Gastric cancer (GC) is the fifth most common cancer worldwide and the fourth leading cause of cancer-related death, with a relatively low survival rate.¹ In Korea, GC is the fourth most common cancer after thyroid, lung, and colorectal cancer.² Advances in early detection and treatment have improved the survival rates in Korea, with the five-year survival rate for surgically treated advanced gastric cancer increasing from 43.9% (1993–1995) to 77.5% (2015–2019).³ Recently reported surgical treatment results for advanced gastric cancer of T2N0M0 or higher have reported a five-year survival rate of up to 88.9%.⁴ The recurrence rate after curative surgery for gastric cancer was reportedly 20–50%.⁵ Therefore, long-term survivors after surgical treatment for gastric cancer are increasing. The recurrence rate of gastric cancer in long-term survivors of more than five years after curative resection is reported to be approximately 6% to 10.8% in Japan and Korea, respectively.^6,7 On the other hand, the rate of late recurrences 10 years after surgical treatment for advanced gastric cancer is still rare. Moreover, gastrointestinal metastases of gastric cancer are rare despite being one of the most common causes of secondary colonic invasion by gastric cancer.⁸ In particular, very few metachronous rectal metastases (Schnitzler’s metastasis) that spread to the rectum 13 years after a curative resection of gastric cancer have been reported.⁹ This paper reports a case of a metachronous rectal metastasis that may have occurred due to venous and lymphangitic spread 13 years after a curative resection of GC.

A 54-year-old man presented with constipation with a six-month duration and a 5 kg weight loss over 10 months. He had a history of subtotal gastrectomy (Billroth-II anastomosis) for advanced gastric cancer 13 years ago. The pathology revealed poorly differentiated adenocarcinoma with serosal penetration and multiple lymph node metastases (pT4a N3aM0). No recurrence was noted after eight years of follow- up. The patient underwent routine annual health checkups for the past four years at the authors’ center, including gastroduodenoscopy, colonoscopy, abdominal sonography, and blood tests. Annual checkup results showed negative.

The patient was not a smoker or heavy alcoholic. He had controlled diabetes mellitus and hypertension for three years. One year before presentation, the patient visited the urology clinic due to voiding difficulties. The prostate-specific antigen (PSA) level was normal (0.30 ng/mL), and transrectal prostatic sonography (estimated prostate volume of 20 cc) suggested benign prostatic hyperplasia (BPH). Symptomatic medication was prescribed, but the voiding difficulties persisted.

The patient’s blood pressure was 125/77 mmHg, heart rate 65/min, respiratory rate 20/min, and body temperature 36.7°C. The general appearance was good. A physical examination revealed no superficial lymph nodes or organomegaly, but a hard, concentric stenosis was palpable at the fingertip on a digital rectal exam (DRE). Blood tests were normal except for slightly elevated creatinine (1.55 mg/dL), and carcinoembryonic antigen (CEA) level (2.39 ng/mL) was also normal. A colonoscopy revealed a firm, circular, in-growing mass in the rectum (Fig. 1). An abdominopelvic CT scan showed a low attenuating mass near the rectal wall, invading the right ureterovesical junction (UVJ), causing hydroureteronephrosis. This showed rectal invasion with concentric tumor infiltration in the mural portion abutting the mid portion of the rectal wall (Fig. 2). An MRI scan confirmed rectal wall thickening with strong mucosal enhancement of the mid rectum and involvement of the prostate, mesorectal fascia, and both seminal vesicles (Fig. 3).

Figure 1. Colonoscopy findings. (A) In a colonoscopy performed two years earlier, an abnormality in the colon wall at the mid-rectum at the six o’clock position was observed, but it was overlooked at the time, and a biopsy was not performed. (B) Upon endoscope insertion, a firm concentric in-growing mass-like lesion with a significantly narrowed rectal lumen was observed at 10 cm from the AV. (C) The findings observed by retroflexion of the narrowed area show a stenotic area tightly constricted the endoscopic scope. (D) Redness, mucosal nodularity, and shallow ulceration were observed in the stricture area during scope withdrawal.

Figure 2. Abdominopelvic CT findings. (A) Right hydronephrosis due to posterior wall invasion of the urinary bladder is shown. (B, C) A roughly sized 3.0×1.2 mass with focal periprostatic fatty infiltration and an abutting mass in the anterior wall of the rectum was observed, and concentric wall thickening was observed in the mid portion of the rectum. (D) In the coronal view, concentric wall thickening of the rectal wall.

Figure 3. Rectal MRI findings. (A) Eccentric wall thickening of the urinary bladder base and a right dilated distal ureter are observed. (B, C) In addition to strong mucosal enhancement in the mid-rectum, concentric target-like wall thickening was observed, and invasion of the prostate, bilateral seminal vesicles, and mesorectal fascia were observed.

A PET-CT scan revealed low FDG uptake on the rectal or prostate area but high FDG uptake (SUL max 7.7) along the right renal parenchyma, suggesting obstructive uropathy (Fig. 4). The biopsy indicated a poorly differentiated carcinoma, favoring a metastasis. An immunohistochemistry study confirmed metastatic gastric adenocarcinoma by diffuse positive for CK7 (cytokeratin-7), focally weakly positive for caudal-type homeobox 2 (CDX-2), and negative for MUC2 (mucin, the intestinal phenotype), CK20, and PSA (Fig. 5). In the case of colon cancer, the positivity of CK20 and CDX-2 and the positivity of intestinal type mucin, namely MUC2, are characteristic in immunochemical staining. In the case of gastric cancer, the positivity of CK7 and the main mucins expressed in the stomach were MUC1, MUC5AC, and MUC6, which stained positive in immunochemical staining. The low FDG uptake and IHC staining results were strongly suggestive of a metastasis from GC rather than from a prostate and rectal origin.

Figure 4. PET-CT findings. (A) This Diffusely increased FDG uptake (SUL max 7.7) along the right renal parenchyma: Possibly induced by obstructive uropathy. (B, C) No significant evidence of well-defined hypermetabolic activity in and around the proximal rectal area: R/O Malignancy low FDG avidity possibly originated from stomach cancer.

Figure 5. Pathology findings. (A) Section showed infiltration of poorly differentiated tumor cells with atypical hyperchromatic nuclei (H&E stain, 200×). (B) Tumor cells were diffusely positive for CK7 (CK7 stain, 200×). (C) Tumor cells negative for CK20 (CK20 stain, 200×). (D) Tumor cells negative for MUC2 (MUC2 stain, 200×).

The patient opted for treatment at another tertiary center owing to the complexity of the surgery required. Two years after surgery, he returned to the authors’ clinic, where no further recurrence was noted.

The recurrence patterns after curative surgery for GC generally include locoregional recurrence, distant hematogenous or lymphatic metastasis, and peritoneal seeding.¹⁰ Hematogenous metastasis is the most common in most cases where recurrence occurs within one year after surgery, and locoregional and peritoneal recurrence are the most common patterns in cases where recurrence occurs after more than a year.¹¹ A secondary colon invasion is not uncommon in advanced gastric cancer, but it is very rare for gastrointestinal metastases to be discovered more than five years after surgery.^5,8 The most frequent site of GC metastasis to the colon was the transverse colon, which may represent direct invasion or extension.^9,12 A large part of recurrence was early recurrence (<2 years), and the late recurrence rate in five-year survivors was from approximately 6% to 10.8%.^6,7 The stage of the disease and level of lymph node metastasis were the most significant factors independently associated with the survival time after a gastrectomy for gastric carcinoma. Patients with more advanced stages of disease (Stage III and IV) or those with extended lymph node metastasis (N2 and N3) frequently die of recurrence within two years after gastrectomy.⁶

Tumors penetrating the serosa with a direct invasion to continuous structures were found more frequently in the early recurrence group than in the late recurrence group. Patients with early recurrence had a higher tendency to have nodal involvement, lymphatic invasion, and vascular invasion. The following variables were significant risk factors for early recurrence: male gender, lymph node metastasis, and vascular invasion.¹³ Many studies have examined the recurrence of gastric cancer within five years after a curative resection, but few studies have examined recurrence after five years. For recurrences within five years after surgery, cancer-related factors and stage were important prognostic factors, and stage IV was the only prognostic factor for recurrences between five and 10 years. For recurrences after 10 years, no appropriate factor was found to predict the prognosis.⁷ In addition, as the treatment results for gastric cancer have recently improved, the five-year survival rate has reached approximately 88.9%, making it very common for patients to survive for more than five years.⁴ Surveillance for late recurrence is crucial, especially for long-term survivors of advanced gastric cancer. On the other hand, although periodic endoscopic examinations and CT scans are usually performed for up to five years after surgery for advanced gastric cancer, there is currently no consensus on the appropriate follow-up examination methods. Japanese guidelines recommend that endoscopy be performed for up to five years, but there is no need for additional follow-up after.¹⁴

According to Han et al., a thorough endoscopic examination must be performed for up to five years after surgery to detect remnant gastric cancer (RGC) after surgery. They showed that the frequency of RGC decreases around 20 years after the primary operation. Accordingly, annual surveillance between the initial gastrectomy and 20 years postoperatively is appropriate for detecting RGC¹⁵. Like this patient, a Schnitzler’s metastasis to the rectum is a rare case that leads to rectal stenosis and symptoms of bowel obstruction. In this case, CT is a reasonable initial approach to detect intestinal metastases from gastric adenocarcinoma. This patient also received periodic health checkups at the authors’ hospital and underwent ultrasound examinations instead of CT, which revealed abnormal findings. How follow-up CT examinations should be performed after gastric cancer surgery has no consensus. Well-established evidence suggests that intensive surveillance after surgery for colorectal cancer improves overall survival.^16,17 Nevertheless, there is a paucity of research on whether routine intensive surveillance improves patient survival in patients with gastric cancer and whether this follow- up method is cost-effective. No consensus exists on whether surveillance carries prognostic survival benefits or how surveillance should be carried out after a radical gastrectomy for GC.¹⁸

A subtle bowel wall abnormality in the rectal area was found during a colonoscopy performed on this patient two years earlier but was overlooked and not noted in the records, and no biopsy was performed. In addition, although there was a voiding difficulty for one year, the PSA level was normal, and no specific findings were found in the prostatic sonography performed at that time, so empirical treatment for BPH was performed, which delayed the diagnosis. A diagnosis might have been made sooner if a CT scan had been performed sooner than when symptoms appeared. Therefore, it is always necessary to consider the quality recommendations regarding mucosal inspection during colonoscopy when performing a colonoscopy mentioned in the guidelines.¹⁹ A rapid cross-sectional imaging study, such as CT, should be considered in patients like this one, who complain of abnormal symptoms, such as constipation or voiding difficulty, even after a long time has passed since gastric cancer surgery.

In this case, the patient had subtle signs of bowel wall abnormality that were missed during earlier examinations, highlighting the importance of vigilant surveillance in long-term survivors. The patient’s voiding difficulties were initially attributed to BPH, delaying the diagnosis of recurrence. This paper reported a rare case of rectal metastasis 13 years after a curative resection for advanced gastric cancer. Although late colorectal metastasis is uncommon, it should be considered in patients presenting with rectal tumors and a history of gastric cancer. The early recognition of symptoms and appropriate imaging are essential for a timely diagnosis.

The published research is compliant with the guidelines for human studies and animal welfare regulations.

Jun Kyeong Lim, Hyun Deok Shin and Suk Bae Kim were involved in the literature review and creation of the manuscript.

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