Frans-jan H. Hulsmans, Anne Bosma, MD, PhD
MD
T. Lok
Tio,
N.
J. Tytgat,
Colorectal In Screening
Villous Adenoma: Transrectal for Invasive Malignancy’
#{149}
#{149}Guido
Exclusion of focal infiltrating malignancy in colorectal villous adenoma is a prerequisite when nonsurgical treatment is considered. In a study of 81 patients with endoscopically identified colorectal villous adenoma screened for malignancy with transrectal ultrasonography (US), 15 patients were excluded because of incomplete follow-up. Twelve carcinomas were present, confirmed with either histopathologic examination after surgical resection (n 9) or biopsies during laser treatment (n = 3). Nine of them were detected with transrectal US on the basis of disruption of the anatomic wall layers (sensitivity, 75%). In 46 of the 54 adenomas transrectal US helped confirm the benign nature of the lesion (specificity, 85%). Seven of the eight false-positive cases happened to be previously treated with surgery or coagulation. Treatment-associated inflammatory changes in the wall layers seemed responsible for this misinterpretation. Because of the high predictive value for a negative result (benign adenoma, 94%), hansrectal US is recommended for the evaluation of villous adenomas to detect malignancy, especially when nonsurgical treatment is considered. Transrectal US should be performed before diagnostic polypectomy. Index terms: Colon, neoplasms, 75.3111, 75.3192 #{149} Colon, US, 75.1298 #{149} Rectum, neoplasms, 757.3111, 757.3192 #{149} Rectum, US, 757.1298 Radiology
I From demic
1992;
the
185:193-196
Department
of Radiology,
C
MD,
PhD #{149}Elizabeth MD, PhD
M. H. Mathus-Vliegen,
adenomas are precurof carcinomas (1). Standard practice is polypectomy of all adenomas larger than 0.5 cm because it enables histopathologic examination of the full specimen. Sessile adenomas too large to be treated with polypectomy are preferentially treated with surgical resection. Ablation by means of laser photocoagulation may be an OLORECTAL
sors
alternative traindications
in case of refusal or conto surgery (2). Prethera-
peutic evaluation of the villous adenoma is essential to rule out the focal presence of malignancy, especially when a nonsurgical therapy is considered. Endoscopic biopsy is unreliable to rule out malignancy (3). Transrectal ultrasonography (US) is a well-known imaging modality because of its abifity to depict the individual layers of the intestinal wall. Therefore, it is increasingly used in the evaluation of rectal pathologic conditions, mainly in the preoperalive assessment of infiltration depth of rectal cancer. Literature dealing with the pretherapeutic evaluation of adenomas is scarce. To the best of our knowledge, only Glaser et al (4) applied transrectab US to differentiate between noninvasive tubulovifious or villous adenoma and infiltrating carcinoma (31 patients). In the present study, the value of transrectal US as a method to screen
for
malignancy
in colorectal
adenomas was evaluated in a barge series of patients. The aim of the study was to find out whether transrectal US could be used to select patients with a coborectal adenoma for nonsurgical treatment.
Aca-
Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands. Received December 24, 1991; revision requested February 18, 1992; revision received March 30; accepted April 13. Supported by grant IKA 87-05 from the Dutch Cancer Society. Address reprint requests to F.J.H.H. 0 RSNA, 1992
MATERIALS
AND
METHODS
FromJanuary 1987 to February 1990, 81 consecutive patients with villous adenoma were examined by means of transrectal US. In this prospective study the criteria for indusion were (a) the adenoma had to be located in the rectum or redo-
MD,
PhD
US
sigmoid and (b) could not be removed entirely by means of snare polypectomy. Furthermore, (c) villous or tububovillous histologic findings without signs of malignancy had to be present at histologic examination of multiple biopsy or polypectomy fragments. Severe dysplasia, without infiltration, was not considered evidence of malignancy. Last, (d) the final diagnosis had to be provided either by means of surgical resection or long-term follow-up after local laser destruction, with or without prior debulking by means of electrocoagulation. The laser destruction was defined as complete when, in a follow-up period of at least 5 months, two 6-weekly endoscopy procedures and large-partide biopsies of the treated area revealed no recurrent adenomatous tissue. The ablated villous adenoma was thus considered to have been benign in origin. Of the 81 patients with an intermediate or extensive (tubulovillous) or villous adenoma (2), a total of 66 could be induded in the study. Ages ranged between 44 and 88 (mean, 67) years. Twelve of the 15 exduded patients were still receiving laser therapy at the end date of the study or had not passed the 5-month follow-up period. Three other patients withdrew from further laser treatment, all of them over 85 years of age. The final diagnosis was based on surgical resection in 27 patients and on a 5-month follow-up after laser ablation in 39 patients. Transrectal US examinations were routimely performed with a nonoptical, radial scanning transducer (model ASU-57 or ASU-59) connected to a basic US unit (Endoscan SSA-520; Aloka, Tokyo). For villous adenomas extending into the distal sigmoid region, a side-viewing echoduodenoscope (EU-M3; Olympus, Lake Success, NY)
or,
more
recently,
a forward-viewing
echocobonoscope (XCF-UM2; Olympus) was used. The ultrasound frequency for these instruments was 7.5 MI-lz, except for the ASU-57 (5 MHz). Because of the availability of the flexible echocobonoscope, all villous adenomas could be reached. After the distal colon was deansed with a phosphate enema, the patient was placed in the left lateral decubitus position. A digital rectal examination was performed to assess the location of the tumor and to relax the anal sphincter muscle before insertion of the nonoptic transducer.
193
After the rectal lumen was filled with deaerated water, the instrument was slowly withdrawn as the rectal wall was scanned. The
latex
balloon,
attached
to the
Table 1 Results of Transrectal
US in the Evaluationof
tip of
study
with
the imaging.
we learned
sion
of the
that excessive
polypoid
the balloon transrectal
Inifitrating
had to be prevented. US the tumors were
With classified
villous adenomas The interpretation
Findings
by
in a way Kimmey
Inifitration
of infiltrating
defined by destruction the deeper wall layers mucosa
(eg,
cancer
was
of one or more of underneath the
submucosa,
muscularis
(CA)
The final
diagnosis
No.
of
Laser-treated Lesions
No. of Patients 8
4/4
17
3/0
46
14/32
49
12
9/3
54
18/36
66
was obtained
by means
of surgical
resection
specimen or 5-month follow-up after complete laser ablation. t CA = US signs of infiltration, suggestive of carcinoma. VA to a benign villous or tububovillous adenoma.
=
layer
nancy in the second underwent surgery
hand, seven
in combination
with
(Ti tumor
according
to the TNM classification). In a later phase, complete destruction of the middle
tive of a T2 tumor.
be visualized toof the outer hypopropria), indica-
In a more
advanced
tumor stage, an irregular border between the outer echo-poor layer (musculans propria) and outer echogenic layer (perirectal fat or subserosa) could be seen. This represented a T3 tumor, especially when the hypoechoic
tumor
perechoic there was
the deeper
extended
within and/or
layers,
6 weeks
the lesion
the
hy-
with
was defined
In addition, the or electrocoagulation
before
previous
correlated
into
perirectal fatty tissue. When no evidence of destruction of
as villous adenoma. of laser coagulation
the
surgical
effects
US examination
resection
the transrectal
were
US results.
RESULTS The results of the transrectal US examination were compared with the final diagnosis (Table 1). Of the 66 patients included, a total of 54 patients had a vilbous adenoma as the final diagnosis, versus 12 with a carcinoma. With transrectal US, the wall layers underneath the adenomatous polyp were assessed as being intact in 49
patients
and
invasive
carcinoma
was considered unlikely (Fig 1). In 46 patients, this was in agreement with the final diagnosis, which was dependent
on
14 surgical
resections
and
32
follow-up studies after successful laser treatment. In three patients infiltraling carcinoma was not detected with transrectal US. Histologic examination of the resected specimens in these cases revealed a Ti, T2, and T3 carcinoma, respectively. The Ti tumor consisted of microscopic infiltration of only two glandular ducts into the 194
Radiology
#{149}
and
histologic
no signs
evaluation
of inifitration,
of the
corresponding
Early of patients, transrectal
echogenic layer could gether with thickening echoic layer (muscularis
Total
6/3
submucosa. Ongoing weight loss reinforced a clinical suspicion of mabig-
of the latter
of
Laser-treated Lesions
3
the border between the inner echo-poor layer (mucosa) and middle echogenic (submucosa)
of Resected
Lesions/No.
pro-
pria, and subserosa or perirectal fat). changes at US consisted of irregularity
thinning
Adenoma
9
(VA)
Total
et 9
presence
Benign
Lesions/No. No. of Patients
Noninfiltration
al (5,6).
The
of
Transrectal USt
or inof the
classified et al and
Carcinoma No. of Resected
compreslesion
at US was by Bolondi
suggested
Adenomas
the
or exophytic
as noninfiltrating filtrating cancer.
wall layers
During
Villous
Final Diagnosis9
the transducer, was also filled with water to prevent feces or mucus strands from interfering
Coborectal
patient,
and
he
within 3 weeks the transrectal US examination. T3 carcinoma frequent endobiopsies did not reveal maliguntil 7 months after the start of therapy. Thus, the tumor stage time of the initial transrectal US
after In the scopic nancy
laser at the remained
unknown.
cases
as a Ti
tumor
and
in five
cases
as a T2 tumor. The sensitivity of transrectal US in the detection of malignant infiltration was 75%. The specificity was 85% with a negative US (no infiltrating
.
Forty-six of 49 patients result of transrectal cancer) had a final
diagnosis of adenoma. alive predictive value
Thus, the negwas 94% (7),
and
the
positive
53%. As apy, 23 of nosis
predictive
to the the of
the influence of previous therclinical history revealed that 54 patients with a final diagvillous adenoma underwent before the initial transrectal
treatment US examination n = 5; partial
coagulation,
(transanab polypectomy n
=
value
tomy
or laser
i8). In the other
was
3i
performed;
underwent
result
of
one
laser
of them
coagulation
be-
fore transrectal US. This relationship between false-positive findings of transrectal US was significant P < .Oi).
and previous (Fisher exact
An additional pathologic nical errors
treatment test,
indication
changes could
terpretation topathobogic
that
rather explain
than techthe misin-
may be found examination
in the of the
his-
specimen. In iO of the 54 vilbous adenomas the final diagnosis was ob-
tamed by means tion (six patients prior two
treatment; cases
the
of segmental did not have
resecany
four
did).
inflammatory edema respectively. Both submucosa: to the
live
treated
results
patients
histology
scribed
reports
In
de-
changes in the and infiltrates, patients belonged
group
with
of transrectal
flammatory changes in the true-negative Because of the small suit is not significant test).
was
resection,
false-positive
US was seen. On the other in the previously treated group, of the 23 examinations were
erroneously interpreted as showing malignant infiltration (Table 2). Two of these patients had undergone transanal excision of the mucosal wall layer. In five patients partial polypecalso
In i7 patients, the deeper wall layers underneath the adenomatous besion were not entirely intact, which led to the diagnosis of infiltrating carcinoma (Fig 2). This invasive malignancy was confirmed in nine patients. Three of these true-positive cases were palliatively treated with a laser. In six patients the tumor was surgically resected, and histopathobogic staging revealed three T3 tumors, one T2 tumor, and two Ti tumors. Falsepositive results occurred in the eight other patients; no malignancy was found after surgical resection (n = 4) or at the 5-month follow-up examinalion after laser ablation (n = 4). The adenoma was overstaged in three
one
false-posi-
US. No inwere mentioned group (n = 6). numbers this re(Fisher exact
DISCUSSION In the malignancy
literature
the
in large
ter) vilbous adenomas i6% and 46% (8,9). it is widely accepted nomas, too large for should be surgically
dude
the
presence
prevalence
(>
2 cm
varies For this
of
in diame-
between reason
that sessile adepolypectomy, resected to ex-
of invasive
cancer
October
1992
1.
2.
Figures
1, 2.
rectal
wall
poor),
sm
a man
aged
malignancy doscopic nomatous
Table Results
=
(1) Benign
and underneath submucosa
adenoma in a man aged the superficial lesion. (echogenic), VA = villous
62 years. The individual wall layers are well delineated and can be recognized in the normal There are no signs of malignant infiltration. m = mucosa, mp = muscularis propria (echoadenoma (moderately echogenic), w = water-filled rectal lumen. (2) Infiltrating carcinoma in
52 years. Underneath the greater part of the adenomatous lesion, the rectal wall layers are still intact. There is, however, a focal as well, infiltrating through the musculans propna into the perirectal fat. This T3 tumor was not sampled during the previous enbiopsies. b = balloon compressing the rectal lesion, CA = carcinoma (echo-poor), mp = double-layered muscularis propna, VA = aderectal lesion, W = water in the balloon surrounding the transducer.
their destruction by malignant infiltration. The recent preliminary results of a magnetic resonance (MR) imaging study involving use of an intrarectab coil for high-resolution images of
2 of Transrectal
and Nontreated
US in Treated
No. of Patients
Adenoma Findings of Transrectal Treatedt
(CA)
No infiltration
with
Adenomas
Villous
as the Final Diagnosis
the
Transanal Resection!
US9
Inifitration
Vilbous
Coagulation*
7
(VA)
Total
Nontreated
Total
16
2/5 3/13
1 30
8 46
23
5/18
31
54
CA = false-positive result compared with the final diagnosis of adenoma, VA = true-negative reThe number of false-positive results in the treated group compared with those in the nontreated group cannot be explained by chance (Fisher exact test, P < .01). t Treated = polypectomy or laser treatment within 5 weeks before the transrectal examination or any S
suit.
previous surgical * Coagulation
treatment of the adenoma. = electrocoagulation or laser coagulation.
in the specimen. Relative contraindicalions may be found in a poor cardiopulmonary status or other concurrent disorders representing an overriding
risk
for
surgery
(iO).
Surgi-
cal treatment can also be refused by the patient. In these cases a combination of piecemeal debulking and further destruction with laser photocoagulation may be an alternative to surgical resection (2,ii). The major drawback of nonsurgical treatment is the lack of complete histobogic examination of the lesion. This lack stresses the need to be optimally informed of the benign nature of the lesion before the start of the therapy. As biopsies are insufficient to rule out malignancy (3,i2-i4), we evaluated the use of transrectal US in tububovilbus adenomas. We expected transrecVolume
185
Number
#{149}
1
tab US to be accurate of carcinoma, because
in the the
detection wall
de-
strucion caused by malignant infiltralion can be visualized (15-i9). In the present study the prevalence of focal carcinoma was only i8% (12 of 66), as malignant lesions detected with endoscopic biopsies or partial polypectomy were already excluded. The fact that 12 carcinomas still remained undetected with endoscopy is explained by the sampling error of the biopsies, especially in large besions. Biopsies often do not extend into the submucosal center of the polyp, which is necessary to diagnose early malignant infiltration (13). Until recently, transrectal US has been the only imaging modality able to depict the intestinal wall layers separately and to allow detection of
rectal
wall
are
promising
as well
(20). As it is not possible to visualize the thin muscularis mucosae with the present imaging technology (6,21), even high-frequency US cannot compete with microscopic evaluation of the resected specimen. This implies that early invasion through the muscularis mucosae into the submucosa may
remain
undetected
with
preop-
erative transrectal US. Such an example in our study is the Ti carcinoma missed with transrectal US: The histobogy report described only two glandular ducts in the submucosa. We agree with other authors that it is not possible
to recognize
an
intramucosal
carcinoma (22,23). We deliberately excluded the presence of lymph nodes from our study. Because transrectal US is able to depict lymph nodes as small as 3 mm in diameter, the visualization of lymph nodes is not a valid parameter; the majority of them will be benign. The discriminating value of US parameters for perirectab lymph nodes has not yet been evaluated in a clinical study. We are convinced that tumor infiltration is a more direct indication of malignancy. As far as we know, only three studies have been published in which transrectal US was used to screen for invasive carcinoma in adenomatous lesions (4,22,24). In two of these studRadiology
#{149} 195
ies the US criterion for malignancy was infiltration into the muscularis propria (22,24). The authors combined the adenomas and Ti tumors into one “benign” group. Although this resulted in a high specificity, the sensitivity was low in both studies (58% and 66%, respectively) compared with 75% in the present study. In comparison with the study by Glaser et al (4) our results are somewhat less favorable, although the inclusion criteria of endoscopic biopsy findings, the transrectal US classification of inifitration, transducer frequency, and even the incidence of malignant inifitration (six of the 31 examined lesions [19%1) were similar to ours (18%). The most remarkable difference was the considerable number of false-positive results in our study (eight of 66), a rate about twice as high as that in the study of Glaser et al (two of 31). The reason for this discrepancy is not readily apparent. One possibility could be artifacts created by the water-filled balloon compressing the polyp into the deeper wall layers. We expected this could create an image suggestive of inifitralion, as was recently confirmed by other authors (24). To overcome this potential problem, we used a modifled scanning technique, in which the rectal lumen and transducer balloon were filled with degassed water. This could not have been a major factor, as false-positive results were encountered in the rest of the study as well. Another explanation for this considerable number of false-positive results may be found in the previous treatment of those patients. It appeared that seven of eight patients with false-positive results had preyously undergone therapy. This ratio differed significantly (P < .01) from the incidence of false-positive results in the rest of the patients with adenoma as the final diagnosis. Four patients with a false-positive result of transrectal US finally underwent treatment with segmental resection. The histopathobogic appearance of two of these benign adenomas suggests a possible basis for the misinterpretation. The inflammatory or probably even fibrotic changes in the layers underneath the adenomatous lesion, as a consequence of the previous therapy, may mimic malignant inifitration during
196
transrectab
Radiology
#{149}
US.
This
finding
stresses the importance of early hansrectal US examination in the diagnostic work-up of the patient. Apart from previous therapy, the location of a polyp near the anal sphincter interfered with imaging. Two of the falsely positive adenomas were located directly behind the anal sphincter. This postanal area is difficult to evaluate (23), partly because of the inability to keep the scanning plane perpendicular to the rectal wall (25,26) and partly because of the short distance between the transducer and the rectal wall immediately above the sphincter. This means that the rectal wall cannot be visualized within the optimal focal range of the transducer, which may result in a blending of the separate layers. Thus, infiltration cannot be exduded. Transrectal lineararray transducers, especially those with an optimal near-field resolution and an axial scanning plane will further improve visualization of this area. In our evaluation of the results of transrectal US, we were aware of the shortcomings in using those adenomas ablated by means of laser as a final diagnosis, because early malignancy might have been eradicated with laser ablation. On the other hand, this may be of limited relevance clinically, as the chosen therapy proved to be appropriate. In addition to Rubesin et al (27), who stated that the radiologist should focus on the detection and determinalion of size of rectal adenomas in an attempt to predict malignancy, we would like to add the even more important
detection
of signs
of infiltra-
lion by means of transrectal US. This is mandatory, especially when nonsurgical therapy of adenomas is considered. The high predictive value for the absence of carcinoma (negative predictive
value,
important treatment
role. Owing interfering
terpretation,
94%)
however,
strengthens
to previous with proper transrectal
Kiznmey MB, Martin KY, Franklin
correlates
7.
8.
9.
The polyp.cancer
sequence
3.
adenoma.
removal Ann
Surg
of the can1987; 205:
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mor of the colon: correlation of histologic, macroscopic, and radiographic features. Radi. ology 1988; 167:673-677. Barwick KW. The use of endoscopic biopsy
11.
bowel
in evaluation 14. 15.
adenomas.
of polypoid
lesions
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YaleJ Biol Med 1986; 59:33-40. Ridell RH. Hands off”cancerous” large bowel polyps. Gastroenterology 1985; 89:432Rifkin
MD, Marks
GJ.
Transrectal
US as an
adjunct
in the diagnosis of rectal and extrarecRadiology 1985; 157:499-502. Wang KY, KimmeyTMB, Nyberg DA, et aL Colorectal neoplasms: accuracy of US in demonstrating the depth of invasion. Radiology tal tumors.
16.
17.
18.
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20. 21.
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1987; 165:827-82g. Konishi F, Ugajin H, Ito K, Kanazawa K Endorectalultrasonography with a 7.5 MHz linear array scanner for the assessment of invasion of rectal carcinoma. mt J Colorectal Dis 1990; 5:15-20. Orrom WJ, Wont WD Rothenberger DA, Jensen LL, Goldberg SM. Endorectal ultrasound in thepreoperative staging of rectal himors. Dis Colon Rectum 1990; 33:654-659. Tio U, Coene PP, van Delden OM, Tytgat GN. Colorectal carcinoma: preoperative TNM dassification with endosonography. Radiology 1991; 179:165-170. Chan TW, Kressel HY, Milestone B, et aL Rectal carcinoma: staging at MR imaging with endorectal coil. Radiology 1991; 181:461-467. Imai Y, Kressel HY, SaulS, et aL Colorectal tumors: an in vitro study of high-resolution MR imaging Radiology 1990; 177:695-701. Mosnierl-I, Ginvarch M, Meduri B, Fritschj, Outters F. Endorectal sonography in the management of rectal villous tumours. Int J Colorectal Dis 1990; 5:90-93. Hildebrandt U, FeifelG, Ecker KW. Rectal endosonography. Baillieres Clin Gastroenterol 1989;
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457. Mathus-Vliegen EMIl, Tytgat GNJ. The potential and limitations of laser photoablation of colorectal adenomas. Gastrointest Endosc 1991; 37:9-17.
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Sivak MVJr, DeCosse II. CA 1989; 39:219-225. Maunoury V, Collet R, Cochelard D, Brunethud JM, Cortot A, ParISJC. Traitement par laser des tumeurs villeuses rectosigmoidiennes: etude d’une serie de 313 malades. Ann Chir 1990; 44:24-29. lida M, Iwashita A, Yao T, et at. Villous tu-
the large boweL Proc R Soc Med 1974; 67:4512.
after endoscopic
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demiology, a basic science for clinical medicine. 1st ed. Boston: Little, Brown, 1985; 59138. Shinya H, Cooperman A, Wolff WI. A rationale for the endoscopic management of colonic polyps. Surg Clin North Am 1982; 62: 861-867. RiChards WO, Webb WA, Morris SJ, Davis RC, McDaniel L, Jones L, Littauer S. Patient mancerous colon 665-672
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DW, SilversteinFE.
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Glaser F, Schiag P, Herfarth C. Endorectal ultrasonography for the assessment of invasion of rectal tumours and lymph node involvement. BrJSurg 1990; 77:883-887. Bolondi L, Caletti C, Casanova P, Villanacci V, Grigioni W, Lab#{244} C. Problems and variations in the interpretation of the ultrasound feature of the normal upper and lower CI tract wall. ScandJ Castroenterol 1986; 123 (suppl):16-.26.
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Heintz A, Buess C, Frank K, Kuntz C, Strunck H,Juninger T. Endoluminal ultrasonic examinahon of sessile polyps and early carcinomas of the rectum. Surg Endosc 1989; 3:92-95. Hildebrandt U, FeifelG. Preoperative staging of rectal cancerby intrarectal ultrasound. Dis Colon Rectum 1985; 28:42-46. Roach T, Lorenz R, Suchy R, Dancygier H, Classen M. Colonic endoscopic ultrasonography: first results of a new technique. Gastromtest Endosc 1990; 36:382-386. Rubesin SE, Levine MS. Laufer I, Herlinger H. Villous adenomas: the scientific and the practi. caL Radiology 1988; 167:869-870.
Livstone EM, Troncale FJ, Sheahan DC. Value of single forceps biopsy of colonicpolyps. Gastroenterology 1977; 73:1296-1298.
October1992
MD
T. Lok
Tio,
N.
J. Tytgat,
Colorectal In Screening
Villous Adenoma: Transrectal for Invasive Malignancy’
#{149}
#{149}Guido
Exclusion of focal infiltrating malignancy in colorectal villous adenoma is a prerequisite when nonsurgical treatment is considered. In a study of 81 patients with endoscopically identified colorectal villous adenoma screened for malignancy with transrectal ultrasonography (US), 15 patients were excluded because of incomplete follow-up. Twelve carcinomas were present, confirmed with either histopathologic examination after surgical resection (n 9) or biopsies during laser treatment (n = 3). Nine of them were detected with transrectal US on the basis of disruption of the anatomic wall layers (sensitivity, 75%). In 46 of the 54 adenomas transrectal US helped confirm the benign nature of the lesion (specificity, 85%). Seven of the eight false-positive cases happened to be previously treated with surgery or coagulation. Treatment-associated inflammatory changes in the wall layers seemed responsible for this misinterpretation. Because of the high predictive value for a negative result (benign adenoma, 94%), hansrectal US is recommended for the evaluation of villous adenomas to detect malignancy, especially when nonsurgical treatment is considered. Transrectal US should be performed before diagnostic polypectomy. Index terms: Colon, neoplasms, 75.3111, 75.3192 #{149} Colon, US, 75.1298 #{149} Rectum, neoplasms, 757.3111, 757.3192 #{149} Rectum, US, 757.1298 Radiology
I From demic
1992;
the
185:193-196
Department
of Radiology,
C
MD,
PhD #{149}Elizabeth MD, PhD
M. H. Mathus-Vliegen,
adenomas are precurof carcinomas (1). Standard practice is polypectomy of all adenomas larger than 0.5 cm because it enables histopathologic examination of the full specimen. Sessile adenomas too large to be treated with polypectomy are preferentially treated with surgical resection. Ablation by means of laser photocoagulation may be an OLORECTAL
sors
alternative traindications
in case of refusal or conto surgery (2). Prethera-
peutic evaluation of the villous adenoma is essential to rule out the focal presence of malignancy, especially when a nonsurgical therapy is considered. Endoscopic biopsy is unreliable to rule out malignancy (3). Transrectal ultrasonography (US) is a well-known imaging modality because of its abifity to depict the individual layers of the intestinal wall. Therefore, it is increasingly used in the evaluation of rectal pathologic conditions, mainly in the preoperalive assessment of infiltration depth of rectal cancer. Literature dealing with the pretherapeutic evaluation of adenomas is scarce. To the best of our knowledge, only Glaser et al (4) applied transrectab US to differentiate between noninvasive tubulovifious or villous adenoma and infiltrating carcinoma (31 patients). In the present study, the value of transrectal US as a method to screen
for
malignancy
in colorectal
adenomas was evaluated in a barge series of patients. The aim of the study was to find out whether transrectal US could be used to select patients with a coborectal adenoma for nonsurgical treatment.
Aca-
Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands. Received December 24, 1991; revision requested February 18, 1992; revision received March 30; accepted April 13. Supported by grant IKA 87-05 from the Dutch Cancer Society. Address reprint requests to F.J.H.H. 0 RSNA, 1992
MATERIALS
AND
METHODS
FromJanuary 1987 to February 1990, 81 consecutive patients with villous adenoma were examined by means of transrectal US. In this prospective study the criteria for indusion were (a) the adenoma had to be located in the rectum or redo-
MD,
PhD
US
sigmoid and (b) could not be removed entirely by means of snare polypectomy. Furthermore, (c) villous or tububovillous histologic findings without signs of malignancy had to be present at histologic examination of multiple biopsy or polypectomy fragments. Severe dysplasia, without infiltration, was not considered evidence of malignancy. Last, (d) the final diagnosis had to be provided either by means of surgical resection or long-term follow-up after local laser destruction, with or without prior debulking by means of electrocoagulation. The laser destruction was defined as complete when, in a follow-up period of at least 5 months, two 6-weekly endoscopy procedures and large-partide biopsies of the treated area revealed no recurrent adenomatous tissue. The ablated villous adenoma was thus considered to have been benign in origin. Of the 81 patients with an intermediate or extensive (tubulovillous) or villous adenoma (2), a total of 66 could be induded in the study. Ages ranged between 44 and 88 (mean, 67) years. Twelve of the 15 exduded patients were still receiving laser therapy at the end date of the study or had not passed the 5-month follow-up period. Three other patients withdrew from further laser treatment, all of them over 85 years of age. The final diagnosis was based on surgical resection in 27 patients and on a 5-month follow-up after laser ablation in 39 patients. Transrectal US examinations were routimely performed with a nonoptical, radial scanning transducer (model ASU-57 or ASU-59) connected to a basic US unit (Endoscan SSA-520; Aloka, Tokyo). For villous adenomas extending into the distal sigmoid region, a side-viewing echoduodenoscope (EU-M3; Olympus, Lake Success, NY)
or,
more
recently,
a forward-viewing
echocobonoscope (XCF-UM2; Olympus) was used. The ultrasound frequency for these instruments was 7.5 MI-lz, except for the ASU-57 (5 MHz). Because of the availability of the flexible echocobonoscope, all villous adenomas could be reached. After the distal colon was deansed with a phosphate enema, the patient was placed in the left lateral decubitus position. A digital rectal examination was performed to assess the location of the tumor and to relax the anal sphincter muscle before insertion of the nonoptic transducer.
193
After the rectal lumen was filled with deaerated water, the instrument was slowly withdrawn as the rectal wall was scanned. The
latex
balloon,
attached
to the
Table 1 Results of Transrectal
US in the Evaluationof
tip of
study
with
the imaging.
we learned
sion
of the
that excessive
polypoid
the balloon transrectal
Inifitrating
had to be prevented. US the tumors were
With classified
villous adenomas The interpretation
Findings
by
in a way Kimmey
Inifitration
of infiltrating
defined by destruction the deeper wall layers mucosa
(eg,
cancer
was
of one or more of underneath the
submucosa,
muscularis
(CA)
The final
diagnosis
No.
of
Laser-treated Lesions
No. of Patients 8
4/4
17
3/0
46
14/32
49
12
9/3
54
18/36
66
was obtained
by means
of surgical
resection
specimen or 5-month follow-up after complete laser ablation. t CA = US signs of infiltration, suggestive of carcinoma. VA to a benign villous or tububovillous adenoma.
=
layer
nancy in the second underwent surgery
hand, seven
in combination
with
(Ti tumor
according
to the TNM classification). In a later phase, complete destruction of the middle
tive of a T2 tumor.
be visualized toof the outer hypopropria), indica-
In a more
advanced
tumor stage, an irregular border between the outer echo-poor layer (musculans propria) and outer echogenic layer (perirectal fat or subserosa) could be seen. This represented a T3 tumor, especially when the hypoechoic
tumor
perechoic there was
the deeper
extended
within and/or
layers,
6 weeks
the lesion
the
hy-
with
was defined
In addition, the or electrocoagulation
before
previous
correlated
into
perirectal fatty tissue. When no evidence of destruction of
as villous adenoma. of laser coagulation
the
surgical
effects
US examination
resection
the transrectal
were
US results.
RESULTS The results of the transrectal US examination were compared with the final diagnosis (Table 1). Of the 66 patients included, a total of 54 patients had a vilbous adenoma as the final diagnosis, versus 12 with a carcinoma. With transrectal US, the wall layers underneath the adenomatous polyp were assessed as being intact in 49
patients
and
invasive
carcinoma
was considered unlikely (Fig 1). In 46 patients, this was in agreement with the final diagnosis, which was dependent
on
14 surgical
resections
and
32
follow-up studies after successful laser treatment. In three patients infiltraling carcinoma was not detected with transrectal US. Histologic examination of the resected specimens in these cases revealed a Ti, T2, and T3 carcinoma, respectively. The Ti tumor consisted of microscopic infiltration of only two glandular ducts into the 194
Radiology
#{149}
and
histologic
no signs
evaluation
of inifitration,
of the
corresponding
Early of patients, transrectal
echogenic layer could gether with thickening echoic layer (muscularis
Total
6/3
submucosa. Ongoing weight loss reinforced a clinical suspicion of mabig-
of the latter
of
Laser-treated Lesions
3
the border between the inner echo-poor layer (mucosa) and middle echogenic (submucosa)
of Resected
Lesions/No.
pro-
pria, and subserosa or perirectal fat). changes at US consisted of irregularity
thinning
Adenoma
9
(VA)
Total
et 9
presence
Benign
Lesions/No. No. of Patients
Noninfiltration
al (5,6).
The
of
Transrectal USt
or inof the
classified et al and
Carcinoma No. of Resected
compreslesion
at US was by Bolondi
suggested
Adenomas
the
or exophytic
as noninfiltrating filtrating cancer.
wall layers
During
Villous
Final Diagnosis9
the transducer, was also filled with water to prevent feces or mucus strands from interfering
Coborectal
patient,
and
he
within 3 weeks the transrectal US examination. T3 carcinoma frequent endobiopsies did not reveal maliguntil 7 months after the start of therapy. Thus, the tumor stage time of the initial transrectal US
after In the scopic nancy
laser at the remained
unknown.
cases
as a Ti
tumor
and
in five
cases
as a T2 tumor. The sensitivity of transrectal US in the detection of malignant infiltration was 75%. The specificity was 85% with a negative US (no infiltrating
.
Forty-six of 49 patients result of transrectal cancer) had a final
diagnosis of adenoma. alive predictive value
Thus, the negwas 94% (7),
and
the
positive
53%. As apy, 23 of nosis
predictive
to the the of
the influence of previous therclinical history revealed that 54 patients with a final diagvillous adenoma underwent before the initial transrectal
treatment US examination n = 5; partial
coagulation,
(transanab polypectomy n
=
value
tomy
or laser
i8). In the other
was
3i
performed;
underwent
result
of
one
laser
of them
coagulation
be-
fore transrectal US. This relationship between false-positive findings of transrectal US was significant P < .Oi).
and previous (Fisher exact
An additional pathologic nical errors
treatment test,
indication
changes could
terpretation topathobogic
that
rather explain
than techthe misin-
may be found examination
in the of the
his-
specimen. In iO of the 54 vilbous adenomas the final diagnosis was ob-
tamed by means tion (six patients prior two
treatment; cases
the
of segmental did not have
resecany
four
did).
inflammatory edema respectively. Both submucosa: to the
live
treated
results
patients
histology
scribed
reports
In
de-
changes in the and infiltrates, patients belonged
group
with
of transrectal
flammatory changes in the true-negative Because of the small suit is not significant test).
was
resection,
false-positive
US was seen. On the other in the previously treated group, of the 23 examinations were
erroneously interpreted as showing malignant infiltration (Table 2). Two of these patients had undergone transanal excision of the mucosal wall layer. In five patients partial polypecalso
In i7 patients, the deeper wall layers underneath the adenomatous besion were not entirely intact, which led to the diagnosis of infiltrating carcinoma (Fig 2). This invasive malignancy was confirmed in nine patients. Three of these true-positive cases were palliatively treated with a laser. In six patients the tumor was surgically resected, and histopathobogic staging revealed three T3 tumors, one T2 tumor, and two Ti tumors. Falsepositive results occurred in the eight other patients; no malignancy was found after surgical resection (n = 4) or at the 5-month follow-up examinalion after laser ablation (n = 4). The adenoma was overstaged in three
one
false-posi-
US. No inwere mentioned group (n = 6). numbers this re(Fisher exact
DISCUSSION In the malignancy
literature
the
in large
ter) vilbous adenomas i6% and 46% (8,9). it is widely accepted nomas, too large for should be surgically
dude
the
presence
prevalence
(>
2 cm
varies For this
of
in diame-
between reason
that sessile adepolypectomy, resected to ex-
of invasive
cancer
October
1992
1.
2.
Figures
1, 2.
rectal
wall
poor),
sm
a man
aged
malignancy doscopic nomatous
Table Results
=
(1) Benign
and underneath submucosa
adenoma in a man aged the superficial lesion. (echogenic), VA = villous
62 years. The individual wall layers are well delineated and can be recognized in the normal There are no signs of malignant infiltration. m = mucosa, mp = muscularis propria (echoadenoma (moderately echogenic), w = water-filled rectal lumen. (2) Infiltrating carcinoma in
52 years. Underneath the greater part of the adenomatous lesion, the rectal wall layers are still intact. There is, however, a focal as well, infiltrating through the musculans propna into the perirectal fat. This T3 tumor was not sampled during the previous enbiopsies. b = balloon compressing the rectal lesion, CA = carcinoma (echo-poor), mp = double-layered muscularis propna, VA = aderectal lesion, W = water in the balloon surrounding the transducer.
their destruction by malignant infiltration. The recent preliminary results of a magnetic resonance (MR) imaging study involving use of an intrarectab coil for high-resolution images of
2 of Transrectal
and Nontreated
US in Treated
No. of Patients
Adenoma Findings of Transrectal Treatedt
(CA)
No infiltration
with
Adenomas
Villous
as the Final Diagnosis
the
Transanal Resection!
US9
Inifitration
Vilbous
Coagulation*
7
(VA)
Total
Nontreated
Total
16
2/5 3/13
1 30
8 46
23
5/18
31
54
CA = false-positive result compared with the final diagnosis of adenoma, VA = true-negative reThe number of false-positive results in the treated group compared with those in the nontreated group cannot be explained by chance (Fisher exact test, P < .01). t Treated = polypectomy or laser treatment within 5 weeks before the transrectal examination or any S
suit.
previous surgical * Coagulation
treatment of the adenoma. = electrocoagulation or laser coagulation.
in the specimen. Relative contraindicalions may be found in a poor cardiopulmonary status or other concurrent disorders representing an overriding
risk
for
surgery
(iO).
Surgi-
cal treatment can also be refused by the patient. In these cases a combination of piecemeal debulking and further destruction with laser photocoagulation may be an alternative to surgical resection (2,ii). The major drawback of nonsurgical treatment is the lack of complete histobogic examination of the lesion. This lack stresses the need to be optimally informed of the benign nature of the lesion before the start of the therapy. As biopsies are insufficient to rule out malignancy (3,i2-i4), we evaluated the use of transrectal US in tububovilbus adenomas. We expected transrecVolume
185
Number
#{149}
1
tab US to be accurate of carcinoma, because
in the the
detection wall
de-
strucion caused by malignant infiltralion can be visualized (15-i9). In the present study the prevalence of focal carcinoma was only i8% (12 of 66), as malignant lesions detected with endoscopic biopsies or partial polypectomy were already excluded. The fact that 12 carcinomas still remained undetected with endoscopy is explained by the sampling error of the biopsies, especially in large besions. Biopsies often do not extend into the submucosal center of the polyp, which is necessary to diagnose early malignant infiltration (13). Until recently, transrectal US has been the only imaging modality able to depict the intestinal wall layers separately and to allow detection of
rectal
wall
are
promising
as well
(20). As it is not possible to visualize the thin muscularis mucosae with the present imaging technology (6,21), even high-frequency US cannot compete with microscopic evaluation of the resected specimen. This implies that early invasion through the muscularis mucosae into the submucosa may
remain
undetected
with
preop-
erative transrectal US. Such an example in our study is the Ti carcinoma missed with transrectal US: The histobogy report described only two glandular ducts in the submucosa. We agree with other authors that it is not possible
to recognize
an
intramucosal
carcinoma (22,23). We deliberately excluded the presence of lymph nodes from our study. Because transrectal US is able to depict lymph nodes as small as 3 mm in diameter, the visualization of lymph nodes is not a valid parameter; the majority of them will be benign. The discriminating value of US parameters for perirectab lymph nodes has not yet been evaluated in a clinical study. We are convinced that tumor infiltration is a more direct indication of malignancy. As far as we know, only three studies have been published in which transrectal US was used to screen for invasive carcinoma in adenomatous lesions (4,22,24). In two of these studRadiology
#{149} 195
ies the US criterion for malignancy was infiltration into the muscularis propria (22,24). The authors combined the adenomas and Ti tumors into one “benign” group. Although this resulted in a high specificity, the sensitivity was low in both studies (58% and 66%, respectively) compared with 75% in the present study. In comparison with the study by Glaser et al (4) our results are somewhat less favorable, although the inclusion criteria of endoscopic biopsy findings, the transrectal US classification of inifitration, transducer frequency, and even the incidence of malignant inifitration (six of the 31 examined lesions [19%1) were similar to ours (18%). The most remarkable difference was the considerable number of false-positive results in our study (eight of 66), a rate about twice as high as that in the study of Glaser et al (two of 31). The reason for this discrepancy is not readily apparent. One possibility could be artifacts created by the water-filled balloon compressing the polyp into the deeper wall layers. We expected this could create an image suggestive of inifitralion, as was recently confirmed by other authors (24). To overcome this potential problem, we used a modifled scanning technique, in which the rectal lumen and transducer balloon were filled with degassed water. This could not have been a major factor, as false-positive results were encountered in the rest of the study as well. Another explanation for this considerable number of false-positive results may be found in the previous treatment of those patients. It appeared that seven of eight patients with false-positive results had preyously undergone therapy. This ratio differed significantly (P < .01) from the incidence of false-positive results in the rest of the patients with adenoma as the final diagnosis. Four patients with a false-positive result of transrectal US finally underwent treatment with segmental resection. The histopathobogic appearance of two of these benign adenomas suggests a possible basis for the misinterpretation. The inflammatory or probably even fibrotic changes in the layers underneath the adenomatous lesion, as a consequence of the previous therapy, may mimic malignant inifitration during
196
transrectab
Radiology
#{149}
US.
This
finding
stresses the importance of early hansrectal US examination in the diagnostic work-up of the patient. Apart from previous therapy, the location of a polyp near the anal sphincter interfered with imaging. Two of the falsely positive adenomas were located directly behind the anal sphincter. This postanal area is difficult to evaluate (23), partly because of the inability to keep the scanning plane perpendicular to the rectal wall (25,26) and partly because of the short distance between the transducer and the rectal wall immediately above the sphincter. This means that the rectal wall cannot be visualized within the optimal focal range of the transducer, which may result in a blending of the separate layers. Thus, infiltration cannot be exduded. Transrectal lineararray transducers, especially those with an optimal near-field resolution and an axial scanning plane will further improve visualization of this area. In our evaluation of the results of transrectal US, we were aware of the shortcomings in using those adenomas ablated by means of laser as a final diagnosis, because early malignancy might have been eradicated with laser ablation. On the other hand, this may be of limited relevance clinically, as the chosen therapy proved to be appropriate. In addition to Rubesin et al (27), who stated that the radiologist should focus on the detection and determinalion of size of rectal adenomas in an attempt to predict malignancy, we would like to add the even more important
detection
of signs
of infiltra-
lion by means of transrectal US. This is mandatory, especially when nonsurgical therapy of adenomas is considered. The high predictive value for the absence of carcinoma (negative predictive
value,
important treatment
role. Owing interfering
terpretation,
94%)
however,
strengthens
to previous with proper transrectal
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October1992
