Introduction
Surveillance colonoscopy is critical to managing large (≥ 20 mm) non-pedunculated
colorectal polyps (LNPCPs) after endoscopic mucosal resection (EMR) as it allows for
the identification and treatment of residual or recurrent polypoid tissue [1 ]
[2 ]. This is predicated on recognizing the post-EMR scar. To facilitate its identification,
sterile carbon particle suspension can be used to create an intraluminal tattoo. However,
it is not biologically inert and can precipitate clinically relevant adverse outcomes
[3 ]
[4 ]
[5 ].
Although current consensus guidelines provide recommendations, they are largely based
on expert opinion, with no evidence available on whether tattoo placement facilitates
scar identification [3 ]
[4 ]. Therefore, we evaluated the ability of simple easy-to-use optical evaluation criteria
to detect the post-EMR scar [6 ], with or without tattoo placement, in a prospective observational cohort of LNPCPs
referred for endoscopic resection.
Method
The Australian Colonic Endoscopic Resection (ACE) study
The Australian Colonic Endoscopic Resection (ACE) study (clinicaltrials.gov identifier:
NCT01368289) is a prospectively collected, multicenter, observational cohort of consecutive
patients referred for the management of LNPCPs ≥ 20 mm (July 2008 to present). Center-specific
Institutional Review Board approval is maintained at each center. Written informed
consent is obtained from each patient prior to study participation.
Consecutive LNPCPs (July 2008 to October 2019) that underwent successful EMR and first
surveillance colonoscopy (SC1), as recommended at 6 months after the index EMR, at
one ACE site were included for this analysis.
Endoscopic mucosal resection technique
A standardized, previously described, inject and resect EMR technique was used [7 ]
[8 ]. All endoscopic procedures were performed by a study investigator (an accredited
gastroenterologist with advanced training and an established tertiary referral practice
in colorectal EMR) or a senior interventional endoscopy fellow under supervision.
Antiplatelet and anticoagulation medications were withheld pre-procedure, in accordance
with consensus recommendations [9 ].
Currently, all colorectal EMRs are performed using high definition Olympus 190 series
variable stiffness colonoscopes (Olympus, Tokyo, Japan). Carbon dioxide is used for
insufflation [10 ]. After lesion identification, optical evaluation under high definition white-light
endoscopy and narrow-band imaging (NBI) is performed to exclude features of submucosal
invasive cancer (SMIC). In a systematic fashion, a submucosal cushion is created with
injection of succinylated gelatin (Gelofusine; B. Braun, Bella Vista, Australia) with
0.4 % indigo carmine and 1:100 000 epinephrine. A microprocessor-controlled generator
(ERBE VIO; Endocut Q, effect 3; ERBE, Tübingen, Germany) is used, with snare excision
being performed [8 ].
After complete resection of the LNPCP, the defect is carefully examined to ensure
no polypoid tissue remains and to assess for deep mural injury (DMI) [11 ]. Areas of significant injury (DMI III–V) are subsequently treated by mechanical
clip closure. Thermal ablation of the resection margin to mitigate the risk of recurrence
is performed using snare-tip soft coagulation (ERBE VIO; Soft coagulation, 80 W, effect
4; ERBE) to create a rim of ablated tissue of 2–3 mm. Clinically significant intraprocedural
bleeding is treated with coagulation forceps or mechanical hemostasis. A tattoo may
be placed distal to the EMR defect as deemed appropriate by the proceduralist. Resection
specimens are collected and evaluated by specialist gastrointestinal pathologists.
Where appropriate, histopathology is confirmed with surgical specimen evaluation.
Surveillance colonoscopy
Prior to SC1, the report and images from the index EMR are reviewed, with the location
and colonic segment of the resected LNPCP being noted. The relationship to relevant
structures such as haustral folds are noted, where appropriate. Once the colonoscope
is in the expected vicinity of the post-EMR scar, patients undergo standardized evaluation
using high definition white-light endoscopy and NBI. After identification of the scar,
previously reported, simple, and easy-to-use optical evaluation criteria are used
for endoscopic confirmation [6 ]. In detail, the scar may be identified as a pale area with disruption of the normal
colonic surface microvasculature and pit pattern, and there may be convergence of
the surrounding mucosal folds ([Fig. 1 ]). Closer inspection of a bland scar with NBI typically demonstrates a non-neoplastic
pit pattern, as opposed to the neoplastic pit pattern seen with residual or recurrent
polypoid tissue. Biopsies are routinely performed.
Fig. 1 Example images of post-endoscopic mucosal resection scars on high definition white-light
endoscopy and narrow-band imaging.
Statistical analysis
Prospectively collected data included: (1) patient characteristics, including age,
sex, and American Society of Anesthesiologists (ASA) classification; (2) lesion characteristics,
including size, location, morphology, surface granularity, Kudo pit pattern, histopathology,
and tattoo placement; and (3) procedure outcomes, including technical success, periprocedural
adverse events, recurrence, and referral for surgery.
The primary outcome was scar identification, stratified by the presence of a tattoo.
Further stratifications by lesion size (20–39 mm, ≥ 40 mm) and histopathology (adenomatous,
serrated) were performed.
SPSS version 26.0 (IBM, Armonk, New York, USA) was used for data analysis. Variables
were analyzed per participant. If two or more eligible lesions were identified in
a single participant, the largest lesion was selected for analysis. Continuous variables
were summarized as median (interquartile range [IQR]). Categorical variables were
summarized as frequencies (%). All analyses were exploratory and two-tailed tests
with a 5 % significance level were used throughout. Fisher exact tests were used to
test for associations between categorical variables.
Results
Between July 2008 to October 2019, 1023 LNPCPs in 1023 patients underwent both successful
EMR and SC1 ([Fig. 2 ]). The median patient age was 69 years (IQR 62–75 years) and 535 (52.3 %) were men
([Table 1 ]). The median lesion size was 35 mm (IQR 30–50 mm). Of the screening colonoscopies
performed, 124 (12.1 %) were for lesions that had an existing tattoo or had had a
tattoo placed at the index EMR. Of these, 12 (9.7 %) were placed at the time of index
EMR because of difficult positioning secondary to looping (n = 4), a redundant colon
(n = 4), or for unclear reasons (n = 4).
Fig. 2 Flow Diagram of consecutive large non-pedunculated colorectal polyps referred for
endosocpic resection
Table 1
Characteristics of the 1023 patients and their large non-pedunculated colorectal polyps
that were treated by endoscopic mucosal resection with a surveillance colonoscopy
performed within 6 months.
No tattoo (n = 899)
Tattoo (n = 124)
Overall (n = 1023)
Age, median (IQR), years
69 (62–75)
70 (63–76)
69 (62–75)
Sex, male, n (%)
468 (52.1)
67 (54.0)
535 (52.3)
Size, median (IQR), mm
40 (30–50)
35 (25–40)
35 (30–50)
Location, n (%)
241 (26.8)
24 (19.4)
265 (25.9)
658 (73.2)
100 (80.6)
758 (74.1)
Paris classification, n (%)[1 ]
64 (7.1)
8 (6.5)
72 (7.1)
501 (55.9)
72 (58.1)
573 (56.1)
37 (4.1)
13 (10.5)
50 (4.9)
276 (30.8)
27 (21.8)
303 (29.7)
19 (2.1)
4 (3.2)
23 (2.3)
Granularity[2 ], n (%)[3 ]
568 (65.1)
53 (42.7)
621 (62.3)
215 (24.7)
61 (49.2)
276 (27.7)
49 (5.6)
6 (4.8)
55 (5.5)
40 (4.6)
4 (3.2)
44 (4.4)
Histopathology, n (%)
750 (83.4)
108 (87.1)
858 (83.9)
130 (14.5)
16 (12.9)
146 (14.3)
19 (2.1)
0 (0.0)
19 (1.9)
IQR, interquartile range.
1 Morphology not classified for two participants.
2
P < 0.001 when comparing tattoo with no tattoo.
3 Granularity not classified for 27 participants
Surveillance colonoscopy
The median time to SC1 was 5 months (IQR 4–6 months). The post-EMR scar was successfully
identified in 1020 patients (99.7 %). In three patients (0.3 %), the scar was not
identified, which in all cases was attributed to poor bowel preparation, with the
scar subsequently being confirmed on repeat surveillance colonoscopy. In all cases
where biopsies were taken (n = 769), histological analysis was either consistent with
the presence of a bland post-EMR scar (n = 655) or showed the presence of residual
or recurrent polypoid tissue (n = 114).
There was no difference in successful scar identification between patients with and
without a tattoo (100.0 % vs. 99.7 %; P > 0.99). On further stratification, no difference in scar identification was found
for LNPCPs 20–39 mm, LNPCPs ≥ 40 mm, serrated LNPCPs, and adenomatous LNPCPs (all
P > 0.99).
A second surveillance colonoscopy (SC2) was performed for 67 patients within the ACE
site, at a median time of 15 months (IQR 12–21 months) following EMR. Of these, nine
(13.4 %) had received a prior tattoo. In all 67 cases, the post-EMR scar was identified.
Discussion
Although tattoo placement is commonly used to facilitate post-EMR scar identification,
the incremental benefit is largely unknown. Moreover, it can lead to adverse outcomes
including: (1) diffusion of the tattoo under the resection site, which can preclude
residual or recurrent polypoid tissue management; (2) peritonitis after transmural
injection; (3) inaccurate lesion localization, specifically during laparoscopic surgery,
owing to inappropriate tattoo placement; (4) increased surgical complexity for rectal
LNPCPs, owing to mesorectal spillage; and (5) tumor seeding [3 ]
[4 ]
[5 ]. This study demonstrates that scar identification did not significantly differ between
patients with and without tattoo placement. By reviewing the index EMR reports and
photodocumentation, including the LNPCP location and colonic segment, scars were readily
identified and then confirmed using simple easy-to-use optical evaluation criteria
[6 ]. Given the potential adverse outcomes associated with the sterile carbon particle
suspension, tattoo placement should be reserved for select lesions, such as those
with suspected SMIC, difficult positioning, or bowel redundancy.
With the widespread availability of high definition colonoscopes, it is now the expectation
that competent endoscopists reliably detect diminutive colorectal polyps. To achieve
this, skill enhancement programs, which include teaching about the optical characteristics
of adenomatous and serrated polypoid tissue, have been developed. The process of identifying
a post-EMR scar is no different; for LNPCPs, this should arguably be easier given
their size ([Fig. 1 ]). However, an emphasis is currently placed on teaching the technical aspects of
high quality EMR and less on the periprocedural management of LNPCPs, including scar
identification. Skill enhancement programs on the gamut of LNPCP management, informed
by evidence-based quality indicators in EMR, are therefore needed [12 ].
This study is not without limitations. It is a single-center analysis, from a center
with recognized expertise in minimally invasive endoscopic resection techniques. Therefore,
confirmation of these findings is needed. The majority of tattoos had been placed
by the referring physician or surgeon. As it was not possible to determine the reasons
for tattoo placement, the generalizability of our results are reduced. Moreover, this
study did not evaluate alternative endoscopic resection techniques, including endoscopic
submucosal dissection and piecemeal cold-snare resection.
In conclusion, this study shows that, at a center that is expert in minimally invasive
endoscopic resection techniques, the post-EMR scar can be reliably identified and
confirmed with simple easy-to-use optical evaluation criteria. In the era of quality
assurance in colonoscopy, skill enhancement programs on LNPCP management must incorporate
training in post-EMR scar identification. Moreover, this potentially negates the role
for universal tattoo placement. Tattooing should be reserved for LNPCPs with suspected
SMIC [13 ] that are either being referred for surgery or being considered for an advanced endoscopic
resection technique. Moreover, it may be appropriate in select cases where lesion
identification is difficult, such as in the transverse or sigmoid colon where bowel
redundancy and loose mesenteric attachments may make re-identification of the resection
site challenging.
