Bumps in the Colon: Utility of EUS for Colonic Submucosal Masses

Emad M. Abu-Hamda, M.D.
Richard A. Erickson, M.D.

Keywords

Colonoscopy, colorectal EUS, sigmoidoscopy, submucosal masses (SMM).

Introduction

Figure 1

Endoscopic ultrasonography (EUS) has played an invaluable role in elucidating the cause of upper gastrointestinal submucosal masses (SMM)(1). The ability to place the ultrasound transducer in very close proximity to the lesion allows detailed imaging of the lesion’s echotexture as well as defining the wall layer (Figure 1) from which it originates; both important clues to the diagnosis. Very little, however, has been described on the role of EUS in the evaluation of colonic submucosal masses. This maybe due to these lesions being less common in the colon as well as to instrumental difficulties. A forward viewing echocolonoscope is available but has not been widely used due to its expense, the lack of indications currently for colon endosonography and its cumbersome maneuvering capabilities due to the less flexible endoscope tip (2). However, when SMM are encountered in the colon, miniprobes can offer a relatively simple method of differentiating these lesions. We describe seven cases in which EUS, several using miniprobes, was an integral part in the work up and diagnosis of submucosal lesions in the colon.

Method for EUS Capture

To evaluate colonic SMM, a 12 MHz Olympus catheter miniprobe UM 2R (Olympus America, Inc.,Lake Success,NY) was advanced through the working channel of the Pentax EC-3801L videocolonoscope (Pentax Precision Instrument Corp., Orangeburg, NY) after air was suctioned out of the colon and the lumen was filled with deaerated water using the Olympus endoscopic water pump (Model UWS-1). This miniprobe has a 2.5 mm outer diameter, which easily fits through the 3.8 mm biopsy channel of the colonoscope. In the three cases with distal lesions, imaging was accomplished using the standard Olympus radial echoendoscope (GF-UM 20 or GF-UM 130). The GF-UM 20 and GF-UM 130 have similar outer diameters at their tips (13.2 mm and 12.7 mm respectively) to the diameter of a Pentax videocolonoscope (12.8 mm). None of these radial echoendoscopes or miniprobe have Doppler capabilities. The miniprobe is limited to 2 cm to 3 cm of tissue imaging, while the radial echoendoscopes can image as deep as 9 cm to 12 cm. The images were scanned from the original thermal prints.

Case/Body

CASE 1
A 77-year-old woman with a past history of adenomatous colon polyps underwent interval surveillance colonoscopy. On advancing to the cecum there was an approximately 2 cm to 3 cm SMM just distal to the ileocecal valve. The lesion had normal overlying mucosa (Figure 2). A catheter miniprobe endoscopic ultrasound was performed. The mass showed a "pillow sign" to palpation with the catheter probe. No biopsy was done. The mass was seen as a hyperechoic homogeneous lesion contiguous with the third echolayer which correlates with the submucosa (Figure 3). It measured 2 cm by 1.5 cm. Its endosonographic appearance was consistent with a lipoma. As the patient was asymptomatic, no further work up was recommended for the lesion.

Figure 2	Figure 3

CASE 2
A 54-year-old woman underwent a screening flexible sigmoidoscopy. Sigmoidoscopy revealed a 1.5 cm submucosal mass in the sigmoid colon. The endoscopist did a follow up sigmoidoscopy one year later and the mass, which was located at 35 cm from the anal verge, had increased in size to approximately 3 cm (Figure 4) There was a second submucosal mass seen at about 10 cm and this measured 2 cm. The patient was then referred for endoscopic ultrasound. After confirming the above endoscopic findings, the Olympus radial echoendoscope (GF-UM 20) was then advanced under both endoscopic and ultrasonographic guidance to the proximal lesion. Air was suctioned out of the colon and the colon lumen was filled with deaerated water. The proximal mass was seen as a
1.7 cm by 1.5 cm hypoechoic mass originating from the muscularis propria (Figure 5). The margins of the mass appeared smooth but the echotexture of the mass was slightly inhomogeneous. The distal lesion appeared similar to the first lesion as a hypoechoic smooth mass arising from the hypoechoic fourth sonographic layer and measured 2.2 cm by 1.4 cm. No peri-colonic adenopathy was seen. These lesions were felt to be possible gastrointestinal stromal tumors (GIST). No attempt at needle aspiration was made. However, as the first lesion had increased in size over the previous year and a new lesion appeared, it was recommended that the patient undergo surgical resection of the lesions. Surgical pathology revealed these lesions to actually be enteric endometriosis invading from the serosa into the muscularis propria.

Figure 4	Figure 5

CASE 3
A 68-year-old woman underwent screening fecal occult blood test which was found to be positive. Work up included a flexible sigmoidoscopy which was normal and an air contrast barium enema which showed extensive lobulated filling defects involving the right colon as well as a portion of the transverse colon. The radiologic differential diagnosis included an infiltrative mural process versus peritoneal implants causing extramural compression versus numerous sessile polyps. At colonoscopy there were multiple multi-lobulated polypoid lesions in the mid-transverse colon extending to the proximal ascending colon (Figure 6). Some were as small as 1 cm and others were larger measuring 3cm to 4 cm. An Olympus catheter mini-probe (12 MHz) was then advanced through the working channel of the colonoscope. These lesions were all very echogenic with shadowing consistent with being air filled (Figure 7). This was consistent with a diagnosis of pneumatosis cystoides intestinalis. Multiple biopsies were taken from one of these lesions and a small amount of air was seen bubbling from the biopsy site lending support to our diagnosis. Histopathology showed denuded surface epithelium with scattered multinucleated giant cells which can be associated with the pneumatosis cystoides intestinalis; however, the biopsies were too small to show classic well formed empty spaces lined with giant cells. A CT scan of the abdomen done subsequently confirmed the diagnosis. As the patient was asymptomatic and the condition is usually benign (3), no further evaluation was recommended.

Figure 6	Figure 7

CASE 4
A 44-year-old woman with symptoms of irritable bowel syndrome underwent a colonoscopy for a long history of recurrent hematochezia. Colonoscopy revealed a 2 cm to 3 cm slightly bluish SMM in the ascending colon just proximal to the hepatic flexure.(Figure 8). She underwent a CT scan of the abdomen and pelvis, which showed a 2.5 cm by 1.5 cm soft tissue density in the ascending colon but could not clarify this any further. There was no lymphadenopathy. She was then referred for endoscopic ultrasound of the mass using a miniprobe (Figure 9). The lesion appeared totally cystic and appeared to arise from the submucosa. The echo-texture of the fluid was that of clear water without any evidence of internal echoes suggesting that it was filled with a serous-type fluid. There were some internal septae within the lesion (Figure 10). There was no surrounding lymphadenopathy. It was felt that the lesion was a lymphangioma of the colon, which is a completely benign lesion therefore since the patient was asymptomatic with regards to this lesion, no further work up was recommended.

Figure 8	Figure 9	Figure 10

CASE 5
A 65-year-old woman underwent a screening colonoscopy. The Pentax video colonoscope was advanced to the cecum where a 5 cm submucosal mass was seen close to the base of the cecum (Figure 11). The overlying mucosa was completely normal. An Olympus catheter miniprobe was then advanced through the working channel of the colonoscope and it was determined that the submucosal mass was actually extrinsic compression from the patient’s uterus (Figure 12).

Figure 11	Figure 12

CASE 6
A 51-year-old woman who had just been diagnosed with breast cancer underwent a screening flexible sigmoidoscopy and was found to have a small SMM in the rectum (Figure 13) and was referred for EUS. The Olympus radial echoendoscope (UM-130) was advanced to the lesion. It was located 9 cm from the anal verge. The lesion was indeed a submucosal mass which was homogenous, hypoechoic and well circumscribed (Figure 14). It appeared to arise from the second, (hyperechoic) endosonographic layer with a very thin layer of overlying mucosa. It measured 7 mm by 9 mm. Since there was such a thin layer of overlying mucosa, it was felt that biopsies using the jumbo forceps with bite-on-bite technique would yield a diagnosis therefore that was performed and biopsies came back positive for carcinoid tumor.

Figure 13	Figure 14

CASE 7
A 43-year-old woman underwent a colonoscopy for hematochezia. A 1 cm by 1 cm submucosal mass was found in the rectum approximately 10 cm from the anal verge. Biopsies revealed only normal colonic mucosa therefore she was referred for EUS. Initial flexible sigmoidoscopy showed the SMM with a central ulceration (Figure 15). EUS was performed with the Olympus radial echoendoscope (UM-20) and the lesion appeared as a slightly inhomogenous hypoechoic mass arising from the second echosonographic layer, the hyperechoic submucosa. The mass itself was seen ulcerating through the mucosa (Figure 16). The lesion was felt to most likely be consistent with a rectal carcinoid or a GIST arising from the muscularis mucosa. Since prior biopsies were non-diagnostic, a transanal excision was done and revealed anaplastic plasmacytoma versus an immunoblastic lymphoma and she was referred to oncology.

Figure 15	Figure 16

Discussion

Gastrointestinal submucosal mass is the term given to any mass or mass-like lesion that protrudes into the lumen of the gastrointestinal tract and is covered with normal overlying mucosa. These lesions can originate from the gastrointestinal wall itself (intramural) or can be caused by extrinsic compression from adjacent structures (extramural). These lesions are usually found incidentally during endoscopy or barium radiography done for other indications. Once a submucosal mass is identified, the role of EUS in the work up is to try to elucidate whether a SMM is intramural or extramural, after which defining the echotexture of the lesion as well as the layer of origin can narrow down the list of differential diagnoses often leading to the correct diagnosis (Table 1). This is extremely difficult to do by endoscopy or barium radiography alone as extramural lesions causing compression of the lumen of the colon are usually indistinguishable form intramural SMM. EUS has become an invaluable tool in our armamentarium in the work up and diagnosis of the etiology of SMM.

SMM in the colon are rare (4) and very little data is available on these SMM as compared to SMM of the upper GI tract. The causes of SMM in the large intestine are slightly different however and warrant mentioning. The usual causes of SMM in the upper GI tract such as gastrointestinal stromal tumors, lipomas carcinoid tumors, varices, duplication cysts, submucosal metastases as well as extrinsic compression from adjacent structures can also present as SMM affecting the colon. Lesions unique to the lower GI tract however include enteric endometriosis and pneumatosis cystoids intestinalis. With the availability of catheter miniprobe EUS, lesions even in the proximal colon can be easily evaluated endosonographically to determine their etiology. It is generally not necessary to perform EUS for lipomas of the colon since many of them have a characteristic endoscopic appearance. However, when the appearance is not classic, EUS can confirm one’s suspicion and provide a definitive diagnosis. The appearance of lipomas of the colon are no different from those of the upper GI tract and endosonographincally appear as hyperechoic homogenous lesions arising from the submucosa (third layer of the GI tract). This finding is essentially diagnostic of lipomas (4). Endometriosis which can affect up to 20% of menstruating females is defined as the presence of functioning extra-uterine endometrial tissue (5). This tissue is located most commonly in the uterosacral ligament but can in rare instances affect the rectosigmoid colon. Symptoms are dependent of the location and degree of tissue infiltration and include infertility, pelvic pain dysmenorrhea and dyspareunia (5). GI symptoms occur in approximately one third of patients (5) and include rectal bleeding which is more prominent during menses as are most of the other symptoms (4). Infiltration of the rectosigmoid colon by endometrial tissue, so called enteric endometriosis, can present as a SMM. Endosonographically, the appearance can be difficult to distinguish from GIST’s. The endosonographic appearance of endometriosis is hypoechoic, and the merging of the muscularis propria and the endometrial tissue simulates the endosonographic features of a GIST (4,5). Clues that may help in differentiating these from GIST’s include occasional thickening of the adjacent submucosa which can occasionally be involved with functioning endometrial tissue, localization to the anterior of lateral rectal wall which is in direct proximity to the uterus (5) or seeing hypoechoic masses adjacent to the rectosigmoid colon representing endometrial deposits in the surrounding tissue (5,6). Management of these lesions is dependent on patient’s symptoms; those who are symptomatic usually require a laparatomy with a segmental resection depending on the site of enteric involvement (5). Pneumatosis Cystoides Intestinalis (PCI) also known as pneumatosis coli refers to the presence of air in the bowel wall. Many theories as to its etiology have been proposed including mechanical theory where trauma to the mucosa allowing luminal air to dissect into the bowel wall, the bacterial theory where gas producing bacteria translocate into the submucosa through mechanical breaches in the mucosa and the pulmonary theory where increased intrathoracic pressure in patients with COPD, asthma and patients on mechanincal ventilation leads to alveolar rupture with air tracking along the mediatinum, retroperitoneum to the mesentery eventually to the bowel wall via breaks in the serosa. Although none of these theories explain all cases of PCI, it is more likely that several mechanisms play a role in the pathogenesis of PCI (3,7). Most patient’s presenting with PCI are asymptomatic and lesions are found incidentally during endoscopic or radiologic examinations done for other indications (7). Patients who are symptomatic can present with a wide variety of symptoms from non specific complaints of abdominal pain and distention, diarrhea, constipation, mucus discharge and excessive flatulence to more specific symptoms of rectal bleeding, those consistent with bowel obstruction and life threatening peritonitis requiring emergent intervention (7). Colorectal PCI presents as broad based submucosal masses, which may have a pale appearance or may be covered by hemorrhagic mucosa (3). Endoscopic appearance however is certainly not characteristic and evaluation by EUS can lead to a definitive diagnosis by showing multiple hyperechoic lesions in the submucosa with acoustic shadowing obscuring the outer layers of the bowel wall due to the air filled cystic spaces in the submucosa (3,7). Management depends on whether these lesions are found incidentally in which case it follows a benign course or whether the patients symptoms are caused by PCI in which case medical, endoscopic or surgical therapy may be indicated. Cystic lymphangioma of the colon are extremely rare lesions that present as submucosal masses in the large intestine (8,9). Most of the cases have been reported from Japan (10). They are felt to represent dilated lymphatic channels lined by endothelial cells, the exact cause of which remains unknown. They are usually found incidentally in asymptomatic patients during routine endoscopy or barium radiography, however patients that have been symptomatic have complained of abdominal pain and rectal bleeding (9). Endoscopically these lesions appear as a solitary SMM with smooth overlying mucosa. The pillow sign is usually positive after applying pressure to the mass with a closed biopsy forceps (9,11). EUS of these lesions shows a characteristic and consistent finding of anechoic multiseptate cystic lesion arising from the submucosa (third layer of the GI tract ) with an intact muscularis propria (9-13). These lesions have no malignant potential and if diagnosed in an asymptomatic patient can be safely left alone (11,12). In patients in whom symptoms may be due to a cystic lymphangioma, then excision either surgically or endoscopically may be undertaken as aspiration of these cysts invariably leads to reaccumultion of cystic fluid (9,10,12). Extramural compression by an adjacent structure is one of the easiest causes of a submucosal mass to be able to evaluate by EUS. In the colorectum, extrinsic compression by surrounding abdominal organs such as the prostate or uterus can present as a SMM. Occasionally, pathologic extrinsic compression from such things as enlarged lymph nodes or extramural endometriosis can present as a SMM. Endosonographically, these are seen a normal five layer GI wall structure which is interposed between the extrinsic organ or mass from the bowel lumen (6). Carcinoid tumors are neuroendocrine tumors arising from enterochromaffin cells. Their management depends on their location, size, depth of invasion and the presence of metastasis. Rectal carcinoid tumors are rarely symptomatic and are usually detected incidentally (1). Endosonographically, they appear as well demarcated, smooth, hypoechoic, homogenous lesions located in the submucosa (third layer of the GI tract ). They can however arise from the first or second layers as well (6). Lesions confined to the submucosa and are less than 2 cm without evidence of lymphadenopathy can be resected endoscopically. Surgery is indicated if there is extension into the muscularis propria or if lymph node involvement is suspected (1,6,14). Primary malignant lymphomas of the colon are rare and account for less than 1% of malignant neoplasms of the colon (15). Lymphomas usually present as mucosal tumors but can occasionally present as a SMM. There are only rare reports describing the EUS appearance of lymphomas. Those reports describe them as a hypoechoic inhomogeneous mass arising from the submuocsa but can also arise from the 2nd or 4th layers depending on the stage of the disease (1,4,15).

Summary

In recent years, EUS has become an indispensable tool in the work up of patients with SMM of the upper GI tract. Now, with the availability of catheter miniprobes, EUS should play a unique role in the diagnosis of large bowel SMM located proximal to the rectosigmoid junction where upper echoendoscope have difficulty negotiating. With more widespread use of colorectal EUS, we should start to see an impact on the choice of therapy for SMM of the colorectum due to the ability to provide accurate information on the appearance, size, layer of origin as well as the nature of these lesions.

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Editor:
John C. Deutsch, M.D.
Duluth, MN

Editorial Board:
Manoop S. Bhutani, M.D.
Galveston, TX
William R. Brugge, M.D.
Boston, MA
Peter R. McNally, D.O.
Denver, CO
Iqbal S. Sandhu, M.D.
Salt Lake City, UT
Thomas J. Savides, M.D.
San Diego, CA