Background: Renal cell carcinoma is well-known for its propensity to metastasize to unusual sites. However, metastasis to the gallbladder has been rarely reported in the literature. Case presentation: A 75-year-old Japanese (Asian) woman presented for further evaluation of a gallbladder polyp, 15 years after right radical nephrectomy for renal cell carcinoma. Computed tomography revealed a 12 mm enhancing pedunculated tumor in the gallbladder fundus. Open simple cholecystectomy was performed and the tumor was histologically confirmed as a metastasis of renal cell carcinoma to the gallbladder. Our patient is alive and has been disease-free for 3 years after cholecystectomy. Conclusions: Although metastasis of renal cell carcinoma is a rare differential diagnosis of gallbladder tumors, simple cholecystectomy is likely to offer a chance of long-term survival for patients with gallbladder metastases of renal cell carcinoma. Keywords: Renal cell carcinoma, Metastasis, Gallbladder Background surviving for 5 years after complete metastasectomy has Metastasis to the gallbladder is rare and in most cases is been reported [4, 6]. found incidentally on autopsy [1, 2]. The rarity and clin- We report a rare case of a patient with gallbladder me- ical similarity of metastasis to the gallbladder to benign tastasis from RCC diagnosed 15 years after primary cancer or other malignant gallbladder diseases make a correct excision, and review the previously reported 38 cases. We diagnosis difficult in clinical practice. discuss the condition’s presentation, surgical treatment, Cancers of the kidney account for 4% of all newly di- and survival outcomes. We also indicated the characteris- agnosed malignancies in men and 3% in women, and in tics of preoperative image findings of gallbladder metasta- most cases they are renal cell carcinomas (RCCs) . sis of RCC, which are considered to be helpful for the Approximately one-third of patients with RCC already preoperative differential diagnosis of gallbladder tumors. have metastases at the time of diagnosis, frequently to It was thought to be clinically important that resection vascular-rich organs such as the lung, bone, and liver. could allow long-term survival for patients with metachro- Patients with distant metastases from RCC have a poor nous and localized RCC recurrences. prognosis with a prospect of surviving for 5 years of < 10% . However, curative resection of metastases in se- Case presentation lected patients may improve long-term survival . In A 75-year-old Japanese (Asian) woman underwent a patients with a solitary metastasis, a 35–50% prospect of right nephrectomy for RCC approximately 15 years ago. Our patient did not present symptoms at admission, and * Correspondence: email@example.com her past medical, social, family, and environmental his- Department of Surgery, Medical Corporation JR Hiroshima Hospital, 3-1-36 tory was not appreciable. Her occupation was home Futabanosato, Higashi-ku, Hiroshima 732-0057, Japan Full list of author information is available at the end of the article manager, and she was on no medication prior to © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Saito et al. Journal of Medical Case Reports (2018) 12:162 Page 2 of 7 blood urea nitrogen 13.6 mg/dL, creatinine 0.64 mg/dL, sodium 137 mEq/L, potassium 3.9 mEq/L, chlorine mEq/L, C-reactive protein 0.03 mg/dL, carcinoembryonic antigen 1.5 ng/mL, carbohydrate antigen 19–94 U/mL, urinalysis pH 7.0, no uric protein, no urinary sugar, no ketone body, no uric blood, no bilirubin, and no white blood cell. No microbial examination was performed. The tumor was 9.1 × 7.8 cm in diameter and confined to the capsule of the kidney. Pulmonary lobectomy was performed for left lung metastasis 11 years after the pri- mary resection and an additional lung partial resection was performed for the metachronous left lung metastasis 14 years after the primary resection. Examinations including whole body computed tom- ography (CT) before each surgery demonstrated no evi- Fig. 1 Ultrasonography shows an iso- to hyperechoic polyp at the dence of distant metastasis. A surveillance follow-up fundus of the gallbladder (yellow bar indicates 10 mm) CT scan revealed a gallbladder lesion. No symptoms suggested cholecystitis, and the only biochemical ab- diagnosis. She did not smoke and consume alcohol, and normality was a slight elevation in levels of aspartate hertemperature was36.3°C,herblood pressure was transaminase and alanine transaminase. Ultrasonog- 122/82 mmHg, and her pulse was 68 per minute. Labora- raphy (US) showed a mass at the gallbladder fundus. Its tory findings at admission are shown below. Her white surface was smooth, and the inner echo was slightly 3/ blood cell count was 3800 × 10 μL, red blood cell count high and homogenous (Fig. 1). 414 × 10 /μL, hemoglobin 13.0 g/dL, hematocrit 39.1%, A contrast-enhanced CT scan showed a 12-mm polyp- platelets 19.6 × 104/μL, total bilirubin 0.7 mg/dL, direct bili- oid mass with high attenuation, enlarged from 4 mm 2 rubin 0.2 mg/dL, aspartate transaminase 23 IU/L, alanine years ago (Fig. 2a, b). It had significantly high intensity transaminase 9 IU/L, total protein 7.3 g/dL, albumin 4.5 g/ in the arterial phase. On the coronal reconstruction dL, lactate dehydrogenase 188 IU/L, γ-glutamyltransferase image, attenuation was inhomogeneous in the mass and 11 IU/L, alkaline phosphatase 201 IU/L, amylase 129 IU/L, relatively higher on the wall side (Fig. 2c, d). There was a b cd Fig. 2 A computed tomography scan shows tumor growth from 4 mm to 12 mm over a span of 2 years (a 2 years prior, b present). A contrast-enhanced computed tomography scan shows high intensity of the tumor during the arterial phase (d yellow arrow) in comparison with plain computed tomography (c yellow arrow) Saito et al. Journal of Medical Case Reports (2018) 12:162 Page 3 of 7 no significant accumulation of contrast agent in any We performed immunohistochemical staining for organ other than the gallbladder. vimentin and cytokeratin 7 (CK7). The tumor stained Based on these image findings and the patient’s med- strongly for vimentin, but staining for CK7 was al- ical history, we initially thought the gallbladder mass most negative (Fig. 4), although for CK7, we observed was a malignant tumor such as a gallbladder carcinoma. a partially nonspecific immune reaction due to use of The possibility that the tumor was metastatic cancer an automated immunostainer. These pathological fea- remained, and we therefore performed open approach tures were similar to those of the renal primary cholecystectomy to confirm the diagnosis and perform tumor. Therefore, we diagnosed the gallbladder tumor adequate treatment. as a metastasis from renal cell carcinoma. Our pa- Theisolatedspecimenshowedapedunculated tient’s postoperative course was uneventful and she tumor in the fundus of the gallbladder, and the sur- was discharged at postoperative day 5. She is alive face of the tumor appeared black as a result of bleed- and recurrence free 3 years after cholecystectomy. ing (Fig. 3a). Microscopically, we observed prominent vascular proliferation in the stalk and basal part of Discussion the tumor (Fig. 3b). The tumor was hypercellular and This report showed a rare case of a patient who under- composed of clear cells arranged in funicular or al- went open simple cholecystectomy and presented gall- veolar growth with vascular interstitial tissue (Fig. 3c). bladder metastasis from RCC. Even when compared The surface of the tumor was covered by epithelium, with previous literature, the period from primary resec- and extensive hemorrhage was observed under the tion to gallbladder metastasis was relatively long. This surface (Fig. 3b). These histopathologic characteristics observation shows that patients with metachronous and coincided with those of the renal tumor resected 15 localized recurrences of RCC could be expected to years earlier (Fig. 3d, e). achieve long-term survival following resection. Fig. 3 The surgical specimen shows a black pedunculated tumor in the fundus of the gallbladder (a white arrow). Pathological examination of hematoxylin and eosin staining shows tumor cells with clear cellular cytoplasm growth (b ×20, c ×200), and it is similar to the features of the renal primary tumor (d ×20, e ×200) Saito et al. Journal of Medical Case Reports (2018) 12:162 Page 4 of 7 Fig. 4 Immunohistochemistry staining for vimentin shows that the tumor cells stain strongly but the gallbladder epithelium is negative. CK7 immunohistochemical staining also shows that the tumor cells barely stain, but the gallbladder epithelium stains strongly Distant metastases of RCC discovered during aut- density on an arterial enhanced phase image. Another opsy are found mostly in the lungs, liver, bones, and characteristic of these cases is the appearance of an contralateral kidney. Metastasis to the gallbladder is echo-bright area on the surface of the tumor, indicating very rare and is found in only 0.4–0.58% of autopsy a submucosal tumor on US . cases due to RCC . Only two reports have described the use of positron Malignant melanomas are the most common cause emission tomography (PET)/CT scans to differentiate of metastatic tumors of the gallbladder in Western gallbladder metastasis from RCC [2, 16]. Kawahara and countries, and metastases from lung, renal, pancreatic, colleagues documented a tumor mass on the gallbladder and colorectal cancers to the gallbladder have also wall on PET/CT images without high accumulation of been reported [2, 7]. To date, only 38 cases of RCC fluorodeoxyglucose (FDG) . The role of PET/CT in metastasizing to the gallbladder have been reported. gallbladder metastasis from RCC remains undefined. Furthermore, there have only been seven cases, in- Although RCC has some typical imaging characteris- cluding this one, in which the metastasis was diag- tics, it remains extremely difficult to distinguish cases nosed 10 or more years after surgical resection of the of primary and metastatic gallbladder carcinoma. In RCC [3, 8–13]. In all these cases, the histological type cases of RCC in which a gallbladder mass is observed was clear cell carcinoma. simultaneously or metachronously, the possibility of On previous report, the processes of metastasis to the gallbladder metastasis should be taken into account, al- gallbladder was grouped into two types, direct invasion though it is difficult to arrive at a preoperative diagno- of the tumor and invasion of the tumor into the capillar- sis of gallbladder metastasis. ies, stating that the latter process is comparatively rare In the present patient, the gallbladder tumor was . Gallbladder metastases occurred simultaneously in polypoid and over 10 mm in size. Furthermore, contrast- half of the cases and recurred metachronously in the other enhanced CT showed a high density on an arterial phase half. Another characteristic of these cases is the wide time imaging. We thought it might be a gallbladder polyp or range: 12 months to 27 years between the resection of the a malignant lesion, so we performed simple cholecystec- primary tumor and the reappearance of the tumor cells. tomy for diagnosis and treatment since no suspicious Dynamic contrast-enhanced CT is useful in the dif- findings of tumor invasion into the muscle layer of the ferential diagnosis of a metastatic gallbladder tumor gallbladder on preoperative imaging or intraoperative from RCC and a primary gallbladder carcinoma, because findings were noted. the former is hypervascular [14, 15]. In the case we de- Kavolius et al. have reported single organ metastasis scribe, contrast-enhanced CT showed the mass had high and recurrence-free survival as prognostic factors after Saito et al. Journal of Medical Case Reports (2018) 12:162 Page 5 of 7 Table 1 Previously reported cases of metastatic renal cell carcinoma of the gallbladder. Permission was granted by Ishizawa T., Okuda J., Kawanishi T. et al. © Asian Surgical Association and published by Elsevier B.V. 2006 to reuse this table Author Age/Sex Mode of Syn or Interval from Other site Op Macroscopic Size (cm) Outcome Year of metastasis Meta primary cancer of meta procedure findings source Saito (present 75/F Solitary Meta 15 y Lung SC Pedunculated 1.2×0.9 2 y alive 2018 case) Botting  66/M Solitary Meta 1 y 7 m (-) SC Polypoid 4.2×2 ND 1963 Terashima  61/M Multiple Syn (-) Bone EC Mass 2×2 2 m death 1990 Satoh et al.  71/M Solitary Syn (-) Pancreas EC Mushroom- 4×2.5 1 y 7 m alive 1991 shaped Fullarton  43/F Multiple Syn (-) Pancreas, SC Mass 3 5 m died from 1991 kidney cancer Golbey  84/M Solitary Meta 13y (-) SC Pedunculated 3.5 ND 1991 Nagler  82/M Solitary Meta 5y (-) EC Polypoid 3×3 ND 1994 Pagano  62/M Solitary Syn (-) Lung SC Round mass 3.5 disease free 1995 King  64/M Solitary Syn (-) (-) SC Polypod unclear 2 y 2 m disease 1995 free Fujii  69/M Multiple Syn (-) Adrenal gland EC Polypoid 2.8×2.5 3 m disease free 1995 Coskun  52/M Multiple Syn (-) bone SC Polypoid 3.5×2.5 ND 1995 Lombardo  77/M Solitary Meta 5 y (-) EC Polypoid 3×3 ND 1996 Kamimoto  53/M Multiple Meta 4 y (-) LC Polypoid 1.5 6 m alive 1996 Sparwasser  46/M Solitary Meta 3 y 8 m (-) Lung SC Polypoid 2.7×2.1 4 y4 m died from 1997 resected cancer Furukawa et al.  41/M Multiple Syn (-) Lung, chest SC Pedunculated 1.9×1.3 ND 1997 wall Uchiyama  64/M Multiple Meta 3 y Kidney SC Pedunculated 1.9×1.1 7 m alive 1997 Celebi  73/M Solitary Syn (-) Lung EC Mushroom- 2.8×2 1 m died from 1998 shaped other disease Ueki  69/F Solitary Syn (-) (-) EC Pedunculated 1.6 7 m disease free 2001 Gekiya  68/M Solitary Meta 15 y (-) SC Polypoid ND 1 y disease free 2002 Aoki  63/M Solitary Meta 27 y (-) SC Pedunculated 7.5×3 6 y disease free 2002 Aoki  80/M Solitary Meta 8 y Lung SC Pedunculated 4.5×2.5 2 y disease free 2002 Miyagi  53/M Solitary Meta 10 y 6 m (-) LC Polypoid 2.5×1.5 ND 2003 Limani  64/M Solitary Meta 1 y (-) LC Mass ND ND 2003 Ishizawa et al. 73/M Solitary Meta 5 y (-) SC Pedunculated 3.5×2 2 y disease free 2006 Hellenthal  39/M Solitary Syn (-) (-) SC Polypoid ND 2 y 6 m alive 2007 Ricci  72/F Solitary Meta 16 y Pancreas LC Mass ND ND 2008 Nojima  61/M Solitary Syn (-) (-) SC Polypoid 1.5 10 m alive 2008 Sand  48/F Solitary Meta 5 y Pancreas, SC ND ND 2 m alive 2009 kidney Patel et al. 64/F Solitary Meta 6 y (-) LC Polypoid 3 ND 2009 Kawahara et al. 73/F Solitary Syn (-) Lung SC Polypoid 1.0×0.8 ND 2010 Shoji et al. 50/M Multiple Meta 3 y Adrenal grand SC Polypoid 1.1×0.9 8 m alive 2010 Fang et al. 45/M Solitary Meta 1 y Lung SC Polypoid 1.9×1.0 2 y 4 m death 2010 Fang et al. 65/F Solitary Meta 1 y Psoas muscle SC Polypoid 2.5×2.5 7 m death 2010 Fang et al. 54/M Solitary Meta 7 y (-) SC Polypoid 1.5×1.0 2 y 3 m alive 2010 Fang et al. 51/M Solitary Meta 6 y Kidney SC Polypoid 1.7×0.8 3 y 1 m alive 2010 Decoene et al. 47/F Solitary Meta 16 y Bone, ovary LC Polypoid 1.9 ND 2011 Saito et al. Journal of Medical Case Reports (2018) 12:162 Page 6 of 7 Table 1 Previously reported cases of metastatic renal cell carcinoma of the gallbladder. Permission was granted by Ishizawa T., Okuda J., Kawanishi T. et al. © Asian Surgical Association and published by Elsevier B.V. 2006 to reuse this table (Continued) Author Age/Sex Mode of Syn or Interval from Other site Op Macroscopic Size (cm) Outcome Year of metastasis Meta primary cancer of meta procedure findings source Jain and Chopra 49/F Solitary Meta 6 y (-) SC Polypoid 1.45×1.0 ND 2013  Ueda et al. 43/M Solitary Meta 1 y (-) EC Pedunculated 2.6 ND 2015 Abbreviations: Syn synchronous metastasis, Meta metachronous metastasis, SC simple cholecystectomy, ND not determined, EC extended cholecystectomy, LC laparoscopic cholecystectomy resection of metachronous metastatic lesions . Chung Conclusions et al. reported eight cases of patients with isolated gall- In conclusion, we describe a rare case of gallbladder me- bladder metastasis recurrence-free survival (observed tastasis from RCC diagnosed 15 years after primary cancer median 1.1 years, range from 0.1 to 6 years) in a cohort resection. In patients with a history of RCC, observation study of 33 renal cell carcinoma cases , and they of a vascular-rich polypoid lesion of the gallbladder should thought that isolated gallbladder single metastasis was raise the possibility of metastasis. Cholecystectomy may an indication for surgery. result in favorable long-term survival of patients with Although extended cholecystectomy is the standard RCC metastases to the gallbladder. operation when there is a strong suspicion of primary Abbreviations gallbladder cancer, it is important to excise metastatic le- CK7: Cytokeratin 7; CT: Computed tomography; FDG: Fluorodeoxyglucose; sions of RCC to the gallbladder. In Table 1, nine cases of PET: Positron emission tomography; RCC: Renal cell carcinoma; US: Ultrasonography simple cholecystectomy, including laparoscopic surgery, for an isolated metastasis to the gallbladder resulted in Acknowledgements cancer-free survival in all cases (including the present Not applicable. case). Therefore, if there is no obvious invasion of the gallbladder bed, a simple resection including laparo- Funding This case report had no source of financial or material support. scopic surgery is expected to be curative. For an adequate follow-up and informed decisions Availability of data and materials about adjuvant immunotherapy with interleukin-2 and Ishizawa et al.  gave their consent to reuse the Table of their publication in Table 1 of this publication. interferon alpha after cholecystectomy, gallbladder me- tastasis of RCC should be differentiated from primary Declarations clear cell carcinoma of the gallbladder through histo- The authors guarantee that the work described in this study has not been chemical examination. Immunohistochemically, primary published previously. clear cell carcinoma of the gallbladder is strongly posi- Authors’ contributions tive for CK7 but negative for vimentin, and metastatic YS wrote this manuscript. HO, MY, SO, TF, MY, MO, YO, HN, EO, and HO RCC of the gallbladder is positive for vimentin but nega- helped to draft the manuscript and revised it critically. All authors have read tive for CK7 . Based on the immunohistochemical and approved the final manuscript. findings, our final diagnosis was metastatic gallbladder Authors’ information tumor from RCC as opposed to primary clear cell car- YS, MY, TF, MY, and YO are Staff Surgeons of the Department of Surgery, cinoma of the gallbladder. Medical Corporation JR Hiroshima Hospital. HO is a Staff Surgeon of the Department of Surgery, Onomichi General Hospital. SO is a Staff Doctor in The follow-up information on the previously reported Palliative Care, Medical Corporation JR Hiroshima Hospital. MO is a Staff cases is not sufficient to demonstrate the curability of Member in Dialysis Surgery, Medical Corporation JR Hiroshima Hospital. HN is cholecystectomy for a metastasis of RCC, since late re- a Pathologist in the Department of Pathology and Laboratory Medicine, Medical Corporation JR Hiroshima Hospital. EO is the Hospital Director, currence is not uncommon with RCC. However, nine Medical Corporation JR Hiroshima Hospital, and HO is a Professor of the patients were reported to be cancer free with the lon- Department of Gastroenterological and Transplant Surgery, Applied Life gest follow-up interval of 6 years after cholecystectomy, Sciences, Institute of Biomedical & Health Sciences, Hiroshima University. and eight of these had a solitary metastasis. These re- Ethics approval and consent to participate ports suggest a favorable prognosis after cholecystec- This case report has been approved by the research ethics committee and tomy, particularly in patients with a solitary metastasis. written informed consent was obtained from the patient for participation of Even for multiple metastases of RCC, cholecystectomy this case report. may be advocated, because the survival rates after cura- Consent for publication tive resection ofsecondand thirdmetastaseshavenot Written informed consent was obtained from the patient for publication of been found to be different from those after a first this case report and any accompanying images. A copy of the written metastectomy . consent is available for review by the Editor-in-Chief of this journal. Saito et al. Journal of Medical Case Reports (2018) 12:162 Page 7 of 7 Competing interests 21. Golbey S, Gerard PS, Frank RG. 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