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A rare case of colorectal metastasis found 8 years and 10 months after gastrectomy for advanced gastric cancer: A case report and literature review

  • Authors:
    • Shuzo Kohno
    • Masahiro Ikegami
    • Se Ryung Yamamoto
    • Hiroaki Aoki
    • Masaichi Ogawa
    • Fumiaki Yano
    • Ken Eto
  • View Affiliations

  • Published online on: April 5, 2023     https://doi.org/10.3892/ol.2023.13789
  • Article Number: 203
  • Copyright: © Kohno et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Colorectal metastasis from gastric cancer is rare and may develop several years after gastric cancer surgery. Therefore, colonoscopic findings provide useful diagnostic information. The present report describes a case of gastric cancer colon metastasis diagnosed 8 years and 10 months after gastrectomy for advanced gastric cancer. A 64‑year‑old male patient underwent gastrectomy in December 2010 and received chemotherapy for 4 years and 10 months after the surgery. Subsequently, the patient was diagnosed as having colorectal cancer by computed tomography in February 2019. Colonoscopy revealed linitis plastica‑like colon stenosis; however, biopsy pathology did not reveal any findings indicating malignancy. Right hemicolectomy was performed, and pathological examination revealed colon metastasis from gastric cancer. The patient received chemotherapy but died of peritoneal carcinomatosis 1 year and 8 months after the colectomy. According to literature, colorectal metastasis from gastric cancer is often attributed to hematogenous metastasis and often exhibits characteristic macroscopic features. Treatments, such as chemotherapy for gastric cancer and/or colorectal resection, are considered effective for gastric cancer colorectal metastasis.

Introduction

Colorectal metastases from gastric cancer rarely occur without dissemination or direct infiltration and may be found several years after gastrectomy (14). Metastasis patterns, diagnosis, and treatment are being investigated from reported cases. In colon metastasis not originating from infiltration of gastric cancer, endoscopic findings often reveal multiple polypoid or linitis plastica-like lesions due to submucosal development (5). There are case reports (2,4,6) of long-term survival following surgical treatment and chemotherapy for recurrent lesions, and it is highly possible that treatment will contribute to improving the prognosis. We aimed to examine the characteristics of solitary colorectal metastasis from gastric cancer by evaluating our case and other reported cases to improve the medical treatment of colorectal metastasis from gastric cancer.

Case report

Patient background, onset and course

A 64-year-old man underwent distal gastrectomy for gastric cancer in December 2010. He had a history of hypertension (which was well controlled with antihypertensive medication) and hyperlipidemia (total cholesterol was 150 mg/dl on antihyperlipidemic medication). The pathological diagnosis was poorly differentiated adenocarcinoma (Fig. S1), type 2, Se, ly +, v +, n +, T4a N1 M0-stage IIIa (according to the 7th edition UICC) (Fig. 1). Postoperative adjuvant chemotherapy with tegafur/gimeracil/oteracil potassium (S-1) was administered in two courses. Computed tomography (CT) in May 2011 revealed peritoneal carcinomatosis; therefore, chemotherapy with docetaxel was administered, given the recurrence. Subsequently, chemotherapy was changed to bi-weekly paclitaxel therapy, and complete remission (CR) was achieved. Contrast-enhanced CT scan taken in December 2014 showed no recurrent lesions, and chemotherapy was discontinued at the patient's request. Thereafter, he remained under outpatient observation for stage IV gastric cancer follow-up. After completion of chemotherapy in December 2014, tumor markers were measured once every 3 months, CT and ultrasonography were performed once every 6 months, and gastrofiberscopy was performed once a year. In February 2019, the patient complained of discomfort in the right abdomen, and a CT scan showed wall thickening from the ascending colon to the transverse colon (Fig. 2). A colonoscopy revealed stenosis and mucosal edema from the hepatic flexure of the transverse colon to the ascending colon; diverticula in the ascending colon was also detected. Biopsy pathology showed no malignant findings. Positron emission tomography-CT examination (Fig. 3) showed accumulation of fluorodeoxyglucose, and colorectal diverticulitis, potential dissemination, and peritoneal carcinomatosis were further diagnosed. The laparoscopic examination showed no ascites, recurrence, or disseminated lesions. No colectomies were performed since there was no obstruction, and no diagnosis of colon cancer was made. Appendectomy was performed, and a white induration in the peritoneum was biopsied; both specimens were submitted for pathological diagnosis, but no malignant findings were observed. A CT scan conducted in October 2019 (Fig. 4) showed worsening of the wall thickening of the ascending colon. Furthermore, carcinoembryonic antigen levels increased to 23.7 ng/ml. Colonoscopy revealed extensive stenosis in the transverse colon, and the biopsy showed no findings indicating malignancy (Fig. 5). Despite these results, right hemicolectomy was performed in November 2019 based on a diagnosis of transverse colon cancer. Gross findings of the resected specimen (Fig. 6) showed a linitis plastica-like tumor that was 20×60 mm in size, extending from the ascending to the transverse colon; the extent of mucosal infiltration was unclear. The pathological diagnosis was poorly differentiated adenocarcinoma, type 4, Se, ly0, v0, Pn1b, BD3, n0, and Cy0, T4a N0 M0-stage IIb (according to the 8th edition UICC). Microscopic findings (Fig. 7) showed atypical cells that infiltrated and proliferated in a cord-like or individual-cell manner with a fibrous stroma and that the spread extended to all layers. Tumor cells were AE1/AE3 positive, cytokeratin (CK)7 positive, CK20 negative, and caudal type homeobox 2 (CDX2) negative on immunostaining (Fig. 8), and gastric cancer recurrence was diagnosed. Thereafter, S-1, oxaliplatin chemotherapy → ramucirumab, paclitaxel chemotherapy → nivolumab chemotherapy → irinotecan chemotherapy → docetaxel chemotherapy were administered; however, the patient died of peritoneal carcinomatosis in July 2021.

Analysis method from case reports

To investigate the characteristics of colon metastasis from gastric cancer, we performed a literature search of English abstracts published on colon metastasis and gastric cancer in the Cochrane Library and PubMed databases. The data were obtained directly from case reports searched in the literature and the present case. We did not acquire any patient cohort data during this study. From the previous case reports, we extracted data on the following factors: age, sex, gastric cancer pathology, macroscopic feature of gastric cancer, other metastatic sites besides the colorectum, metastatic site in the colorectum, chemotherapy after the diagnosis of colorectal metastasis, and prognosis. We tested for significant differences in each factor between the synchronous (n=13) and metachronous (n=24) gastric cancer colonic metastasis case groups. The prognosis after diagnosis of colon metastasis between the two groups was determined.

Statistical analysis

Categorical data were represented as n (%). Continuous data were described as mean ± standard deviation (SD). To compare 13 syncronous and 24 metacronous colon metastasis case groups, Fisher's exact test was used to determine significant differences between covariates for gastric cancer pathology, macroscopic features, recurrent colon tumor macroscopic features, other metastatic sites besides the colorectum, metastatic site in the colorectum, and chemotherapy after the diagnosis of colorectal metastasis. Continuous data for age were analyzed by unpaired t-test. Prognosis was analyzed using Kaplan-Meier survival curve and log-rank test. Estimated mean survival, estimated median survival, and their respective standard errors (SE) and 95% confidence intervals (CI) were calculated. All statistical analyses were performed using IBM SPSS Statistics for Windows, version 22.0 (IBM Japan, Ltd., Tokyo, Japan). A two-sided P-<0.05 was considered significant.

Discussion

We described the case of a patient with stage IV gastric cancer who underwent chemotherapy and achieved CR. He was found to have developed colorectal metastases 8 years and 10 months after gastrectomy and died 1 year and 8 months after undergoing a right hemicolectomy.

Regarding cancer metastasis from other organs to the gastrointestinal tract, the most reported metastatic site is the colorectum, followed by the stomach and duodenum (7). The proportion of metastatic lesions from other organs in colorectal cancer is considered to be approximately 1%; however, it may be slightly higher at postmortem (7). In addition, the detection of colorectal metastases is thought to increase a greater awareness of the need to follow up on primary tumors (7). The most common primary organs of colorectal metastases are the lung, ovary, mammary gland, prostate, kidney, and skin (7). The incidence of multiple primary cancer after gastric cancer surgery is 2.0-7.6% (8), and colorectal cancer often occurs. In a single institutional report of secondary primary colorectal carcinoma in Asia (9), 17 of 1,031 resected colorectal cancers had metastasized from other sites. Of the 17 cases, six and five were breast and gastric cancers, respectively. The incidence of gastric cancer is high in East Asia (9). Genes are involved in the carcinogenic mechanism, but in cancers that occur in multiple organs, it is important to know whether they are metastases or multiple individual cancer occurrences. Classification of a cancer as metastatic or second primary cancer is essential. The criteria for multiple secondary tumors (MPCs) are reported by Warren and Gates in 1932 (10). According to them, ‘each of the tumors must present a definite picture of malignancy, each must be distinct, and the probability of one being a metastasis of the other must be excluded’. Malignant lesions with characteristics other than these are treated as metastases. Evidence of such metastasis to distant organs is confirmed from pathological features; however, recent determinations using immunostaining are believed to have increased accuracy. Immunohistochemical staining is effective in determining whether the lesions are of the same origin; this is reportedly effective in demonstrating metastasis (11,12). Immunohistochemical markers are useful in diagnosing metastatic adenocarcinoma with increased sensitivity and specificity to determine the primary site (12,13). The staining pattern of CDX2, CK7, and CK20 reveals whether the metastasis is gastric or colorectal (12). CDX2 is a homeobox gene that encodes a gut-specific transcription factor and is expressed in the epithelial cell nuclei of the intestine from the duodenum to the rectum. AE1/AE3 stains almost all epithelial cells. Gastric cancer is generally CK7-positive and CK20-negative, while colon cancer is generally CK7-negative and CK20-positive. Our findings revealed a similar pattern (CK7-positive and CK20-negative) of immunohistochemical staining. However, immunohistochemical staining does not aid in determining whether rare cancers in multiple organs occur due to the same gene.

In our case, the patient achieved CR from stage IV gastric cancer after chemotherapy, and CT scan revealed colon metastasis 8 years and 10 months postoperatively. To investigate the characteristics of colon metastasis from gastric cancer, we summarized the reported cases of gastric cancer colon metastasis. Synchronous colorectal metastases differ from metachronous; we found 24 metachronous (14,6,1429) (Table I) and 13 synchronous cases (5,25,3040), as classified and listed in Table II. Several reports have set the boundary between synchronous and metachronous metastases as diagnosed after 2 months, 6 months, and 1 year from the primary diagnosis. Our report is based on the Surveillance Epidemiology and End Results approach, which has the largest number of cases of metachronous cancer. According to this classification (41), metachronous cancer is defined as cancer of other organs diagnosed ≥2 months after the first cancer.

Table I.

Cases of metachronous gastric cancer colorectal metastasis.

Table I.

Cases of metachronous gastric cancer colorectal metastasis.

RCT
PGT
First author/s, yearNo.Age, yearsSexNEt
SCM: OMSBPPathologyMFDFI, monthsCACOOutcome(Refs.)
MFStageLNMPathologyCTX
Ogiwara et al, 1994153FJPNUNIIc+III (advanced)UNYesPorUND, S: nonePorUNPol132UNUN(1)
Tanakaya et al, 2004268MJPNUNType IVIIIAYesSig, PorUNIC: noneACSig, PorPol96UNDeath 16 Mo after SS(14)
Tseng et al, 2004374MUNUNUNUNYesUNUNS, R: UNACACPol108YesDeath 6 Mo after SS(15)
Pace et al, 2009477MITAUNType II or IIIIIIAYesSig, ModYesA:nonePorPor, SigUN15UNUN(16)
Lim et al, 2011543FKORUNType IIIIIYesPorUNR:noneNDMPorLPL34FOL-FOXAlive 14 Mo after SS(17)
Mayumi et al, 2013674MJPNUNType IIIIVNoPor1st, S-1; 2nd, S-1, CDDP; 3rd, CPTT: ovaryUNPorType II381st, CPT; 2nd, PTXDeath 28 Mo after SS(18)
T:intes-tineUNPorUN49Capecia tbine, CDDPDeath 17 Mo after 3rd Sur
Watanabe et al, 2013763MJPNUNType IIIIBNoModTS-1T:PerNDMMod-PorType II34YesAlive 15 Mo after SS(19)
Noji et al, 2014861MJPNUNUNIINoPor, SigUNT:LNUNPor, SigUN108RefusedAlive 17 Mo after SS(2)
Noji et al, 2014946FJPNUNUNIIIAYesSigYesR: ovary, LNUNMod, PorPol108YesAlive 24 Mo after SS(2)
Oh et al, 20141069FUSAUNType II or IIIIIYesPor1st, FOL FOX; 2nd, ECXS:UNPorNo resec tionsType II or III471st, FOL FOX; 2nd, FOL FIRIUN(20)
Tomita et al, 20151170FJPNUNType IVIIIAYesSigS-1T:UNNDMSigUN33S-1Death 37 Mo after SS(21)
A:PerUNNo resec tionsUN47S-1, DOCDeath 23 Mo after 3rd Sur
Fujimoto et al, 20161258FJPNUN0-IIc+IIaIaNoPor, Sig1st, S-1; 2nd, S-1, CDDP, RTXS: ovaryUNPor, Sig0-IIc28S-1, DOCAlive 30 Mo after SS(6)
Ikeda et al, 20161369FJPNUN0-IIc SigIbYesPor, SigNoT:LNNonePor,SMTL47RefusedDeath 7 Mo after SS(22)
Uemura et al, 20161464MJPNUN0-IIaNoWNoR:LNWWPol24UNAlive 6 Mo after SS(23)
Higuchi et al, 20181555MJPNUNType IIIIVYesMod PorS-1C:noneNDMMod-SMTL10FPDeath 20 Mo after SS(24)
Higuchi et al, 20181659MJPNUNType IVIIIBYesTub, PorS-1T:UNPor. SigPor. SigLPL23S-1Death 25 Mo after SS(24)
Su et al, 20181778MTWUNAdvan ced GCIIIBUNPorFOL FOXR, T:UNUNPorType II18UNDeath 6 Mo after SS(25)
Mizuguchi et al, 20181860′MJPNUNType IIIIIBYesTub, PorS-1A: LNPorTub, PorLPL26NoneDeath 6 Mo after SS(26)
Elghali et al, 20191962MTUNUNUNIBNoSigNoT: LNUNSigUN96YesUN(3)
Yang et al, 20202057MCNUNUNIIIAYesPor, SigSOXA: skin, LNPorPor. SigLPL30YesDeath 9 Mo after SS(27)
Okazaki et al, 20202170FJPNUNUNIVUNPorSOXC: noneNDMPorPol48SOXAlive 12 Mo after SS(28)
Then et al, 20212266MUSAUNUNUNUNUNUNT:UNNDMACUN24NoneUN(29)
Wang et al, 20212342MCNUNUNIIIAYesPorL-OHP, CF, 5-FURS: PerUNPorMass70PTX, CF, 5-FUDeath 76 Mo after SS(4)
S: LNPorPorPol110Epiru bicin, L-OHP, Capecita bineDeath 44 Mo after 3rd Sur
S LNPorPorMass138Suniti nib + S-1Death 16 Mo after 4th Sur
S: LNPorPorMass151UNDeath 3 Mo after 5th Sur
Present study2473MJPNAsianType IIIIIAYesPor1st, S-1; 2nd, DOC; 3rd, PTX.T: noneNDMPorLPL1181st, SOX; 2nd, RAM, PTX; 3rd Niv; 4th, CPT; 5th, DOCDeath 20 Mo after SS-

[i] A, ascending colon; AC, adenocarcinoma; BP, biopsy pathology; C, caecum; CACO, chemotherapy after colectomy; CDDP, cisplatin; CF, folic acid; CN, China; CPT, irinotecan; CTX, chemotherapy; D, descending colon; DCM, diagnosis of colorectal metastasis; DFI, disease-free interval; DOC, docetaxel; DX, diagnosis; ECX, epirubicin, cisplatin and xeloda; Et, ethnicity; F, female; FOLFIRI, folic acid, 5-fluorouracil and irinotecan; FOLFOX, folic acid, 5-fluorouracil and oxaliplatin; FP, 5-FU, cisplatin; FU, fluorouracil; GC, gastric cancer; IC, ileo-cecal lesion; ITA, Italy; JPN, Japan; KOR, Korea; LN, lymph node; LNM, lymph node metastasis; LPL, linitis plastica-like lesion; L-OHP, oxaliplatin; M, male; MCS, metastatic colonic site; MF, macroscopic features; Mo, months; Mod, moderately differentiated adenocarcinoma; N, nationality; NDM, not detected malignancy; Niv, nivolumab; OMS, other metastatic site; Per, peritoneum; PGT, primary gastric tumor; Pol, polypoid lesion; Por, poorly differentiated adenocarcinoma; PTX, paclitaxel; R, rectum; RAM, ramucirumab; RCT, recurrent colon tumor; RS, remnant stomach; RTX, radiation therapy; S, sigmoid colon; SCM, site of colonic metastasis; Sig, signet ring cell carcinoma; SMTL, submucosal tumor like lesion; SOX, S-1, oxaliplatin; SS, second surgery; Sur, surgery; S-1, tegafur gimeracil oteracil potassium; T, transverse colon; Tub, tubular adenocarcinoma; TUN, Tunisia; TW, Taiwan; W, well-differentiated adenocarcinoma; UN, unknown; USA, United States of America.

Table II.

Cases of synchronous gastric cancer colorectal metastasis.

Table II.

Cases of synchronous gastric cancer colorectal metastasis.

PGTRCT


First author/s, yearNo.Age, yearsSexNEtMacroscopic featuresStagePathologySCM: OMSBPMFCACOutcome(Refs.)
Metayer et al, 1991165MFRUNType II or IIIIVSigC, T, S:UNSigPolNoneDeath within a month after DX(30)
Tomikashi et al, 2002257MJPNUNType IIIIVPorAll colon: bonesPorPolFPAlive 7 months after DX(31)
Lee et al, 2004341MTWUNType IVIVSigT, D, S:WB, LNPor, SigPolHDFLDeath 1 month after DX(32)
Nakamura et al, 2008486FJPNUNType IIIIVPor, SigT:PerPor, Sig0-IIa+IIcNoneDeath 10 months after DX(33)
Tural et al, 2012574FTURUNUNIVWellR:noneWellPolTCFAlive several months after CTX(34)
Reyes-Diaz et al, 2012658MESUNUNIVSigC, A, S, R:LNSigUNCDDPDeath 12 months after DX(35)
Gao et al, 2014780MCNUNType II or IIIIVPor, SigA, T, D, S:UNSigPolXelodaDeath 3 months after DX(36)
Lee et al, 2015855FKORUN0-IIcIVSigS, R: boneSigPolFOL FOXAlive >16 months after CTX(37)
Patel et al, 2016959FUSACAUUNIVSigA, T, S:LNSigLPLFOL FOXAlive 1 months after surgery(38)
Makker et al, 20161060FUNUNType I or IIIVSigR:B, L, PlPor, SigPol+LPLDCFLDeath 12 months after DX(39)
Sonoda et al, 20171181MJPNAsianType IIIIVPor, SigT:PerPor, Sig0-IIaUNUN(5)
Su et al, 20181277MTWUNUNIVPorR, T:UNNDMPolFOL FOXDeath 6 months after DX(25)
Meheershahi et al, 20201355MUSAUNType IVIVPorS:UNPor, SigType IIUNUN(40)

[i] A, ascending colon; B, bone; BP, biopsy pathology; C, caecum; CAC, chemotherapy after colectomy; CAU, Caucasian; CDDP, cisplatin; CN, China; CTX, chemotherapy; D, descending colon; DCFL, docetaxel, cisplatin, 5-fluorouracil, leucovorin; FU, fluorouracil; DX, diagnosis; ES, Spain; Et, ethnicity; F, female; FOLFOX, folic acid, 5-fluorouracil and oxaliplatin; FP, 5-FU, cisplatin; FR, France; HDFL, high-dose 5-fluorouracil and leucovorin; JPN, Japan; KOR, Korea; L, lung; LN, lymph node; LNM, lymph node metastasis; LPL, linitis plastica-like lesion; M, male; MF, macroscopic feature; N, nationality; NDM, no detected malignancy; OMS, other metastatic site; Per, peritoneum; PGT, primary gastric tumor; Pl, pleura; Pol, polypoid lesion; Por, poorly differentiated adenocarcinoma; R, rectum; RCT, recurrent colon tumor; S, sigmoid colon; Sig, signet ring cell carcinoma; SCM, site of colonic metastasis; T, transverse colon; TCF, docetaxel, cisplatin, 5FU; TUR, Turkey; TW, Taiwan; UN, unknown; USA, United States of America; Well, well differentiated adenocarcinoma; WB, whole body.

CT is reportedly effective in diagnosing metastasis to the colorectum after gastric cancer surgery. It has a very high rate of detection, especially when a helical CT outcome is interpreted by a radiologist (42). Most of the reported cases of gastric cancer and colorectal metastasis were diagnosed by CT and endoscopy. Diagnostic colonoscopy was performed in almost all cases for both metachronous and synchronous colon metastases, and the findings were polypoid or linitis plastica-like. In many of the reviewed cases, the biopsy results obtained using colonoscopy were not described, and no malignant findings were reported (17,19,24,25,28,29) (Tables I and II). In our case, more than 8 years had passed since the gastric cancer surgery, and no malignant findings were obtained upon examination. Therefore, the large intestine was not resected during the second laparoscopic surgery, and the diagnosis of colon metastasis was slightly delayed. Endoscopic biopsy diagnosis may be ineffective in colorectal metastasis due to the presence of metastatic lesions under the mucosa (42). Even if no malignant findings are revealed by biopsy, resection is a better option when it is feasible based on the diagnostic imaging.

Similar to a previous report (42), most of the colon metastases from gastric cancer (Tables I and II) are poorly differentiated and signet ring cell adenocarcinomas. In general, when the tissue is intestinal, the metastases are often hematogenous, whereas when it is poorly differentiated (diffuse type), the metastases are often lymphatic/disseminated (43). It is assumed that there is a mechanism responsible for the many hematogenous metastases of poorly differentiated adenocarcinoma to the colorectum from gastric cancer. Poorly differentiated and signet ring cell adenocarcinomas are rare primary colorectal cancers, and metastasis from gastric cancer should be considered when biopsy results by colonoscopy show such findings (1).

Sonoda et al (5) divided and investigated the metastatic pathways of colorectal metastasis from gastric cancer without peritoneal carcinomatosis, as follows: i) metastatic pathway from the gastrointestinal lumen; ii) lymphatic metastasis; and iii) hematogenous metastasis. According to them, there are many metastases from the gastrointestinal lumen, but the route is not considered in each report. Lymphatic metastasis to the colorectum, other than the transverse colon, is unlikely, and as reported by Noji et al (2), metastasis to the colorectum from the ovary or disseminated lesion is also possible. In this report (Tables I and II), many cases show macroscopic findings that cause submucosal infiltration, and many do not show malignant findings on the mucosal surface. Since metastasis from the gastrointestinal tract often presents with mucosal lesions and is often transplanted to the anastomotic stapler site, it is considered that the frequency of gastric cancer metastasis to the colon via the gastrointestinal tract is extremely low. Lymphatic metastasis is unlikely in colonic metastasis from a site distant from the stomach without dissemination, and therefore, hematogenous metastasis is mostly considered. Cancer stem cells are involved in carcinogenesis and metastasis, and their markers are attracting attention in research. It is known that CD44 and G-protein coupled receptor 5 (LGR5) are closely related to gastric cancer (44,45). Although these were not investigated in the case reported in our study, we believe that evaluating these markers will be useful in future research on colorectal metastasis from gastric cancer.

There are cases in which signet ring cell adenocarcinoma of the mammary gland (46,47) and small-cell carcinoma of the lung present with metastases to the colon (48) with submucosal infiltration. In addition, cases in which signet ring cell adenocarcinoma of the sigmoid colon and rectum metastasized to the stomach (49,50), and poorly differentiated adenocarcinoma of the mammary gland metastasized to the stomach (51,52) with submucosal invasion have been reported. In many reports, metastatic lesions from other organs that grow under the mucosa of organs of the gastrointestinal tract show polypoid or linitis plastica-like findings (4652). In general, metastases from other organs to the gastrointestinal tract are often hematogenous, are thought to infiltrate submucosal lymphatics, and develop as linitis plastica (16,53). Regarding gastrointestinal metastasis from breast cancer, many are estrogen and progesterone receptor-positive, suggesting a relationship with chemocain (51). In addition, the metastasis is related to cancer-related adipocytes (54), and the relationship with submucosal and subserosal adipocytes of the gastrointestinal tract is also considered, although currently, it remains unclear. When tumor cell metastases occur submucosally, the smooth muscle acts as a barrier to tumor infiltration. Furthermore, it is thought that the tumor growth suppression mechanism of the muscle is involved in the growth and infiltration of cancer in the submucosa (55). In our case, colonic metastasis occurred at the same site as the colonic diverticulum. It has been reported (56) that the microbiome is involved in cancer development. In our case, metastasis of the microbiome is unlikely, considering that the metastasis developed mainly in the submucosa. Furthermore, after cancer onset, the patient had achieved CR for a long time. In addition, in the referenced previous case report, the role of the microbiome was not mentioned; therefore, the relationship between metastasis and infection is unknown.

In cases of metastasis, it is possible that cancer lesions that have already metastasized before chemotherapy administration for gastric cancer may recur when chemotherapy is discontinued. Although patient prognosis has been extended due to advances in chemotherapy for advanced gastric cancer, there is no standard protocol for discontinuing chemotherapy for stage IV gastric cancer. Therefore, it is difficult to decide on the discontinuation of chemotherapy, as in the reported case.

In summary, a comprehensive study of published cases of gastric cancer colon metastasis, comparison between macroscopic classifications of gastric cancer, and these macroscopic features have not been reported. In our study, no differences were observed between the synchronous and metachronous metastasis groups. Similarly, there were no significant differences between the two groups in terms of sex, gastric cancer pathology, macroscopic feature of gastric cancer, other metastatic sites besides the colorectum, metastatic site in the colorectum, and chemotherapy after the diagnosis of colorectal metastasis. In cases of metachronous colorectal metastases, the rate of early gastric cancer was higher, and the stage was considered lower than in cases of synchronous metastases. According to the characteristics of recurrence (Tables I and II), the stage of gastric cancer differs depending on the age at which gastric cancer develops; therefore, a comparison was made based on the age at which the metastasis to the colorectum was diagnosed (Table III). For synchronous and metachronous metastases, the mean age of patients was 65.2±13.2 years and 63.2±10.4 years, respectively, and there was no significant difference between the two groups (P=0.608). In metachronous cases, the period from the initial surgery for gastric cancer to the discovery of colorectal metastasis was 55.3±9.9 months, which is considered a long interval. The average ± standard error of prognosis after diagnosis of colorectal metastases was 22.90±3.33 months and 8.37±1.73 months for metachronous and synchronous colorectal metastases, respectively (Table IV). The prognosis for metachronous metastasis was significantly longer than for synchronous metastasis (P=0.008) (Fig. 9). According to this case, both synchronous and metachronous metastases were of stage IV, but the prognosis of synchronous metastases was shorter than the overall survival rate (57) of stage IV gastric cancer.

Table III.

Comparison between patients with synchronous gastric cancer colorectal metastases and patients with metachronous gastric cancer colorectal metastases.

Table III.

Comparison between patients with synchronous gastric cancer colorectal metastases and patients with metachronous gastric cancer colorectal metastases.

Synchronous colorectal metastasesMetachronous colorectal metastasis


VariablesNo.ValueNo.ValueP-value
Mean age ± SD, years1365.2±13.22363.2±10.40.608a
Gastric cancer pathology, n (%)13 22 >0.999b
    Poorly differentiated 12 (92.3) 19 (86.4)
    Well-to-moderate differentiated 1 (7.7) 3 (13.6)
Gastric cancer macroscopic features, n (%)9 16 >0.999b
    Early 1 (11.1) 3 (18.8)
    Advanced 8 (88.9) 13 (81.3)
Recurrent colon tumor macroscopic features, n (%)12 19 0.274b
    Polypoid or early 9 (75.0) 10 (52.6)
    Advanced 3 (25.0) 9 (47.4)
Other metastatic sites besides the colorectum, n (%)9 18 0.201b
    Yes 8 (88.9) 11 (61.1)
    No 1 (11.1) 7 (38.9)
Metastatic site in the colorectum, n (%)13 24 0.667b
    Colon 8 (61.5) 18 (75.0)
    Rectum 2 (15.4) 3 (12.5)
    Colon and rectum 3 (23.1) 3 (12.5)
Chemotherapy, n (%)11 19 >0.999b
    Yes 9 (81.8) 15 (78.9)
    No 2 (18.2) 4 (21.1)

a Unpaired t test;

b Fisher's exact test. Data are presented as mean ± SD or n (%). The number of cases differs for some variables due to unknown/missing data.

Table IV.

Prognostic comparison between patients with synchronous and metachronous gastric cancer colorectal metastases.

Table IV.

Prognostic comparison between patients with synchronous and metachronous gastric cancer colorectal metastases.

Mean survival, monthsMedian survival, months


GroupsEstimated mean survivalSE95% CIEstimated median survivalSE95% CI
Synchronous8.371.734.98–11.77104.880.43–19.57
Metachronous22.903.3316.36–29.43204.5511.07–28.93
Whole19.112.8413.53–24.69204.8810.44–29.56

[i] Data are presented as estimated mean survival or estimated median survival, and their respective SE and 95% CI. Log-rank test P-value=0.0081. SE, standard error.

We found that metachronous colorectal metastasis from gastric cancer has a better prognosis than synchronous metastasis. First, the prognosis after gastric cancer surgery without MPC is better than with MPC. Synchronous MPC has a worse prognosis than metachronous MPC; however, when MPC occurs, the prognosis of metachronous colorectal metastasis deteriorates rapidly. This phenomenon has been reported as a reason for the treatment effect for gastric cancer in metachronous secondary primary cancer (58). Therefore, in gastric cancer metastasis, the therapy is expected to affect the colorectal metastasis.

In terms of prognosis after the diagnosis of colonic metastases, metachronous metastasis was associated with a favorable outcome when considering the reported case. The reasons for this are as follows: i) when metachronous gastric cancer has metastasized to the colorectum, the cancer lesions often remain localized or do not spread widely; ii) the effect of chemotherapy and resection on colonic metastases improves prognosis.

As reported by Mayumi et al (18) and Wang et al (4), long-term survival has been achieved in some cases by performing several resections and chemotherapy treatments for repeated recurrence. This suggests that surgical resection and chemotherapy may be effective for gastric metastasis to the colorectum.

The use of chemotherapy is based on the treatment guidelines of each country. In the reported cases, there were cases in which the prognosis was considered to have improved by administering chemotherapy using the same protocol or the same anticancer drug after recurrence due to colorectal metastasis (6,18,20,21,24). In cases of metachronous recurrence, if the chemotherapy protocol before recurrence was effective and the chemotherapy was discontinued, the same treatment should be considered first. However, it would be good to consider changing the protocol if lesion progression is observed.

Future research on the mechanisms of cancer metastasis and analysis of similar cases is expected to lead to findings that will guide the development of novel and rational treatment approaches. In particular, research advances involving biomarkers, immunohistochemistry, and liquid biopsies should be expected.

Limitation: Since some case reports did not describe the stage and type of gastric cancer at the time of diagnosis or the pathological results of the endoscopic biopsy performed to diagnose colon metastasis, these items could not be statistically processed and examined.

In conclusion, colon metastases from gastric cancer may develop even after a prolonged period of treatment for gastric cancer and often result in polypoid, linitis plastica-like submucosal endoscopic findings. Such findings are similar to those of hematogenous colonic metastases from other organs. The results of biopsy pathology often show no malignant findings; however, poorly differentiated adenocarcinoma and signet ring cell carcinoma are common. When such findings are obtained, metastatic colorectal cancer should be suspected. It has been suggested that treatment for gastric cancer may have a therapeutic effect on gastric cancer colorectal metastasis and that resection and/or chemotherapy for gastric cancer metastases are effective.

Supplementary Material

Supporting Data

Acknowledgements

The authors would like to thank Professor Koji Nomura (Department of Pathology, The Jikei University Katsushika Medical Center, Tokyo, Japan) for his pathological assessment. This abstract was presented at the 45th conference of Japanese College of Surgeons (December 22, 2020-December 24, 2020; Kurume, Japan), and was published as Abstract no. O4-04 (J-GLOBAL ID: 202102291766857226 21A0001180).

Funding

Funding: No funding was received.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Authors' contributions

SK, MI, SRY, HA, MO, FY and KE contributed to the study conception and design. Material preparation, data collection and analysis were performed by SK, SRY and HA. The first draft of the manuscript was written by SK, and all authors commented on previous versions of the manuscript. SK and MI confirm the authenticity of all the raw data. KE gave final approval of the version to be published. All authors have read and approved the final manuscript.

Ethics approval and consent for participate

Ethical review and approval were waived for this case report because of the retrospective nature of the published data.

Patient consent for publication

Written informed consent for publication was obtained from the patient antemortem.

Authors' information

SK is a member of the Japan Surgical Society, the Japanese Society of Gastroenterological Surgery, the Japanese Society of Gastroenterology, the Japan Gastroenterological Endoscopy Society, the Japan Society of Clinical Oncology, and the Japanese Gastric Cancer Association.

Competing interests

The authors declare that they have no competing interests.

References

1 

Ogiwara H, Konno H, Kitayama Y, Kino I and Baba S: Metastases from gastric adenocarcinoma presenting as multiple colonic polyps: Report of a case. Surg Today. 24:473–475. 1994. View Article : Google Scholar : PubMed/NCBI

2 

Noji T, Yamamura Y, Muto J, Kuroda A, Koinuma J, Yoshioka T, Murakawa K, Otake S, Hirano S and Ono K: Surgical resection of colorectal recurrence of gastric cancer more than 5 years after primary resection. Int J Surg Case Rep. 5:954–957. 2014. View Article : Google Scholar : PubMed/NCBI

3 

Elghali MA, Fadhl H, Hamila F, Mestiri S, Jarrar MS and Letaief R: Colon metastasis, 8 years after gastrectomy, for stage I gastric cancer. J Gastrointest Cancer. 50:127–129. 2019. View Article : Google Scholar : PubMed/NCBI

4 

Wang Y, Ma P, Liu K, Xu D and Liu Q: Gastric cancer with repeated metastasis in the colonic lumen: A case report and multi-surgical experience. J Int Med Res. 49:30006052110184202021.PubMed/NCBI

5 

Sonoda H, Kawai K, Yamaguchi H, Murono K, Kaneko M, Nishikawa T, Otani K, Sasaki K, Yasuda K, Tanaka T, et al: Lymphogenous metastasis to the transverse colon that originated from signet-ring cell gastric cancer: A case report and review of the literature. Clin Res Hepatol Gastroenterol. 41:e81–e86. 2017. View Article : Google Scholar : PubMed/NCBI

6 

Fujimoto D, Hirono Y, Goi T and Yamaguchi A: Sigmoid colonic metastasis by lymphatic spread occurring with unilateral Krukenberg tumor considered to be caused by stage IA early gastric cancer: A case report. Oncol Lett. 11:668–672. 2016. View Article : Google Scholar : PubMed/NCBI

7 

Galanopoulos M, Gkeros F, Liatsos C, Pontas C, Papaefthymiou A, Viazis N, Mantzaris GJ and Tsoukalas N: Secondary metastatic lesions to colon and rectum. Ann Gastroenterol. 31:282–287. 2018.PubMed/NCBI

8 

Kim C, Chon H, Kang B, Kim K, Jeung HC, Chung H, Noh S and Rha S: Prediction of metachronous multiple primary cancers following the curative resection of gastric cancer. BMC Cancer. 13:3942013. View Article : Google Scholar : PubMed/NCBI

9 

Kan JY, Hsieh JS, Pan YS, Wang WM, Chen FM, Jan CM, Huang YS, Huang TJ and Wang JY: Clinical characteristics of patients with sporadic colorectal cancer and primary cancers of other organs. Kaohsiung J Med Sci. 22:547–553. 2006. View Article : Google Scholar : PubMed/NCBI

10 

Warren S and Gates O: Multiple primary malignant tumors: A survey of the literature and statistical study. Am J Cancer. 16:1358–1414. 1932.

11 

Vidarsdottir H, Tran L, Nodin B, Jirström K, Planck M, Jönsson P, Mattsson JSM, Botling J, Micke P and Brunnström H: Immunohistochemical profiles in primary lung cancers and epithelial pulmonary metastases. Hum Pathol. 84:221–230. 2019. View Article : Google Scholar : PubMed/NCBI

12 

Park SY, Kim BH, Kim JH, Lee S and Kang GH: Panels of immunohistochemical markers help determine primary sites of metastatic adenocarcinoma. Arch Pathol Lab Med. 131:1561–1567. 2007. View Article : Google Scholar : PubMed/NCBI

13 

Zhong J, Chen Y and Wang LJ: Emerging molecular basis of hematogenous metastasis in gastric cancer. World J Gastroenterol. 22:2434–2440. 2016. View Article : Google Scholar : PubMed/NCBI

14 

Tanakaya K, Takeuchi H, Yasui Y, Takeda A, Umeda Y and Murakami I: Metastatic carcinoma of the colon similar to Crohn's disease: A case report. Acta Med Okayama. 58:217–220. 2004.PubMed/NCBI

15 

Tseng LJ, Jao YT, Wu CJ, Lin RC, Kuo JY, Chang KK and Mo LR: Metastatic gastric carcinoma presenting as multiple submucosal colonic cysts. Gastrointest Endosc. 59:317–318. 2004. View Article : Google Scholar : PubMed/NCBI

16 

Pace U, Contino G, Chiappa A, Bertani E, Bianchi PP, Fazio N, Renne G, Di Meglio G and Andreoni B: Metachronous colon metastases from gastric adenocarcinoma: A case report. Case Rep Oncol. 2:92–96. 2009. View Article : Google Scholar : PubMed/NCBI

17 

Lim SW, Huh JW, Kim YJ and Kim HR: Laparoscopic low anterior resection for hematogenous rectal metastasis from gastric adenocarcinoma: A case report. World J Surg Oncol. 9:1482011. View Article : Google Scholar : PubMed/NCBI

18 

Mayumi K, Terakura M, Hamano G, Ikebe T, Takemura M and Hori T: A case of repeated postoperative recurrence of gastric cancer treated via laparoscopic approach. Gan To Kagaku Ryoho. 40:2176–2178. 2013.(In Japanese). PubMed/NCBI

19 

Watanabe M, Narusaka T, Hayashi D, Matsumura T, Nonaka Y, Kurose M, Tokuda N and Miyake T: A case of metastatic carcinoma of the colon after curative resection for gastric cancer. Gan To Kagaku Ryoho. 40:2182–2184. 2013.(In Japanese). PubMed/NCBI

20 

Oh SY, Cunningham J and Saif MW: Colonic metastasis from gastric cancer. Clin Colorectal Cancer. 13:255–256. 2014. View Article : Google Scholar : PubMed/NCBI

21 

Tomita Y, Fujii Y, Miura S, Fujita J, Morioka E, Kaida D, Ohonishi T, Ohono Y, Noguchi M, Funaki H, et al: A successful case of treatment of colonic metastasis and peritoneal recurrence of type 4 gastric cancer by using colectomy and chemotherapy. Gan To Kagaku Ryoho. 42:1591–1593. 2015.(In Japanese). PubMed/NCBI

22 

Ikeda K, Sato T, Maezawa Y, Kano K, Satoyoshi T, Segami K, Nakajima T, Ogata T, Cho H and Yoshikawa T: Case of colon metastasis from early gastric cancer 4 years after laparoscopic assisted distal gastrectomy. Gan To Kagaku Ryoho. 43:2208–2210. 2016.(In Japanese). PubMed/NCBI

23 

Uemura N, Kurashige J, Kosumi K, Iwatsuki M, Yamashita K, Iwagami S, Baba Y, Sakamoto Y, Miyamoto Y, Yoshida N, et al: Early gastric cancer metastasizing to the rectum, possibly via a hematogenous route: A case report and review of literature. Surg Case Rep. 2:582016. View Article : Google Scholar : PubMed/NCBI

24 

Higuchi I, Akiyama Y, Ishikawa A, Hosomi S, Tanigawa T, Hasuike Y and Miyamoto M: Two cases of colon metastasis of gastric cancer by different metastasis pathway. Gan To Kagaku Ryoho. 45:127–129. 2018.(In Japanese). PubMed/NCBI

25 

Su WC, Tsai HL, Wu CC, Tsai SY, Yeh YS, Ma CJ and Wang JY: Two rare cases of synchronous and metachronous colonic metastases in patients with advanced gastric cancer. World J Surg Oncol. 16:212018. View Article : Google Scholar : PubMed/NCBI

26 

Mizuguchi N, Koyama M, Obana A, Kitamura K, Matsumura T, Okada K, Karikomi K, Masamura S, Suzuki H and Suwa T: A case of metachronous ascending colon metastasis from gastric cancer that was difficult to diagnose. Gan To Kagaku Ryoho. 45:2075–2077. 2018.(In Japanese). PubMed/NCBI

27 

Yang S, Liu XL, Guo XL, Song B, Li SZ, Sun XF and Feng Y: Solitary metastasis to the skin and colon from gastric cancer after curative gastrectomy and chemotherapy: A case report. Medicine (Baltimore). 99:e215322020. View Article : Google Scholar : PubMed/NCBI

28 

Okazaki Y, Shibutani M, Nagahara H, Fukuoka T, Iseki Y, Wang E, Maeda K, Hirakawa K and Ohira M: A case of submucosal-like tumor at cecum that was diagnosed as colon metastasis from gastric cancer. Gan To Kagaku Ryoho. 47:2343–2345. 2020.(In Japanese). PubMed/NCBI

29 

Then EO, Grantham T, Deda X, Ramachandran R and Gaduputi V: Metastatic gastric cancer to the colon. World J Oncol. 12:127–131. 2021. View Article : Google Scholar : PubMed/NCBI

30 

Metayer P, Antonietti M, Oumrani M, Hemet J, Lemoine F and Basuyau J: Metastases of a gastric adenocarcinoma presenting as colonic polyposis. Report of a case. Dis Colon Rectum. 34:622–623. 1991. View Article : Google Scholar : PubMed/NCBI

31 

Tomikashi K, Mitsufuji S, Kanemasa H, Sakai M, Wakabayashi N and Tsuchihashi Y: Gastric cancer metastatic to the colon. Gastrointest Endosc. 55:5612002. View Article : Google Scholar : PubMed/NCBI

32 

Lee HC, Yang MT, Lin KY, Tu HY, Zhang TA and Chen PH: Metastases from gastric carcinoma to colon in the form of multiple flat elevated lesions: A case report. Kaohsiung J Med Sci. 20:552–557. 2004. View Article : Google Scholar : PubMed/NCBI

33 

Nakamura H, Fu K, Fukui H, Hurlstone DP, Kaji Y, Ishikawa T and Fujimori T: A solitary colonic metastasis from gastric cancer detected at an early stage. Gastrointest Endosc. 67:1000–1004. 2008. View Article : Google Scholar : PubMed/NCBI

34 

Tural D, Selçukbiricik F, Erçalışkan A, Inanç B, Günver F and Büyükünal E: Metachronous rectum metastases from gastric adenocarcinoma: A case report. Case Rep Med. 2012:7268412012. View Article : Google Scholar : PubMed/NCBI

35 

Reyes-Díaz ML, Torres-Arcos C, Oliva-Mompeán F, Curado-Soriano A, Lizarralde-Gómez CJ and Cuaresma-Soriano F: Colonic metastasis of diffuse signet ring cells gastric carcinoma. Rev Esp Enferm Dig. 104:442–443. 2012.(In Spanish). View Article : Google Scholar : PubMed/NCBI

36 

Gao B, Xue X, Tai W, Zhang J, Chang H, Ma X, Qi Y, Cui L, Yan F and Pan L: Polypoid colonic metastases from gastric stump carcinoma: A case report. Oncol Lett. 8:1119–1122. 2014. View Article : Google Scholar : PubMed/NCBI

37 

Lee IH, Lee JE, Byeon SW, Lee HJ, Huo SM, Yoon SB, Kim JS, Lee SH and Roh SY: A case of advanced gastric cancer presenting as multiple colonic lymphoid hyperplasia. Korean J Gastroenterol. 66:221–226. 2015.(In Korean). View Article : Google Scholar : PubMed/NCBI

38 

Patel YA, McCall SJ, Zhang X, Jaffe T and Shimpi RA: Radiographic and endoscopic regression of metastatic gastric cancer to the colon in the setting of 5-aminosalicylic acid use. J Gastrointest Oncol. 7:E88–E92. 2016. View Article : Google Scholar : PubMed/NCBI

39 

Makker J, Karki N, Sapkota B, Niazi M and Remy P: Rare presentation of gastroesophageal carcinoma with rectal metastasis: A case report. Am J Case Rep. 17:611–615. 2016. View Article : Google Scholar : PubMed/NCBI

40 

Mehershahi S, Mantri N, Sun H, Shaikh D and Patel H: Metastasis from gastric signet ring cell adenocarcinoma presenting as a rectosigmoid stricture: A rare case. Cureus. 12:e85522020.PubMed/NCBI

41 

Curtis RE, Freedman DM, Ron E, Ries LAG, Hacker DG, Edward BK, Tucker MA and Fraumeni JF Jr: New malignancies following cancer survivors: SEER cancer registries, 1973–2000. National Cancer Institute; Bethesda, MD, USA: pp. 9–14. 2006

42 

Jang HJ, Lim HK, Kim HS, Cho EY, Lee SJ, Kim KA and Choi D: Intestinal metastases from gastric adenocarcinoma: Helical CT findings. J Comput Assist Tomogr. 25:61–67. 2001. View Article : Google Scholar : PubMed/NCBI

43 

Duarte I and Llanos OL: Patterns of metastases in intestinal and diffuse types of carcinoma of the stomach. Hum Pathol. 12:237–242. 1981. View Article : Google Scholar : PubMed/NCBI

44 

Razmi M, Ghods R, Vafaei S, Sahlolbei M, Saeednejad Zanjani L and Madjd Z: Clinical and prognostic significances of cancer stem cell markers in gastric cancer patients: A systematic review and meta-analysis. Cancer Cell Int. 21:1392021. View Article : Google Scholar : PubMed/NCBI

45 

Choi YJ, Kim N, Lee HS, Park SM, Park JH, Yoon HY, Shin CM, Park YS, Kim JW and Lee DH: Expression of leucine-rich repeat-containing G-protein coupled receptor 5 and CD44: Potential implications for gastric cancer stem cell marker. J Cancer Prev. 21:279–287. 2016. View Article : Google Scholar : PubMed/NCBI

46 

Fayemi AO, Ali M and Braun EV: Metastatic carcinoma simulating linitis plastica of the colon. A case report. Am J Gastroenterol. 71:311–314. 1979.PubMed/NCBI

47 

Malhotra A, Guturu P, Basim MS and Raju GS: A rare case of breast cancer metastasis presenting as linitis plastica of the stomach and colon (with videos). Gastrointest Endosc. 70:552–553. 2009. View Article : Google Scholar : PubMed/NCBI

48 

Hsiao SC, Chen YH, Lo CC and Lin CI: A noteworthy treatment of metastatic small-cell lung cancer with afatinib, followed by subsequent development of rare metastatic lesions in the ascending and sigmoid colon. Cancer Rep (Hoboken). 3:e12432020.PubMed/NCBI

49 

Li B, Li Q, Li X, Zhang G and Shen L: Signet-ring cell cancer of the colon presenting as facial and gastroduodenal metastasis 7 years after sigmoidectomy. Endoscopy. 46 (Suppl 1):E220–E221. 2014. View Article : Google Scholar : PubMed/NCBI

50 

Iwai N, Okuda T, Harada T, Oka K, Hara T, Inada Y, Tsuji T, Komaki T, Dohi O, Yoshida N, et al: Gastric metastasis from colorectal cancer mimicking a submucosal tumor. Case Rep Gastroenterol. 14:338–345. 2020. View Article : Google Scholar : PubMed/NCBI

51 

Fu JX, Zou YN, Long-Li L and Wang XJ: Widespread metastasis to the stomach 10 years after primary breast cancer: A case report and review of the literature. Medicine (Baltimore). 99:e225272020. View Article : Google Scholar : PubMed/NCBI

52 

Woo J, Lee JH, Lee KE, Sung SH and Lim W: Gastric metastasis as the first presentation one year before diagnosis of primary breast cancer. Am J Case Rep. 19:354–359. 2018. View Article : Google Scholar : PubMed/NCBI

53 

Feczko PJ, Collins DD and Mezwa DG: Metastatic disease involving the gastrointestinal tract. Radiol Clin North Am. 31:1359–1373. 1993. View Article : Google Scholar : PubMed/NCBI

54 

Nieman KM, Romero IL, Van Houten BV and Lengyel E: Adipose tissue and adipocytes support tumorigenesis and metastasis. Biochim Biophys Acta. 1831:1533–1541. 2013. View Article : Google Scholar : PubMed/NCBI

55 

Harryman WL, Marr KD, Hernandez-Cortes D, Nagle RB, Garcia JGN and Cress AE: Cohesive cancer invasion of the biophysical barrier of smooth muscle. Cancer Metastasis Rev. 40:205–219. 2021. View Article : Google Scholar : PubMed/NCBI

56 

Khatun S, Appidi T and Rengan AK: The role played by bacterial infections in the onset and metastasis of cancer. Curr Res Microb Sci. 2:1000782021.PubMed/NCBI

57 

Sano T, Coit DG, Kim HH, Roviello F, Kassab P, Wittekind C, Yamamoto Y and Ohashi Y: Proposal of a new stage grouping of gastric cancer for TNM classification: International gastric cancer association staging project. Gastric Cancer. 20:217–225. 2017. View Article : Google Scholar : PubMed/NCBI

58 

Ikeda Y, Saku M, Kawanaka H, Nonaka M and Yoshida K: Features of second primary cancer in patients with gastric cancer. Oncology. 65:113–117. 2003. View Article : Google Scholar : PubMed/NCBI

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Copy and paste a formatted citation
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Spandidos Publications style
Kohno S, Ikegami M, Yamamoto S, Aoki H, Ogawa M, Yano F and Eto K: A rare case of colorectal metastasis found 8 years and 10 months after gastrectomy for advanced gastric cancer: A case report and literature review. Oncol Lett 25: 203, 2023.
APA
Kohno, S., Ikegami, M., Yamamoto, S., Aoki, H., Ogawa, M., Yano, F., & Eto, K. (2023). A rare case of colorectal metastasis found 8 years and 10 months after gastrectomy for advanced gastric cancer: A case report and literature review. Oncology Letters, 25, 203. https://doi.org/10.3892/ol.2023.13789
MLA
Kohno, S., Ikegami, M., Yamamoto, S., Aoki, H., Ogawa, M., Yano, F., Eto, K."A rare case of colorectal metastasis found 8 years and 10 months after gastrectomy for advanced gastric cancer: A case report and literature review". Oncology Letters 25.5 (2023): 203.
Chicago
Kohno, S., Ikegami, M., Yamamoto, S., Aoki, H., Ogawa, M., Yano, F., Eto, K."A rare case of colorectal metastasis found 8 years and 10 months after gastrectomy for advanced gastric cancer: A case report and literature review". Oncology Letters 25, no. 5 (2023): 203. https://doi.org/10.3892/ol.2023.13789