DOI:10.2214/AJR.08.1298
AJR 2008; 191:1517-1522
© American Roentgen Ray Society
MRI for Detection of Extramural Vascular Invasion in Rectal Cancer
Neil J. Smith1,
Oliver Shihab2,
Abed Arnaout3,
R. Ian Swift1 and
Gina Brown4
1 Department of Surgery, Mayday University Hospital, Croydon, United
Kingdom.
2 Pelican Cancer Foundation, North Hampshire Hospital, Basingstoke, United
Kingdom.
3 Department of Histopathology, Mayday University Hospital, Croydon, United
Kingdom.
4 Department of Clinical Radiology, Royal Marsden National Health Service Trust,
Downs Rd., Sutton, Surrey SM2 5PT, United Kingdom.
Received May 19, 2008;
accepted after revision May 29, 2008.
Presented as a poster at the 2007 annual meeting of the Association of
Coloproctology of Great Britain and Ireland, Glasgow, Scotland.
N. Smith's research post was funded by the Croydon Colorectal Cancer
Charity, which had no involvement in the study design; in the collection,
analysis, or interpretation of the data; or in the writing of the report.
Address correspondence to G. Brown
(gina.brown{at}rmh.nhs.uk).
Abstract
OBJECTIVE. Extramural vascular invasion is a pathologic feature
predictive of distant relapse and poor survival among patients with colorectal
cancer. This article illustrates the use of high-spatial-resolution MRI to
identify extramural vascular invasion.
CONCLUSION. Objective MRI features that correlate with
histopathologic findings can be identified and used to evaluate extramural
vascular invasion on preoperative images. The MRI extramural vascular invasion
score provides additional staging information, which is important when
selective neoadjuvant therapy is being considered.
Keywords: colorectal cancer • extramural vascular invasion • MRI
Introduction
The accuracy and reproducibility of preoperative MRI in identifying
prognostic risk factors such as depth of invasion and safety of the surgical
circumferential resection margin are accepted
[1,
2]. MRI-based staging is
increasingly recommended [3]
because patients at highest risk can undergo preoperative adjuvant treatment,
which has a better outcome and less toxicity than does postoperative treatment
[4].
Histologic extramural vascular invasion has long been recognized as an
independent predictor of local and distant recurrence and poorer overall
survival
[5–7].
It is defined as the presence of malignant cells within endothelial
cell–lined blood vessels beyond the muscularis propria
[8] and is reported to occur in
as many as 52% of cases of colorectal cancer
[5,
8–10].
It is possible to detect extramural vascular invasion with MRI
[11]. It has been found that
the severity of MRI-detected extramural vascular invasion correlates with
relapse-free survival [12] and
may be important when preoperative treatment strategies are being considered
for patients with this particularly poor prognostic feature. To our knowledge,
the radiologic characteristics of extramural vascular invasion have not been
adequately described in the literature. This article illustrates the imaging
criteria associated with extramural vascular invasion by showing the
correlation between findings on MR images and in whole-mount pathologic
sections. The grades of severity important in the preoperative assessment of
extramural vascular invasion are depicted.
Recognizing Vascular Structures with MRI
High-spatial-resolution MRI facilitates visualization of vascular
structures in situ within the mesorectum over a series of adjacent images.
Veins may be recognizable on T2-weighted images as serpiginous or tortuous
linear structures [11]. Larger
vessels may appear black owing to signal void, and smaller vessels may be
recognized because of tortuosity and branching
(Fig. 1). Very small unnamed
vessels may radiate outward from the edge of the muscularis propria into the
perirectal fat (Fig. 2). Larger
named vessels, such as the superior rectal vein and middle rectal vein, may be
visualized in a consistent anatomic position, and a contralateral paired
vessel may be present, helping with identification (Figs.
3 and
4). It is not always possible,
however, to determine with absolute certainty whether a structure is vascular,
and this lack of clarity is an important limitation in the radiologic
assessment of extramural vascular invasion.
View larger version (119K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 1 —79-year-old man with bulky upper rectal tumor. T2-weighted
sagittal MR image shows serpiginous structure (white arrow) with very
low signal intensity. This appearance is typical of major vessel, in this
example, superior rectal vein. Smaller tributaries (black arrow) also
are tortuous but of high signal intensity.
|
|
View larger version (196K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 4 —59-year-old woman with upper rectal tumor. Axial T2-weighted
MR image below level of tumor clearly shows right middle rectal vein
(black arrow). Origin of left middle rectal vein (white
arrow) emerging from edge of muscularis also is evident.
|
|
Depth of tumor invasion can indicate the potential for extramural vascular
invasion. By definition, histologically defined extramural vascular invasion
must be associated with tumors that are at least category T3. Therefore, a
small tumor clearly limited to within the muscularis propria (category T2 or
T1) has no potential for invading extramural vessels. Assessment of MR images
for features suggestive of extramural vascular invasion must include the
following four components: pattern of tumor margin, location of tumor relative
to major vessels, caliber of vessel, and vessel border.
Pattern of Tumor Extension and Margins
Radiologically, the tumor margin may appear nodular or smooth. Tumor
invasion into the small noncharacterizable veins that radiate outward from the
bowel wall gives rise to a nodular border (Fig.
5A,
5B). This finding can be
differentiated from desmoplasia, which appears as fine stranding of low signal
intensity (Fig. 6A,
6B,
6C).
View larger version (121K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 5B —70-year-old woman with rectal cancer. Histopathologic
photograph of megablock section corresponding to A shows
circumferential involvement of entire wall extending into perirectal fat.
Nodular protrusions (arrows) are not associated with vascular
invasion. (H and E, x1.5)
|
|
View larger version (155K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 6A —61-year-old man with rectal cancer. Adjacent axial MR images
show multiple areas of stranding extending radially from tumor edge. Some
stranding is simply desmoplasia, defined by fine low-signal-intensity spikes
evident in C. However, at least one example of more irregular nodular
intermediate-signal-intensity stranding (arrow, B) represents
MRI extramural vascular invasion score 3.
|
|
View larger version (156K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 6B —61-year-old man with rectal cancer. Adjacent axial MR images
show multiple areas of stranding extending radially from tumor edge. Some
stranding is simply desmoplasia, defined by fine low-signal-intensity spikes
evident in C. However, at least one example of more irregular nodular
intermediate-signal-intensity stranding (arrow, B) represents
MRI extramural vascular invasion score 3.
|
|
View larger version (130K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 6C —61-year-old man with rectal cancer. Histopathologic
photograph of megablock section corresponding to A and B shows
circumferential tumor extending into perirectal fat in posterior aspect. Focal
evidence of extramural vascular invasion (arrows) is present. (H and
E, x1.5)
|
|
Location of Tumor Relative to Vessels
Whenever tumor is seen to lie close to a vessel, the radiologist should
consider the possibility of extramural vascular invasion (Fig.
7A,
7B). Histologically, vascular
invasion occurs when the tumor directly penetrates a vessel wall before
extending along the lumen. Therefore, the presence of tumor signal intensity
within a vascular structure is highly suggestive of extramural vascular
invasion.
View larger version (135K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 7A —82-year-old woman with polypoid tumor of rectum. Axial
T2-weighted MR image shows vein emerging from edge of bowel wall very close to
base of tumor, but vessel is of normal caliber, and no definite tumor signal
intensity appears within it (MRI extramural vascular invasion score 2).
|
|
View larger version (147K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 7B —82-year-old woman with polypoid tumor of rectum. Photograph
of histopathologic section corresponding to A shows invasive moderately
differentiated adenocarcinoma arising in severely dysplastic tubulovillous
adenoma. Tumor invades posterior wall of rectum, extending into perirectal
fat. Focal microscopic evidence of vascular invasion (arrow) is
beyond resolution of MRI. (H and E, x2.5)
|
|
Vessel Caliber and Border
As tumor invades along the lumen, the vessel expands. Tumor signal
intensity is intermediate (gray), and therefore any expansion of a
low-signal-intensity vessel by tumor invasion usually is identifiable. The
caliber or size of any vessels seen on MR images can be described as normal,
slightly expanded (Fig. 8), or
grossly expanded (Fig. 9).
Eventually, the tumor may expand through and beyond the vessel wall,
disrupting the border, which can be described as either smooth (normal) or
irregular or nodular (Fig.
9).
View larger version (179K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 8 —61-year-old man with rectal tumor. Axial T2-weighted MR image
shows multiple small veins containing tumor of intermediate signal intensity.
One vessel (white arrow) is slightly expanded by tumor, and another
(gray arrow) is of normal caliber (MRI extramural vascular invasion
score 3).
|
|
View larger version (166K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 9 —53-year-old woman with rectosigmoid tumor. Sagittal
T2-weighted MR image shows gross nodular expansion of vessel (white
arrow) draining into superior rectal vein (gray arrows). Tumor
of intermediate signal intensity is evident within superior rectal vein at
this level, slightly expanding it. Normal-caliber vessel containing signal
void extends inferiorly beyond expanded section (MRI extramural vascular
invasion score 4).
|
|
Grading the Severity of MRI-Detected Extramural Vascular Invasion
The degree of extramural vascular invasion visible at MRI ranges from very
minimal to very extensive. According to the four criteria (tumor margin, tumor
location relative to vessels, vessel size, and vessel border), a 5-point
grading system for the MRI-based preoperative assessment of extramural
vascular invasion has been proposed
[12]. This MRI extramural
vascular invasion score is logical. The lowest score, 0, correlates with the
absence of any feature suggestive of extramural vascular invasion. The maximum
score, 4, is given when the most overt features (grossly expanded and
irregular vessel border) are seen. It is helpful for radiologists to be able
to score MRI extramural vascular invasion because it has been shown that
higher scores are associated with poor survival. Lower scores are not
associated with histologic extramural vascular invasion or with adverse
outcome [12]. Stratification
of patients into prognostic groups according to MRI extramural vascular
invasion score is clinically relevant both for preoperative treatment of
patients at high risk and for postoperative follow-up.
Limitations and Strengths of MRI-Based Assessment of Extramural Vascular Invasion
Because of limitations of resolution, microscopic examples of extramural
vascular invasion are not detectable with MRI (Fig.
7A,
7B). Patients with
large-vessel invasion have the worst outcome
[8]. Therefore, the clinical
significance of extramural vascular invasion not detectable on MR images may
be minimal [12]. In contrast,
extensive vascular invasion can destroy the vessel wall, leaving little
evidence of normal venous cellular architecture, and such cases may be
underreported by pathologists. The main advantage of using contiguous 3-mm
slices for MRI is the ability to ascertain that tumor actually lies within a
vessel, either because the vessel is seen in the typical anatomic position of
one of the main vascular structures, such as the middle rectal vein (Fig.
10A,
10B,
10C,
10D), or because a normal,
unexpanded vein is seen extending beyond the area of tumor signal intensity in
the same or an adjacent image slice (Fig.
11A,
11B,
11C,
11D).
View larger version (162K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 10A —75-year-old man with rectal cancer. Coronal MR image shows
tumor growing along line of vein (white arrow) on right side forming
expanding nodule (black arrow). Normal vein (gray arrows)
also is present (MRI extramural vascular invasion score 4).
|
|
View larger version (125K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 10B —75-year-old man with rectal cancer. Photograph of
histopathologic section confirms presence of extramural deposit
(arrow), but its relation to vascular structure cannot be appreciated
in this axial section. Consequently, any extramural vascular invasion can
easily be overlooked by pathologist, who does not have benefit of multiple
contiguous H and E–stained sections through tumor. (H and E,
x1.5)
|
|
View larger version (170K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 10C —75-year-old man with rectal cancer. Photograph of same
histologic section as B specially treated with Van Gieson stain because
of lack of clarity in B. Stain colors elastic tissue black, collagen
red, and other tissue yellow, making it clear that extramural vascular
invasion is present. Tumor cells are evident in lumen of small venule
(white arrow). Adjacent arteriole (black arrow) does not
contain tumor.
|
|
View larger version (124K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 11A —49-year-old man with rectal tumor. Photograph of
histopathologic section shows tumor nodule apparently extending laterally from
right side of primary tumor. Extramural vascular invasion within nodule is not
visible. (H and E)
|
|
View larger version (139K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 11B —49-year-old man with rectal tumor. Serial ascending axial MR
images through tumor suggest nodule lies within tubular structure running
parallel to bowel wall and signal void (arrow, D) indicating
structure is vein (MRI extramural vascular invasion score 4).
|
|
View larger version (138K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 11C —49-year-old man with rectal tumor. Serial ascending axial MR
images through tumor suggest nodule lies within tubular structure running
parallel to bowel wall and signal void (arrow, D) indicating
structure is vein (MRI extramural vascular invasion score 4).
|
|
View larger version (140K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 11D —49-year-old man with rectal tumor. Serial ascending axial MR
images through tumor suggest nodule lies within tubular structure running
parallel to bowel wall and signal void (arrow, D) indicating
structure is vein (MRI extramural vascular invasion score 4).
|
|
Conclusion
Extramural vascular invasion is an important prognostic factor in
colorectal cancer. Recognition of invasion is important in the preoperative
staging of rectal tumors. The criteria used for MRI extramural vascular
invasion scoring are based on pathologic and anatomic considerations, and the
scoring system is straightforward and logical. Prognostic stratification based
on MRI extramural vascular invasion score has been found to correlate with
clinical outcome. In addition, MRI can be seen to contribute additional
staging information, depicting gross vascular invasion that is not necessarily
recognized histologically.
Acknowledgments
We thank M. Elmahallawy for preparing the Van Gieson stain and Barbara
Bannerman for assistance in the preparation of the manuscript. We thank the
radiologists, pathologists, surgeons, and nurse specialists who were members
of the MERCURY Study Group and were responsible for the conception and design
of the study and collection of data in the original MERCURY study. The
following hospitals took part in MERCURY: Pelican Cancer Foundation, The Ark,
North Hampshire Hospital; Royal Marsden Hospital Colorectal Network, Royal
Marsden Hospital; Epsom and St. Helier NHS Trust; Mayday University Hospital;
North Hampshire Hospital; Leeds Hospitals Teaching Hospitals, Leeds General
Infirmary; St. James's University Hospital; Norwegian Radium Hospital; Frimley
Park Hospital; Ashford and St. Peter's NHS Trust; Krankenhaus im
Friedrichshain; Llandough Hospital; Karolinska University Institute.
References
- MERCURY Study Group. Diagnostic accuracy of preoperative magnetic
resonance imaging in predicting curative resection of rectal cancer:
prospective observational study. BMJ2006; 333:779[Abstract/Free Full Text]
- MERCURY Study Group. Extramural depth of tumour invasion at
thin-section MR in patients with rectal cancer: results of the MERCURY Study.
Radiology 2007;243
: 132–139[Abstract/Free Full Text]
- National Institute for Clinical Excellence (Great Britain).
Improving outcomes in colorectal cancer. London,
United Kingdom: National Institute for Clinical Excellence,2004
- Sauer R, Becker H, Hohenberger W, et al. Preoperative versus
postoperative chemoradiotherapy for rectal cancer. N Engl J
Med 2004; 351:1731
–1740[Abstract/Free Full Text]
- Bokey EL, Chapuis PH, Dent OF, et al. Factors affecting survival
after excision of the rectum for cancer: a multivariate analysis.
Dis Colon Rectum 1997;40
: 3–10[CrossRef][Medline]
- Horn A, Dahl O, Morild I. Venous and neural invasion as predictors
of recurrence in rectal adenocarcinoma. Dis Colon
Rectum 1991; 34:798
–804[CrossRef][Medline]
- Harrison JC, Dean PJ, el-Zeky F, Vander Zwaag R. From Dukes through
Jass: pathological prognostic indicators in rectal cancer. Hum
Pathol 1994; 25:498
–505[CrossRef][Medline]
- Talbot IC, Ritchie S, Leighton MH, Hughes AO, Bussey HJ, Morson BC.
The clinical significance of invasion of veins in cancer of the rectum.
Br J Surg 1980;67
: 439–442[Medline]
- Sunderland D. The significance of vein invasion by cancer of the
rectum and sigmoid: a microscopic study of 210 cases.
Cancer 1949; 2:429
–437[Medline]
- Horn A, Dahl O, Morild I. The role of venous and neural invasion on
survival in rectal adenocarcinoma. Dis Colon Rectum1990; 33:598
–601[CrossRef][Medline]
- Brown G, Radcliffe AG, Newcombe RG, Dallimore NS, Bourne MW,
Williams GT. Preoperative assessment of prognostic factors in rectal cancer
using high-resolution magnetic resonance imaging. Br J
Surg 2003; 90:355
–364[CrossRef][Medline]
- Smith NJ, Barbachano Y, Norman AR, Swift RI, Abulafi AM, Brown G.
Prognostic significance of magnetic resonance imaging-detected extramural
vascular invasion in rectal cancer. Br J Surg2008; 95:229
–236[CrossRef][Medline]
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati What's this?
Top
Abstract
Introduction
