, Germany.
¹⁰ Department of Endocrinology, University Hospital Centre Zagreb, Zagreb, Croatia.
¹¹ Endocrinology in Charlottenburg, Berlin, Germany.
¹² Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK.
¹³ Department of Clinical and Biological Sciences, San Luigi Hospital, University of Turin, Turin, Italy.
¹⁴ Department of Endocrinology, Hôpital Haut Lévêque, CHU de Bordeaux, Pessac, France.
¹⁵ Department for Obesity, Reproductive and Metabolic Disorders, Clinic for Endocrinology, Diabetes and Metabolic Diseases, Clinical Centre of Serbia, Faculty of Medicine, University of Belgrade, Belgrade, Serbia.
¹⁶ Department of Clinical Science, University of Bergen, Bergen, Norway; Department of Medicine, Haukeland University Hospital, Bergen, Norway.
¹⁷ School of Medicine, National University of Ireland Galway, Galway, Ireland.
¹⁸ Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Carl Gustav Carus, Technical University, Dresden, Germany.
¹⁹ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; UCSF Benioff Children's Hospital Oakland Research Institute, Oakland, CA, USA.
²⁰ Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK; Department of Endocrinology, Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK.
²¹ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK; Department of Endocrinology, Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK; Division of Endocrinology and Diabetes, Department of Internal Medicine I, University Hospital Würzburg, University of Würzburg, Würzburg, Germany.
²² Department of Hepato-Pancreato-Biliary and Liver Transplant Surgery, Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK.
²³ Department of Internal Medicine, Division of Endocrinology, Erasmus University Medical Centre, Rotterdam, Netherlands.
²⁴ Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence, Italy.
²⁵ Department of Internal Medicine, Maxima Medisch Centrum, Eindhoven, Netherlands; Department of Health Services Research and CAPHRI School for Public Health and Primary Care, Maastricht University, Maastricht, Netherlands.
²⁶ Division of Endocrinology and Diabetes, Department of Internal Medicine I, University Hospital Würzburg, University of Würzburg, Würzburg, Germany; Comprehensive Cancer Center Mainfranken, University Hospital Würzburg, University of Würzburg, Würzburg, Germany; Central Laboratory, University Hospital Würzburg, University of Würzburg, Würzburg, Germany.
²⁷ Medizinische Klinik and Poliklinik IV, Klinikum der Universität, Ludwig-Maximilians-Universität München, Munich, Germany; Klinik für Endokrinologie, Diabetologie und Klinische Ernährung, Universitätsspital Zürich, Zurich, Switzerland.
²⁸ Bernoulli Institute for Mathematics, Computer Science and Artificial Intelligence, University of Groningen, Groningen, Netherlands.
²⁹ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK; Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK; Department of Endocrinology, Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK; NIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust and University of Birmingham, Birmingham, UK. Electronic address: w.arlt@bham.ac.uk.

PMID: 32711725
PMCID: PMC7447976
DOI: 10.1016/S2213-8587(20)30218-7

Abstract

Background: Cross-sectional imaging regularly results in incidental discovery of adrenal tumours, requiring exclusion of adrenocortical carcinoma (ACC). However, differentiation is hampered by poor specificity of imaging characteristics. We aimed to validate a urine steroid metabolomics approach, using steroid profiling as the diagnostic basis for ACC.

Methods: We did a prospective multicentre study in adult participants (age ≥18 years) with newly diagnosed adrenal masses. We assessed the accuracy of diagnostic imaging strategies based on maximum tumour diameter (≥4 cm vs <4 cm), imaging characteristics (positive vs negative), and urine steroid metabolomics (low, medium, or high risk of ACC), separately and in combination, using a reference standard of histopathology and follow-up investigations. With respect to imaging characteristics, we also assessed the diagnostic utility of increasing the unenhanced CT tumour attenuation threshold from the recommended 10 Hounsfield units (HU) to 20 HU.

Findings: Of 2169 participants recruited between Jan 17, 2011, and July 15, 2016, we included 2017 from 14 specialist centres in 11 countries in the final analysis. 98 (4·9%) had histopathologically or clinically and biochemically confirmed ACC. Tumours with diameters of 4 cm or larger were identified in 488 participants (24·2%), including 96 of the 98 with ACC (positive predictive value [PPV] 19·7%, 95% CI 16·2-23·5). For imaging characteristics, increasing the unenhanced CT tumour attenuation threshold to 20 HU from the recommended 10 HU increased specificity for ACC (80·0% [95% CI 77·9-82·0] vs 64·0% [61·4-66.4]) while maintaining sensitivity (99·0% [94·4-100·0] vs 100·0% [96·3-100·0]; PPV 19·7%, 16·3-23·5). A urine steroid metabolomics result indicating high risk of ACC had a PPV of 34·6% (95% CI 28·6-41·0). When the three tests were combined, in the order of tumour diameter, positive imaging characteristics, and urine steroid metabolomics, 106 (5·3%) participants had the result maximum tumour diameter of 4 cm or larger, positive imaging characteristics (with the 20 HU cutoff), and urine steroid metabolomics indicating high risk of ACC, for which the PPV was 76·4% (95% CI 67·2-84·1). 70 (3·5%) were classified as being at moderate risk of ACC and 1841 (91·3%) at low risk (negative predictive value 99·7%, 99·4-100·0).

Interpretation: An unenhanced CT tumour attenuation cutoff of 20 HU should replace that of 10 HU for exclusion of ACC. A triple test strategy of tumour diameter, imaging characteristics, and urine steroid metabolomics improves detection of ACC, which could shorten time to surgery for patients with ACC and help to avoid unnecessary surgery in patients with benign tumours.

Funding: European Commission, UK Medical Research Council, Wellcome Trust, and UK National Institute for Health Research, US National Institutes of Health, the Claire Khan Trust Fund at University Hospitals Birmingham Charities, and the Mayo Clinic Foundation for Medical Education and Research.

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Figures

**Figure 2**
Imaging test results Maximum tumour diameter in patients with ACC (A), other malignant tumours (B), ACA (C), and other benign tumours (D) and distributions of patients with ACC according to positive or negative results for tumour diameter and imaging characteristics with unenhanced CT tumour attenuation cutoff of 10 HU (E) or 20 HU (F). ACA=adrenocortical adenoma. ACC=adrenocortical carcinoma. HU=Hounsfield units.

**Figure 3**
Diagnostic accuracy of single-test and multiple-test strategies for detecting ACC (A) Diagnostic accuracy of the three index tests (tumour diameter, imaging characteristics [unenhanced CI attenuation >20 HU], and urine steroid metabolomics) as single tests, in double combinations, and as a triple-test strategy. (B) Flowchart illustrating the distribution of ACC cases when applying the triple-test strategy in the order: tumour diameter, imaging characteristics (unenhanced CT attenuation >20 HU), and urine steroid metabolomics. ACC=adrenocortical carcinoma. HU=Hounsfield units. ImChar=imaging characteristics. USM-HR=urine steroid metabolomics profile indicating high risk of ACC. USM-LR=urine steroid metabolomics profile indicating low risk of ACC. USM-MR=urine steroid metabolomics profile indicating moderate risk of ACC.

See this image and copyright information in PMC

Comment in

Urine metabolomic phenotyping for detection of adrenocortical carcinoma: still a long way to go.
Anyfanti P, Nikolaidou B, Gkaliagkousi E. Anyfanti P, et al. Lancet Diabetes Endocrinol. 2020 Nov;8(11):876-877. doi: 10.1016/S2213-8587(20)30341-7. Lancet Diabetes Endocrinol. 2020. PMID: 33065057 No abstract available.
Urine metabolomic phenotyping for detection of adrenocortical carcinoma: still a long way to go - Authors' reply.
Bancos I, Taylor AE, Chortis V, Sitch AJ, Lang K, Prete A, Gilligan LC, Biehl M, Deeks JJ, Arlt W; ENSAT EURINE-ACT Investigators. Bancos I, et al. Lancet Diabetes Endocrinol. 2020 Nov;8(11):877-878. doi: 10.1016/S2213-8587(20)30345-4. Lancet Diabetes Endocrinol. 2020. PMID: 33065058 No abstract available.

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Urine steroid metabolomics for the differential diagnosis of adrenal incidentalomas in the EURINE-ACT study: a prospective test validation study

Collaborators

Affiliations

Urine steroid metabolomics for the differential diagnosis of adrenal incidentalomas in the EURINE-ACT study: a prospective test validation study

Authors

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Affiliations

Abstract

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