Laparoscopic Right Hemicolectomy Using a Fluorescent Ureteral Catheter for Ascending Colon Metastasis of Endometrial Cancer in a Patient with Horseshoe Kidney: A Case Report.

A 61-year-old woman with a body mass index of 40 had undergone a radical hysterectomy and wedge resection for endometrial cancer (endometrioid adenocarcinoma, pStage IB) 27 years earlier and had been followed up in our gynecology department. She had a history of hypertension, hyperuricemia, and carpal tunnel syndrome. Routine follow-up tests revealed elevated tumor marker levels (CA125: 38 U/mL, CA19-9: 120 U/mL, CEA: 2.0 U/mL). Contrast-enhanced computed tomography (CECT) demonstrated wall thickening of the ascending colon with enlargement of the paracolic lymph nodes; however, no other apparent metastatic lesions were identified ( Figure 1a, b ). In addition, a horseshoe kidney was identified ( Figure 1c ). Although no duplicated renal pelvis was observed, the ureters coursed ventrally to the kidneys ( Figure 1d ). Accessory renal arteries arising directly from the abdominal aorta were identified ( Figure 1e ). Positron emission tomography-computed tomography indicated increased uptake at the tumor site (maximum standardized uptake value: 35.18). Colonoscopy demonstrated a 50-mm type 5 tumor in the ascending colon ( Figure 1f ). The biopsy showed estrogen receptor-positive adenocarcinoma, raising the suspicion of metastatic endometrial carcinoma. Case images. (a) (b) Contrast-enhanced computed tomography reveals wall thickening of the ascending colon (arrow) with enlargement of the paracolic lymph nodes (circles). (c) A horseshoe kidney is identified. (d) The ureters and gonadal vessels course ventral to the kidney. (e) Accessory renal arteries arising directly from the abdominal aorta. (f) Colonoscopy demonstrates a 50-mm type 5 tumor in the ascending colon. * ureter; # gonadal vessels. The preoperative diagnosis was endometrial cancer with metastasis in the ascending colon, and surgical resection was planned. Several factors made laparoscopic surgery difficult, including high obesity, a history of pelvic surgery, and anatomical variation of the horseshoe kidney. The anatomical features were clarified by preoperative CECT ( Figure 2 ). To safely perform the laparoscopic surgery, FUCs were inserted in the bilateral ureters preoperatively. Schematic illustration of the case. The black arrows indicate accessory renal arteries. Under general anesthesia, Near-Infrared Ray Catheter (NIRC™) FUCs were inserted in the bilateral ureters using a cystoscope and fluoroscope with the patients in the lithotomy position, and laparoscopic right hemicolectomy with fluorescent ureteral navigation was performed. Intraoperatively, severe adhesions were observed around the pelvic cavity, which were carefully dissected. Furthermore, there was a large amount of visceral fat, which extended the operative time. After the adhesions were dissected, colonic mobilization was performed using an inferior approach. During this procedure, the right ureter was easily identified using fluorescence ( Figure 3a-d ). Owing to fluorescent ureteral navigation, the right ureter could be easily identified and secured while maintaining the dissection layer that preserved Gerota's fascia, which included the kidney, ureter, gonadal vessels, and duodenum. The procedure was completed without any inadvertent injury ( Figure 3e ). After colonic mobilization, lymph node dissection was performed along the left border of the superior mesenteric vein. Subsequently, the ileocolic vein and artery were cut. Extracorporeal anastomosis was performed using a functional end-to-end anastomosis technique. The operative time was 379 minutes, and the blood loss was low. Surgical findings. Colonic mobilization is performed using an inferior approach under near-infrared fluorescence imaging. (a) White-light imaging. (b) Near-infrared fluorescence imaging. The ureter can be identified. (c) (d) Under the fluorescence visualization, the dissection layer can be maintained to perform the complete mesocolic excision. (e) The procedure is completed without any inadvertent injury. * ureter; # gonadal vessels; ¶ kidney; † duodenum. The postoperative course was uneventful, and the patient was discharged on postoperative day 10. The macroscopic findings revealed a type 5 tumor with a maximum size of 55 mm in the ascending colon ( Figure 4a ). The histological examination showed that the lesion was predominantly located in the submucosa, with carcinoma cells proliferating in fused tubular and tubular patterns and invaded the subserosal tissue. Focal morular-like structures were also observed. Definitive histological evidence of endometriosis was not observed. The histological features were similar to those of the endometrial cancer resected 27 years earlier ( Figure 4b-e ). Immunohistochemical findings showed CK7 (focally +), CK20 (-), estrogen receptor (+), progesterone receptor (+), PAX8 (+), vimentin (+), β-catenin (focally + in the nucleus), CD10 (focally +), CDX2 (focally +), and p53 (–), SATB2 (–). The Ki-67 labeling index was approximately 50% ( Figure 4f-i ). Therefore, the lesion was diagnosed as endometrial cancer with metastasis to the ascending colon. Tumor findings. (a) A type 5 tumor approximately 5.5 cm × 3 cm in size at the ascending colon is observed. (b) (c) Histological findings of the resected colonic tumor demonstrate fused tubular structures (hematoxylin and eosin-stained, b: 10×, c: 40×). The histological appearance differs from that of typical colorectal adenocarcinoma. (d) (e) Histological findings of the endometrial cancer resected 27 years earlier. The tumor is endometrioid carcinoma. Despite degradation of the aged specimen, the histological features are similar to those of the current specimen. (hematoxylin and eosin-stained, d: 10×, e: 40×) (f) Immunohistochemical staining shows positive for estrogen receptor. (g) Immunohistochemical staining shows positive for progesterone receptor. (h) Immunohistochemical staining shows positive for PAX8, which is a marker characteristic of gynecologic tumors. (i) Immunohistochemical staining for SATB2, which is a marker typically expressed in colorectal carcinoma, is negative. The patient received systemic chemotherapy (paclitaxel and carboplatin, 6 courses) and was alive without recurrence 13 months after surgery.

Informed Consent Written informed consent was obtained from the patient.

We presented a case of laparoscopic right hemicolectomy using fluorescent ureteral navigation in a patient with obesity with recurrent endometrial carcinoma and anatomical variations associated with a horseshoe kidney. In this case, preoperative CT demonstrated an abnormal ureteral course anterior to the renal isthmus and accessory renal arteries, indicating a potentially increased risk of ureteral injury during laparoscopic surgery. This case highlights the usefulness of FUCs for safe real-time ureteral identification and precise dissection in colorectal surgery performed under complex anatomical conditions. FUCs are especially beneficial for patients with advanced colorectal cancer located close to the ureter, severe obesity, or severe adhesions from prior abdominal surgery[ 11 ]. Furthermore, FUCs can be useful in patients with anatomical variations such as urinary diversion with an ileal conduit[ 12 ]. In the present case, the patient had severe obesity and a history of laparotomy in the pelvic cavity, which may have increased the risk of ureteral injury. In anatomical variation associated with a horseshoe kidney, in which the ureteral course is unusual, additional care is required to prevent ureteral injury. Therefore, fluorescent ureteral navigation-guided minimally invasive surgery is considered extremely beneficial. Regarding the safety and usefulness of FUCs, Ryu et al.[ 10 ] reported the results of 20 patients who underwent minimally invasive surgery with FUC insertion. The authors suggested that this technique may be useful for the education and training of non-expert surgeons by facilitating an understanding of the ureteral course and enabling clear recognition of the appropriate dissection line. Furthermore, in a recent report of 141 consecutive patients with colorectal cancer who underwent minimally invasive surgery with fluorescent ureteral navigation, FUC insertion was a relatively safe and simple procedure, with a reported insertion time of 12 minutes, blood loss of 10 mL, no ureteral injuries, and no conversion to laparotomy[ 11 ]. In this patient, the FUCs were inserted in 12 minutes without catheter-related complications. In addition, FUCs can be clearly visualized without releasing them under laparoscopic fluorescence observation, and contribute to maintaining the appropriate anatomical layer while securing the ureter. Horseshoe kidney is a relatively rare congenital anomaly characterized by fusion of the lower poles of the bilateral kidneys, with a reported incidence of 0.17–0.25%[ 1 ]. It is frequently associated with anatomical variations, including accessory renal arteries and abnormal urinary tract courses. Because the renal hilum is often located ventrally, the ureters usually run along the ventral aspect of the kidney; however, variations such as dorsal passage to the renal isthmus, lateral course, or duplicated ureters have also been reported. Accessory renal arteries are present in nearly 70% of patients with a horseshoe kidney and may arise from various vessels, including the abdominal aorta, common iliac artery, internal iliac artery, and inferior mesenteric artery[ 14 ]. Therefore, detailed preoperative imaging evaluation, including three dimensional computed tomography (3D-CT) angiography, is essential to avoid inadvertent vascular or ureteral injury[ 15 ]. Although 3D-CT angiography was not performed for this patient, thin-slice CECT in axial and coronal sections allowed accurate identification of the ureteral course and accessory renal arteries. In particular, accessory renal arteries were identified arising from the abdominal aorta and the right common iliac artery ( Figure 2 ). Therefore, detailed preoperative identification of anatomical variations is essential for safely performing the surgical procedures. Late recurrence occurring more than 5 years after surgery for endometrial cancer have been reported in the lungs (22.4%), local lymph nodes (20.7%), and carcinomatosis (20.3%)[ 4 ]. As in this case, recurrence after a long time period following surgery is extremely rare. To the best of our knowledge, only 5 cases of recurrent endometrial carcinoma more than 20 years after surgery have been reported ( Table 1 )[ 2 , 5 - 8 ]. Of the five reported cases, recurrence occurred in the lungs in three cases, rectum in one case, and vagina in one case. Except for one patient who received palliative chemotherapy because of poor general condition, surgical resection was performed in the patients with metastatic recurrence to the lung or rectum. In some patients, adjuvant chemotherapy[ 2 , 5 ] or hormonal therapy[ 7 ] is administered after surgery. Radiotherapy is selected as the treatment modality for patients with vaginal recurrence[ 8 ]. In the present case, metastasis of endometrial carcinoma to the ascending colon was detected 27 years after the initial surgery. Long-term follow-up was continued because a nodular lesion was detected in the pelvis on follow-up CT, which fortuitously allowed the detection of tumor marker elevation. No distant metastases other than the ascending colon lesion were identified; therefore, laparoscopic right hemicolectomy was performed for resection of the metastatic lesion. Cases of Late Recurrence of Endometrial Carcinoma More than 20 Years after Initial Surgery Reported in the Literature. H: hysterectomy, BSO: bilateral salphingo-oophorectomy, L: lymphadenectomy, CT: chemotherapy, HT: hormone therapy The present case highlights the importance of considering the possibility of endometrial cancer recurrence even after a prolonged disease-free interval in women with a history of definitive treatment for endometrial carcinoma. In conclusion, we reported an extremely rare case of ascending colon metastasis from endometrial carcinoma in a patient with a horseshoe kidney. Fluorescent ureteral navigation-guided minimally invasive surgery enabled safe and precise dissection during laparoscopic right hemicolectomy. This procedure may be useful in preventing ureteral injury during colorectal surgery, especially in patients with anatomical variations. Considering the possibility of recurrence in the differential diagnosis of a tumor, regardless of the time elapsed since curative treatment in women with a history of endometrial carcinoma is important.

A horseshoe kidney is a relatively rare congenital anomaly in which the bilateral kidneys are fused at their lower poles, with a reported incidence of approximately 1 in 400–600 individuals[ 1 ]. It is frequently associated with anatomical variations in the vascular and pelvicalyceal ureteral systems, which increases the risk of inadvertent injury during colorectal surgery. Endometrial cancer is one of the most common malignancies among women in developed countries. In general, late recurrence (recurrence occurring more than 5 years after surgery) is considered extremely rare[ 2 ]. Accordingly, current guidelines recommend limiting oncological follow-up to 5 years after treatment[ 3 ]. The rate of late recurrence more than 5 years after surgery for endometrial cancer is approximately 1% (23/2233)[ 4 ]; however, only a limited number of cases have described recurrence or metastasis occurring more than 20 years after surgery for endometrial cancer[ 2 , 5 - 8 ]. Furthermore, cases of late metastasis to the colon, as observed in the present case, are extremely rare. In recent years, fluorescent ureteral catheters (FUCs) have been introduced, which are applicable in colorectal surgery[ 9 , 10 ]. FUCs can be useful in patients with locally advanced cancers close to the ureter, history of pelvic surgery[ 11 ], and anatomical variations[ 12 ]. However, to the best of our knowledge, only one case has reported the effectiveness of FUCs in colorectal surgery for a patient with a concomitant horseshoe kidney[ 13 ]. Herein, we report a case of a patient with a horseshoe kidney who underwent laparoscopic surgery with fluorescent ureteral catheter placement for recurrent endometrial cancer in the ascending colon. In addition, we have provided a review of the relevant literature.

The authors declare that there are no conflicts of interest