Comparison
of high-frequency transabdominal ultrasonography and spiral computed
tomography with colonoscopy in diagnosis of colon cancer
Sumnyan W.1, Komut O.2,
LiguL.3
1Dr. Wangju Sumnyan, Assistant Professor,
Department of Radiology & Imaging, Tomo Riba Institute of Health and
Medical Sciences (TRIHMS), Naharlagun, Arunachal Pradesh, 2Dr. Ojing Komut Assistant
Professor, Department of Surgery, Tomo Riba Institute of
Health and Medical Sciences (TRIHMS), Naharlagun, Arunachal Pradesh, 3Dr.
Leena Ligu, Consultant Gynaecologist, RK
Mission Hospital, Itanagar, Arunachal Pradesh.
Corresponding
Author: Dr. W. Sumnyan, Assistant Professor, Department
of Radiology & Imaging, Tomo Riba Institute of Health and Medical Sciences
(TRIHMS), Naharlagun, Arunachal Pradesh. Email: sumnyanwang@gmail.com, dr.aridita@gmail.com
Abstract
Objective:
To compare high-frequency transabdominal ultrasonography (USG) and spiral
computed tomography (CT) with colonoscopy
in diagnosis of colon cancer. Design: A prospective comparative
study of accuracy of USG and CT scan with colonoscopy. Subjects: Sixty patients
with a clinical suspicion of colon cancer after a detailed clinical history and
a thorough clinical examination were included. Patients with a known diagnosis
of colon cancer or in whom histopathological diagnosis could not be established
were excluded. Methods: All 60 patients who met the inclusion and
exclusion criteria underwent transabdominal USG, CT scan-abdomen & pelvis,
followed by colonoscopy. The CT and USG scans were reported by different
radiologists without previous knowledge of any findingsof the other test or of
the subsequent colonoscopy. The colonoscopy was performed by different
clinicians, none of whom was aware of the USG or CT diagnosis. Result:
Colonoscopy diagnosed 29 patients with colon cancer out of 60 enrolled
patients. USG detected colon cancer in
all the 29 patients with a sensitivity of 100% and a specificity of 87.1%. CT
scan diagnosed colon cancer in all the 29 patients with a sensitivity of 100%
and a specificity of 74.2%. Conclusions: Colonoscopy is still necessary
when a suspicious lesion is identified. However, CT and USG can screen out
suspected patients who can be subsequently referred for colonoscopy.
This would reduce the need for colonoscopy in a large proportion of clinically
suspected patients andalso avoidan invasive procedure like colonoscopy as first
line investigation in elderly patients suspected of having colonic cancer.
Key words: Colorectal cancer, Colonoscopy,
CT scan, Ultrasonography.
Author Corrected: 6 th September 2018 Accepted for Publication: 11th September 2018
Introduction
Colorectal
cancer (CRC) accounts for 10% of all tumour types world wide. It is the third
most common tumour in men and the second in women with higher in males (ratio:
1.4). There is a 10-fold difference in incidence between several regions across
the globe. CRC is the fourth most common cancer-related cause of death (∼8% of all cancer deaths), in
the world [1,2]. A rapid increase in both CRC incidence and mortality are now
observed in many medium-to-high HDI countries particularly in Eastern Europe,
Asia and South America [2].
Malignant
lesions arise from a preexisting adenoma in many cases. The American Cancer
Society has published recommendations for CRC screening according to the stratification
of individuals based on risk. Accordingly, patients are categorized into three
groups: average (age ≥ 50 years), moderate (family history of CRC, personal history
of small adenomatous polyps or CRC) or high risk (inflammatory bowel disease,
family history of familial adenomatous polyposis or nonpolyposis colon cancer).
In spite
of the availability of numerous tests for CRC screening for detecting early stage
cancer or adenomas, there are limitations attached to each procedure.
Colonoscopy is one of the screening tests and is very popular as it has the
advantages of direct visualization of the colonic mucosa and having the option
of taking a biopsy directly from the polyps or lesions. However, colonoscopy is
invasive and require a rigorous bowel preparation which is frequently
unsatisfactory and distressing, especially in the geriatric population. They
often require admission prior to the investigation, which adds up to the
expense. Furthermore, the results are often inconclusive in the geriatric
population due to retained faeces or incontinence. It fails to visualize the
caecum in 5–10% of cases. Computed tomography (CT) colonography is minimally
invasive but has the limitation of a cumulative radiation dose when repeatedly
performed. In spite of certain advantages of requiring no sedation and being
non-invasive, current clinical practice guidelines do not include specific
recommendations on CT colonography for screening. It needs to be established
whether CT colonography is preferable to colonoscopy in this context [3,4].
A detailed
transabdominal USG examination forms an essential part of the investigation of
the abdomen. USG screening can help in the diagnosis of large bowel diseases
like colonic cancer or diverticulosis. It is a safe, widely available, cheap,
noninvasive imaging technique. It allows real-time examination of the abdomen
without the use of any radiation and can be performed at any time. It has a
disadvantage that the evaluation of the bowel depends more on the operator
experience and expertise than the sonographic evaluation of other abdominal
organs [5].
This study
was conducted to determine the accuracy of high-frequency transabdominal USG
and CT colonography compared with colonoscopy in the diagnosis of colon cancer.
Aims and Objectives
To determine the sensitivity and specificity of
high-frequency transabdominal ultrasonography and Computed tomography in the
diagnosis of colon cancer compared with Colonoscopy.
Materials & Methods
A prospective comparative study was done at the Department
of Radiology, RK Mission Hospital, Itanagar, Arunachal Pradesh to compare the
sensitivity and specificity of high-frequency transabdominal ultrasonography
and CT scan with colonoscopy in the diagnosis of colon cancer in patients
clinically suspected of having the disease from September 2016 to June 2018.
A total of 60 patients were included in the study sample.
Inclusion and exclusion criteria were as follows:
Inclusion criteria- Patients with a clinical
suspicion of colon cancer after a detailed clinical history and a thorough
clinical examination. The major clinical complaints included history of
alteration in bowel habits, melena, rectal bleeding, abdominal cramps, presence
of abdominal lump, and other complaints specific for colon cancer. The clinical
examination stressed on the presence of palpable abdominal lump.
Exclusion criteria- Patients with a known
diagnosis of colon cancer or in whom histopathological diagnosis could not be
established were excluded from the study.
All 60 patients who met the inclusion and exclusion criteria
underwent transabdominal sonography, CT scan-abdomen & pelvis, followed by
colonoscopy. The CT and USG studies were reported by different radiologists
without knowledge of the findings of the other study or of the subsequent
colonoscopy. The colonoscopy was performed by a number of different clinicians,
none of whom was aware of the USG or CT diagnosis.
Institutional ethics committee approval was obtained before
the study. An informed, bilingual, written consent was obtained before
including the patients as study subjects.
Procedure- A standard ultrasound
scanner (ACUSON X300, SIEMENS) with a selection of transducers from 3.0 to 10.0
MHz was used for the transabdominal ultrasonography in all patients. A complete
abdominal and pelvic scan was performed using appropriate low frequency
transducers followed by specific examination of the colon using the high-frequency
transducers. An attempt was made in all the patients to identify the whole
extent of the colon with slight compression wherever necessary. The sonographic
criteria used for diagnosis of a possible colon carcinoma were [1] a localized
and irregular thickening of the colonic wall with heterogenous low echogenicity
[2], an irregular contour [3], a lack of demonstrable movement or change of
configuration of the bowel on real-time scanning, and [4] absence of wall
stratification [6].
CT scan was performed using DEFINITION PERSPECTIVE 128 SLICE
(SIEMENS, GERMANY) with 5 mm thick slices at a pitch of 1.5 through the whole
abdomen and pelvis. A total of 60 ml of iodine-based IV contrast agent (60%)
was administered manually just before the start of the CT scan. Neither rectal
air nor contrast medium was used, as this would have been unpleasant for the
patient, and introduced the problem of incontinence. The diagnostic appearance
of colonic cancer was, typically, of a circumferential or focal mass with an
uneven, lobulated configuration [7].
The patient then underwent routine bowel preparation with
colonoscopy performed the following day. A colonoscopy diagnosis of malignancy
was confirmed by biopsy.
Results
This prospective study was done betweenSeptember 2016 to
June 2018and enrolled 60 patients during this period. All these 60 patients
with clinical suspicion of colon cancer underwent ultrasonography, computed
tomography and colonoscopy.
Of the 29 patients who had colon cancer, 18 (62%) were males
and 11 (38%) were females. The age range of patients varied from 19 years to 80
years. The mean age of the patients was 52.2 years [Table 1].
Table-1: Age distribution among
subjects
Age group |
No. of cases |
<20 yrs |
1 |
20 - 30 yrs. |
2 |
30 – 40 yrs |
5 |
40 – 50 yrs |
4 |
50 – 60 yrs. |
7 |
60 – 70 yrs |
4 |
≥71 yrs |
6 |
Table-2: Site distribution of colon
cancer among subjects
Site |
No. of cases |
Percentage |
Cecum |
3 |
10.3% |
Ascending colon |
5 |
17.2% |
Hepatic flexure |
1 |
3.4% |
Transverse colon |
4 |
14% |
Splenic flexure |
1 |
3.4% |
Descending colon |
2 |
7% |
Sigmoid colon |
4 |
14% |
Recto sigmoid region |
9 |
31% |
Total |
29 |
100% |
Table-3: Comparison of Ct and USG
detection of colon cancer
Investigation |
True +ve |
True -ve |
False +ve |
False -ve |
Sensitivity % |
Specificity % |
PPV % |
NPV % |
CT |
29 |
23 |
8 |
0 |
100% |
74.2% |
78.4% |
100% |
USG |
29 |
27 |
4 |
0 |
100% |
87.1% |
87.9% |
100% |
The most common clinical
presentation was that of an alteration in bowel habits with predominance of
constipation (90%). The other major complaints included melena, abdominal
cramps, and rectal bleeding.
Colonoscopy was significantly abnormal in 30 of the 60
patients (50%). Colon cancer was visually diagnosed by colonoscopy in 29 of
these patients and malignancy was confirmed by histology in all cases (48.3%).
One patient had features suggestive of ulcero-proliferative colitis, which on
histology was shown to have nonspecific colitis. Colonoscopy could be passed
beyond the visualized growth in only 9 of the 29 patients who had colon cancer.
Large obstructive growth prevented the passage of the colonoscope proximally in
the 20 patients.
The commonest presentation of colon cancer on
ultrasonography was that of an echo poor focal/asymmetrical bowel thickening.
Ultrasonography correctly diagnosed colon cancer in all the 29 patients with no
false negatives but four false positives. In one false positive case deserves
ultrasonography erroneously suggested a growth involving the sigmoid colon.
This turned out to be a growth arising from the small bowel and the histologic
diagnosis of the operated specimen proved to be suggestive of leiomyosarcoma.
Computed tomography correctly diagnosed colon cancer in all
the 29 cases. There were no false negatives but eight false positives. Three
false positives were in the cecum, two in the ascending colon and three in the
rectosigmoid region, suggesting that particular care is needed in interpreting
the bowel in these regions. The commonest CT presentation of colon cancer was
that of an asymmetrical wall thickening occurring in 25 (86%) patients. Focal
mass was the presentation in the other 5 (14%) patients. CT also correctly
detected the small bowel mass that turned out to be leiomyosarcoma.
On ultrasonography, the wall thickness of the colon growth
varied from 0.9 cm to 6.5 cm, with a mean wall thickening of 2.0 cm. The wall thickness
on Computed tomography ranged from 1.1 cm to 6.5 cm, with a mean value of 2.2
cm. The mean value of wall thickening in colon cancer appeared more on CT than
on ultrasonography by 0.2 cm.
There were thus 29 colonoscopically diagnosed and histologically
proven cancers in the 60 patients who had all three investigations completed.
Nine were in the recto sigmoid region, four at the sigmoid colon, two in the
descending colon, one in the splenic flexure, four in the transverse colon, one
in the hepatic flexure, five in the ascending colon, and three in the cecum
[Table 2].
Ultrasonography detected colon cancer in all the 29 patients
with a sensitivity of 100% and a specificity of 87.1%. USG provided additional
useful information in five patients. Computed tomography diagnosed colon cancer
in all the 29 patients with a sensitivity of 100% and a specificity of 74.2%.
CT provided additional useful information in six patients [Table 3].
Discussion
Several studies discussing the use of transabdominal USG in the
diagnosis of colonic cancer have been published. Some advocated the limited use
of USG in specific situations, for example as a supplement to barium enema
where the cecum was poorly seen [8] or in the Accident and Emergency department
[9,10].
Jeremy Price and Constantine Metreweli, in 1988 concluded
that ultrasound is a useful primary diagnostic technique for colonic neoplasms,
with a predictive value of 79% in detecting clinically non-palpable lesions.
This study involved 1700 abdominal ultrasound scans over a period of 2 years,
including a search for bowel disease in the scanning routine [11].
In another study, Shirahama et al [6] in 1994 described four
sonographic patterns that allowed correct diagnosis of colonic carcinoma in 90%
of patients as used in this study and described in the methods in this paper.
Colonoscopy was used to confirm the USG diagnosis of colonic cancer in the
study.
Several studies have used orally or rectally introduced
water in an attempt to improve visualization of the colon. The single study
using oral administration of water, termed “sono-enterocolonography”, was
performed on 56 patients who had already undergone BE, followed by colonoscopy
in those with abnormal findings [12]. This gave a sensitivity for lesions
larger than 10 mm of 89% but has not been repeated. Two studies used rectally
introduced water, termed “hydrocolonic-sonography” [13, 14]. Despite giving
good results, this involves colonic instillation of up to 1500 ml of water,
which strongly decreases the advantage of this technique in the elderly
population. The larger of these studies [14] compared transabdominal USG,
hydrocolonic-sonography and colonoscopy. The specificity of transabdominal USG
for the detection of colon cancer was 99% and sensitivity was 33%. The results
of hydrocolonic-sonography appear very good, with a sensitivity for cancer of
97% and of 91% for polyps of 7 mm or greater in diameter. Unfortunately, these
results were not duplicated in another study [15] which compared
hydrocolonic-sonography with colonoscopy and found a sensitivity for cancer
detection of 0% and for polyps of 7 mm or greater of 12.5%. The marked
discrepancy between the two centres is difficult to explain but, even if the
accuracy of the technique were confirmed, it is just as invasive as barium enema
(BE) with its attendant problems in the elderly.
W K Loftus et al. in 1999 concluded that both transabdominal
ultrasound and CT are possible alternatives to colonoscopy in the investigation
of symptomatic patients with suspected colonic cancer. USG had a sensitivity
and specificity of 100% and CT a sensitivity of 100% and a specificity of 84%.
USG and CT were poor at detecting polyps. If the detection of polyps greater
than 2 cm is included, then USG sensitivity falls to 67% and CT sensitivity
falls to 89% and specificity rises to 88% [16].
Transabdominal USG in our study detected colon cancer in all
the 29 patients with a sensitivity of 100% and a specificity of 88.6%. It also
demonstrated the adjacent visceral invasion and provided other useful
information in 5 patients.
A number of studies have used CT in the detection of colonic
cancer. A retrospective review of pre-operative CT using an early generation
scanner showed a sensitivity of 84% in detecting histologically proven cancers
[7]. Two studies from one centre specifically applied the use of CT to the
elderly. BE was used as the gold standard in one study [14], which found that
CT had a sensitivity of 100% and specificity of 86% in detecting cancer, very
similar to our study. From the study, J. J. Day et al. in 1993, concluded that
CT should be the initial investigation of the large bowel in the frail elderly
patients requiring inpatient bowel preparation; the more unpleasant BE could be
reserved for those cases where CT is equivocal or severe symptoms are
unexplained [4]. CT alone was performed in a second study from the same centre
[17].
None of the patients with normal CT had confirmatory BE or
colonoscopy and nor did over half of those thought to have cancer. As a result,
it is not possible to make any statistical assessment from this study. The
technique used in these two studies, however, had considerable advantages for
the elderly patient in that only oral contrast medium was used without routine
IV contrast medium or rectal contrast medium or air. Bowel preparation was not
used in either of the studies.
W K Loftus et al. in 1999 concluded that both transabdominal
ultrasound and CT are possible alternatives to colonoscopy in the investigation
of symptomatic patients with suspected colonic cancer. USG had a sensitivity
and specificity of 100% and CT a sensitivity of 100% and a specificity of 84%.
USG and CT were poor at detecting polyps. If the detection of polyps greater
than 2 cm is included, then USG sensitivity falls to 67% and CT sensitivity
falls to 89% and specificity rises to 88% [18].
Okizuka H, et al. in 1995 demonstrated cancer in 89% of
cases, using ultrafast CT with IV contrast medium [19].
Two studies in 1996 introduced the use of CT colonography as
a technique in the evaluation of the colon [20,21]. The results in both studies
were promising but the use of a bowel preparation and problems in retaining the
air means that they are poorly suited to the elderly population. Computed
tomographic (CT) colonography is a rapidly evolving technique that enables two-
and three-dimensional views of the surface of the colon. In current clinical
practice, CT colonography is used to evaluate those segments of the colon that
are not visible as a result of incomplete colonoscopy and also to evaluate the
colon proximal to an obstructing carcinoma [22, 23, 24].
Our study used both iodinated oral contrast (2% to 3%) and
iodine-based intravenous contrast medium (60%). Full opacification of the colon
was achieved in only 60% of the patients. The oral contrast medium could be
taken over a longer period with improved bowel opacification, ideally by
starting the oral contrast preparation the night before the CT scan was
performed. Bowel opacification can also be improved by administrating gastric
hurrying agents like metoclopramide along with the oral contrast medium. The
problem of incontinence did not occur as neither rectal contrast medium nor air
was used. No serious adverse reaction was reported with the use of IV contrast
medium. However, 3 (5%) of the 60 patients complained of vomiting and 2 (3.3%)
had amild rash. CT detected all cancers found at colonoscopy with a sensitivity
of 100% and a specificity of 77.5%. False positives were primarily due to
faecal material giving the impression of a mass lesion.
Colonoscopy, itself, is not adequate in all the patients. In
patients having consecutive colonoscopies on the same day, the second study
found polyps larger than 1 cm, which was missed on the first colonoscopy, in 6%
[25].
Conclusion
This study shows that transabdominal USG and CT are useful
in the diagnosis of colonic cancer in symptomatic patients. It supports the
previous studies that demonstrated the suitability of these radiological
investigations in the evaluation of colonic cancer.
Both techniques avoid the bowel preparation and the possible
admission required for colonoscopy or BE in the elderly. CT has the
disadvantage of a higher false positive rate. Both the techniques were
sensitive for the mean diameter of cancers diagnosed in this study but smaller
lesions may well be missed. It is not suggested that either technique is useful
for screening asymptomatic patients but, although numbers were relatively
small, this study showed good results in diagnosing colonic cancers in those
patients with symptoms. Review of the combined findings of USG and CT with the
occasional repeat study, should further improve results. Colonoscopy is still
necessary when a suspicious lesion is identified. However, CT and USG can
screen out suspected patients who can then be referred for colonoscopy. This
would reduce the need for barium enema and colonoscopy in a large proportion of
clinically suspected patients and yet no carcinoma would be missed. This
implies that significant savings could be made by using USG or CT rather than
colonoscopy as the first line investigation in elderly patients suspected of
having colonic cancer.
Relevance of the Study: This study re-emphasizes
the roles of CT scan and ultrasound in diagnosis of colon cancer in symptomatic
patients in a resource limited settings. Very few studies have been conducted
in remote centers with limited resources. This study justifies the usage of CT
scan and USG in these settings.
Authors contribution
1.
Dr Wangju Sumnyan: Study concept and design
and investigator of the study.
2.
Dr OjingKomut: Study concept and
design, co-investigator
3.
Dr Leena Ligu: Study concept and drafting
the work.
Acknowledgement- We acknowledge the
contribution of Dr Aridita Datta for
helping us in writing the manuscript of this paper.
References
1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C,
Rebelo M et al. Cancer incidence and
mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int.
J. Cancer.2015 Mar;136(5): E359-86.doi:
10.1002/ijc.29210.[pubmed]
2. Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal
A, Bray F. Global patterns and trends in colorectal cancer incidence and
mortality. Gut.2017;66(4):683-91. doi: 10.1136/gutjnl-2015-310912.[pubmed]
3. Martın-Lopez JE, Beltran-Calvo C, Rodrıguez-Lopez R,
Molina-Lopezl T. Comparison of the accuracy of CT colonography and colonoscopy
in the diagnosis of colorectal cancer. Colorectal Disease. 2014 Mar; 16(3):
O82–9.doi: 10.1111/codi.12506.[pubmed]
4.
Day JJ, Freeman AH, Coni NK, Dixon AK. Barium enema or computed
tomography for the frail elderly patient? Clin Radiol .1993 Jul; 48:
48-51.doi: https://doi.org/10.1016/S0009-9260(05)80108-4.[pubmed]
5. Bor R,Fabian A,Szepes Z. Role of ultrasound in colorectal
diseases.World J Gastroenterol. 2016 Nov ; 22(43): 9477–87.doi: 10.3748/wjg. v22.i43.9477.[pubmed]
6. Shirahama M, Koga T, Ishibashi H, Uchida S, Ohta Y.
Sonographic features of colon carcinoma seen with high-frequency transabdominal
ultrasound. J Clin Ultrasound.1994 Jul-Aug;
22(6):359-65.https://doi.org/10.1002/jcu.1870220602.
7. Balthazar E J, Megibow A J, Hulnick D, Naidich DP.
Carcinoma of the colon: Detection and preoperative staging by CT. AJR. 1988 Feb
; 150(2):301-6.DOI: 10.2214/ajr.150.2.301.[pubmed]
8. Owens AP, Banerjee B, Morewood DJW: Sonography as an aid
to diagnosis of caecal carcinoma in the elderly. Clin Radiol. 1983 Nov;
34:669-72.[pubmed]
9. Sianesi M, Rossi A, Miselli A, Farinon AM. Ultrasonic
detection of colonic carcinoma in emergency. Dis Colon Rectum.1984 Mar;
27(3):168-71.[pubmed]
10. Khoo HT. The ultrasonic demonstration of colonic
carcinoma. Aust Rdiol .1981 Mar;25(1):23-30.[pubmed]
11. Price J,Metreweli C. Ultrasonographic diagnosis of
clinically non-palpable primary colonic neoplasms. BJR .1988;61(723):190-5.DOI:
10.1259/0007-1285-61-723-190.
12. Hirooka N, Ohno T, Misonoo M, Kobayashi C, MushaH,. Mori
H, et al. Sono-enterocolonography by oral water administration. J Clin
Ultrasound .1989 Oct;17(8): 585-9.[pubmed]
13. LimbergB.Diagnosis of large bowel tumors by colonic
sonography. Lancet.1990 Jan; 335(8682):144-6.[pubmed]
14. Limberg B. Diagnosis and staging of colonic tumors by
conventional abdominal sonography as compared with hydrocolonic sonography. N
Engl J Med. 1992; 327:65-9.
15. Chui DW, Gooding GA, McQuaid KR,Griswold V,Grendell JH.
Hydrocolonic ultrasonography in the detection of colonic polyps and tumors. N
Engl J Med.1994 Dec; 331 (25):1685-8.DOI: 10.1056/NEJM199412223312504.[pubmed]
16. W K Loftus, C Metreweli, Sung JJ, Yang WT, Leung VK, Set
PA.Ultrasound, CT and colonoscopy of colonic cancer. Br JRadiol .1999
Feb;72(854):144-8.doi: 10.1259/bjr.72.854.10365063.[pubmed]
17. Fink, M., Freeman AH, Dixon AK,Coni NK. Computed tomography of the colon in elderly
people. Br Med J. 1994; 308(6935):1018.[pubmed]
18. Loftus WK, Metreweli C, Sung JJ, Yang WT, Leung VK, Set
PA. Ultrasound, CT and colonoscopy of colonic cancer. Bri J Radiol. 1999 Feb;
72(854):144-8.[pubmed]
19. Okizuka H, Sugimura K, Shinozaki N, Watanabe K.
Colorectal carcinoma: evaluation with ultrafast CT. Clin Imaging .1995 Oct-Dec;
19(4):247–51.[pubmed]
20. Amin Z, Boulos PB, Lees WR. Technical report: spiral CT
pneumocolon for suspected colonic neoplasms. Clin Radiol. 1996 Jan;
51(1):56–61.[pubmed]
21. Hara AK, Johnson CD, Reed JE, Ahlquist DA, Nelson H,
Ehman RL, McCollough CH, Ilstrup DM. Detection of colorectal polyps by computed
tomographic colography: feasibility of a novel technique. Gastroenterology.1996
Jan; 110(1):284-90.[pubmed]
22. Macari M, Berman P, Dicker M, Milano M, Megibow AJ.
Usefulness of CT colonography in patients with incomplete colonoscopy. AJR Am J
Roentgenol .1999 Sep; 173(3):561-4. DOI: 10.2214/ajr.173.3.10470879.[pubmed]
23. Morrin MM, Kruskal JB, Farrell RJ, Goldberg SN, McGee
JB, Raptopoulus V. Endoluminal CT colonography after incomplete endoscopic
colonoscopy. AJR Am J Roentgenol .1999 Apr; 172:913-8.doi:
10.2214/ajr.172.4.10587120
24. Fenlon HM, McAneny DB, Nunes DP, Clarke PD, Ferrucci JT.
Occlusive colon carcinoma: virtual colonoscopy in the preoperative evaluation
of the proximal colon. Radiology. 1999 Feb; 210(2):423-8.DOI:
10.1148/radiology.210.2. r99fe21423.
25. Rex DK, Cutler CS, Lemmel GT, Rahamani EY, Clark DW,
Helper DJ, et al.Colonoscopic miss
rates of adenomas determined by back-to-back colonoscopies.
Gastroenterology.1997 Jan; 112(1):24-8.[pubmed]