The Use of Endoscopic Ultrasound-Guided Fine-Needle Aspiration for Investigation of Submucosal and Extrinsic Masses of the Colon and Rectum

• Introduction
• Patients and Methods
• EUS-FNA Technique
• Results
• Discussion
• Acknowledgment
• References

Background and Study Aim: Ensdoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) has been reported as a useful technique for histological diagnosis of submucosal or extrinsic gastrointestinal and pancreatic lesions. The aim of this study was to evaluate the use of EUS-FNA for the diagnosis of lesions either within or adjacent to the wall of the colon and rectum.
Patients and Methods: A total of 22 patients with a lesion within the wall of, or adjacent to, the colon or rectum underwent EUS-FNA. They were divided into two groups: patients who had previously had a malignancy (the ”previous +ve” group, n = 11), and patients who had not previously had a malignancy (the ”previous -ve” group, n = 11). In the four patients who had lesions located proximal to the sigmoid colon, EUS-FNA was performed using a guide wire and overtube. The success rates for adequate tissue sampling and for detecting malignant and benign masses by EUS-FNA were evaluated and the success rate for detection was compared with the success rate of EUS and computed tomography.
Results: Sufficient tissue for evaluation was obtained from 21 of the 22 patients (95.5 %). The overall rate of detection of malignant and benign masses was 95.5 % (21/22) for EUS-FNA and 81.8 % (18/22) for pre-EUS-FNA imaging investigations. Of the 11 patients in the previous +ve group, ten were diagnosed with recurrences of primary malignancies; of the 11 patients in the previous -ve group, four were diagnosed with primary malignancies and seven were diagnosed with benign lesions. There were no complications related to the EUS-FNA procedure.
Conclusions: EUS-FNA is a safe technique which is useful in the planning of treatment for patients who have a mass within the wall or adjacent to the wall of the entire length of the colon or rectum.

Introduction

Endoscopic ultrasound (EUS) has entered the clinical arena as a tool that is able to demonstrate the detailed structure of the gastrointestinal tract and surrounding tissues using high-frequency ultrasound. It has been used in the detection of lesions in or adjacent to the gastrointestinal wall [1] [2] [3] [4], in the staging of malignancy [5] [6] [7] [8] [9], and, using a convex-type echo endoscope with Doppler function, for the assessment of blood flow within and surrounding a lesion [10] [11].

In addition to the role of EUS in the imaging diagnosis and staging of malignancies in various organs, many authors have reported the usefulness of EUS-guided fine-needle aspiration (EUS-FNA) as a technique for histological diagnosis of submucosal lesions or lesions which are extrinsic to the gastrointestinal tract, especially in the upper gastrointestinal tract and pancreas [12] [13] [14] [15]. In the colorectal region, the use of EUS-FNA in the investigation of idiopathic pelvic masses has also been reported [16] [17] and the use of EUS-FNA in the management of patients with perirectal masses has recently become more routine [18] [19]. However, questions about the types and location of colon lesions that can be investigated by EUS-FNA still remain, and it can therefore be assumed that the use of EUS-FNA via the colorectal route has been insufficiently investigated. It is not clear whether the indications for EUS-FNA via the colorectal route should be limited to pelvic masses. The aim of this study was to assess the use of EUS-FNA in the entire large intestine.

Patients and Methods

From May 1998 to July 2002, EUS was performed in the colon or rectum in 127 patients. Of these patients, 22 patients (14 men, 8 women; mean age 59 years, range 42 - 74) were shown to have a submucosal mass in, or an extrinsic mass attached to, the colon or rectum (no patients had multiple lesions) and underwent EUS-FNA. These 22 patients were divided into two large groups: patients who had previously had a malignancy, the ”previous +ve” group (n = 11); and patients who had not previously had a malignancy, the ”previous -ve” group (n = 11). The previous +ve group was subdivided into patients who had previously had rectal carcinoma, the ”previous +ve/rectal” group (n = 6) and patients who had previously had another type of malignancy, the ”previous +ve/other” group (n = 5). All six patients in the previous +ve/rectal group had undergone a low anterior resection, and their anastomoses were located in the rectum. In all these patients the new masses were located in the pelvis, close to the anastomosis. The previous +ve/other group consisted of patients with gastric carcinoma (n = 2), ovarian carcinoma (n = 1), bile duct carcinoma (n = 1), and rectal carcinoid (n = 1). These tumors were attached to the rectum (n = 3), to the sigmoid colon (n = 1), or to the transverse colon (n = 1). The masses in patients in the previous -ve group were located in or adjacent to the rectum (n = 8), adjacent to the descending colon (n = 2), or in the cecum (n = 1).

In the previous +ve group, the lesions were detected during follow-up examination for their previous malignancy (n = 7) or during an initial examination for the investigation of anal pain (n = 4). In the previous -ve group the lesions were detected during an initial examination for the investigation of a positive fecal occult blood test found during a routine medical examination (n = 3), or for the investigation of an abnormality in defecation (n = 3), hematochesia (n = 2), abdominal fullness (n = 2), or abdominal pain (n = 1). The initial means of detecting a patient’s lesion were colonoscopy (n = 12), computed tomography (CT) (n = 8), and abdominal ultrasonography (n = 2). The median diameter of the tumors measured by EUS was 25.0 mm, with an interquartile range of 18.0 mm (in the previous +ve/rectal group the median was 24.5 mm; in the previous +ve/other group the median was 35.0 mm; and in the previous -ve group the median was 35.0 mm). In all cases except for one, a lesion in the descending colon (patient 20), prior endoscopic biopsy failed to obtain sufficient samples from the target lesion. The previous endoscopic biopsy specimen from patient 20 showed malignant cells, but it was not possible to make a definitive pathological diagnosis from this specimen because a small quantity of malignant cells was dispersed in severely necrotic tissue, and no typical cell arrangement or other histological characteristics were identified.

The diagnosis before EUS-FNA, utilizing prior EUS, CT, and abdominal ultrasonography imaging results, was of malignancy in 19 patients (patients 1 - 11; 12, 14, and 16 - 21) and of a benign lesion in three patients (patients 13, 15, and 22), based on the endosonographers’ interpretation of the images.

EUS-FNA was performed using a convex array echo endoscope connected to an ultrasound scanning system: either an FG36UX echo endoscope (Pentax Precision Instrument Corp., Tokyo, Japan) connected to an EUB-525 system (Hitachi Medico Corp., Tokyo, Japan); or a GF-UCT240 echo endoscope (Olympus Optical Corp., Ltd., Tokyo, Japan) connected to a Prosound-5500 system (Aloka Corp., Ltd., Tokyo, Japan). The patients were prepared for EUS-FNA by administration of electrolyte lavage solution (Niflec, polyethylene glycol 4000; Ajinomoto Pharma, Japan) on the morning of the procedure. Following EUS-FNA, antibiotics were administered once. Post-procedure complications were assessed by observing the hospitalized patient until the next day and also by checking the blood cell count and C-reactive protein level on the next day. A diagnosis of a benign lesion was determined by surgery or by careful observation of the patient and confirmation that there was no increase in the size of the lesion, as assessed by CT or EUS, for more than 6 months (in case a biopsy had missed malignant tissue and been classified as ”benign” when malignancy did in fact exist). Informed, written consent for EUS-FNA was obtained from all patients.

EUS-FNA Technique

EUS was performed initially in order to evaluate the target lesion and surrounding abnormalities, using an echo endoscope with a radial view (Olympus CF-UM200), which is used exclusively for the colon and rectum, or a miniature probe (Olympus UM-2R) through an endoscopic channel. Patients were sedated with midazolam, as required, to achieve conscious sedation. The convex-type echo endoscope has a long, straight, hard tip, with an oblique view, so it is difficult to insert the endoscope into the proximal colon from the rectum. This problem was resolved by insertion of a standard colonoscope (Olympus CF-Q240I) through an overtube (Olympus ST-C3) to the right-sided colon, then leaving the overtube in the left-sided colon in order to keep the sigmoid colon straight, so allowing insertion of the echo endoscope more proximally in the colon. The echo endoscope could also be safely inserted more proximally by using a guide wire (0.045 inch, 3500 mm) through the accessory channel (Figure [1]). The overtube and guide wire technique was used in four patients with lesions proximal to the sigmoid colon (patients 11, 20, 21, and 22). A 22-G aspiration biopsy needle with a 1950-mm-long metal sheath and a 22-G, 34-mm-long adjustable needle was used through the accessory channel. The aim was to obtain a specimen which was easily visible to the naked eye when placed in a bottle of 10 % formaldehyde. If the specimen was oily, it was sprayed on a glass slide for fixation by steam formaldehyde. The FNA procedure was repeated until at least three specimens were obtained.

Results

The study results are summarized in Table [1]. The overall success rate for obtaining sufficient tissue by EUS-FNA was 95.5 % (21/22). In one patient from the previous +ve/rectal group we were unable to obtain adequate tissue to make a diagnostic assessment and a transanal biopsy under spinal anesthesia was performed, which confirmed the presence of adenocarcinoma. The other five patients in the previous +ve/rectal group were diagnosed with anastomotic recurrence of rectal carcinoma by EUS-FNA. Five of the 22 patients (patients 10, 11, 20, 21, and 22) (22.7 %) had lesions proximal to the rectum.

The overall success rate of detecting malignant and benign masses with EUS-FNA was 95.5 % (21/22). However, imaging investigations alone, without the histological findings of EUS-FNA, had a success a rate of 81.8 % (18/22) (Table [2]). The P value of the difference between EUS-FNA diagnosis and imaging diagnosis was 0.17 (Fisher’s exact probability), with an odds ratio of 4.67 and 95 % confidence interval of 0.477 - 45.62. Ten patients in the previous +ve group (five patients with rectal carcinomas, two with gastric carcinoma, one with ovarian carcinoma, one with bile duct carcinoma, and one with rectal carcinoid) were diagnosed with recurrences of primary malignancies by obtaining adenocarcinoma or carcinoid tissue using EUS-FNA. Primary malignancies were diagnosed histologically, before treatment, in four out of the 11 patients in the previous -ve group (ovarian carcinoma in patient 17, malignant lymphoma in patient 18, a rectal gastrointestinal stromal tumor in patient 19, and neuroendocrine carcinoma in patient 20). All the patients who were diagnosed with malignancy by EUS-FNA underwent surgery and/or chemotherapy, combined with radiation therapy. The remaining patients, including four who were suspected of having malignancies before EUS-FNA (patients 12, 14, 16, and 21), were diagnosed as having benign lesions (hemangioma, abscess, fibrosis, lipoma, or epidermoid cyst). Antibiotics were administered to the patient with a perirectal abscess, an appendectomy was performed in the patient with an abscess of the appendix, and the others were observed, without surgery. It was concluded that these were indeed all benign lesions when they had shown no increase in size after an observation period of more than 6 months. No complications occurred following EUS-FNA in this study.

Figures [2], [3] show the colonoscopic and EUS images obtained from two patients who underwent evaluation of the right-sided colon and the histological views obtained after EUS-FNA.

Discussion

EUS-FNA has been recognized as a useful tool in differentiating between benign and malignant tumors located within or attached to the upper gastrointestinal wall [20] [21] [22] [23] [24] [25] [26] and in the staging of malignancies [27] [28] [29]. However, EUS-FNA has been performed in fewer patients with colorectal lesions. The reasons for this may be that: a) there may be a lower incidence of submucosal tumors in the colon and rectum than in the upper gastrointestinal tract [30]; b) colorectal lesions may be less likely to be found as incidental findings by abdominal ultrasonography or other noninvasive examinations; and c) some physicians may avoid using EUS-FNA for lesions of the colonic area proximal to the rectum because of difficulties in inserting the specialized colonic echo endoscope. Previous reports concerned with EUS-FNA indicate that perirectal lesions comprised only 1.9 % to 4.6 % of all indications for EUS-FNA examinations in each institution, and there is not a single report describing the performance of EUS-FNA proximal to the left-sided colon in the literature [12] [13] [14] [15] [31]. In our institution, EUS-FNA was performed in the colon and rectum in only 5.8 % of all cases done to date. The use of EUS-FNA for the colon and rectum may increase in the future if patients with previous malignancy are carefully followed up, especially those with rectal carcinoma detected by colonoscopy, ultrasonography, and CT, and if the recognized indications for EUS-FNA expand to the investigation of lesions of the entire colon and rectum.

In the six cases of recurrence of rectal carcinoma (patients 1 - 6), the presence of adenocarcinoma tissue was verified in five patients. In the other cases of previous malignancy (patients 7 - 11), treatment decisions were based on whether the tissue obtained suggested recurrence of malignancy. In the 11 patients with no previous malignancy, four lesions were diagnosed as primary malignancies and seven were suspected to be benign lesions by EUS-FNA. In three of these seven patients the choice of treatment was altered because the EUS-FNA results differed from those of the imaging diagnoses (patients 12, 14, and 16). EUS-FNA can be applied not only to recurrences in colonic anastomoses or in the peritoneum adjacent to the colon and rectum, but also to idiopathic pelvic and abdominal masses adjacent to the colon and rectum. In addition, EUS-FNA can be easily performed in perirectal lesions because they are close to the anus and the convex tip can be set adjacent to the lesion. Therefore, perirectal location of a lesion is thought to be a good indication for EUS-FNA. However, EUS-FNA has not been performed for lesions in or adjacent to the colon proximal to the rectum because of the difficulty in inserting the echo endoscope and because of the relatively low incidence of these tumors.

Despite this difficulty, we were able to perform EUS-FNA for lesions proximal to the rectum. Bhutani & Nadella described that, in expert hands, the forward-oblique-viewing upper echo endoscope can be advanced safely to the sigmoid/left-sided colon for EUS imaging of benign and malignant colonic lesions [4]. We consider that, by using an overtube and a guide wire, the forward-oblique-viewing upper echo endoscope can be advanced proximal to the left-sided colon more safely and that EUS-FNA can be performed for lesions for which EUS images cannot be obtained via the upper gastrointestinal tract. Of course, greater effort is required to advance the echo endoscope in patients who have severe colonic tortuosity or redundancy, adhesions, or diverticula. It may be feasible to extend the indications for EUS-FNA to submucosal lesions or lesions attached to the entire large intestine, even to lesions as proximal as the terminal ileum.

The overtube technique was used in the early days of colonoscopy, but gradually became unnecessary in the clinical setting as advances in techniques and instruments allowed the performance of total colonoscopy without its use. Some anxiety remains that employing the overtube technique may increase the incidence of perforation during insertion of the overtube. To the best of our knowledge, there is no literature on the frequency of perforation caused by the use of the overtube technique, although there has been a report of colonic submucosal hematoma related to the use of an overtube [32]. As with CT-guided FNA, with a low rate of complications [33] [34], we think the overtube technique entails little risk, and that that small risk can be decreased further by inserting the overtube with the greatest of care. In addition, EUS-FNA using the overtube technique possesses some inherent advantages, such as the visualization of real-time images and the fact that bone and bowel gas do not hamper its use.

In conclusion, EUS-FNA has been established as a practical and safe technique in the entire colon and rectum. It can be performed by employing an overtube and a guide wire when the target lesion is located proximal to the rectum. EUS-FNA is useful for deciding on the treatment for lesions in, or attached to, the entire length of the colon and rectum which cannot be diagnosed by other examination techniques.

Acknowledgment

The authors would like to express their gratitude to Mr. John Cole for reading our draft and giving us suggestions on language and style.

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Y. Niwa, M. D.

Division of Therapeutic Medicine, Department of Internal Medicine, Nagoya University Graduate School of Medicine

65 Tsuruma-cho · Showa-ku · Nagoya 466-8560 · Japan

Fax: + 81-52-744-2180

eMail: yniwa@med.nagoya-u.ac.jp

References

• 1 Niwa Y, Nakazawa S, Tsukamoto Y. et al . A new method for evaluating gastric ulcer healing by endoscopic ultrasonography.  Scand J. Gastroenterol ;  26 457-464
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• 2 Rösch T, Lorenz R, Dancygier H. et al . Endosonographic diagnosis of submucosal upper gastrointestinal tract tumors.  Scand J Gastroenterol. 1992;  27 1-8
  PubMedSuche in Google Scholar
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  PubMedSuche in Google Scholar
• 4 Bhutani M S, Nadella P. Utility of an upper echo endoscope for endoscopic ultrasonography of malignant and benign conditions of the sigmoid/left colon and the rectum.  Am J Gastroenterol. 2001;  96 3318-3322
  CrossrefPubMedSuche in Google Scholar
• 5 Rösch T, Lorenz R, Braig C. et al . Endoscopic ultrasonography in diagnosis and staging of pancreatic and biliary tumors.  Endoscopy. 1992;  24 (Suppl 1) 304-308
  PubMedSuche in Google Scholar
• 6 Fockens P, Manshanden C G, van Lanschot J J. et al . Prospective study on the value of endosonographic follow-up after surgery for esophageal carcinoma.  Gastrointest Endosc. 1997;  46 487-491
  PubMedSuche in Google Scholar
• 7 Kameyama H, Niwa Y, Arisawa T. et al . Endoscopic ultrasonography in the diagnosis of submucosal lesions of the large intestine.  Gastrointest Endosc. 1997;  46 406-411
  PubMedSuche in Google Scholar
• 8 Reed C E, Mishra G, Sahai A V. et al . Esophageal cancer staging: improved accuracy by endoscopic ultrasound of celiac lymph nodes.  Ann Thorac Surg. 1999;  67 319-322
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  CrossrefPubMedSuche in Google Scholar
• 12 Wiersema M J, Vilmann P, Giovannini M. et al . Endosonography-guided fine-needle aspiration biopsy: diagnostic accuracy and complication assessment.  Gastroenterology. 1997;  112 1087-1095
  PubMedSuche in Google Scholar
• 13 Gress F G, Hawes R H, Savides T J. et al . Endoscopic ultrasound-guided aspiration biopsy using linear array and radial scanning endosonography.  Gastrointest Endosc. 1997;  45 243-250
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  PubMedSuche in Google Scholar
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  PubMedSuche in Google Scholar
• 17 Sailer M, Bussen D, Fein M. et al . Endoscopic ultrasound-guided transrectal biopsies of pelvic tumors.  J Gastrointest Surg. 2002;  6 342-346
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  CrossrefPubMedSuche in Google Scholar
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  PubMedSuche in Google Scholar
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  CrossrefPubMedSuche in Google Scholar
• 24 Ando N, Goto H, Niwa Y. et al . The diagnosis of gastrointestinal stromal tumors with EUS-guided fine-needle aspiration with immunohistochemical analysis.  Gastrointest Endosc. 2002;  55 37-43
  CrossrefPubMedSuche in Google Scholar
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Y. Niwa, M. D.

Division of Therapeutic Medicine, Department of Internal Medicine, Nagoya University Graduate School of Medicine

65 Tsuruma-cho · Showa-ku · Nagoya 466-8560 · Japan

Fax: + 81-52-744-2180

eMail: yniwa@med.nagoya-u.ac.jp