Flat lesions missed at conventional
colonoscopy (CC) and visualized by CT
colonography (CTC): a pictorial essay
Francesca Coppola,
1Daniele Regge,
2Nicola Flor,
3Dimitris Papadopoulos,
1Rita Golfieri
11Radiology Unit, Department of Digestive Disease and Internal Medicine, S. Orsola Malpighi Hospital, Bologna, Italy 2Radiology Unit, IRCC, Candiolo, Turin, Italy
3Radiology Unit, San Paolo Hospital, Milan, Italy
Abstract
The purpose of this study is to describe our experience with cases of false negative findings at conventional colonoscopy (CC) that were identified by CT colonog-raphy (CTC). Conventional colonoscopy (CC) is the universally accepted gold-standard technique for the diagnosis of colonic polyps and cancers, however occa-sionally this method can generate false negative findings. We present examples of false negatives at CC, correctly identified by CT colonography (CTC), and later con-firmed at a second endoscopy, describing the reasons of false negative, when possible.
CT colonography is a highly sensitive technique for polyps and colorectal cancer (CRC) detection [1] across a broad spectrum of accepted indications and protocols (prepa-ration, fecal tagging, CO2automatic insufflation,
hypot-onization). Its sensitivity is high especially for detecting polyps greater than 10 mm; however, CTC is less accurate than CC for small and diminutive polyps [1–4].
However, when CC is performed by inexperienced operators and non-gastroenterologists or when lesions have atypical morphologies disappointing low sensitivities may occasionally be reported [5]. The commonalities of typical lesions missed at CC usually concern their location and shape: false negative results can be generated when incomplete colonoscopies are performed (cecum not reached), when lesions are hidden behind haustral folds or when they are flat or present atypical morphologies. On
the other side, typical lesions missed at CTC are usually located in the rectosigmoid colon and in the splenic flex-ure, due to a minor effect of the insufflation in this seg-ments [1]. Right colon is usually easier to distend and consequently evaluate at CTC, while the increased dis-tance in CC makes right colon assessment more difficult. For the above reported reasons CT colonography and CC should be considered equivalent in terms of sensitivity in CRC detection and complementary [1].
Flat lesions
The majority of CRCs develop from adenomatous pol-yps following the adenoma–carcinoma sequence; the remaining do not follow this developing pattern [6–8]. Many experts believe that flat neoplasms may be the precursor lesions accounting for a significant proportion of these cancers [8]. Suzuki et al. [9] reported that flat cancers represent approximately 70% of T1 lesions and up to 10% of all cancers (in 1,026 patients).
The identification of superficial small invasive cancers without an adenomatous component has introduced the concept of colorectal cancer coming ‘‘de novo’’ [10] and studies also suggested that flat lesions could be more aggressive than non-flat adenomas [11–13].
Previous works on the sensitivity of CTC for non-polypoid lesions used the term flat lesion when the height was less than half the lesion diameter [14–17].
There are different positions in the literature regard-ing the prevalence and the potential malignant evolution of flat lesions. Some Japanese studies reported a high incidence of high-grade dysplasia in flat adenomas, especially in the depressed ones [9]. Suzuki et al. [9] demonstrated that 10% of cancers had a flat shape with diameter ranging from 8 to 15 mm.
Correspondence to: Francesca Coppola; email: francesca.coppola@ aosp.bo.it
ª Springer Science+Business Media New York 2013 Published online: 13 December 2013
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Abdom Imaging (2014) 39:25–32 DOI: 10.1007/s00261-013-0052-2
The malignant potential of flat lesions has not been shown in Western studies [12].
Pickhardt et al. [18] showed a prevalence of flat le-sions at CTC of 4.2% (59 total lele-sions in 52 of 1,233 patients) in an asymptomatic population screening; among the 59 flat lesions, 29 (49.2%) were adenomatous, 5 of which advanced (8.5%) and only one big flat lesion
Fig. 2. 3D visualization of a 2.5-cm ‘‘saddle-shape lesion’’ with a central depression.
Fig. 3. The lesion was confirmed at a second CC performed immediately after CTC. The lesion was found in the same position and with the same morphology described at CTC. Hemicolectomy was performed and adenocarcinoma with low grade of cellular differentiation was diagnosed at pathological examination.
Fig. 1. A 51-year-old man, with a positive fecal occult blood test (FOBT) participating to colorectal cancer (CRC) screen-ing program. CC was interrupted when the endoscope reached the splenic flexure due to reduced tolerance of the patient. A CTC performed after the incomplete CC showed a large atypical lesion, a ’saddle shape lesion’, in the distal sigmoid colon, close by the rectum. A–C Axial and coronal CTC: visualization of the lesion located in the distal sigmoid tract. CAD (Im3D CAD; Turin, Italy) used as a second reader confirmed the presence of the lesion.
was malignant. Rembacken et al. [13] showed that lesions smaller than 1 cm in size, both flat and non-flat, rarely had neoplastic focuses.
Some investigators suggested that the variation in the incidence of high-grade dysplasia in flat lesions between Eastern and Western countries may be secondary to differences in pathology reports. Japanese pathologists diagnose higher grades of dysplasia [6, 19] because en-doscopists use chromoendoscopic techniques which are more sensitive than traditional CC to detect flat lesions [11]. These techniques are now widely used in Western
countries to improve the detection of flat lesions in endoscopic screening programs [20].
The clinical importance of flat adenomas remains unclear. The natural progression of these lesions is unknown and the size associated to an increased risk of malignancy is controversial as some investigators reported a higher risk of malignancy only with larger lesions [21].
Fig. 5. 3D endoluminal assessment shows the flat polyp on a fold of the ascending colon.
Fig. 6. Following the CTC finding the patient underwent a second CC, which did not detect the flat lesion. Eight months later the patient underwent a third CC, with the radiologist present in the endoscopy room. This last exam confirmed the flat lesion of the right colon and mucosectomy was performed. The final diagnosis was a serrated adenoma, with foci of adenocarcinoma. The patient underwent right hemicolec-tomy.
Fig. 4. A 73-year-old woman with diverticulitis performed CC. Due to acute inflammation the endoscope did not bypass the sigmoid colon. The 2D axial scan of the CTC study performed after the incomplete CC identified a 1.5-cm
flat polyp in the right colon with high diagnostic confidence. A–C Axial CTC: visualization of the lesion located in the ascending colon, in the supine, right lateral and prone scan, respectively.
Endoscopically, flat and depressed lesions are de-scribed as non-exophytic, flat, and/or depressed mucosal lesions with a height less than half the diameter of the lesion and they are usually located in the ascending co-lon. According to the Japanese Research Society classi-fication of colorectal lesions, slightly depressed lesions (type IIc) and flat elevated with depression lesions (type
IIa/IIc) (Figs.1, 2, 3) have a higher likelihood of har-boring a carcinoma with submucosal invasion than flat elevated lesion (type IIa) (Figs.4, 5, 6). Laterally spreading tumors (LST) (Figs.7,8,9) are distinguished from other flat and depressed lesion by their size (greater than 10 mm in diameter). LST can be divided in granu-lar-type LST (with superficial spreading nodules forming a flat and broad lesion) (Figs.10, 11, 12) and flat-type LST (smaller than granular-type and usually located in the right colon). Flat-type LST have shown a higher incidence of developing a carcinoma with submucosal invasion than granular-type LST (Figs.13, 14, 15, 16). Serrated adenomas can be hardly recognizable endo-scopically as they can present as flat lesions, but with sizes that can vary from a few millimeters to several centimeters, resulting in difficult diagnosis. Histopatho-logic examination is required as several reports have described a correlation with serrated adenoma and invasive adenocarcinoma [22–24].
We describe five patients with flat colonic lesions missed at CC and visualized at CTC. All lesions were visualized at both 2D and 3D analyses, while computer-aided diagnosis (CAD) software correctly identified only three of them.
The preparation for the exam consisted in low fiber diet and PEG; fecal tagging was obtained with 50 mL of Gastrografin and 500 mL of H2O 3 h before the
exami-nation. Colonic distension was obtained by insufflating 3 or more L of CO2 with an automatic insufflator
fol-lowing intramuscular injection of hyoscine-butyl-bro-mide. Intravenous contrast (IV) was not used.
Fig. 8. 3D visualization of the lesion localized between two haustral folds. CC was recommended.
Fig. 7. A 66-year-old woman with positive FOBT participat-ing to a CRC-screenparticipat-ing program. Due to contraindications to CC for comorbidity (two coronary aortic by-pass, arterial hypertension, previous sigmoidectomy for diverticular dis-ease), CTC was recommended. A CTC detected a 2.5-cm
‘‘lateral spreading lesion’’ in the ascending colon, close to ileocecal-valve. Second reader CAD confirmed the atypical lesion of the right colon. B In the prone scan the lesion, highlighted by a thin layer of Gastrografin, is more easily recognizable.
Summary
CTC is a highly sensitive technique for detection of colorectal lesions (polyps and cancers), when both cathartic and tagging agents are used in combination for bowel preparation. CTC has a small chance to miss atypical and right-sided colonic lesions, in particular
when all colonic segments are well distended. CC can miss lesions in the right colon when it is incomplete (cecum not reached) or when the lesions have atypical morphologies, or if it is performed by inexperienced operators or non-gastroenterologists.
In case of colonic lesions diagnosed by CTC with high diagnostic confidence and not confirmed by CC, it is
Fig. 10. A 78-year-old woman with a negative FOBT examination and without familiar history of CRC. CTC was performed to evaluate the extent of diverticular disease. Beside a severe grade diverticular disease, the radiologist
detected an asymmetric focal parietal thickening of the right rectal wall causing mild lumen stenosis (A). B Axial CTC. Visualization of the right rectal thickening in the prone scan.
Fig. 9. The endoscopic examination, performed under anaesthesia, did not immediately identify the lesion, because it was localized behind a fold. Due to the presence of the radiologist in the endoscopic room, the endoscopist confirmed the lesion at
the second check (A). The flat lesion was removed during the same endoscopic session with ‘‘piecemeal technique’’ and dia-thermic coagulation (B). Histological examination diagnosed a tubular-villous polyp with low grade dysplasia.
Fig. 11. Sigmoidoscopy was recommended and confirmed the presence of rectal substenosis without mucosal abnor-malities; biopsies were taken at the level of the stenosis, yielding a pathological diagnosis consistent with tubular adenoma, with low grade dysplasia.
Fig. 12. Owing to the discrepancies between negative CC and pathological diagnosis, a second CC was performed one month later, by the same endoscopist using chromoendos-copy which revealed a large mucosal lesion on the right rectal wall, close to the substenotic segment which could not be completely removed by mucosectomy. Multiple biopsies were taken and pathologic examination revealed a serrated ade-noma.
Fig. 15. A second colonoscopy was recommended. CC confirmed the flat lesion in the same place and with the same morphology and size described at CTC. Notice the corre-spondence between the 3D endoluminal view and the CC vision of the lesion.
Fig. 14. A, B 3D endoluminal visualization of the lesion. Fig. 13. A 66-year-old man, with a negative FOBT exami-nation, a history of polypectomy and a recent incomplete performed CTC. The exam visualized a 1.9-cm flat lesion on the rectal back wall. A–C Axial, sagittal, and coronal view of the lesion with a soft tissue and bone window. Im3D CAD, used as second reader, confirmed the lesion.
b
mandatory to repeat CC in the presence of a radiologist or, at least, considering the correct location and shape of the lesion, as reported at CTC.
CTC is complementary to CC for the detection of atypical shaped and right-sided colonic lesions.
Conflict of interest The authors do not have any competing interest to be disclosed.
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Fig. 16. The lesion was endoscopically removed. Pathologic examination revealed a tubulovillous adenoma with low grade dysplasia.
