Three-Dimensional Endorectal Ultrasound Using a New Freehand Software Program: Results in 35 Patients with Rectal Cancer

• Introduction
• Materials and Methods
• Basic Principles of 3D Ultrasound
• Single-Tracked Freehand Systems
• 3D Reconstruction
• Visualization of 3D Ultrasound Images
• Results
• Discussion
• Conclusion
• References

Background and Study Aims: This paper describes experience in the staging of rectal cancer using a new software program for three-dimensional endoscopic ultrasonography (EUS) that works without electromagnetic sensors and can be used even with electronic radial or linear rectal probes.
Materials and Methods: From May 2003 to March 2004, 35 three-dimensional endorectal ultrasound (ERUS) examinations were carried out using this program. The indication for ERUS was local staging of rectal cancer in all cases. The three-dimensional software imaging program forms part of a new ultrasound scanning system (Hitachi 6500 or 8000) and allows reconstruction of the two-dimensional EUS images in six different scans.
Results: Thirty-five rectal cancers were assessed using two-dimensional and three-dimensional EUS. Using two-dimensional imaging, it was not possible to assess precisely the degree of involvement of the mesorectum (more or less than 50 %). No differences were evident with three-dimensional EUS for superficial tumors (T1 and T2N0), but in six of 15 patients classified as having T3N0 lesions, three-dimensional EUS revealed malignant lymph nodes, a finding that was confirmed surgically in five of the six cases. Three-dimensional EUS also made it possible to assess the degree of infiltration of the mesorectum precisely in all cases, demonstrating complete invasion of the mesorectum in eight cases. These findings were confirmed in all cases by the surgical data. Two-dimensional EUS correctly assessed 25 of the 35 rectal tumors (71.4 %) in relation to the T and N classifications, and three-dimensional EUS increased this figure to 31 correct evaluations out of 35 (88.6 %).
Conclusion: Three-dimensional ERUS is easy to carry out using this new software program. There is no need for an external sensor mounted at the tip of the probe, and manipulation of the rectal probe is facilitated. Three-dimensional ERUS can be carried out using linear and radial electronic probes with the same ultrasound equipment. Three-dimensional ERUS allows more precise staging of lesions and better definition of the mesorectal margins, and this has a direct impact on therapeutic decision-making in patients with rectal cancer.

Introduction

Several studies in the field of endoscopic ultrasound (EUS) technology have reported advantages with three-dimensional (3D) EUS [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12] [13]. However, most 3D EUS studies have been carried out using a catheter-type miniature probe system [3] [6] [9]. Some studies have previously reported benefits with a prototype 3D EUS system using a linear-array ultrasound endoscope for 3D guidance during interventional procedures; however, the scanning method used in the system had limitations, and since the ultrasound probe was not positioned at the tip of the endoscope, it was difficult to obtain clinically adequate images in the stomach without geometrical distortion [14] [15] [16]. A recent study attempted to solve this problem and maximize the performance of 3D EUS using a linear ultrasound endoscope with a miniature electromagnetic position sensor attached to the tip of the scope, which can be used for freehand scanning in any position [17]. However, the problem with this technique was that the electromagnetic sensor increased the size of the probe. The present report describes experience with a new software program for 3D EUS imaging without an electromagnetic sensor, which can be used with both electronic radial and linear rectal probes.

Materials and Methods

From May 2003 to March 2004, 35 3D endorectal ultrasound (ERUS) examinations were carried out using this new software program. The indication for EUS was local staging of rectal cancer in all 35 cases. Standard ERUS was performed before 3D ERUS scanning. The 3D rectal examinations were conducted using a rigid radial electronic probe (Hitachi R54). The 3D software forms part of a new ultrasound scanning system (Hitachi 6500 or 8000) and makes it possible to reconstruct the two-dimensional (2D) EUS pictures in six different scans. The acquisition time is very quick, at around 10 - 25 s. The acquisition time depends on the number of images recorded.

Basic Principles of 3D Ultrasound

Two types of system have been developed, using either a series of two-dimensional images produced by one-dimensional arrays, or using two-dimensional arrays to produce 3D images directly. Two criteria have to be met to avoid inaccuracies: the relative position and angulation of the acquired 2D images have to be known accurately; and the images have to be acquired rapidly and/or gated to avoid artefacts due to respiratory, cardiac, and involuntary motion.

Single-Tracked Freehand Systems

The operator holds an assembly consisting of the transducer and an attachment, and manipulates it over the anatomy. Two-dimensional images are digitized as the transducer is moved, while meeting two criteria: the exact relative angulation and position of the ultrasound transducer have to be known for each digitized image; and the operator has to ensure that no significant gaps are left when the anatomy is being scanned.

3D Reconstruction

The 3D reconstruction process involves the generation of a 3D image from a digitized set of 2D images. The approach used involves the voxel-based volume. The 2D images are built into a 3D voxel-based volume (a 3D grid) by placing each digitized 2D image in its correct location in the volume. The main advantages of this are that that no information is lost during the 3D reconstruction, and that a variety of rendering techniques are possible; however, large data files are generated.

Visualization of 3D Ultrasound Images

The ability to visualize information in the 3D image depends critically on the rendering technique. Three basic types are used.

Surface-based viewing technique. An operator or algorithm identifies the boundaries of structures in order to create a wire-frame representation. These structures are shaded and illuminated so that surfaces or structures or organs can be visualized.

Multiplanar viewing techniques (Figure [1]). Orthogonal views: three perpendicular planes are displayed simultaneously and can be moved or rotated. Polyhedral: the 3D images are presented as a multisided volume (polyhedron). The appropriate ultrasound image is “painted” onto each face of the polyhedron, which can be visually manipulated.

Volume-based rendering techniques. The 3D image is projected onto a 2D plane by casting rays through the 3D image. The voxel values intersected by each ray can be multiplied by various factors and added to produce different effects: multiplied by one and then added, to form a radiograph-like image; multiplied by factors to produce translucency; or displaying only the voxel with the maximum intensity along each ray.

Results

No complications occurred during the study. Thirty-five rectal cancers were assessed using 2D and 3D EUS. All of the tumors were located in the middle and lower parts of the rectum; stenotic tumors had been excluded from the study. Three-dimensional EUS was possible in all cases. Two-dimensional EUS data classified the tumors as T1N0 (n = 2), T2N0 (n = 3), T3N0 (n = 15), T3N1 (n = 12), and T4N1 (n = 3). It was not possible with 2D images to assess the degree of involvement of the mesorectum precisely (more or less than 50 %). No difference was found with 3D ERUS for superficial tumors (T1 and T2N0), but in six of 15 patients classified as having T3N0 lesions, 3D ERUS showed malignant lymph nodes, and this finding was confirmed surgically in five of the six cases (Table [1]). Three-dimensional EUS made it possible to assess the degree of infiltration of the mesorectum precisely (Figure [2]) in all cases and revealed complete invasion of it in eight cases. These findings were confirmed in all cases by the surgical data. In summary, for rectal cancer, 2D EUS assessed 25 of the 35 rectal tumors correctly (71.4 %) in relation to the T and N classifications, and 3D EUS improved this result to 31 correct evaluations out of 35 (88.6 %).

When the accuracy of 2D and 3D imaging for T staging (T1 - T2 vs. T3 - T4) was compared, no differences were seen between the two techniques (34 of 35 staging procedures accurate with both techniques). However, patients classified on 3D as having T3N0 lesions developed fewer hepatic metastases than those classified on 2D imaging as having T3N0 lesions (one of nine vs. six of 15; 11 % vs. 40 %; P = 0.002). This difference was due to the fact that seven of the 15 rectal lesions staged as T3N0 with 2D imaging proved to be pT3N1 in the resected specimens. By contrast, eight patients in whom 3D ERUS revealed extensive mesorectal infiltration (more than two-thirds of the thickness of the mesorectum) also developed metastases (hepatic or peritoneal carcinomatosis; four of eight vs. seven of 27; 50 % vs. 26 %; P < 0.001).

Discussion

Three-dimensional ERUS is a new technique that is still undergoing development. Sumiyama et al. [17] recently reported experience using 3D EUS with electronic linear probes, and concluded that 3D EUS with a linear-array ultrasound endoscope was accurate and represented a consistent method. They stated that 3D EUS facilitated the anatomical interpretation of ultrasound images and reduced procedural difficulties with scanning. Previous experience using 3D EUS using mechanical miniprobes has been reported for cardiovascular procedures [18], and using rigid electronic probes for the assessment of gynecological tumors [19] [20]. More recently, 3D EUS findings using mechanical miniprobes have also been reported for pancreaticobiliary diseases [3] [6] [9] and anal diseases [7].

The experience described in the present study is rather different, as 3D ERUS was carried out using a new software program allowing the use of linear or radial electronic probes. The software is incorporated into the ultrasound system’s computer, and an external sensor attached to the tip of the EUS scope is not required. The most important question is whether this 3D EUS system is useful [21] [22].

With regard to the locoregional staging of rectal cancer, several reports on 3D EUS imaging have been of considerable interest, describing better parietal staging [4] [5], with accurate staging even in patients with stenotic lesions, and more accurate EUS-guided biopsies [23]. The present results show that the mesorectal margins are better defined using 3D EUS than with 2D EUS, allowing more accurate parietal staging. This precise definition of mesorectal involvement has a direct impact on therapeutic decision-making, as cancer extending to the margins of the mesorectum is classified as a T4 lesion even when a pelvic organ is not involved [24]. These lesions have to be treated with preoperative chemoradiotherapy.

Conclusion

Three-dimensional ERUS using this new software program is easy to perform. There is no need for an external sensor to be mounted at the tip of the probe, and manipulation of the rectal probe is facilitated. Three-dimensional ERUS allows more precise staging of lesions and better definition of the mesorectal margins, and this has a direct impact on therapeutic decision-making in patients with rectal cancer.

Competing interests: None

References

• 1 Kallimanis G, Garra B S, Tio T L. The feasibility of three-dimensional endoscopic ultrasonography: a preliminary report.  Gastrointest Endosc. 1995;  41 235-239
  PubMedSearch in Google Scholar
• 2 Odegaard S, Nesje L B, Molin S O. Three-dimensional intraluminal sonography in the evaluation of gastrointestinal diseases.  Abdom Imaging. 1999;  24 449-451
  CrossrefPubMedSearch in Google Scholar
• 3 Kanemaki N, Nakazawa S, Inui K. Three-dimensional intraductal ultrasonography: preliminary results of a technique for diagnosis of diseases of pancreatobiliary system.  Endoscopy. 1997;  29 726-731
  PubMedSearch in Google Scholar
• 4 Hünerbein M, Schlag P M. Three-dimensional endosonography for staging of rectal cancer.  Ann Surg. 1997;  225 432-438
  CrossrefPubMedSearch in Google Scholar
• 5 Ivanov K D, Diavoc C D. Three-dimensional endoluminal ultrasound: new staging technique in patients with rectal cancer.  Dis Colon Rectum. 1997;  40 47-50
  CrossrefPubMedSearch in Google Scholar
• 6 Tokiyama H, Yanai H, Nakamura H. et al . Three-dimensional endoscopic ultrasonography of lesions of the upper gastrointestinal tract using a radial-linear switchable thin ultrasound probe.  J Gastroenterol Hepatol. 1999;  14 1212-1218
  CrossrefPubMedSearch in Google Scholar
• 7 Gold D M, Bartram C I, Halligan S. et al . Three-dimensional endoanal sonography in assessment anal canal injury.  Br J Surg. 1999;  86 365-370
  CrossrefPubMedSearch in Google Scholar
• 8 Calleja J L, Albillos A. Three-dimensional endosonography for staging of rectal cancer.  Gastrointest Endosc. 1998;  47 317-318
  PubMedSearch in Google Scholar
• 9 Marusch F, Koch A, Schmidt U. Routine use of transrectal ultrasound in rectal carcinoma: results of a prospective multicenter study.  Endoscopy. 2002;  34 385-390
  Thieme ConnectPubMedSearch in Google Scholar
• 10 Chung C Y, McCray W H, Dhaliwal S. et al . Three-dimensional esophageal varix model quantification of variceal volume by high-resolution endoluminal US.  Gastrointest Endosc. 2000;  52 87-90
  CrossrefPubMedSearch in Google Scholar
• 11 Hünerbein M, Ghadimi B M, Gretschel S, Schlag P M. Three-dimensional endoluminal ultrasound: a new method for the evaluation of gastrointestinal tumors.  Abdom Imaging. 1999;  24 445-448
  CrossrefPubMedSearch in Google Scholar
• 12 Hünerbein M, Gretschel S, Ghadimi B M, Schlag P M. Three-dimensional endoscopic ultrasound of the esophagus: preliminary experience.  Surg Endosc. 1997;  11 991-994
  CrossrefPubMedSearch in Google Scholar
• 13 Liu Y T, Miller L S, Chung J Y. et al . Validation of volume measurements in esophageal pseudotumors using 3D endoluminal ultrasound.  Ultrasound Med Biol. 2000;  26 735-741
  CrossrefPubMedSearch in Google Scholar
• 14 Tamura S, Hirano M, Chen X. et al . Intrabody three-dimensional position sensor for an ultrasound endoscope.  IEEE Trans Biomed Eng. 2002;  49 1187-1194
  CrossrefPubMedSearch in Google Scholar
• 15 Sumiyama K, Suzuki N, Katutani H. et al . A novel 3-dimensional EUS technique for real-time visualization of the volume data reconstruction process.  Gastrointest Endosc. 2002;  55 723-728
  CrossrefPubMedSearch in Google Scholar
• 16 Molin S O, Nesje L B, Gilja O H. et al . 3D endosonography in gastroenterology: methodology and clinical implications.  Eur J Ultrasound. 1999;  10 171-177
  CrossrefPubMedSearch in Google Scholar
• 17 Sumiyama K, Suzuki N, Tajiri H. A linear-array freehand 3-D endoscopic ultrasound.  Ultrasound Med Biol. 2003;  29 1001-1006
  CrossrefPubMedSearch in Google Scholar
• 18 Klingensmith J D, Schoenhagen P, Tajaddini A. et al . Automated three-dimensional assessment of coronary artery anatomy with intravascular ultrasound scanning.  Am Heart J. 2003;  145 795-805
  CrossrefPubMedSearch in Google Scholar
• 19 Ayoubi J M, Franchin R, Ferretti G. et al . Three-dimensional ultrasonographic reconstruction of the uterine cavity: virtual hysteroscopy?.  Eur Radiol. 2002;  12 2030-2033
  PubMedSearch in Google Scholar
• 20 Liu J B, Miller J S, Bagley D H, Goldberg B B. Endoluminal sonography of the genitourinary and gastrointestinal tracts.  J Ultrasound Med. 2002;  21 323-337
  PubMedSearch in Google Scholar
• 21 Yoshimoto K. Clinical application of ultrasound 3D imaging system in lesions of the gastrointestinal tract.  Endoscopy. 1998;  30 145-148
  PubMedSearch in Google Scholar
• 22 Yoshino J, Nakazawa S, Inui K. et al . Surface-rendering imaging of gastrointestinal lesions by three-dimensional endoscopic ultrasonography.  Endoscopy. 1999;  31 541-545
  Thieme ConnectPubMedSearch in Google Scholar
• 23 Hünerbein M, Dohmoto M, Haensch W, Schlag P M. Evaluation and biopsy of recurrent rectal cancer using three-dimensional endosonography.  Dis Colon Rectum. 1996;  39 1373-1378
  CrossrefPubMedSearch in Google Scholar
• 24 Heald R J, Ryall R D. Recurrence and survival after total mesorectal excision for rectal cancer.  Lancet. 1986;  i 1479-1482
  CrossrefPubMedSearch in Google Scholar

M. Giovannini, M. D.

Institut Paoli-Calmettes

232, Boulevard de Ste.-Marguérite · 13273 Marseille Cédex 9 · France

Fax: +33-4-91 22 36 58

Email: hdjchir@marseille.fnclcc.fr

References

• 1 Kallimanis G, Garra B S, Tio T L. The feasibility of three-dimensional endoscopic ultrasonography: a preliminary report.  Gastrointest Endosc. 1995;  41 235-239
  PubMedSearch in Google Scholar
• 2 Odegaard S, Nesje L B, Molin S O. Three-dimensional intraluminal sonography in the evaluation of gastrointestinal diseases.  Abdom Imaging. 1999;  24 449-451
  CrossrefPubMedSearch in Google Scholar
• 3 Kanemaki N, Nakazawa S, Inui K. Three-dimensional intraductal ultrasonography: preliminary results of a technique for diagnosis of diseases of pancreatobiliary system.  Endoscopy. 1997;  29 726-731
  PubMedSearch in Google Scholar
• 4 Hünerbein M, Schlag P M. Three-dimensional endosonography for staging of rectal cancer.  Ann Surg. 1997;  225 432-438
  CrossrefPubMedSearch in Google Scholar
• 5 Ivanov K D, Diavoc C D. Three-dimensional endoluminal ultrasound: new staging technique in patients with rectal cancer.  Dis Colon Rectum. 1997;  40 47-50
  CrossrefPubMedSearch in Google Scholar
• 6 Tokiyama H, Yanai H, Nakamura H. et al . Three-dimensional endoscopic ultrasonography of lesions of the upper gastrointestinal tract using a radial-linear switchable thin ultrasound probe.  J Gastroenterol Hepatol. 1999;  14 1212-1218
  CrossrefPubMedSearch in Google Scholar
• 7 Gold D M, Bartram C I, Halligan S. et al . Three-dimensional endoanal sonography in assessment anal canal injury.  Br J Surg. 1999;  86 365-370
  CrossrefPubMedSearch in Google Scholar
• 8 Calleja J L, Albillos A. Three-dimensional endosonography for staging of rectal cancer.  Gastrointest Endosc. 1998;  47 317-318
  PubMedSearch in Google Scholar
• 9 Marusch F, Koch A, Schmidt U. Routine use of transrectal ultrasound in rectal carcinoma: results of a prospective multicenter study.  Endoscopy. 2002;  34 385-390
  Thieme ConnectPubMedSearch in Google Scholar
• 10 Chung C Y, McCray W H, Dhaliwal S. et al . Three-dimensional esophageal varix model quantification of variceal volume by high-resolution endoluminal US.  Gastrointest Endosc. 2000;  52 87-90
  CrossrefPubMedSearch in Google Scholar
• 11 Hünerbein M, Ghadimi B M, Gretschel S, Schlag P M. Three-dimensional endoluminal ultrasound: a new method for the evaluation of gastrointestinal tumors.  Abdom Imaging. 1999;  24 445-448
  CrossrefPubMedSearch in Google Scholar
• 12 Hünerbein M, Gretschel S, Ghadimi B M, Schlag P M. Three-dimensional endoscopic ultrasound of the esophagus: preliminary experience.  Surg Endosc. 1997;  11 991-994
  CrossrefPubMedSearch in Google Scholar
• 13 Liu Y T, Miller L S, Chung J Y. et al . Validation of volume measurements in esophageal pseudotumors using 3D endoluminal ultrasound.  Ultrasound Med Biol. 2000;  26 735-741
  CrossrefPubMedSearch in Google Scholar
• 14 Tamura S, Hirano M, Chen X. et al . Intrabody three-dimensional position sensor for an ultrasound endoscope.  IEEE Trans Biomed Eng. 2002;  49 1187-1194
  CrossrefPubMedSearch in Google Scholar
• 15 Sumiyama K, Suzuki N, Katutani H. et al . A novel 3-dimensional EUS technique for real-time visualization of the volume data reconstruction process.  Gastrointest Endosc. 2002;  55 723-728
  CrossrefPubMedSearch in Google Scholar
• 16 Molin S O, Nesje L B, Gilja O H. et al . 3D endosonography in gastroenterology: methodology and clinical implications.  Eur J Ultrasound. 1999;  10 171-177
  CrossrefPubMedSearch in Google Scholar
• 17 Sumiyama K, Suzuki N, Tajiri H. A linear-array freehand 3-D endoscopic ultrasound.  Ultrasound Med Biol. 2003;  29 1001-1006
  CrossrefPubMedSearch in Google Scholar
• 18 Klingensmith J D, Schoenhagen P, Tajaddini A. et al . Automated three-dimensional assessment of coronary artery anatomy with intravascular ultrasound scanning.  Am Heart J. 2003;  145 795-805
  CrossrefPubMedSearch in Google Scholar
• 19 Ayoubi J M, Franchin R, Ferretti G. et al . Three-dimensional ultrasonographic reconstruction of the uterine cavity: virtual hysteroscopy?.  Eur Radiol. 2002;  12 2030-2033
  PubMedSearch in Google Scholar
• 20 Liu J B, Miller J S, Bagley D H, Goldberg B B. Endoluminal sonography of the genitourinary and gastrointestinal tracts.  J Ultrasound Med. 2002;  21 323-337
  PubMedSearch in Google Scholar
• 21 Yoshimoto K. Clinical application of ultrasound 3D imaging system in lesions of the gastrointestinal tract.  Endoscopy. 1998;  30 145-148
  PubMedSearch in Google Scholar
• 22 Yoshino J, Nakazawa S, Inui K. et al . Surface-rendering imaging of gastrointestinal lesions by three-dimensional endoscopic ultrasonography.  Endoscopy. 1999;  31 541-545
  Thieme ConnectPubMedSearch in Google Scholar
• 23 Hünerbein M, Dohmoto M, Haensch W, Schlag P M. Evaluation and biopsy of recurrent rectal cancer using three-dimensional endosonography.  Dis Colon Rectum. 1996;  39 1373-1378
  CrossrefPubMedSearch in Google Scholar
• 24 Heald R J, Ryall R D. Recurrence and survival after total mesorectal excision for rectal cancer.  Lancet. 1986;  i 1479-1482
  CrossrefPubMedSearch in Google Scholar

M. Giovannini, M. D.

Institut Paoli-Calmettes

232, Boulevard de Ste.-Marguérite · 13273 Marseille Cédex 9 · France

Fax: +33-4-91 22 36 58

Email: hdjchir@marseille.fnclcc.fr