British Journal of Radiology 74 (2001),1017-1022 © 2001 The British Institute of Radiology
Transit endoscopic ultrasound of colorectal cancer using a 12 MHz catheter probe
K Akahoshi, MD, PhD1,
S Yoshinaga, MD1,
A Soejima, MD1,
T Nagaie, MD, PhD2,
N Koyanagi, MD, PhD2,
K Nakanishi, MD, PhD3,
N Harada, MD, PhD4 and
H Nawata, MD, PhD4
Departments of 1Gastroenterology, 2Surgery and 3Pathology, Aso Iizuka Hospital, Iizuka 820-8505 and 4The Third Department of Internal Medicine, Faculty of Medicine, Kyushu University, Fukuoka 812-0054, Japan
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Abstract
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The objective of this study was to examine the accuracy of a 12 MHz ultrasound catheter probe in the pre-operative staging of colorectal cancer by assessing the depth of tumour infiltration and involvement of pericolonic lymph nodes. 159 patients with colorectal cancer who underwent ultrasound examination with a 12 MHz catheter probe were studied prospectively. The results of this imaging procedure were compared with the histological findings of the resected specimens. The accuracy of the 12 MHz ultrasound catheter probe for depth of invasion (T category) was 85% (131/154) for all tumours, 87% (46/53) for pT1 tumours, 60% (9/15) for pT2 tumours, 89% (74/83) for pT3 tumours and 67% (2/3) for pT4 tumours. The accuracy for tumours of the rectum and colon was 81% and 89%, respectively. The accuracy of the probe for nodal staging (N category) was 67% (76/114) overall. The sensitivity was 70% (33/47), the specificity 64% (43/67), the positive predictive value 58% (33/57) and the negative predictive value 75% (43/57). Endoscopic ultrasound using a 12 MHz catheter probe accurately assessed tumour stage, although nodal staging remained suboptimal. This method may aid in the selection of treatment for patients with colorectal cancer.
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Introduction
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Different treatment concepts, including local excision, radical resection and multimodality therapy, are available for colorectal cancer depending on the tumour stage [1, 2]. Consequently, access to an accurate and reliable method for staging these tumours pre-operatively is essential if patients are to receive appropriate treatment. However, it is difficult to assess the depth of tumour invasion by the routine methods of barium enema, colonoscopy and CT. Endoscopic ultrasound (EUS) examination has added a new dimension to the evaluation of tumour invasion and lymph node involvement in gastrointestinal cancer [2–21]. A number of studies have reported the usefulness of conventional EUS for staging colorectal cancer [4–15, 21]. However, conventional EUS has several disadvantages, including the high cost of equipment, the use of two instruments (one for endoscopy and one for EUS), limited manoeuverability of the echoendoscope and the failure of the endoscope to traverse tight stenoses and reach the caecum. The ultrasound catheter probe (UCP) has been developed to solve these problems. This system is half as expensive as the standard EUS system. The major advantage of the 12 MHz UCP system is that it can be used with a wide variety of endoscopes. It can be inserted through the working channel of a conventional colonoscope and used under direct endoscopic visualization. However, experience in the pre-operative staging of colorectal cancer with the relatively low frequency 12 MHz UCP has not been reported. We therefore performed a prospective study to examine the accuracy of the 12 MHz UCP in the pre-operative staging of colorectal cancer.
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Materials and method
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Patients
159 consecutive patients with a diagnosis of colorectal cancer, confirmed by preliminary endoscopy and endoscopic biopsies, were evaluated between November 1997 and March 2000. The patients consisted of 90 men and 69 women, with a mean age of 68 years (range 40–89 years). The tumour was located in the caecum in 8 patients, in the ascending colon in 16 patients, in the transverse colon in 9 patients, in the descending colon in 10 patients, in the sigmoid colon in 40 patients, and in the rectum in 76 patients. Surgical resection was performed in 141 patients and endoscopic resection in 18 patients. The resected tumours were assessed histopathologically according to the TNM staging system [22]. Findings from the pre-operative 12 MHz UCP were compared with the pathological findings in the resected specimens. The pathologist (KN) was blinded to the results of the EUS examination. There were 54 pT1 tumours, 17 pT2 tumours, 85 pT3 tumours and 3 pT4 tumours. EUS was performed prior to surgery after obtaining informed consent from the patients.
Method
A 12 MHz ultrathin mechanical radial scanning probe (Fujinon Sonoprobe System, SP-701; Fuji Photo Optical Co., Omiya, Japan) was used in this study (Figure 1
). This probe is available for a broad variety of endoscopes and is inserted through an ordinary 2.8 mm working channel. The cost of the probe is about $2700. A single probe can be used for approximately 50 examinations.
A brief description of the procedure follows. The colonoscope was inserted with the patient in the left lateral position. The lesion was first observed on endoscopy, and the colonic lumen was filled with de-aerated water to create an appropriate interface image. The UCP was then introduced through the instrument channel of the endoscope and advanced to just above the tumour, under direct control of the videocolonoscope. All examinations were performed by a single, well trained endosonographer (KA). The procedure took about 10 min and there were no complications.
The normal colonic wall was observed to have five layers [2, 17]. A 12 MHz UCP image of a normal colonic wall is shown in Figure 2. The first layer was hyperechoic and the second hypoechoic, corresponding with the interface echo and the mucosa, respectively. The third layer was hyperechoic, representing the submucosa, the fourth layer was hypoechoic, representing the muscularis propria, and the fifth layer corresponded to the subserosa, serosa (or adventitia) and interface echo.
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Figure 2. Five-layered structure of normal colonic wall imaged using the 12 MHz ultrasound catheter probe. m, mucosa; sm, submucosa; mp, muscularis propria; ss,s, subserosa, serosa, or adventitia.
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The primary tumour was visualized with the probe as a hypoechoic mass. Tumours involving the first three echo layers but not the fourth layer were staged as T1 (Figure 3). Tumours involving the fourth echo layer without breach of the outer margin were staged as T2. Tumours involving the outer margin were staged as T3 (Figure 4). Extension of the tumour into contiguous organs was staged as T4.
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Figure 3. Ultrasound catheter probe scan of a T1 tumour. A hypoechoic mass (large arrow) extends into the submucosa (arrow-sm). Note that the muscularis propria is intact beneath the hypoechoic mass.
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Figure 4. Ultrasound catheter probe scan of a T3 tumour. A hypoechoic mass (arrow) extends through the muscularis propria into the serosal layer.
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A lymph node metastasis was diagnosed when well defined, round or elliptical structures adjacent to the colonic wall were hypoechoic compared with the surrounding tissues (Figure 5). The regional lymph nodes were classified as non-cancerous if such structures were not visualized [3].
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Figure 5. Ultrasound catheter probe scan of a lymph node metastasis (arrow) in a patient with rectal cancer.
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Results
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12 MHz UCP diagnosis of the depth of tumour invasion
The overall accuracy of the 12 MHz UCP for determining the depth of invasion was 85%. The accuracy was 87% (46/53 cases) for pT1 tumours, 60% (9/15 cases) for pT2 tumours, 89% (74/83 cases) for pT3 tumours and 67% (2/3 cases) for pT4 tumours (Table 1). Based on the findings using the 12 MHz UCP, 7% (11 cases) were overstaged, mainly because of peritumoral inflammatory changes, 8% (12 cases) were understaged, mainly because of focal invasion and 3% (5 cases) could not be staged because of ultrasonic attenuation. A further analysis of the accuracy according to T stage of rectal and colonic cancer is given in Table 2. The accuracy of the 12 MHz UCP in assessing the infiltration depth of rectal and colonic tumours was 81% (61/75) and 89% (70/79), respectively.
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Table 1. Correlation between pre-operative assessment of tumour infiltration by endoscopic ultrasound using the ultrasound catheter probe (uT) and by histopathology (pT) in 159 patients with colorectal cancer
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Detection of pericolonic lymph node metastasis
The lymph node status was confirmed histopathologically in 114 patients. 45 patients were treated with endoscopic resection or local resection and therefore no information on lymph node metastasis was available. The presence or absence of lymph node metastasis was determined correctly in 67% (76/114) of cases (Table 3).
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Table 3. Correlation between pre-operative assessment of lymph node involvement by endoscopic ultrasound with the ultrasound catheter probe (uN) and by histopathology (pN) in 114 patients with colorectal cancer
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Discussion
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Once a diagnosis of colorectal cancer has been established by endoscopic biopsy, accurate staging is necessary to indicate the most appropriate management. At present, EUS is the only modality that reliably stages colorectal cancer pre-operatively [2, 4–17, 21]. However, EUS has a number of shortcomings when using a conventional echoendoscope. With a conventional echoendoscope it is impossible to scan whilst observing the lesion directly because the ultrasonic transducer is behind the endoscopic observation port. Furthermore, conventional EUS allows limited manoeuverability of the echoendoscope, because the probe has a large calibre and a rigid tip [16, 17]. Use of a conventional echoendoscope to image small lesions can therefore be technically demanding. The UCP has been developed to solve these problems. The 12 MHz UCP, which can be passed through the accessory channel of a standard colonoscope, provides easier scanning of proximal or stenotic lesions. In this study, 8 lesions were located in the caecum and 16 lesions in the ascending colon. Scanning these lesions with the UCP was simple, and the probe successfully detected all tumours. Furthermore, this system is approximately half the cost of the standard EUS system.
The reported accuracy of conventional EUS for evaluating the depth of colorectal tumour invasion ranges from 60% to 92% (Table 4) [5–15]. Only a few studies have reported UCP results in the T staging of colorectal cancer [2, 16, 17]. The reported accuracy of the UCP for evaluating the depth of colorectal tumour invasion ranges between 82% and 90% [2, 16, 17]. These values are similar to our results. In our data, the overall accuracy of the 12 MHz UCP in assessing the infiltration depth of colorectal tumours was 85%. There was no significant difference in the accuracy of the 12 MHz UCP whether the tumour was located in the rectum or colon. In this study using a 12 MHz UCP, we encountered only 5 cases (3%) in which the depth of invasion could not be assessed due to ultrasonic attenuation. Overstaging was caused mainly by peritumoral inflammatory changes. The overstaging may have occurred because probe images cannot be used to distinguish inflammatory changes from carcinomatous infiltration. Understaging was caused mainly by focal invasion. Careful, complete scanning is necessary to reduce understaging. The axial resolution of the 12 MHz UCP is 0.35 mm. The inability to recognize focal microinvasion is therefore a limitation of this procedure.
The accuracy, sensitivity and specificity of conventional EUS for nodal staging of colorectal cancers have previously been reported to be between 65% and 88%, 17% and 94% and 53% and 97%, respectively (Table 5) [5–9, 11–15]. Only two studies [2, 17] have reported the accuracy, sensitivity and specificity of the UCP, being 85–87%, 50–63% and 95%, respectively. In our data on N staging with the 12 MHz UCP, the accuracy was 67% overall; sensitivity and specificity were 70% and 64%, respectively. Nodal staging with EUS remains suboptimal. EUS clearly visualized enlarged lymph nodes in the 24 false positive patients. A long-standing discussion has been conducted as to whether certain ultrasound features can be used to distinguish malignant from benign lymph nodes. Computer analysis of lymph node echo patterns has shown no difference between benign and malignant nodes that would allow reliable discrimination by ultrasound [20]. Lymph node metastasis cannot therefore be excluded by ultrasound features when lymph nodes are seen on pre-operative UCP imaging. EUS-guided fine needle aspiration has recently added a new dimension and increased the accuracy in determining benign vs malignant lymph nodes [23]. If applicable, EUS-guided fine needle aspiration should be performed to exclude the possibility of local lymph node metastasis.
Certain early tumours without lymph node metastasis may be treated effectively with endoscopic resection. However, ours and previous studies report that the sensitivity of nodal staging with the UCP is comparatively low (50–70%) [2, 17]. This might be explained by lymph nodes that are too small to be visible, by micrometastases within inflamed nodes, or by nodes that are out of reach of the probe [3, 11]. The present UCP is therefore less useful for planning endoscopic resection than for staging of the mural extent [11, 24]. More accurate diagnosis of lymph node status is expected through future improvements in the image quality of the probe.
Laparoscopic surgery is safe, effective and possibly even beneficial for many benign conditions such as colorectal polyps. However, there is, at present, controversy over laparoscopic resection of colorectal cancer, because some cases of port site metastases have been reported [25, 26]. The true incidence and the exact pathogenesis of port site metastases are still unknown. However, there is evidence of an increased risk of port site metastases in carcinomas with penetration through the serosa (T3) [27]. Moreover, it has recently been suggested that the extent of laparoscopic lymph node dissection can be modified according to the tumour stage. Hida et al [28] analysed the distribution of lymph node metastases in 164 patients with colorectal cancer and concluded that central lymph node dissection may not be required in patients with T1 cancer. However, dissection of the intermediate and main lymph nodes should be performed in T2 tumours and more advanced tumours. Ours and previous studies [2, 17] show that the UCP can accurately assess the T stage. Consequently, pre-operative UCP imaging may influence the decision to perform laparoscopic colectomy.
Compared with surgery alone, pre-operative neoadjuvant therapy plus surgery for advanced rectal cancer (uT3 and uT4) results in better survival rates, better local control and comparable or better toxity compared with standard post-operative adjuvant regimens [14, 29, 30]. Accurate staging is therefore crucial in the selection of patients for trials evaluating neoadjuvant treatment. Our results and those of other published studies [2, 17] show that the UCP can precisely differentiate (90–95%) between early colorectal carcinoma (T1/2) and advanced cancer (T3/4). On the basis of these data, the UCP may provide valuable information in deciding the best surgical approach. Use of this probe may therefore become routine in the pre-operative evaluation of candidates for colorectal operations.
This study confirmed the value of the 12 MHz UCP in the accurate staging of the mural extent of colorectal cancer but is in agreement with other studies that nodal assessment is suboptimal with ultrasound alone. However, the 12 MHz UCP has good manoeuverability, the ability to scan under precise visual control, as well as being available for a broad variety of endoscopes, and is relatively inexpensive. The 12 MHz UCP should therefore become an important imaging technique for clinical TN staging of colorectal carcinoma.
Received for publication January 24, 2001.
Revision received May 29, 2001.
Accepted for publication June 19, 2001.
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Abstract
Introduction
