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A Voice from the Past: Rediscovering the Virchow Node with Prostate-Specific Membrane Antigen-Targeted 18F-Dcfpyl Positron Emiss

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A Voice from the Past: Rediscovering the Virchow Node with Prostate-Specific Membrane Antigen-Targeted 18F-Dcfpyl Positron Emiss History A Voice From the Past: Rediscovering the Virchow Node With Prostate- specific Membrane Antigen-targeted 18F-DCFPyL Positron Emission Tomography Imaging Rudolf A. Werner, Christian Andree, Mehrbod S. Javadi, Constantin Lapa, Andreas K. Buck, Takahiro Higuchi, Martin G. Pomper, Michael A. Gorin, Steven P. Rowe, and Kenneth J. Pienta ore than 150 years ago, German pathologist In recent years, positron emission tomography (PET) ra- Rudolf Ludwig Karl Virchow (1821-1901) de- diotracers targeting prostate-specific membrane antigen scribed the finding of the involvement of the left (PSMA), including 68Ga-PSMA-11 and 18F-DCFPyL, have M 1 4,5 supraclavicular node in gastric cancer. It is now known been increasingly used to image men with prostate cancer. that a number of abdominal and thoracic malignancies have PET imaging with these agents offers greatly improved sen- a propensity to metastasize to this anatomic site, which is sitivity over conventional imaging modalities for detect- commonly referred to as Virchow node. Cancers known ing low volume sites of tumor burden.6,7 Because of the to spread to Virchow node include malignancies of the lung, outstanding sensitivity afforded by PSMA-targeted PET, it pancreas, and esophagus, and adenocarcinoma of the gastric can be directly visualized that many patients with ad- corpus, kidney, ovary, testicle, stomach, corpus uteri, cervix vanced prostate cancer can harbor disease within Virchow uteri, colon, and rectum.2 Metastasis to Virchow node has node (Fig. 1).3,7-10 This observation has served as an op- also been reported in men with prostate cancer; however, portunity to re-explore the exemplary life and career of this has generally been observed at a low frequency of only Rudolf Ludwig Karl Virchow. 0.5%.3 RUDOLF LUDWIG KARL VIRCHOW—“POPE Financial Disclosure: Martin G. Pomper is a coinventor on a patent covering 18F- OF MEDICINE” IN THE 19TH CENTURY DCFPyL and is entitled to a portion of any licensing fees and royalties generated by this AND SOCIAL REFORMER technology. This arrangement has been reviewed and approved by the Johns Hopkins Uni- versity in accordance with its conflict-of-interest policies. He has also received research Remembered as the most influential pathologist in the 19th funding from Progenics Phamaceuticals, the licensee of 18F-DCFPyL. Michael A. century, Virchow was also famous as a liberal politician and Gorin has served as a consultant to, and has received research funding from, Progenics Phamaceuticals. Kenneth J. Pienta has received research funding from as one of the leaders of the “Deutsche Fortschrittspartei” Progenics Phamaceuticals. Steven P. Rowe has received research funding from Progenics (German Progressive Party), the liberal political move- Phamaceuticals. The remaining authors declare that they have no relevant financial ment in Germany. In a time of competing political ide- interests. Funding Support: This study was supported by the Prostate Cancer Foundation Young ologies including nationalism, socialism and conservatism, Investigator Award, funds raised by the James Buchanan Brady Urological Institute, and the “Progressive Party” led the opposition to the consti- by the National Institutes of Health grants CA134675 and CA183031. This project has tutional forces of the Prime Minister of Prussia, Otto von received funding from the European Union’s Horizon 2020 research and innovation pro- gramme under the Marie Sklodowska-Curie grant agreement no. 701983. Bismarck. However, because of his role in the 1848 From the Division of Nuclear Medicine and Molecular Imaging, The Russell H. Morgan “Märzrevolution” (March Revolution), Virchow was finally Department of Radiology and Radiological Science, Johns Hopkins University School of forced to leave Berlin and was subsequently appointed as Medicine, Baltimore, MD; the Department of Nuclear Medicine and Comprehensive Heart Failure Center, University Hospital Würzburg, Würzburg, Germany; the Institut für the first Chair of Pathological Anatomy at the Univer- Geschichte der Medizin, Christian-Albrechts-Universität Kiel, Kiel, Germany; the De- sity of Würzburg in 1849.11,12 Five years later, the Charité partment of Biomedical Imaging, National Cardiovascular and Cerebral Research Center, Berlin reassigned him as the first Chair of Pathological Suita, Japan; and The James Buchanan Brady Urological Institute and Department of Urology, Johns Hopkins University School of Medicine, Baltimore, MD Anatomy and Physiology due to his increasing interna- Address correspondence to: Steven P. Rowe, M.D., Ph.D., Division of Nuclear Medi- tional popularity and reputation.11,13,14 Known as the cine and Molecular Imaging, The Russell H. Morgan Department of Radiology and Ra- father of cellular pathology, Virchow established the journal diological Science, Johns Hopkins University School of Medicine, 601 N. Caroline St., Baltimore, MD 21287. E-mail: [email protected] “Archiv für pathologische Anatomie und Physiologie und für Submitted: February 4, 2018, accepted (with revisions): March 22, 2018 klinische Medizin” in a close collaboration with his friend 18 © 2018 Elsevier Inc. https://doi.org/10.1016/j.urology.2018.03.030 All rights reserved. 0090-4295 Figure 1. Images from a 18F-DCFPyL PET-CT scan in a 57-year-old man with untreated, biopsy-proven Gleason 5 + 4 = 9 prostate cancer with serum prostate specific antigen level of 109.2 ng/mL. (A) Whole-body maximum intensity projection image demonstrates extensive adenopathy including a left supraclavicular Virchow node (red arrow) as well as radiotracer- avid lymph nodes in left cervical levels IV and V, the mediastinum (red arrowhead), the retrocrural space (thin red arrow), the retroperitoneum (double thin red arrow), and the pelvis. The (B) CT, (C) PET, and (D) PET-CT axial images at the level of the Virchow node show that its small size (5-mm short axis, red arrows) would make it occult on conventional anatomic imaging and indicate the importance of molecular imaging with a PSMA-targeted agent to uncover this site of disease. Additional axial PET-CT images through (E) the mediastinum, (F) the retrocrural space, and (G) the retroperitoneum dem- onstrate additional involved lymph nodes (red arrowhead in [E], thin red arrow in [F], and double thin red arrow in [G]) and suggest a pathway for involvement of the Virchow node, that is, the cancer likely spread up to the cisterna chyli in the proximity of the retrocrural node, then through the thoracic duct where it was able to establish sites of metastasis in both the mediastinum and left supraclavicular fossa. CT, computed tomography; PET, positron emission tomography; PET-CT, positron emission tomography-computed tomography; PSMA, prostate-specific membrane antigen. (Color version available online.) Benno Reinhardt (1819-1852). Pursuing the goal of trans- political power and scientific knowledge, he pushed the con- forming the esoteric medicine in Germany to a scientific struction of the first sewer system of Berlin.19 discipline, this journal is still with us today and is now known as “Virchows Archiv”, the official journal of the Eu- ropean Society of Pathology.15 VIRCHOW AND HIS AFTERMATH As a broadly influential thinker of his day, Virchow’s With close to 2000 publications, Virchow has made major career in social science remains equally as remarkable as contributions to the field of cellular pathology and should his work in medicine. More specifically, he is credited with be remembered for the introduction of certain medical terms founding the newspaper “Die medicinische Reform” (Medical that are still used today; Virchow defined the term “embolus” Reform), popularizing the term “social medicine,” and pro- along with its thrombosis mechanism, the word “amyloid” moting the concept of physicians serving as “attorney(s) and its reaction with iodine and sulphuric acid in the brain, of the poor.” One of his most famous contributions in and the term “granuloma.”11,20,21 medical literature is the “Report on Typhus Epidemic in Upper Silesia.” Asked by the Education Minister of Prussia, Virchow investigated the 1848 typhus epidemic in Upper Silesia (now THE VIRCHOW NODE within the borders of Poland) and stated that Prussian au- Indisputably, the first description of an enlarged supracla- thorities had failed in preventing the outbreak of this dev- vicular lymph node involved in metastatic malignancies astating disease. Outlining a revolutionary program, Virchow dates back to Virchow. In 1848, he outlined in his article emphasized the urgent need for improvement of social con- “Zur Diagnose der Krebse im Unterleibe“ (Fig. 2): ditions in this area, which are democratic self-government, disestablishment of the Catholic Church, and agricul- …namentlich bei Krebsen des Magens, des Pankreas, der tural cooperatives.16-18 Another example of his contribu- Eierstöcke, etc., wie sich der Prozess allmählich von den tion to social medicine is his report “Reinigung und Lymphdrüsen des Unterleibs auf die im hinteren Mediastinum Entwässerung Berlins” in which, through a combination of neben dem Ductus thoracicus gelegenen Drüsen fortsetzt und UROLOGY 117, 2018 19 Figure 2. (A) Original German article, “Zur Diagnose der Krebse im Unterleibe” by Rudolf Karl Ludwig Virchow, published in the Medicinische Reform (45:248) in 1848. The article is within the section titled “Kleinere Mittheilungen” (Brief Commu- nication). Description of the Virchow node and the name of the author (Virchow) were both highlighted in a red frame. (B) Excerpt of “Zur Diagnose der Krebse
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