Case Report J. St. Marianna Univ.Vol. 9, pp. 73–79, 2018

1 Department of Gastrointestinal and General Surgery, Kawasaki Municipal Tama Hospital2 Department of Gastrointestinal and General Surgery, Yokohama City Seibu Hospital, St. Marianna University School of

Medicine3 Department of Gastrointestinal and General Surgery, St. Marianna University School of Medicine

A Case of Concomitant Small Bowel GIST and Colorectal Cancer

Treated by Simultaneous Laparoscopic Resection

Tsukasa Shimamura1, Yukihito Kokuba2, Daisuke Sasaki1, Yutoku Yoshida2, Ryuichi Oshima2, and Takehito Otsubo3

(Received for Publication: May 31, 2018)

AbstractThis report documents simultaneous laparoscopic resection of a small bowel gastrointestinal stromal tumor

(GIST) and transverse colon cancer that were diagnosed preoperatively and concomitantly. The patient was an88-year-old man who was referred to us when computed tomography (CT) performed as follow-up for prostatecancer revealed what appeared to be a small bowel tumor. Abnormal tracer uptake in the small bowel and trans‐verse colon was observed on FDG-positron emission tomography/CT images, so we performed lower gastroin‐testinal endoscopy and discovered a type 2 transverse colon cancer. Laparoscopic partial colectomy and partialsmall bowel resection were performed for a pathological lesion suspected of being GIST, following which adefinitive histopathological diagnosis of transverse colon cancer and small bowel GIST were confirmed. Al‐though GIST can be complicated by other malignant tumors, complication by colorectal cancer is uncommon. Aliterature search revealed only 8 patients who had undergone simultaneous resection for small bowel GIST andcolorectal cancer, and 5 of the 8 were treated by open surgery. There are scattered reports indicating that, as inour case, laparoscopy was performed. We present a rare case of concomitant small bowel laparoscopic resectionand review the relevant literature.

Key wordsSmall intestinal GIST, colorectal cancer, laparoscopy

Introduction

Gastrointestinal stromal tumors (GISTs) accountfor 0.2–0.5% of all tumors of gastrointestinal origin,and of these, 20–30% occur in the small intestine,making it a comparatively rare condition. There hasbeen an increasing number of reports of GIST com‐plicated by malignant tumors, and the combined fre‐quency of the synchronous and metachronous occur‐rences ranges from 9.3% to 26.8%.1–3) However,reports of concomitant small bowel GIST and color‐ectal cancer are rare, and in the majority of the re‐ported cases, the small bowel tumor was detected in‐cidentally during surgery for the colorectal cancer,

and thus simultaneous resection was performed. Inaddition, most cases were managed by means of opensurgery; very few were managed laparoscopically.This report documents simultaneous laparoscopic re‐section of a small bowel GIST and transverse coloncancer that were diagnosed preoperatively and con‐comitantly. We present a rare case of concomitantsmall bowel laparoscopic resection and review therelevant literature.

Case

The patient was an 88-year-old man with a his‐tory of prostate cancer for whom follow-up computedtomography (CT) revealed what appeared to be a

47

73

Figure 1. Contrast-enhanced abdominal CT image that

prompted the patient’s referral to our depart‐

ment. The image depicts a neoplastic lesion in

the small intestine that measured 4 cm and ex‐

hibited non-homogenous internal contrast en‐

hancement and extramural invasion.

Figure 2. FDG-PET/CT image of the small bowel lesion

obtained shortly after the CT study. Abnormal

uptake of tracer (SUVmax = 8.4) was observed.

small bowel tumor. His medical history includedstroke, appendicitis, but no impaired glucose toler‐ance. Contrast-enhanced abdominal CT had been per‐formed, and a neoplastic lesion with unclear marginsand that measured 4 cm along the major axis wasseen in the small intestine. Inhomogeneous internalcontrast enhancement and extramural invasion werenoted, but no intestinal obstruction, surroundinglymph node enlargement, or any other abnormalitywas observed in any other organ (Fig. 1), and the pa‐tient was referred to us.

In the absence of symptoms, we first obtainedoutpatient blood tests that showed a hemoglobin con‐centration of 9.3 g/dL, which was indicative of mi‐crocytic hypochromic anemia. As for tumor markerconcentration, the level of carcinoembryonic antigen(CEA) was 1.1 ng/mL (reference value: <5.0 ng/mL)and cancer antigen 19–9 (CA19-9) was 6.5 U/mL(reference value: 37.0 U/mL).

The lesion was examined by means of 18F-fluo‐rodeoxyglucose positron emission tomography/CT(FDG-PET/CT), which showed abnormal tracer up‐take. The maximum standardized uptake value (SUV‐max) was 8.3, consistent with a small bowel tumor.The small intestinal tumor noted on CT did not ad‐here to or infiltrate the surroundings as it moved inthe pelvis (Fig. 2). Abnormal uptake in the transversecolon, with an SUVmax of 18.6 was also depicted(Fig. 3).

Lower gastrointestinal endoscopy was then per‐formed, and a type 2 tumor that occupied about threefourths of the lumen of the transverse colon was de‐tected and biopsied (Fig. 4). Histopathologically, thetumor was shown to be a moderately to highly differ‐entiated adenocarcinoma. Subsequent barium enemarevealed circumferential stenosis of the right trans‐verse colon (Fig. 5). The small bowel tumor showedno adhesion in the periphery or invasion, and neithersurrounding lymph node enlargement nor a disorderof intestinal passage was observed. Metastatic tumor,small bowel cancer, lymphoma etc. were suspected,but it was diagnosed that the possibility of GIST washigher than the above findings. Small bowel tumorscan be difficult to diagnose even after an invasive ex‐amination, and because the patient was elderly, wewanted to avoid such an examination. If GIST is sus‐pected, resection is the first choice, and after obtain‐ing the patient’s informed consent, it is our policy toperform simultaneous resection of colon cancer andsmall bowel tumor.

Although our patient was older but appeared to

be able to withstand surgery, we performed laparos‐copically assisted surgery under a diagnosis of trans‐verse colon cancer (cT3N0M0, c Stage IIa) and sus‐pected small intestinal GIST because stenosis due tothe colon cancer and progression of anemia were ob‐served. The surgery was performed as follows: A 4-cm incision was made in the epigastrium, 1 port wasplaced in the incision, and 3 additional abdominalports were placed. Upon laparoscopic examination, asmall tumor was found in the jejunum, approximately20 cm caudal to the ligament of Treitz. The pneumo‐

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Shimamura T Kokuba Y et al74

Figure 3. FDG-PET/CT also showed abnormal uptake of

tracer (SUVmax = 18.6) in the transverse co‐

lon.

Figure 4. Gastrointestinal endoscopy depicted a type 2

colorectal cancer that occupied three fourths of

the luminal diameter of the transverse colon.

Figure 5. Barium enema performed after the endoscopic

examination revealed circumferential stenosis

of the right transverse colon.

peritoneum was suspended, and traction was appliedto the section of small intestine containing the tumor.The section was exteriorized through the epigastricincision, and the tumor was resected extracorporeally.Because the transverse colon cancer was mainly onthe right, the pneumoperitoneum was re-established,and laparoscopic D2 lymph node dissection was per‐formed. We then mobilized the section of colon be‐tween the hepatic flexure and ascending colon, ap‐plied traction, exteriorized the section head, andperformed a partial colectomy (transverse colon). Allanastomoses were functional end-to-end anastomo‐

ses. We were guided in our decision making by thepatient’s advanced age and the fact that his perform‐ance status was between 3 and 4.

Upon macroscopic inspection of the surgicalspecimens, the cancer in the transverse colon meas‐ured approximately 55 mm x 35 mm and was deter‐mined to be a type 2 transverse colon cancer. The tu‐mors in the small intestine appeared to be solidsubmucosal tumors with indistinct margins that occu‐pied a section of small intestine measuring 35 mm x35 mm. A solid submucous tumor covered with nor‐mal mucosa was also present that protruded outsidethe intestinal tract (Fig. 6).

Histopathologically, the cancer was classified asa type 2, 55 × 35 mm, tub1>tub2, pT3, int, ly0, v1,pN0, PM0, DM0, cM0, pStage IIa, CurA transversecolon cancer. Spindle-shaped cells proliferating infascicles were seen upon examination of the smallbowel tumors (Fig. 7). The cells were immunohisto‐chemically positive for c-kit and CD34 (Fig. 8a, b),and small bowel GIST was diagnosed. The GIST was35 mm in maximum diameter, the MIB-1 prolifera‐tion index was <1%, and the mitotic count was <5/50 per high-power field. The tumor was classifiedas a low-risk tumor according to both the modifiedFletcher system and Miettinen system.

The postoperative course was good, there wereno complications, and the patient was transferred to arehabilitation hospital on postoperative day 34. The

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Simultaneous laparoscopic bowel resections 75

Figure 6. Resected specimen (cut surface of the tumor).

Upon macroscopic inspection, solid tumors

measuring 4 cm were observed.

Figure 7. H&E-stained section of one of the small bowel

tumors (×20 magnification). A proliferation of

spindle-shaped cells is seen.

Figure 8. Immunohistochemical staining for (a) c-kit (×4 magnification) and (b) CD34 (×10 mag‐

nification) were positive, and GIST was diagnosed.

patient died of pneumonia 18 months after the sur‐gery, but without any sign of tumor recurrence.

Discussion

GIST is widely defined as a mesenchymal tumororiginating in the gastrointestinal tract and derivedfrom the interstitial cells of Cajal (ICCs), which func‐tion as pacemakers for gastrointestinal peristalsis4).Due to mutations in the c-Kit gene, these tumorsshow overexpression of c-Kit protein, a receptor tyro‐sine kinase, but the definition also includes tumorsthat do not fall into a c-Kit mutation class. The vari‐ous GISTs comprise 0.2–0.5% of all tumors of gas‐trointestinal origin5), with 60–70%, 20–30%, and 5%onset in the stomach, small intestine, and colon, re‐spectively. Small bowel GIST is the most difficult todiagnose upon imaging, and early detection is chal‐lenging because patients are often asymptomatic

when the tumors are small. Fujita et al. studied pa‐tients with gastric or small bowel GIST and reportedthat whereas 48.5% of patients with incidentally de‐tected gastric GIST were asymptomatic, 95% of pa‐tients with small bowel GIST had some kind ofsymptoms4). The prognosis of small bowel GIST isless favorable than that of gastric GIST6,7), with re‐ports indicating a 10-year-survival rate of 80.4% forgastric GIST vs. 42.4% for small bowel GIST4).

With respect to GIST concomitant with malig‐nant tumors, Agaimy et al. reported that of 4777cases of GIST, 444 (9.3%) were complicated by asynchronous or metachronous malignant tumor3,8).Approximately half of these complicating cancerswere of gastrointestinal origin, with colorectal canceraccounting for 22%8). Non-gastrointestinal cancersthat complicate cases of GIST include prostate can‐cer, lymphoreticular tumors, and breast cancer3). Co‐

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Shimamura T Kokuba Y et al76

Table 1. Reported cases of concomitant small bowel GIST and colorectal cancer.

Report year Author Age Sex Cancer onset siteColorectal

cancerp stage

GISTOnset site

GISTTiming of diagnosis

GISTMaximum

diameter (mm)Surgical method

2005 Kusano et al.9) 70 Woman Ascending colon Ⅱ Ileum Intraoperative 15 Laparotomy

2008 Tsujimoto et al.16) 92 Man Transverse colon Ⅱ Ileum Intraoperative 50 Laparotomy

2009 Ogawa et al.17) 68 Woman Ascending colon Ⅲa Jejunum Intraoperative 70 Laparoscopy

2010 Kanazawa et al.18) 65 Woman Sigmoid colon Ⅱ Jejunum Intraoperative 15 Laparotomy

2013 Yagi et al.8) 87 Woman Transverse colon Ⅱ Jejunum Intraoperative 50 Laparotomy

2013 Yagi et al.8) 84 Woman Ascending colon Ⅱ Ileum Postoperative 7 Laparotomy

2013 Nanno et al.19) 77 Man Ascending colon Ⅲa Ileum Preoperative 50 Laparoscopy

2016 Tsukamoto et al.20) 70 Woman Cecum Ⅰ Ileum Preoperative 90 Laparoscopy

2018 Our case 88 Man Transverse colon Ⅱ Jejunum Preoperative 35 Laparoscopy

lon cancer and GIST are presented simultaneously inour case. The etiologies of those neoplasms are sus‐pected as follows: (1) those two neoplasms were oc‐curred incidentally and unrelated, (2) those two neo‐plasms share common pathogenesis, or (3) one tumorpromotes the onset of the other. To date, pathogenesisof those two neoplasms is considered to be incidentaloccurrence and unrelated9). When GIST is diagnosed,it is also necessary to examine the patient for gastro‐intestinal cancer including colorectal cancer.

We searched ICHUSHI Web using the keywords "small intestinal GIST" and "colorectal can‐cer", and, after excluding academic meeting ab‐stracts, we found 8 reported cases of concomitantsmall bowel GIST and colorectal cancer (Table 1). Inaddition, in this case only GIST was found in the pre‐ceding case, two cases diagnosed with GIST and col‐orectal cancer before surgery were diagnosed withcolorectal cancer in advance, and one case was post‐operative, 5 cases were diagnosed intraoperatively.For colorectal cancer cases, CT examination was per‐formed for all cases in the search of metastases be‐fore surgery, so the interpretation of the CT examina‐tion seemed to be important for finding other lesions.Three of the cases were diagnosed preoperatively andtreated simultaneously by laparoscopic resection,which has become increasingly popular, and the other5 cases were treated by open surgery. The case re‐ported herein brings the total number to 9, with amean maximum GIST diameter of 61.3 mm (35–90mm) for tumors resected laparoscopically and asmaller mean maximum GIST diameter of 27.4 mm

(7–50 mm) for those treated by open surgery. Thisdifference in size might be due to the fact that laparo‐scopic surgery allows for a more comprehensive ex‐amination of the abdominal cavity, even though thereare fewer opportunities to directly palpate the gastro‐intestinal tract. Small bowel tumors were identifiedintraoperatively by means of palpation in 2 of the 5patients who underwent open surgery. However, pal‐pation is useful only when extra-intestinal invasion isseen upon visual inspection; otherwise, small bowellesions are difficult to detect. Laparoscopic surgerywill be performed increasingly in the future, and thuswe believe that the opportunities for palpation willdecrease, and this might in turn decrease opportuni‐ties for intraoperative diagnosis.

If this scenario unfolds, preoperative examina‐tion will increase in importance. When we searchedICHUSHI Web using the keyword "small intestinalGIST" (excluding academic society abstracts) for the5 years between 2010 and 2014, we found a total of43 cases. We added these 43 cases to the cases, in‐cluding ours, shown in Table 1 and thus identified 52reported cases in which attempts were made to diag‐nose small bowel GIST by means of CT. The meanmaximum diameter of the GIST for all cases was47.9 mm (range: 3–170 mm), and the mean maxi‐mum diameter of the GIST for the 33 cases identifiedpreoperatively by means of CT was 61.6 mm (range:20–170 mm). It was not possible to identify the tu‐mors on the CT image in the remaining 19 cases. Themean maximum tumor diameter in these cases was27.3 mm (range: 3–60 mm), significantly smaller

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Simultaneous laparoscopic bowel resections 77

than that of tumors that could be identified on the CTimage (p <0.01).

According to the GIST treatment guidelines, it isdifficult to identify lesions of approximately 2 cmwith no gastrointestinal invasion10), and it is prefera‐ble to obtain 3-dimensional data by means of multi‐detector CT (MDCT) with a slice thickness of 2 mminstead of 5 mm. The small bowel GIST in our casemeasured 35 mm and was relatively large and easy toidentify. Radiologists must exercise caution when in‐terpreting diagnostic images, and we believe thatMDCT is useful for diagnosis. As noted in the surgi‐cal treatment guidelines, the characteristics of theGIST should be thoroughly understood, but surgeonswho are experienced in performing laparoscopic sur‐gery can safely resect gastric and small bowel GISTsmeasuring <5 cm by considering the site of origin10).We believe that the diagnosis of small-diameter tu‐mors will increase the likelihood of management bylaparoscopic surgery. Recently, laparoscopic surgeryhas tended to be selected due to its minimal invasive‐ness, and although it was a retrospective study, onereport showed the usefulness of laparoscopic surgeryin the elderly11).

Based on the above, we believe that it is impor‐tant to perform careful preoperative diagnosis to fa‐cilitate the performance of simultaneous laparoscopicresection of concomitant GIST and colorectal cancer,as in the present case, although a possible limitationis whether it is possible to perform diagnosis usingCT scans when the tumor diameter is approximately2 cm. However, the reported cases indicate that smallbowel GISTs with a diameter of 15 mm have beenidentified using MDCT12), and we believe that MDCTwill prove to be useful for the diagnosis of smallGISTs. We have also seen a number of fairly recentreports documenting the diagnosis of small bowel le‐sions by means of capsule endoscopy or double-bal‐loon endoscopy13,14), and increasing the diagnostic po‐tential of these types of examination may be usefulfor the diagnosis of these tumors. The recurrence rateof small bowel GIST is high15), making conscientiousdiagnosis important.

Conclusion

This report documents a case of concomitantsmall bowel GIST and transverse colon cancer thatwere diagnosed preoperatively and then resected si‐multaneously under laparoscopic guidance. The pre‐operative diagnosis of concomitant diseases allowedus to perform simultaneous laparoscopic resections.

In comparison to open surgery, laparoscopic surgeryyields fewer opportunities for intraoperative palpa‐tion. This means that with widespread adoption oflaparoscopic resection, preoperative diagnosis willbecome increasingly important.

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