A Transanal Endoscopic Ultrasound-guided Fine-needle Aspiration Biopsy for an Intrapelvic Tumor Diagnosed as Recurrence of a Smooth Muscle Tumor of Uncertain Malignant Potential Following Uterine Morcellation.

A 71-year-old woman presented to our department with a chief symptom of dull pain in the right lower quadrant. Three years previously, she had undergone uterine morcellation for a myoma ( Fig. 1a ). She took medications for hypertension and hyperthyroidism. She had a nonspecific family history. She was a never-smoker and social drinker. Microscopic findings of the specimen obtained by uterine morcellation, a transanal EUS-FNAB, and a second operation for the intrapelvic tumor. a) Uterine morcellation; sparse, round, and well-shaped nuclei indicate myoma [Hematoxylin and Eosin (H&E) staining]. b-d) The EUS-FNAB at the sigmoid colon; (b) dense, malformed, and nucleolus-rich nuclei. In addition, mitosis is recognized (H&E staining). (c) Cytoplasm is well stained by anti-alpha-smooth muscle actin antibody. (d) Some nuclei are stained by anti-Ki67 antibody. MIB1 index is 20%. e-h) Second operation; (e) denser, malformed, and nucleolus-rich nuclei. In addition, mitosis is recognized. (f) The specimen includes necrotic areas (H&E staining). (g) Cytoplasm is well stained by anti-alpha-smooth muscle actin antibody. (h) The MIB1 index is 10%. All microscopic photographs are magnified 400×. Scale bars indicate 20 μm. EUS-FNAB: endoscopic ultrasound-guided fine-needle aspiration biopsy During the physical examination, her body temperature was 36.6°C, and neither tenderness nor palpable mass was observed. The laboratory findings on admission are summarized in Table . Mild systemic inflammation and elevated serum carbohydrate antigen 125 levels were observed. Contrast-enhanced computed tomography (CT) demonstrated a right-intrapelvic irregular mass, 55 mm in diameter, with hypoenhancement. The tumor surrounded the right ureter and iliac artery ( Fig. 2 ). A right ureteral stent was indwelled; however, the urinary cytology was negative for malignancy. Next, we investigated the colon and terminal ileum. During colonoscopy, the scope was advanced to the terminal ileum as much as possible, and enteroclysis was performed. However, there were no significant findings ( Fig. 3 ). Laboratory Findings on Admission. WBC: white blood cells, Hb: hemoglobin, Plt: platelet, CRP: C-reactive protein, BUN: blood urea nitrogen, CRN: creatinine, T-Bil: total bilirubin, AST: aspartate aminotransferase, ALT: alanine aminotransferase, Alb: albumin, INR: prothrombin time-international normalized ratio, CEA: serum carcinoembryonic antigen, CA19-9: serum carbohydrate antigen 19-9, CA125: serum carbohydrate antigen 125, IL2-R: serum soluble interleukin-2 receptor Images of contrast-enhanced computed tomography. CE-CT demonstrated a right-intrapelvic irregular mass 55 mm in diameter with hypoenhancement. The tumor surrounded the right ureter and iliac artery. Right hydronephrosis was also observed. Yellow solid arrows indicate the tumor. CE-CT: contrast-enhanced computed tomography Radiological enteroclysis with an endoscopic view in the terminal ileum. There was an insignificant finding in the terminal ileum and colon. Four days after colonoscopy, we attempted a transanal EUS-FNAB using the following instruments: a colonoscope (EC-L600ZP7; Fujifilm, Tokyo, Japan), a 0.035-inch ultra-stiff guidewire (Wrangler SUS endoscopic guidewire; Piolax Medical Devices, Yokohama, Japan), a linear echoendoscope (EG-580UT; Fujifilm), and a 22-gauge Franseen needle (Acquire; Boston Scientific, Marlborough, USA). First, we inserted the colonoscope into the cecum and placed an ultra-stiff guidewire. The linear echoendoscope was then placed over the guidewire. Finally, an EUS-FNAB was performed at the cecum and sigmoid colon for pelvic tumors ( Fig. 4 ). Specimens were procured over 2 passes at the cecum and 1 pass at the sigmoid colon, with 10 strokes in both. Unfortunately, a rapid on-site evaluation was unavailable at our institution. Ceftriaxone sodium at 1.0 g/day for 3 days was intravenously administered prophylactically. The postprocedure course was uneventful. Fluoroscopic images with the endosonographic image of transanal EUS-FNAB. a) The EUS-FNAB at the cecum. b) The EUS-FNAB at the sigmoid colon. EUS-FNAB: endoscopic ultrasound-guided fine-needle aspiration biopsy Hematoxylin and Eosin staining of the obtained specimen revealed atypical cells that mimicked epidermal differentiation with nuclear atypia and 5 mitotic counts per 10 high-power fields (HPFs). However, it was difficult to assess the coagulative necrosis in the EUS-FNAB specimen. Immunohistochemical (IHC) staining for alpha-smooth muscle actin (α-SMA) and Ki67 revealed that this tumor was derived from smooth muscle and involved a high cell proliferation activity element with an MIB1 index of 20% ( Fig. 1b-d ). The provisional diagnosis was suspicious STUMP derived from the previous uterine morcellation for myoma. Therefore, we consulted a gynecologist. The patient underwent surgical curettage for a definitive diagnosis. The obtained specimen revealed nuclear atypia and coagulative necrosis but included 1 mitotic count per 10 HPFs. An IHC analysis of α-SMA and Ki67 revealed that this tumor was derived from smooth muscle and had an MIB1 index of 10% ( Fig. 1e-h ). The final pathological diagnosis was recurrence of STUMP rather than leiomyosarcoma caused by previous uterine morcellation for the myoma.

We encountered a rare case of an intrapelvic tumor diagnosed by a transanal EUS-FNAB with recurrence of STUMP caused by previous uterine morcellation for myoma. An EUS-FNAB is a low-invasive, well-established tissue acquisition technique, especially for solid pancreatic masses, with a very accurate diagnostic yield (sensitivity and specificity, 85-89% and 96-99%) and has a significant impact on patient management ( 1 , 7 ). However, an EUS-FNAB through the rectum is suggested only for confirmation of suspected recurrent colorectal cancer ( 1 ). In addition, an EUS-FNAB at the proximal colon remains challenging because of difficulty performing echoendoscope intubation due to scope oblique viewing, stiffness, and lumen flexibility. However, if physicians could obtain specimens from a tumorous lesion of unknown origin in the abdominal cavity, an EUS-FNAB would also affect patient management. We believe that physicians can perform a transanal EUS-FNAB in cases with a lesion close to the retroperitoneal fixed organs, including the cecum, ascending or descending colon, and rectum. Furthermore, if the lesion exists apart from the colon, an EUS-FNAB of intraperitoneal organs, including the sigmoid and transverse colon, would be possible, taking advantage of those colonic mobilities. However, such an approach would depend on the colonic length and shape, limiting the scope trajectory. In the present case, the target lesion was dominant in the right pelvic cavity and could have involved heterogeneous components, including necrosis. Before performing the EUS-FNAB, we speculated that puncture would more easily access the cecum due to the scope trajectory. However, puncture at the sigmoid colon depends on this length and shape. Therefore, attempting an EUS-FNAB in both the cecum and sigmoid colon was considered reasonable. However, the EUS-FNAB at the cecum did not help obtain a diagnosis because of the presence of necrotic tissue, but the EUS-FNAB from the sigmoid colon aided in the diagnosis because sufficient material was able to be collected. Descriptions of adverse events (AEs) in recent articles have been conflicting ( 8 , 9 ). Razik et al. initially investigated lower endoscopic ultrasonography (EUS)-related AEs in isolation from other lower endoscopic procedures. They reported that the rates of AEs with lower EUS without and with a FNAB were 1% (5/495) and 9% (2/23), respectively. These results were not significant compared to the findings of upper EUS with or without an FNAB. Unfortunately, details of lower EUS-FNAB-derived AEs were not mentioned in their study. Those authors also reported no lethal AEs with EUS, regardless of an upper or lower approach and the presence or absence of an FNAB. However, they did not include patients who underwent an EUS-FNAB of the proximal colon. Therefore, evaluations of transanal EUS should be performed in a well-designed study, including EUS-FNABs in the proximal colon ( 9 ). A CT-guided biopsy for pelvic tumors is a viable alternative strategy ( 10 ); however, no head-to-head comparative study of CT-guided biopsy and EUS-FNAB has yet been conducted. Although an EUS-FNAB with a forward-viewing echoendoscope might be able to overcome scope intubation issues ( 11 ), it would be difficult to pinpoint the target lesion with the narrow scanning range (90°) of such an approach ( 3 ). The overtube and guidewire techniques ( 12 , 13 ) assist with scope intubation, although they are costly. We performed ultra-stiff guidewire-assisted scope intubation using a shallow oblique view (40°) echoendoscope under fluoroscopic and endoscopic guidance ( 3 ). A dedicated echoendoscope (EG-580UT) was advanced in the lumen under constant recognition of the scope tip in the endoscopic view. This advantage avoids the risk of perforation by the scope tip and scope obstruction when the scope tip takes over the colonic haustra. Notably, the guidewire did not emerge in front of the scope tip; therefore, we must always confirm whether or not the scope tip has taken over each haustrum following the guidewire. However, this procedure has some drawbacks. The technical success of an EUS-FNAB is dependent on the location and size of its target lesion; such a biopsy would be impossible if a small lesion were located on the backside of the scope. Uterine morcellation using laparoscopic instruments has been introduced as a minimally invasive approach. However, in 2021, the American College of Obstetricians and Gynecologists stressed keeping in mind the following when carrying out uterine morcellation: the importance of the pre-evaluation and stratification of malignancy of the uterine corpus, the risk of dissemination of an occult uterine malignancy as well as benign uterine tissue, and the need to obtain informed consent concerning the advantages and drawbacks ( 5 ). Uterine morcellation carries a risk of inducing dissemination to malignant and benign tissues. Leiomyosarcoma has a low prevalence of 1/750 to 1/570 but is not reliably identifiable preoperatively ( 5 ). Therefore, uterine morcellation is not recommended for patients who are postmenopausal or over 50 years old because of the increased prevalence of this lesion ( 5 ). For benign disease, uterine morcellation has been associated with intraperitoneal implants in cases of endometriosis (1.4%), adenomyosis (0.57%), parasitic leiomyomas (0.9%), and rarely disseminated peritoneal leiomyomatosis ( 5 , 14 ). In the present case, the intrapelvic tumor was revealed to be STUMP recurrence following uterine morcellation. According to the World Health Organization (WHO) classification 2014, uterine smooth muscle tumors are classified as benign leiomyomas, malignant leiomyosarcomas, and STUMP ( 15 ). The Stanford criteria for leiomyosarcoma require at least 2 of the following criteria to be met: marked cellular atypia, ≥10 mitoses/10 HPFs, and coagulative tumor cell necrosis, whereas absence of necrosis and atypia with ≤4 mitoses indicating leiomyoma ( 16 ). The WHO classification indicates that a uterine smooth muscle tumor not diagnosed unequivocally as benign or malignant should be defined as STUMP ( 15 ). In addition, STUMP was identified in 0.06% of patients who underwent electric power uterine morcellation ( 6 ). Therefore, STUMP recurrence following uterine morcellation has been reported even in benign cases ( 17 , 18 ). In the present case, the initial diagnosis of uterine morcellation was myoma; however, intrapelvic recurrence was discrepantly diagnosed as STUMP. In the first uterine morcellation, the specimen could not be evaluated as a whole. Therefore, it is reasonable to consider the possibility of a heterogeneous giant myoma including lurking STUMP cells. In the present case, spillage of these STUMP cells occurred after morcellation, not the malignant transformation of myoma cells. We remind physicians who encounter an intrapelvic tumor of unknown etiology following previous uterine morcellation to consider recurrence derived from the morcellation, even if the previous diagnosis was myoma. We demonstrated the potential utility of a transanal EUS-FNAB for the cytopathological diagnosis of intrapelvic tumors.

An endoscopic ultrasound-guided fine-needle aspiration biopsy (EUS-FNAB) is a well-established tissue sampling method ( 1 ), although it remains challenging to perform using a linear echoendoscope in the proximal colon because of its depictability and scope of intubation ( 2 - 4 ). Uterine morcellation has emerged as a minimally invasive approach that reduces the size of the uterus or leiomyoma by creating smaller pieces to remove tissue through small incisions or with laparoscopic instruments ( 5 ). However, presumed leiomyomas include unexpected leiomyosarcoma, uterine cancer, and smooth muscle tumors of uncertain malignant potential (STUMP) with a certain probability ( 5 , 6 ). Therefore, this novel technique carries a risk of inducing intrapelvic dissemination of occult uterine neoplasms ( 5 ). We herein report an intrapelvic tumor diagnosed using a transanal EUS-FNAB as recurrence of STUMP following uterine morcellation.

The authors state that they have no Conflict of Interest (COI).