Early gastric cancer metastasizing to the rectum, possibly via a hematogenous route: a case report and review of literature
© The Author(s). 2016
Received: 25 November 2015
Accepted: 29 May 2016
Published: 7 June 2016
The most common pattern of recurrence of gastric cancer (GC) is peritoneal dissemination. However, rectal metastasis via hematogenous or lymphatic spread is exceedingly rare. We present a case of a 65-year-old man with an intramucosal GC who developed a rectal recurrence, possibly via a hematogenous route.
A 65-year-old man underwent curative endoscopic submucosal dissections for the intramucosal GCs at the anterior wall of the fornix twice. The third GC at the similar location was treated by radical laparoscopic proximal gastrectomy; microscopic examination revealed well-differentiated tubular adenocarcinoma confined to the lamina propria mucosae (T1aN0M0, stage IA). Follow-up colonoscopy revealed a 30-mm submucosal mass in the rectal wall 2 years later, and a metastasis of gastric origin was suspected histopathologically. After a staging laparoscopy confirmed the absence of findings suggestive of serosal involvement or peritoneal dissemination, including negative peritoneal washing cytology, a laparoscopic low anterior resection with lymph node dissection was performed. Microscopically, the tumor was found to mainly be located in the submucosal layer and showed features of moderately differentiated tubular adenocarcinoma. The serosal surface was free of disseminated tumor. Lymph node metastases were identified. Immunohistochemically, there were foci of carcinoma cells that were positive for cytokeratin 20; however, they were negative for cytokeratin 7. Negative staining for caudal-type homeobox 2, a transcription factor indicating goblet cell differentiation, combined with absence of intramucosal carcinoma in the rectal mucosa, suggested a diagnosis of metastatic adenocarcinoma of gastric origin. The absence of evidence of peritoneal dissemination suggested hematogenous or lymphatic spread.
Although rectal metastasis from GC, particularly when attributable to hematologic or lymphatic metastasis, is very rare, metastatic gastric adenocarcinoma should be considered as a differential diagnosis for patients who present with a rectal tumor and a past history of GC, even if it is an early GC.
Gastric cancer (GC) is the fourth most commonly diagnosed cancer and the second most common cause of cancer mortality worldwide . Despite improvements in diagnosis and treatment, the prognosis of patients with recurrent GC remains poor [2, 3], the recurrence rate after curative surgery for GC reportedly ranging from 20 to 50 % [4–8].
Based on the findings of pertinent studies, the recurrence patterns after curative surgery for GC have been classified as follows: (1) locoregional recurrence, (2) peritoneal recurrence, and (3) distant (including hematogenous) metastasis [3, 6, 9–11]. Of these, metastasis of GC to the colorectal region by hematogenous or lymphatic spread is very rare. There are a few English language reports of such cases [12–16], all of which had advanced-stage disease. We report a case of a metachronous rectal metastasis caused by hematologic or lymphatic spread 2 years after curative resection of a recurrent intramucosal GC.
Thirteen months later, he underwent the second ESD for the second early GC at the similar location (Fig. 1a, lower), which was confirmed to be an intramucosal well-differentiated tubular adenocarcinoma; the resection margin was negative for tumor. Again, no ulcer scar or lymphovascular invasion was identified. A perforation that occurred during ESD was closed immediately by clipping and was treated conservatively.
Three years after the second curative ESD, he underwent laparoscopic proximal gastrectomy with lymph node dissection for the third GC at the similar location (Fig. 1b, upper and lower). The adjacent non-neoplastic mucosa showed atrophic changes, and microscopic examination of the specimen revealed well-differentiated tubular adenocarcinoma, which was still confined to the lamina propria (Fig. 1c). The morphologic features of this tumor differed from those of the first and second tumors; this one was diagnosed as being of gastric type. Neither lymphatic nor venous invasion was identified, and the surgical margins were free of tumor.
The recurrence patterns after curative surgery for GC have been classified as follows: (1) locoregional recurrence, (2) peritoneal recurrence, and (3) distant (including hematogenous) metastasis [3, 6, 9–11, 18]. The most common pattern of spread of these tumors is via peritoneal dissemination. As to distant metastases, intestinal metastasis from GC is rare; however, the most common cause of secondary neoplastic infiltration of the colon is GC . Metastatic colonic lesions can occur by direct extension of the initial primary GC via the gastrocolic ligament, peritoneal metastasis, or hematologic or lymphatic dissemination [13, 19].
Literature reports of colorectal recurrence from gastric cancer
Histological type of GC
Stage (AJCC seventh edition)
Pattern of recurrence
Lymph node metastasis
Histological type of recurrence
Ogiwara et al.
Pace U et al.
Lim S W et al.
Tural D et al.
Sung Young Oh
There are only a few published studies regarding surgical treatment of GC recurrence. According to several reports on the role and outcomes of surgical treatment for non-hepatic intra-abdominal recurrences from GC, surgical resection is the treatment of choice for selected patients in whom the recurrent tumors are completely resectable [20, 21]. Nunobe et al. reported the outcomes of surgery with curative intent in 36 selected patients with locoregional recurrence. Their median survival after surgery was about 23 months, seven of the 36 patients (19.4 %) surviving more than 3 years after surgery . In the present case, the factors favoring curative surgical resection were that there was no evidence of exposure of tumor or peritoneal dissemination, the recurrence had appeared late and was isolated, and the intra-abdominal recurrent tumor could be completely resected en bloc. Interestingly, our case confirms what others have reported: that metastatic lesions may have regional lymphatic metastases like primary rectal cancer (Table 1). Ogiwara et al. reported a case of polypoid colonic metastases with regional lymph node metastases 11 years after the resection of a GC . Additionally, Pace et al. reported a case of a signet ring cell carcinoma of the stomach metastasizing to the ascending colon with regional lymph node metastases . Therefore, it is necessary to investigate for possible lymphatic metastases preoperatively and perform systematic lymph node dissection if indicated when resecting a recurrent tumor.
In the recent studies, a local recurrence rate after curative ESD for GC is generally low (in the range 0.1–1.1 %) [23, 24]. On the other hand, a higher incidence of metachronous GCs (in the range 1.8–15.9 %) has been reported [24–27]. In the present case, all three GCs were located at the similar part, the anterior wall of the fornix. However, the pathological records of the first and second ESDs demonstrated that those ESDs were performed curatively, and three tumors did not have any specific characteristics. Considering the rates of local recurrence and metachronous GC, it is extremely difficult to consider that local recurrence occurred twice after curative ESDs. Rather, it is possible that metachronous GCs occurred twice after curative ESD at the similar part.
In summary, we found the tumor at the rectum which appeared to be a submucosal tumor, and there were no findings of serosal exposure of tumor, peritoneal dissemination, and cancerous ascites. These findings support that the metastatic rectal lesion was due to hematologic or lymphatic dissemination, but not peritoneal metastasis. In our case, at least two distinct types of GCs, namely a gastric type and a Lauren’s intestinal type, were identified by gastrectomy and ESD, respectively. However, which type of GC caused rectal metastasis was obscured. Importantly, we confirmed that a rectal tumor was derived from an intramucosal GC, which is an extremely rare event.
We here report a case of rectal metastasis caused by hematologic or lymphatic metastasis 2 years after curative resection for “early” GC. Although rectal metastasis from GC, particularly when attributable to hematologic or lymphatic metastasis, is very rare, metastatic gastric adenocarcinoma should be considered as a differential diagnosis for patients who present with a rectal tumor and a past history of GC, even if it is an early GC.
Written informed consent was obtained from the patient for publication of this case report and any accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal.
ESD, endoscopic submucosal dissection; GC, gastric cancer
No funding was received for this study.
We thank Trish Reynolds who provided medical writing services on behalf of Edanz Group Ltd.
Open AccessThis 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.
- Kamangar F, Dores GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol. 2006;24(14):2137–50. doi:10.1200/JCO.2005.05.2308.View ArticlePubMedGoogle Scholar
- Macdonald JS, Smalley SR, Benedetti J, Hundahl SA, Estes NC, Stemmermann GN, et al. Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction. N Engl J Med. 2001;345(10):725–30. doi:10.1056/NEJMoa010187.View ArticlePubMedGoogle Scholar
- Yoo CH, Noh SH, Shin DW, Choi SH, Min JS. Recurrence following curative resection for gastric carcinoma. Br J Surg. 2000;87(2):236–42. doi:10.1046/j.1365-2168.2000.01360.x.View ArticlePubMedGoogle Scholar
- Lee SE, Ryu KW, Nam BH, Lee JH, Choi IJ, Kook MC, et al. Prognostic significance of intraoperatively estimated surgical stage in curatively resected gastric cancer patients. J Am Coll Surg. 2009;209(4):461–7. doi:10.1016/j.jamcollsurg.2009.06.001.View ArticlePubMedGoogle Scholar
- Deng J, Liang H, Wang D, Sun D, Pan Y, Liu Y. Investigation of the recurrence patterns of gastric cancer following a curative resection. Surg Today. 2011;41(2):210–5. doi:10.1007/s00595-009-4251-y.View ArticlePubMedGoogle Scholar
- Wu CW, Lo SS, Shen KH, Hsieh MC, Chen JH, Chiang JH, et al. Incidence and factors associated with recurrence patterns after intended curative surgery for gastric cancer. World J Surg. 2003;27(2):153–8. doi:10.1007/s00268-002-6279-7.PubMedGoogle Scholar
- Huang KH, Chen JH, Wu CW, Lo SS, Hsieh MC, Li AF, et al. Factors affecting recurrence in node-negative advanced gastric cancer. J Gastroenterol Hepatol. 2009;24(9):1522–6. doi:10.1111/j.1440-1746.2009.05844.x.View ArticlePubMedGoogle Scholar
- Sakar B, Karagol H, Gumus M, Basaran M, Kaytan E, Argon A, et al. Timing of death from tumor recurrence after curative gastrectomy for gastric cancer. Am J Clin Oncol. 2004;27(2):205–9.View ArticlePubMedGoogle Scholar
- Maehara Y, Hasuda S, Koga T, Tokunaga E, Kakeji Y, Sugimachi K. Postoperative outcome and sites of recurrence in patients following curative resection of gastric cancer. Br J Surg. 2000;87(3):353–7. doi:10.1046/j.1365-2168.2000.01358.x.View ArticlePubMedGoogle Scholar
- Roviello F, Marrelli D, de Manzoni G, Morgagni P, Di Leo A, Saragoni L, et al. Prospective study of peritoneal recurrence after curative surgery for gastric cancer. Br J Surg. 2003;90(9):1113–9. doi:10.1002/bjs.4164.View ArticlePubMedGoogle Scholar
- Moon YW, Jeung HC, Rha SY, Yoo NC, Roh JK, Noh SH, et al. Changing patterns of prognosticators during 15-year follow-up of advanced gastric cancer after radical gastrectomy and adjuvant chemotherapy: a 15-year follow-up study at a single Korean institute. Ann Surg Oncol. 2007;14(10):2730–7. doi:10.1245/s10434-007-9479-4.View ArticlePubMedGoogle Scholar
- Ogiwara H, Konno H, Kitayama Y, Kino I, Baba S. Metastases from gastric adenocarcinoma presenting as multiple colonic polyps: report of a case. Surg Today. 1994;24(5):473–5.View ArticlePubMedGoogle Scholar
- Pace U, Contino G, Chiappa A, Bertani E, Bianchi PP, Fazio N, et al. Metachronous colon metastases from gastric adenocarcinoma: a case report. Case Rep Oncol. 2009;2(2):92–6. doi:10.1159/000215945.View ArticlePubMedPubMed CentralGoogle Scholar
- Lim SW, Huh JW, Kim YJ, Kim HR. Laparoscopic low anterior resection for hematogenous rectal metastasis from gastric adenocarcinoma: a case report. World J Surg Oncol. 2011;9:148. doi:10.1186/1477-7819-9-148.View ArticlePubMedPubMed CentralGoogle Scholar
- Tural D, Selcukbiricik F, Ercaliskan A, Inanc B, Gunver F, Buyukunal E. Metachronous rectum metastases from gastric adenocarcinoma: a case report. Case Rep Med. 2012;2012:726841. doi:10.1155/2012/726841.PubMedPubMed CentralGoogle Scholar
- Oh SY, Cunningham J, Saif MW. Colonic metastasis from gastric cancer. Clin Colorectal Cancer. 2014;13(4):255–6. doi:10.1016/j.clcc.2014.09.009.View ArticlePubMedGoogle Scholar
- Lauren P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathol Microbiol Scand. 1965;64:31–49.PubMedGoogle Scholar
- D'Angelica M, Gonen M, Brennan MF, Turnbull AD, Bains M, Karpeh MS. Patterns of initial recurrence in completely resected gastric adenocarcinoma. Ann Surg. 2004;240(5):808–16.View ArticlePubMedPubMed CentralGoogle Scholar
- Jang HJ, Lim HK, Kim HS, Cho EY, Lee SJ, Kim KA, et al. Intestinal metastases from gastric adenocarcinoma: helical CT findings. J Comput Assist Tomogr. 2001;25(1):61–7.View ArticlePubMedGoogle Scholar
- Takeyoshi I, Ohwada S, Ogawa T, Kawashima Y, Ohya T, Kawate S, et al. The resection of non-hepatic intraabdominal recurrence of gastric cancer. Hepatogastroenterology. 2000;47(35):1479–81.PubMedGoogle Scholar
- de Liano AD, Yarnoz C, Aguilar R, Artieda C, Ortiz H. Surgical treatment of recurrent gastric cancer. Gastric Cancer. 2008;11(1):10–4. doi:10.1007/s10120-007-0444-5.View ArticlePubMedGoogle Scholar
- Nunobe S, Hiki N, Ohyama S, Aikou S, Sano T, Yamaguchi T. Outcome of surgical treatment for patients with locoregional recurrence of gastric cancer. Langenbecks Arch Surg. 2011;396(2):161–6. doi:10.1007/s00423-010-0730-2.View ArticlePubMedGoogle Scholar
- Kosaka T, Endo M, Toya Y, Abiko Y, Kudara N, Inomata M, et al. Long-term outcomes of endoscopic submucosal dissection for early gastric cancer: a single-center retrospective study. Dig Endosc. 2014;26(2):183–91. doi:10.1111/den.12099.View ArticlePubMedGoogle Scholar
- Suzuki H, Oda I, Abe S, Sekiguchi M, Mori G, Nonaka S, et al. High rate of 5-year survival among patients with early gastric cancer undergoing curative endoscopic submucosal dissection. Gastric Cancer. 2016;19(1):198–205. doi:10.1007/s10120-015-0469-0.View ArticlePubMedGoogle Scholar
- Nakajima T, Oda I, Gotoda T, Hamanaka H, Eguchi T, Yokoi C, et al. Metachronous gastric cancers after endoscopic resection: how effective is annual endoscopic surveillance? Gastric Cancer. 2006;9(2):93–8. doi:10.1007/s10120-006-0372-9.View ArticlePubMedGoogle Scholar
- Kobayashi M, Narisawa R, Sato Y, Takeuchi M, Aoyagi Y. Self-limiting risk of metachronous gastric cancers after endoscopic resection. Dig Endosc. 2010;22(3):169–73. doi:10.1111/j.1443-1661.2010.00987.x.View ArticlePubMedGoogle Scholar
- Han JS, Jang JS, Choi SR, Kwon HC, Kim MC, Jeong JS, et al. A study of metachronous cancer after endoscopic resection of early gastric cancer. Scand J Gastroenterol. 2011;46(9):1099–104. doi:10.3109/00365521.2011.591427.View ArticlePubMedGoogle Scholar