Intraductal optical coherence tomography during endoscopic retrograde cholangiopancreatography for investigation of biliary strictures

• Introduction
• Patients and methods
• Patients
• ERCP and OCT examination
• Interpretation of OCT images
• Statistical analysis
• Results
• Study population (Table 1)
• OCT assessment
• Diagnostic accuracy (Table 2)
• Discussion
• References

Background and study aims: Optical coherence tomography (OCT) uses infrared light reflectance to produce high-resolution cross-sectional tissue images. The aim of this study was to demonstrate the feasibility of biliary intraductal OCT during endoscopic retrograde cholangiopancreatography (ERCP) and to assess the potential of the method to detect malignant biliary strictures.

Patients and methods: Thirty-seven patients with biliary strictures were studied during therapeutic ERCP. Malignant strictures were defined as those that demonstrated malignant cells in brushing and/or biopsy specimens, and/or endoscopic ultrasound-guided fine-needle aspiration and/or surgery. Strictures that did not have malignant cells in resected specimens and were without clinical/radiological evidence of disease progression for at least a 12-month follow-up period were considered as benign. Two OCT criteria for malignancy were considered: unrecognizable layer architecture; and presence of large, nonreflective areas compatible with tumor vessels. Sensitivity and specificity for brushings/biopsies as well as OCT criteria were calculated.

Results: Nineteen patients had malignant and 16 had benign strictures. In two patients, OCT assessment could not be performed due to tight strictures. Malignancy was confirmed by biliary brushings/biopsies in 12/19 (63 %) patients. OCT revealed that two malignancy criteria were encountered in 10/19 (53 %) and at least one criterion in 15/19 (79 %) patients with malignant strictures. No patient with benign stricture met both criteria and 5/16 met one criterion (31 %). Combining brushings/biopsy with the observation of at least one OCT criterion resulted in the diagnosis of malignancy in 16/19 (84 %) patients.

Conclusions: OCT may improve the sensitivity and diagnostic accuracy of biliary brushings/biopsies alone.

Introduction

Optical coherence tomography (OCT) is a technique that has been developed during the past decade for performing high-resolution, cross-sectional tomographic imaging in human tissue by measuring the intensity of reflected infrared light [1] [2] [3] [4] [5].

OCT imaging from the gastrointestinal tract is performed in humans using a catheter device that can be inserted through the accessory channel of a standard endoscope. Up to now, the most investigated organs have been the esophagus, stomach, colon, and pancreatic duct [6] [7] [8] [9] [10] [11] [12] [13]. To our knowledge, there are only two in vivo pilot studies with a limited number of patients evaluating the feasibility of intraductal biliary OCT during endoscopic retrograde cholangiopancreatography (ERCP) [14] [15]. ERCP with tissue sampling is the diagnostic test of choice in patients with suspected malignant biliary stricture. However, the sensitivity of brush cytology alone for the diagnosis of malignant biliary strictures is only about 50 % in most series, due mainly to its limited cellular yield [16] [17] [18]. Even by combining two sampling techniques, such as biopsy forceps, sensitivity may increase only up to about 65 % [17].

The aim of the present study was to demonstrate the feasibility of biliary intraductal OCT during ERCP and assess the potential of this technique for improving accuracy of diagnosis for malignant biliary strictures.

Patients and methods

Patients

Thirty-seven nonconsecutive patients with biliary strictures undergoing therapeutic ERCP for biliary drainage were assessed prospectively by OCT between January 2005 and October 2007. In all patients, proximal or distal biliary strictures with upstream dilation were identified by imaging studies (computed tomography [CT] and/or magnetic resonance cholangiopancreatography [MRCP]) prior to ERCP. Exclusion criteria were: prior biliary stenting (≥6 months) with plastic or metal stents; anastomotic strictures following liver transplantation; difficult common bile duct cannulation requiring a percutaneous access; and anticipated unavailability for long-term follow-up (≥12 months). Patients were followed up prospectively with clinical evaluation and complementary imaging studies. Malignant strictures were defined as those that either demonstrated malignant cells in tissue samples or showed a clinical course during a 12-month follow-up suggesting malignancy based on a new radiologic abnormality, including a regional or distant mass. Strictures were considered as benign if tissue samples did not contain malignant cells and if the above criteria were not encountered during the 12-month follow-up period. The protocol was approved by the institutional review board of our hospital, and informed consent was obtained from each patient.

ERCP and OCT examination

ERCP was performed with a therapeutic video duodenoscope (TJF-160, Olympus, Tokyo, Japan), under general anesthesia with endotracheal intubation. All procedures were initially performed with the patient placed in the supine position, with repositioning if necessary for complete visualization of the biliary tree. Biliary sphincterotomy was conducted. Cholangiography was performed with a standard catheter and iodinated contrast medium. Fluoroscopic images of the stricture were obtained.

The principles and the technical details of OCT have been published elsewhere [4]. A mid-focus OCT probe (PENTAX Corporation Tokyo, Japan/Lightlab Imaging Ltd. Boston, USA) was used, with an outer diameter of 0.75 mm, a penetration depth of approximately 1 mm, and a resolution of about 10µm. The probe consisted of a cord of glass fibers covered by a protective transparent plastic sheath which remained stationary while the rotating cord had a pullback movement of 1 mm/sec. It was inserted in the accessory channel of the duodenoscope through a standard transparent ERCP catheter, and scanning was performed throughout the stricture with the OCT probe kept in the catheter. A radio-opaque marker allowed correct positioning of the probe. The infrared light probe generates high-resolution cross-sectional tissue images and films, represented as radial and longitudinal scanning, with an acquisition rate of 10 frames/second.

Interpretation of OCT images

For every patient, one radial scanning throughout the stricture as well as two longitudinal scannings (one backward and one forward movement) were conducted and saved in a film format.

Previous studies have already shown the potential of OCT to identify the layered structure of the normal bile duct, which was made possible by visualization of the different back-scattering characteristics within each layer [13] [14] [15].

Based on OCT images, two criteria suggesting malignancy were considered. First, we evaluated the presence of a disorganized and subverted layer structure, based on prior data concerning malignant pancreatic strictures [12]. Second, we identified large hypo- or nonreflective areas, found on at least five consecutive cross-sectional images, which could be considered as tumor vessels. This observation was based on a previous series regarding assessment of biliary strictures by cholangioscopy, which revealed that the presence of large, tortuous vessels indicated malignancy with a sensitivity of 61 % and a specificity of 100 % [19].

Image analysis was performed during ERCP in knowledge of clinical data by two endoscopists familiar with OCT images (MA, OL). There was no pathologist present in the endoscopy theater during the procedure. All images were reviewed after the results of brushings were disclosed.

Statistical analysis

Descriptive statistics were expressed as the median and interquartile range (IQR) for continuous variables. Considering the predefined criteria as gold standard (presence of malignant cells in brushings or biopsies or endoscopic ultrasound [EUS]-guided fine-needle aspiration [FNA] or surgery), sensitivity, specificity, and positive and negative predictive values for different modalities to diagnose malignancy were calculated. The corresponding 95 % confidence intervals (CI) were calculated for these values using the Blyth–Still–Casella method [20] [21]. The following diagnostic modalities were assessed: (A) intraductal brushings and/or biopsies; (B) at least one OCT criterion; (C) both OCT criteria; (D) brushings/biopsies combined with one criterion; and (E) brushings/biopsies combined with both OCT criteria. Statistical significance was considered for P-values ≤0.05. Statistical analyses were performed using SPSS software, version 15.0 (SPSS Inc., Chicago, Ilinois, USA), and the StatXact software, version 5.0 (Cytel Software Corp., Cambridge, Massachusetts, USA).

Results

Study population ([Table 1])

Out of 37 patients, two had very tight strictures impeding deep cannulation of the common bile duct (CBD) at the time of the intended examination; therefore OCT evaluation could not be carried out, and these patients were excluded. Satisfactory OCT images were obtained in 35 patients.

Pathology specimens were available in 31 patients (89 %). Twenty-nine patients (83 %) had undergone biliary brushings and/or biopsies during ERCP. EUS-FNA was performed in seven patients, and histology specimens were also obtained during surgery (n = 4) or autopsy (n = 1). Based on all sampling techniques, malignant cells were identified in 16/35 patients (46 %). If only brushing and/or biopsies obtained during ERCP were considered, malignant cells were identified in 12/35 (34 %).

According to predefined criteria described in the previous section (gold standard), strictures were diagnosed as malignant in 19/35 patients (54 %). Pathological confirmation of malignancy was based on biliary brushings and/or biopsies in 12 patients, EUS-FNA in two patients, FNA on a liver metastasis in one patient and surgical specimen in one patient. In three patients in whom there was no pathological confirmation of malignancy, clinical outcome and subsequent imaging studies confirmed advanced neoplasia and liver metastasis. Sixteen patients had benign strictures (46 %). In three patients benign findings were confirmed by surgical specimens and by negative biliary brushings/biopsies combined with clinical and radiological follow-up. The median follow-up duration was 17.5 months (IQR 12 – 29).

OCT assessment

The wall structure of the bile duct was identifiable in all patients. As already described, we identified three layers [13]. The inner, hyporeflective layer represented the biliary epithelium and showed a median thickness of 0.02 mm (IQR 0.02 – 0.04). The intermediate layer appeared hyper-reflective, corresponded to the connective-fibro-muscular tissue surrounding the epithelium, and measured a median thickness of 0.29 mm (IQR 0.25 – 0.33). Finally, the outer layer was hyporeflective with hyper-reflective strips, was visible up to a median depth of 0.7 mm (IQR 0.65 – 0.88), and represented less dense connective tissue with smooth muscle fibers ([Fig. 1] ).

In 14 patients, the stricture wall showed a disorganized layer architecture, which was one of the criteria suggested for malignancy. Large, nonreflective areas, of a surface of at least 0.03 mm², suggestive of tumor vessels, were observed in 15 patients ([Fig. 2]). Additional OCT findings are illustrated in [Fig. 3] and [Fig. 4].

Diagnostic accuracy ([Table 2])

Ductal brushings or biopsies correctly identified malignancy with a sensitivity of 67 % and specificity of 100 %. The presence of at least one or both OCT criteria showed a sensitivity of 79 % and 53 %, respectively. By combining ductal cytology/histology with at least one criterion increased sensitivity to 84 %. By intention-to-diagnose analysis, including the two patients in whom OCT could not be performed (n = 37), accuracy was 70 % for at least one OCT criterion, 70 % for both OCT criteria, and respectively 70 % and 73 % for brushings/biopsies combined with one or both OCT criteria.

When only data from the 18 patients without a detectable mass by imaging techniques (CT scan, MRCP, EUS) were analyzed, sensitivity and specificity reached 100 % when the presence of both OCT criteria was considered.

Discussion

Accurate characterization of a biliary stricture is essential because the choice of the appropriate management depends on whether the stricture is benign or malignant. Indeed, many patients with benign strictures can be treated successfully by the transient placement of biliary stents and do not require surgery [20]. However, results based on tissue sampling of the bile duct during ERCP remain suboptimal.

The present study is the largest dealing with the use of OCT in the biliary tract which shows that it increased the sensitivity of ERCP combined with intraductal cytology to detect malignancy from 67 % to 84 %.

The spatial resolution of OCT images (0.01 mm) is nearly equivalent to histological images and up to 10-fold better than that of available high-frequency intraductal ultrasound (IDUS) imaging [21]. IDUS is a similar technique performed during ERCP to identify malignant biliary strictures [22] [23] [24] [25] [26] [27] [28]. Three prospective [22] [25] [26] and two retrospective [23] [24] studies have shown that IDUS can increase the accuracy of differential diagnosis of ERCP to 92 %. A recent, well-designed, prospective study confirmed that IDUS could enhance the accuracy of standard techniques in evaluation of indeterminate biliary strictures [28]. However, the same study also showed a lack of utility when using formal IDUS criteria, and underlined the importance of subjective evaluation and overall experience of the endosonographer, thus suggesting that IDUS findings may have limited reproducibility [28]. Therefore, OCT could be considered a useful alternative to IDUS for complementary intraductal imaging in case of indeterminate biliary stricture. Peroral cholangioscopy is another diagnostic tool that provides direct visualization of the biliary mucosa and allows directed biopsies. Visualization can be enhanced with narrow band imaging; nevertheless, the system is still fragile and difficult to maneuver [29].

A drawback of the limited depth of field in OCT is its relative inability to detect malignancy due to extraductal causes, such as metastases and pancreatic cancer. In our series, no malignancy criteria were identified in two of eight patients with pancreatic cancer. In the same group of patients, intraductal brushings or biopsies were also less contributive, with a sensitivity of 50 %. However, a mass was diagnosed in all these patients, based on EUS, CT or MRCP. EUS-FNA probably plays a crucial role in determining the final diagnosis in patients with a biliary stricture associated with a mass, therefore undermining the utility of OCT. Nevertheless, as suggested by previous publications regarding IDUS, the difficulty resides in patients with no recognizable mass [30] [31]. In this group of patients (n = 18), OCT had an accuracy of 100 %, therefore indicating a well-defined subgroup where clinical impact of OCT would be more important. However, a potential bias is the fact that the majority of benign strictures were due to chronic pancreatitis, thus limiting the generalization of our results.

Additionally, gold standard criteria for malignancy included positive intraductal brushings/biopsies, which was also one of the diagnostic modalities assessed. This might seem contradictory; however, as the specificity of this technique reaches 100 %, only the negative results are interesting to study.

Further development includes a new linear-array OCT with a higher resolution rate (up to 0.027mm) but the same frame acquisition and penetration depth, which, up to now, has been tested only in animals and surgical specimens [4]. Linear-array OCT appeared superior compared with radial-array OCT in recognizing biliary wall microstructure, particularly at the level of the intermediate fibro-connective-submucosal layer. In the future, this modality could be useful in characterizing ductal changes in patients with inflammatory biliary strictures, such as sclerosing cholangitis. However, the diagnostic accuracy of this device should also be compared with advanced cytologic techniques such as digital image analysis (DIA) and fluorescence in situ hybridation (FISH) [28].

In conclusion, OCT of the biliary system is a promising tool providing high-resolution images during ERCP. In association with intraductal cytology, it is of clinical value in distinguishing between benign and malignant biliary strictures, especially in patients with no identifiable mass. Further development with linear-array OCT probes may improve the diagnostic capacity of this technique.

Competing interests: Mrs Annette Stellke is employed by Pentax Europe. Pentax provided the OCT material and technical support during the study. No financial aid was provided.

References

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M. ArvanitakisMD, PhD 

Department of Gastroenterology
Erasme University Hospital
Université Libre de Bruxelles

Route de Lennik 808
1070 Brussels
Belgium

Fax: +32-2-5554697

Email: marianna.arvanitaki@erasme.ulb.ac.be

References

• 1 Tearney G J, Brezinski M E, Bouma B E. et al . In vivo endoscopic optical biopsy using optical coherence tomography.  Science. 1997;  276 2037-2039
  CrossrefPubMedSearch in Google Scholar
• 2 Tearney G J, Brezinski M E, Southern J F. et al . Optical biopsy in human pancreatobiliary tissue using optical coherence tomography.  Dig Dis Sci. 1998;  43 1193-1199
  CrossrefPubMedSearch in Google Scholar
• 3 Huang D, Swanson E A, Lin C P. et al . Optical coherence tomography.  Science. 1991;  254 1178-1181
  CrossrefPubMedSearch in Google Scholar
• 4 Testoni P A, Mangiavillano B, Mariani A. Optical coherence tomography for investigation of the pancreato-biliary system: still experimental?.  JOP. 2007;  8 156-165
  PubMedSearch in Google Scholar
• 5 Das A, Sivak M V, Chak A. et al . High-resolution endoscopic imaging of the GI tract: a comparative study of optical coherence tomography versus high-frequency catheter probe EUS.  Gastrointest Endosc. 2001;  54 219-224
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• 6 Bouma B E, Tearney G J, Compton C C, Nishioka N S. High-resolution imaging of the human esophagus and stomach in vivo using optical coherence tomography.  Gastrointest Endosc. 2000;  4 467-474
  PubMedSearch in Google Scholar
• 7 Evans J A, Poneros J M, Bouma B E. et al . Optical coherence tomography to identify intramucosal carcinoma and high-grade dysplasia in Barrett’s esophagus.  Clin Gastroenterol Hepatol. 2006;  4 38-43
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  CrossrefPubMedSearch in Google Scholar
• 9 Familiari L, Strangio G, Consolo P. et al . Optical coherence tomography evaluation of ulcerative colitis: the patterns and the comparison with histology.  Am J Gastroenterol. 2006;  101 2833-2840
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  CrossrefPubMedSearch in Google Scholar
• 11 Testoni P A, Mariani A, Mangiavillano B. et al . Preliminary data on the use of intraductal optical coherence tomography during ERCP for investigating main pancreatic duct stricture.  Gut. 2006;  55 1680-1681
  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
• 13 Testoni P A, Mariani A, Mangiavillano B. et al . Main pancreatic duct, common bile duct and sphincter of Oddi structure visualized by optical coherence tomography: an ex vivo study compared with histology.  Dig Liver Dis. 2006;  38 409-414
  CrossrefPubMedSearch in Google Scholar
• 14 Seitz U, Freund J, Jaeckle S. et al . First in vivo optical coherence tomography in the human bile duct.  Endoscopy. 2001;  33 1018-1021
  Thieme ConnectPubMedSearch in Google Scholar
• 15 Poneros J M, Tearney G J, Shiskov M. et al . Optical coherence tomography of the biliary tree during ERCP.  Gastrointest Endosc. 2002;  55 84-88
  CrossrefPubMedSearch in Google Scholar
• 16 de Bellis M, Sherman S, Fogel E L. et al . Tissue sampling at ERCP in suspected malignant strictures (part 1).  Gastrointest Endosc. 2002;  56 552-561
  CrossrefPubMedSearch in Google Scholar
• 17 de Bellis M, Sherman S, Fogel E L. et al . Tissue sampling at ERCP in suspected malignant strictures (part 2).  Gastrointest Endosc. 2002;  56 720-730
  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
• 23 Tantau M, Pop T, Badea R. et al . Intraductal ultrasonography for the assessment of preoperative biliary and pancreatic strictures.  J Gastrointestin Liver Dis. 2008;  17 217-222
  PubMedSearch in Google Scholar
• 24 Tamada K, Tomiyama T, Wada S. et al . Endoscopic transpapillary bile duct biopsy with the combination of intraductal ultrasonography in the diagnosis of biliary strictures.  Gut. 2002;  50 326-331
  CrossrefPubMedSearch in Google Scholar
• 25 Domagk D, Poremba C, Dietl K H. et al . Endoscopic transpapillary biopsies and intraductal ultrasonography in the diagnosis of bile duct strictures: a prospective study.  Gut. 2002;  51 326-331
  PubMedSearch in Google Scholar
• 26 Vazquez-Sequeiros E, Baron T H, Clain J E. et al . Evaluation of indeterminate bile duct strictures by intraductal US.  Gastrointest Endosc. 2002;  56 372-379
  CrossrefPubMedSearch in Google Scholar
• 27 Farrell R J, Agarwal B, Brandwein S L. et al . Intraductal US is a useful adjunct to ERCP for distinguishing malignant from benign biliary strictures.  Gastrointest Endosc. 2002;  56 681-687
  CrossrefPubMedSearch in Google Scholar
• 28 Levy M J, Baron T H, Clayton A C. et al . Prospective evaluation of advanced molecular markers and imaging techniques in patients with indeterminate bile duct strictures.  Am J Gastroenterol. 2008;  103 1263-1273
  CrossrefPubMedSearch in Google Scholar
• 29 Itoi T, Sofuni A, Itokawa F. et al . Peroral cholangioscopic diagnosis of biliary-tract diseases by using narrow-band imaging.  Gastrointest Endosc. 2007;  66 730-736
  CrossrefPubMedSearch in Google Scholar
• 30 Stavropoulos S, Larghi A, Verna E. et al . Intraductal ultrasound for the evaluation of patients with biliary strictures with no abdominal mass on computed tomography.  Endoscopy. 2005;  37 715-721
  Thieme ConnectPubMedSearch in Google Scholar
• 31 Krishna N B, Saripalli S, Safdar R. et al . Intraductal US in evaluation of biliary strictures without a mass lesion on CT scan or magnetic resonance imaging: significance of focal wall thickening and extrinsic compression at the stricture site.  Gastrointest Endosc. 2007;  66 90-96
  CrossrefPubMedSearch in Google Scholar

M. ArvanitakisMD, PhD 

Department of Gastroenterology
Erasme University Hospital
Université Libre de Bruxelles

Route de Lennik 808
1070 Brussels
Belgium

Fax: +32-2-5554697

Email: marianna.arvanitaki@erasme.ulb.ac.be