ORIGINAL ARTICLE: Clinical Endoscopy

High-definition colonoscopy versus Endocuff versus EndoRings

versus full-spectrum endoscopy for adenoma detection at
colonoscopy: a multicenter randomized trial
Douglas K. Rex, MD,1 Alessandro Repici, MD,2 Seth A. Gross, MD,3 Cesare Hassan, MD,4
Prasanna L. Ponugoti, MD,1 Jonathan R. Garcia, BA,1 Heather M. Broadley, MS,1 Jack C. Thygesen, BA,1
Andrew W. Sullivan, BA,1 William W. Tippins,1 Samuel A. Main,1 George J. Eckert, MAS,5
Krishna C. Vemulapalli, MBBS, MPH6
Indianapolis, Indiana; New York, New York, USA; Milan, Rome, Italy; Granada, West Indies

GRAPHICAL ABSTRACT

Background and Aims: Devices used to improve polyp detection during colonoscopy have seldom been
compared with each other.
Methods: We performed a 3-center prospective randomized trial comparing high-definition (HD) forward-
viewing colonoscopy alone to HD with Endocuff to HD with EndoRings to the full spectrum endoscopy
(FUSE) system. Patients were age
50 years and had routine indications and intact colons. The study colonoscop-
ists were all proven high-level detectors. The primary endpoint was adenomas per colonoscopy (APC).
Results: Among 1188 patients who completed the study, APC with Endocuff (APC mean  standard deviation:
1.82  2.58), EndoRings (1.55  2.42), and standard HD colonoscopy (1.53  2.33) were all higher than FUSE
(1.30  1.96; P < .001 for APC). The APC for Endocuff was higher than standard HD colonoscopy (P Z .014).
Mean cecal insertion times with FUSE (468  311 seconds) and EndoRings (403  263 seconds) were both longer
than with Endocuff (354  216 seconds; P Z .006 and .018, respectively).
Conclusions: For high-level detectors at colonoscopy, forward-viewing HD instruments dominate the FUSE sys-
tem, indicating that for these examiners image resolution trumps angle of view. Further, Endocuff is a dominant
strategy over EndoRings and no mucosal exposure device on a forward-viewing HD colonoscope. (Clinical trial
registration number: NCT02345889.) (Gastrointest Endosc 2018;88:335-44.)

(footnotes appear on last page of article)

Colonoscopy prevents colon cancer through detec- behind folds, adequate distension, clean colon, and
tion and removal of precancerous lesions.1 More sufficient inspection time to visually process the
effective detection of adenomas is associated with exposed mucosa.4 The use of high-definition (HD)
better prevention of postcolonoscopy cancer.2,3 Critical colonoscopes aids in detection5 and is now widely
elements of effective detection include optimal considered fundamental to detection and effective
maneuvering of the colonoscope to expose mucosa therapeutics.

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Comparing HD colonoscopy, Endocuff, EndoRings, and FUSE system Rex et al

Although optimal maneuvers and lesion recognition might impede passage of the colonoscope with Endocuff
ability during colonoscopy examination are the core of or EndoRings, if there was a known coagulopathy, for
effective detection and can be taught to colonoscopists,6,7 inability to provide informed consent, for any known polyp
adjunctive devices and techniques have also been widely syndrome or inflammatory bowel disease or Lynch syn-
investigated. These include tools to highlight flat and sub- drome, or if the indication was a known therapeutic proced-
tle precancerous lesions such as chromoendoscopy8,9 and ure including polypectomy (Table 1). Patients were
electronic chromoendoscopy10,11 and mucosal exposure excluded after randomization if their bowel preparation
devices such as Endocuff,12 EndoRings,13 and ultra-wide- was considered inadequate for polyp examination, if the
angle endoscopes such as full spectrum endoscopy patient was found to have a polyp syndrome (World
(FUSE).14 Health Organization criteria were used to classify patients
Available data with mucosal exposure devices have often with serrated polyposis syndrome20) based on the findings
compared such devices with standard colonoscopy in 2- of the colonoscopy, or if the patient was diagnosed with
arm studies. The most robust data are available for Endo- inflammatory bowel disease during the study colonoscopy.
cuff12,15-18 and indicate that Endocuff produces an average As part of this intent-to-treat analysis, patients remained in
7% gain in the adenoma detection rate (ADR).12 Data are the analysis if Endocuff or EndoRings on a pediatric
more limited with EndoRings and are largely from a colonoscope could not pass the sigmoid colon.
single randomized tandem study showing that EndoRings
reduced the miss rate for adenomas.14 Data on the value Interventions
of the FUSE system have been mixed, with FUSE The study was performed at 3 sites, 2 in the United
resulting in a lower miss rate in an initial tandem study14 States and 1 in Italy. The original plan was to conduct
but no improvement in a subsequent randomized trial in the study at 4 sites, but the fourth site never initiated the
patients with positive fecal immunochemical tests.19 To trial. At each site one endoscopist with a proven high
the extent that mucosal exposure devices are effective, it (
40% in screening colonoscopy) baseline ADR (D.K.R.,
remains uncertain which colonoscopists can improve A.R., and S.A.G.) performed every withdrawal. All 3 sites
detection with these devices. That is, do all endoscopists had extensive experience with control arm equipment,
improve detection by use of mucosal exposure devices FUSE, and Endocuff before initiation. Two sites were less
or are the benefits confined or result predominantly for familiar with EndoRings, and the endoscopists performed
colonoscopists with low baseline ADRs? enough procedures with EndoRings before study initiation
In this study, we sought to evaluate the utility of to be very familiar with its use. Fellows were allowed to
mucosal exposure devices in the hands of colonoscopists insert the colonoscope, but cecal insertion times were eval-
with known high ADRs when using standard equipment. uated separately when fellows participated in insertion.
In addition, we sought to directly compare 3 mucosal A computer-generated sequence was used to randomize
exposure devices with each other, namely Endocuff versus the patients. Each site was provided with a series of opa-
EndoRings versus FUSE. que envelopes numbered sequentially with the concealed
randomization. Enrollment and assignment of patients to
study arms occurred at the individual sites. The randomiza-
METHODS tion was revealed only after the patient provided informed
consent.
We conducted a prospective randomized controlled trial At all 3 sites, Olympus HD colonoscopes (Olympus, To-
comparing HD forward-viewing white-light colonoscopy kyo, Japan) were used for the control arm and the arms
(referred to as the standard or control arm), versus HD with Endocuff and EndoRings. These were 190 series or
forward-viewing white-light colonoscopy plus Endocuff, H180 series colonoscopes, and the colonoscopists had the
versus HD forward-viewing white-light colonoscopy with discretion to select an adult or pediatric instrument. If an
EndoRings, versus the FUSE system. Patients were random- adult instrument could not pass an angulated sigmoid, the
ized in a 1:1:1:1 ratio. The study was conducted at 3 aca- protocol required an attempt with a pediatric instrument
demic endoscopy units in Indianapolis, Indiana; Milan, in the same randomization arm. Thus, patients randomized
Italy; and New York, New York. The study was reviewed to Endocuff were required to have an attempt using the pe-
and approved by the Institutional Review Board at diatric colonoscope with the pediatric Endocuff device.
Indiana University on January 14, 2015, and all subjects The resolution of the FUSE system was improved by the
gave informed consent. The trial was registered at manufacturer while the study was in progress. All 3 sites
Clinicaltrials.gov (NCT02345889). had access and incorporated the most up to date FUSE co-
Participants were aged
50 years and undergoing colo- lonoscopes as they became available. Both adult and pedi-
noscopy for colorectal cancer screening, surveillance of atric FUSE colonoscopes were available at each site.
polyps, or symptoms. Patients were excluded if there was The Endocuff device used was the original device with 2
any previous surgical resection of the colon, if there was a rows of fingers (Arc Medical Design, Leeds, UK). The En-
known colonic stricture or severe diverticular disease that doRings device was manufactured in Israel by EndoAid

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Rex et al Comparing HD colonoscopy, Endocuff, EndoRings, and FUSE system

TABLE 1. Inclusion and exclusion criteria Conventional adenomas were uniformly dysplastic le-
Inclusion criteria
sions that were characterized as tubular, tubulovillous, or
villous with dysplasia as low grade or high grade. Serrated
 Screening, surveillance, or diagnostic colonoscopy
class lesions included hyperplastic polyps, sessile serrated
 Age
50 years
polyps, and traditional serrated adenomas.
Exclusion criteria Because of the failure to initiate the study at 1 planned
 Any large-bowel resection site and slow randomization at another, randomization was
 Inflammatory bowel disease continued beyond the initial planned number at 2 sites
 Any polyposis syndrome (see Results). Proximal colon refers to the cecum,
 Any family history of polyposis syndromes
ascending colon, and hepatic flexure.
 Referral for a previous incomplete colonoscopy
 Referral for removal of a polyp
Sample size and statistical analysis
Based on previous studies at Indiana University, we esti-
 Referral for positive fecal blood test
mated that the baseline APC in the standard colonoscopy
 Anticipated severe sigmoid angulation group would be 1.7 with a coefficient of variation of 1.5.
To demonstrate an increase in APC to 2.2 (an absolute in-
crease of .5 or a 29% increase) in any of the 3 increased
Ltd (Caesarea, Israel). During the study, the device was mucosal exposure groups, a sample size of 287 patients
modified from a 3-ring device to a 2-ring device, and the per group, or total sample of 1148 subjects was needed,
EndoRings used were changed as soon as the new device assuming 80% power, and 2-sided 5% significance level.
was available. Generalized estimating equation methods were used to
The FUSE system and colonoscopes were provided by analyze the combined data across all 3 sites, using site as
Endochoice (Marrietta, Ga). The EndoRings devices were the cluster effect. Age and Boston Bowel Preparation Score
provided by EndoAid. The Endocuff devices were provided assumed normal distributions, insertion and withdrawal
by the U.S. Endocuff distributor (Medivators Inc, Minneap- times assumed log-normal distributions, count data used
olis, Minn). No other industry support was provided for the a negative binomial model, and binary data used logistic
trial. There was no industry involvement in the design of regression. Similar analyses, without using generalized esti-
the trial or its conduct, and no industry had access to or mating equation for clustering, were performed for ana-
reviewed the study data or the manuscript before lyses of each site separately. Pair-wise tests between all
publication. groups were performed when the overall group effect
Each of the study endoscopists was asked to force the was significant. A 5% significance level was used for all
inspection time during withdrawal to approximately 8 mi- tests, with no adjustment for multiple comparisons. Ana-
nutes to remove inspection time as a variable that could lyses were performed using SAS, version 9.4 (SAS institute,
affect the detection results. Inspection time was measured Inc, Cary, NC). To assess the effect of changing the FUSE
during withdrawal by an assistant using a stopwatch. The and EndoRings technology during the study, APC was
stopwatch was started as soon as the cecum was cleaned plotted against time for the EndoRings and FUSE groups,
and cecal inspection initiated. It was stopped for all maneu- with a spline added to the plot to evaluate trends.
vers, including polypectomy and biopsy sampling, and dur-
ing all washing and suctioning of the colon. For the FUSE
device, the endoscopist tried to observe all 3 screens, but 2 RESULTS
individuals (usually the technician and the registered nurse
in the room) were assigned to watch the 2 lateral images (1 Data on patients screened, deemed ineligible, and
assistant assigned to each screen) to help ensure that any refusal to participate were collected only in Indianapolis.
exposed polyp was recognized. The flow of patients through the study, including those
excluded after randomization at all 3 sties, are described
Outcomes in Figure 1.
The primary outcome was the rate of conventional Exclusions after screening and before randomization
adenomas per colonoscopy (APC). Secondary outcomes were tracked at Indianapolis only. Subjects who passed
included the ADR (percent of patients with
1 conven- initial screening at Indianapolis but were excluded before
tional adenoma), number of sessile serrated polyps randomization included 17 identified to have some degree
per colonoscopy, the sessile serrated detection rate of prior colon resection, 4 referred for a previous incom-
(number of patients with
1 sessile serrated polyp), the plete colonoscopy (this reason for referral was not evident
colonoscope insertion times, the failure rate of insertion, to screeners in the initial portion of the study), 9 with ev-
and the detection targets noted above for the right side idence of inflammatory bowel disease, 4 with serrated pol-
of the colon (cecum, ascending, and hepatic flexure). No yposis syndrome, 1 with familial adenomatous polyposis, 1
interim analysis was performed. with a positive fecal blood test, and 6 considered unable to

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Comparing HD colonoscopy, Endocuff, EndoRings, and FUSE system Rex et al

Screened
n=1377

Eligibility & refusals

(From Indianapolis only)
Ineligible (59)
Declined (56)

Randomization
n=1262

Control colonoscopy Endocuff EndoRings FUSE

n=316 n=316 n=315 n=315

Excluded (n=21) Excluded (n=17) Excluded (n=20) Excluded (n=16)

Inadequate bowel Inadequate bowel Inadequate bowel Inadequate bowel
preparation (17) preparation (16) preparation (18) preparation (14)
Polyposis identified during Polyposis identified during Ineligibility recognized Polyposis identified during
study procedure (1) study procedure (1) after randomization (2) study procedure (1)
Ineligibility recognized after Ineligibility recognized after
randomization (1) randomization (1)
Ulcerative colitis
identified(1)
Cecum not intubated (1)

Completed Completed Completed Completed

n=295 n=299 n=295 n=299

Figure 1. Flow of patients through the study. FUSE, Full spectrum endoscopy.

give informed consent by the investigator for reasons promptly repaired. The procedure was completed using
including dementia, anxiety, and inadequate English lan- a standard Olympus colonoscope, and the patient was
guage skill. Seventeen were excluded by the investigator included in the study.
based on evidence of severe sigmoid diverticular disease There were 1188 subjects who completed the study, of
in prior colonoscopy reports (considered to make passage whom 299 were randomized to Endocuff, 295 (Fig. 2) to
of the colonoscope with Endocuff or EndorRings likely to EndoRings, 299 to FUSE, and 295 to the control arm
fail) or recent diverticulitis. colonoscopy. The mean age of all subjects who
There were 1262 patients randomized, of whom 74 completed the study was 62.6 years (standard deviation,
were excluded after randomization (Fig. 1). One patient 8.3), and there were 582 women (49%). There were 784
was excluded from the control arm for failure to intubate subjects who completed the study at Indianapolis, 302 at
the cecum (Fig. 1). Three patients were excluded when Milan, and 102 at New York. Table 2 shows demographic
they were recognized to have serrated polyposis features and procedure indications for the 4 colonoscopy
syndrome during the study colonoscopy. Six patients groups. There were no significant differences in these
were randomized to EndoRings and 4 to Endocuff and factors between groups, either overall or at the individual
included in the intent to treat analysis in whom the study sites. More than 90% of patients had polyp
instrument could not pass the sigmoid with either adult surveillance or screening as their indication.
or pediatric versions. There were 3 patients in the
EndoRings arm and 1 in the Endocuff arm in whom the Detection
adult scope with device could not pass the sigmoid Considering only patients with the indication screening
colon, but the pediatric colonoscope and device were and who were randomized to the control arm, the fraction
successfully passed to the cecum. In 1 patient the FUSE of subjects with at least 1 conventional adenoma (the ADR
processor failed during the procedure and could not be using standard forward-viewing HD instruments) was 39 of

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Rex et al Comparing HD colonoscopy, Endocuff, EndoRings, and FUSE system

The detection endpoints in a per protocol analysis are

shown in Supplementary Table 2, available online at
www.giejournal.org. Compared with the intention to treat
analysis shown in Table 3, the per protocol analysis does
not include the 10 patients in whom the colonoscope
could not be passed through the sigmoid colon with a
device on the tip and the 1 patient in whom the FUSE
system failed. Differences in results between the
intention to treat and per protocol analyses were minor.
There were no differences between modalities in APC
for conventional adenomas
10 mm either overall (P Z
.306) or at any of the study sites. Supplementary Table 1
shows the actual numbers of histologically identified
conventional adenomas and sessile serrated polyps
Figure 2. The Endocuff (left) and the revised EndoRings (right) devices
used in the study. according to lesion size and location in the colon (right
side of colon including cecum, ascending flexure, and
64 subjects (61%) at Indianapolis, 19 of 44 (43%) at Milan, hepatic flexure vs distal to the hepatic flexure).
and 16 of 19 (84%) at New York, consistent with previous There were some statistically significant differences in
internal data at each site that the study endoscopists were the detection of sessile serrated polyps between modalities
high-level detectors. (Table 3), but the trends were not consistent and, although
Table 3 summarizes detection in each study arm for statistically significant, were numerically minor. Because
all sites combined and individual sites. The control the technology for FUSE and EndoRings were changed
colonoscopy arm, Endocuff, and EndoRings were all during the study, APC was plotted against time for each
superior to FUSE for the primary endpoint (P < .001). technology, and no significant trends over time were
Overall, the highest APC was achieved with Endocuff observed for FUSE (P Z .46) or EndoRings (P Z .83).
at 1.82 (2.58). Endocuff was superior to control
colonoscopy (.014). The most marked differences in Procedure times
detection with Endocuff were in New York, where the APC For the entire study, cecal insertion time was longer with
was 2.00 (standard deviation, 2.34) with Endocuff and FUSE compared with Endocuff (P Z .006) and control colo-
<1 with the other 3 modalities (.75  .94 for EndoRings, noscopy (P Z .016) (Table 4). Further, EndoRings insertion
.80  1.37 for FUSE, .92  1.15 for control). There were no time was longer than that for Endocuff (P Z .020). A
differences in Indianapolis (P Z .151) or Milan (P Z .848) gastroenterology fellow was involved in the insertion phase
between the modalities for the primary endpoint. in 39% of colonoscopies at Indianapolis, 61% of
The ADR was also significantly higher with Endocuff, En- colonoscopies in Milan, and none of the colonoscopies in
doRings, and control colonoscopy compared with FUSE New York. When only colonoscopies in which no fellow
(P  .006). Further, Endocuff was superior to EndoRings participated in insertion were considered, the cecal
(P < .001) and control colonoscopy (P Z .003). There insertion time was still longer with FUSE than the other 3
were no significant differences between study arms in arms (P  .017), and EndoRings insertion time was longer
ADR within sites. Similar findings were observed for the than Endocuff insertion time (P Z .014). When insertion
polyp detection rate as were seen with ADR. times by site were evaluated, FUSE was longer than
Evaluation by location in the colon showed that APCs were Endocuff (P  .02) and standard (P  .03) at all sites, FUSE
higher in the right side of the colon (cecum, ascending, and was longer than EndoRings in Indianapolis, EndoRings was
hepatic flexure) for Endocuff (P < .001), EndoRings (P Z longer than Endocuff (P Z .023) and standard (P Z .003) in
.043), and control (P Z .003) compared with FUSE New York, and FUSE was longer than EndoRings (P Z .004)
(Supplementary Table 1, available online at www.giejournal. and standard was longer than Endocuff (P Z .050) in Milan.
org). APC for Endocuff in the right side of the colon was The mean Boston Bowel Preparation Score overall
higher than control colonoscopy (P Z .034). When was 8.12 (standard deviation, 1.33), with no significant
analyzed by site, APC with Endocuff was higher in the right difference between the study arms, but was higher at In-
side of the colon in New York when compared with dianapolis (8.75  .84) and New York (8.47  1.23) than
EndoRings (P Z .005) and control (P Z .030), but there at Milan (6.39  .76). There were no colorectal perfora-
were no differences in right-sided colon ADR between modal- tions in any of the study patients.
ities in Indianapolis (P Z .563) or in Milan (P Z .966). Very
similar differences between modalities were seen in right- DISCUSSION
sided colon ADR at New York specifically; however, these dif-
ferences in right-sided colon ADR between modalities were In this prospective randomized controlled trial we
again not seen in Indianapolis (P Z .382) or Milan (P Z .805). compared adenoma detection with a control arm of HD

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Comparing HD colonoscopy, Endocuff, EndoRings, and FUSE system Rex et al

TABLE 2. Demographics and procedure indications

Study arm
Control* (n [ 295) Endocuffy (n [ 299) EndoRingsz (n [ 295) Full spectrum endoscopy (n [ 299)

Mean age, y (SD) 62.6 (8.3) 63.2 (8.2) 62.3 (7.9) 62.3 (8.7)
Female 139 (47%) 141 (47%) 156 (53%) 146 (49%)
Race
White 272 (92%) 276 (92%) 276 (94%) 269 (90%)
Black 13 (4%) 15 (5%) 13 (4%) 20 (7%)
Hispanic 5 (2%) 6 (2%) 5 (2%) 4 (1%)
Asian 4 (1%) 2 (1%) 1 (<1%) 5 (2%)
Other 1 (<1%) 0 (0%) 0 (0%) 0 (0%)
Indication
Screening 127 (43%) 126 (42%) 123 (42%) 128 (43%)
Surveillance 151 (51%) 150 (50%) 152 (52%) 154 (52%)
Diagnostic 16 (5%) 23 (8%) 20 (7%) 16 (5%)
SD, Standard deviation.
*Control: high-definition forward-viewing Olympus 190 or H180 colonoscope.
yControl instrument with Endocuff.
zControl instrument with EndoRings.

forward-viewing colonoscopy to HD forward-viewing colo- appear to be able to compensate for a more limited angle
noscopy with the adjunctive mucosal exposure devices En- of view by their manipulation and deflection of the instru-
docuff and EndoRings and with the FUSE colonoscopy ment tip to expose mucosal surfaces on the proximal sides
system. Although a number of studies have compared of the haustral folds and flexures. Because we found that
individual mucosal exposure devices with standard the FUSE colonoscope was also inferior with regard to
colonoscopy, to our knowledge this is the first study to the time for cecal insertion (possibly because the FUSE
compare mucosal exposure devices with each other. insertion tubes are “floppier” than Olympus instruments),
A principal finding of our study was that the FUSE we conclude that in the hands of careful examiners, HD
colonoscope system was inferior to HD forward-viewing forward-viewing colonoscopes have superior performance
Olympus colonoscopes with or without adjunctive devices. to the FUSE colonoscopes. It is possible that a wide-
Thus, APCs and the ADR were higher with Olympus angle instrument with image resolution comparable with
colonoscopes compared with the FUSE system. This result Olympus HD colonoscopes might provide superior detec-
is different from that obtained in the initial tandem tion. However, to our knowledge, no such device exists at
colonoscopy study comparing the FUSE system with the present time, and the FUSE colonoscope is being with-
standard-definition colonoscopes,14 which found that drawn from the commercial market after purchase of
FUSE was superior for detection. Further, the result is EndoChoice by Boston Scientific. Thus, whether a super
different from a prospective randomized trial comparing wide-angle colonoscope can outperform a 170-degree
an early generation of FUSE colonoscopes with standard- angle of view HD instrument is uncertain and must await
definition forward-viewing colonoscopes in a fecal development of new technology and further investigation.
immunochemical test–positive population in Italy.19 In Our data indicate that with regard to adjunctive devices
that study, there was no difference in detection between that fit over the tip of an HD forward-viewing colonoscope,
the very-wide-angle FUSE system and the forward-viewing Endocuff is a dominant strategy over EndoRings and no
standard-definition colonoscopes. However, there was a device. First, there was a significant increase of APC with
nonsignificant trend in that study toward better detection Endocuff compared with control colonoscopy, and ADR
of large adenomas by standard endoscopy. In our study, was higher with Endocuff compared with EndoRings
we used HD Olympus colonoscopes and state-of-the-art and control colonoscopy. A marked difference in detection
FUSE instruments as they became available during the with Endocuff at one center, which contributed the small-
study interval. Although the FUSE colonoscopes were est group of patients to the overall study, had an important
also considered HD, our subjective impression is that the effect on this conclusion, although a numerical increase
resolution of the Olympus instruments was superior to with a trend toward statistical significance was also seen
FUSE. Our results indicate that in the hands of high-level at the largest participating site. There was no disadvantage
detectors, high image resolution is more important to with Endocuff with regard to insertion. Thus, overall Endo-
detection than angle of view. Thus, skilled examiners cuff produced improved detection with no detriment to

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Rex et al Comparing HD colonoscopy, Endocuff, EndoRings, and FUSE system

TABLE 3. Detection endpoints in the intent to treat analysis

Study arm
Control Endocuff EndoRings Full spectrum
(n [ 295) (n [ 299) (n [ 295) endoscopy (n [ 299)

Adenomas per colonoscopy

All sites* 1.53 (2.33)y 1.82 (2.58) 1.55 (2.42) 1.30 (1.96)
Indianapolis 1.89 (2.69) 2.17 (2.88) 1.97 (2.77) 1.59 (2.18)
Milan .83 (1.18) .80 (1.25) .72 (1.17) .68 (1.19)
New Yorkz .92 (1.15) 2.00 (2.34) .75 (.94) .80 (1.32)
Adenoma detection rate
All sitesx 166 (56%){ 191 (64%) 167 (57%) 154 (52%)
Indianapolis 117 (61%) 137 (70%) 127 (65%) 115 (58%)
Milan 37 (47%) 35 (47%) 29 (39%) 28 (37%)
New York 12 (48%) 19 (68%) 11 (46%) 11 (44%)
Sessile serrated polyp per colonoscopy
All sitesk .17 (.54)y .17 (.54) .20 (.81) .18 (.74)
Indianapolis .24 (.64) .23 (.63) .29 (.98) .25 (.89)
Milan .03 (.16) .04 (.26) .01 (.12) .03 (.16)
New York .04 (.20) .07 (.26) .04 (.20) .04 (.20)
Sessile serrated polyp detection rate
All sites** 36 (12%){ 33 (11%) 33 (11%) 30 (10%)
Indianapolis 33 (17%) 29 (15%) 31 (16%) 27 (14%)
Milan 2 (3%) 2 (3%) 1 (1%) 2 (3%)
New York 1 (4%) 2 (7%) 1 (4%) 1 (4%)
Polyp detection rate
All sitesyy 226 (77%){ 247 (83%) 231 (78%) 212 (71%)
Indianapoliszz 162 (84%) 175 (89%) 171 (87%) 155 (78%)
Milan 46 (59%) 50 (68%) 42 (56%) 38 (51%)
New York 18 (72%) 22 (79%) 18 (75%) 19 (76%)
*Control, Endocuff, and EndoRings higher than FUSE (all P < .001). Endocuff > control (P Z .014).
yDesignated polyp type per colonoscopy (standard deviation).
zEndocuff > EndoRings (P Z .008), FUSE (P Z .011), and control (P Z .027) in New York; no difference in study arms for APC at Indianapolis (P Z .137) or Milan (P Z .848).
xEndocuff (P < .001), EndoRings (P Z .001), and control (P Z .006) all higher than FUSE. Endocuff higher than EndoRings (P < .001) and control (P Z .003). No differences in
ADR by site.
{Number of patients with designated polyp type (%).
kEndoRings higher than FUSE (P < .001) and control (P < .001). FUSE higher than control (P < .001).
**Endocuff (P Z .009) and control (P < .001) higher than FUSE. Control higher than Endocuff (P Z .047) and EndoRings (P Z .004).
yyEndocuff (P < .001), EndoRings (P Z .002), and control (P < .001) higher than FUSE. Endocuff higher than EndoRings (P Z .008) and control (P < .001).
zzAt Indianapolis Endocuff (P Z .004) and EndoRings (P Z .015) were higher than FUSE.

insertion except for an occasional patient with an angulated that each 1% gain in ADR resulted in a 3% drop in the risk
sigmoid colon in which passage of the colonoscope required of interval cancer and a 5% drop in the risk of fatal interval
removal of the cuff. Further, the finding that Endocuff cancer.3 Whether such impacts on interval cancer will
resulted in gains in detection even in high-level detectors, occur in very high-level detectors is uncertain, but our re-
who would be expected to have superior technique with sults indicate that potentially important gains in ADR are
standard instruments, suggests that Endocuff could poten- achievable with Endocuff even by detectors with very high
tially produce detection gains for examiners with any base- ADRs using standard instruments. Endocuff was associated
line level of detection. Thus, Endocuff may overcome with gains in APC of 17% to 40% compared with the other
mucosal exposure problems that cannot be overcome with 3 arms. This difference in overall adenoma detection could
an HD forward-viewing colonoscope alone. also result in important protective effects against interval
In this study, Endocuff allowed an ADR that was at least 7 cancer, although the relationship of APC to interval cancer
percentage points higher (95% confidence interval, 3%- protection has not yet been described. Although we did
16%) than the other 3 arms of the study. A study found not formally address the cost-effectiveness of Endocuff,

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Comparing HD colonoscopy, Endocuff, EndoRings, and FUSE system Rex et al

TABLE 4. Procedure times

Study arm
Control Endocuff EndoRings Full spectrum endoscopy

Cecal insertion time, sec n Z 295 n Z 299 n Z 295 n Z 299

All sites* 422 (319) 354 (216) 403 (263) 468 (311)
Indianapolis 366 (243) 320 (179) 352 (191) 395 (225)
Milan 642 (405) 503 (254) 581 (356) 731 (385)
New York 170 (62) 193 (93) 251 (110) 242 (80)
Cecal insertion time when n Z 173 n Z 169 n Z 172 n Z 176
no fellow was involved, sec
All sitesy 320 (256) 265 (173) 331 (222) 380 (252)
Indianapolis 283 (185) 239 (127) 277 (127) 340 (169)
Milan 556 (378) 438 (269) 588 (345) 718 (401)
Inspection time, sec n Z 295 n Z 299 n Z 295 n Z 299
All sitesz 444 (103) 419 (95) 417 (147) 421 (112)
Indianapolis 418 (91) 392 (89) 388 (160) 378 (83)
Milan 501 (109) 492 (78) 484 (92) 522 (120)
New York 467 (95) 414 (84) 438 (96) 454 (81)
Values in parentheses are standard deviations. n, Number of insertions in designated group performed with no participation by a fellow.
*FUSE longer than Endocuff (P Z .006) and control (P Z .016), EndoRings longer than Endocuff (P Z .020) (site difference similar but not shown).
yWhen no fellow was involved in insertion FUSE was longer than Endocuff (P < .001), EndoRings (P Z .017), and control (P Z .001); EndoRings longer than Endocuff (P Z .014).
By site: FUSE longer than Endocuff and control at all sites; EndoRings longer than Endocuff and control in New York, FUSE longer than EndoRings in Milan, and control longer
than Endocuff in Milan.
zNo significant difference overall. By site, control significantly longer than Endocuff, EndoRings, and FUSE in Indianapolis.

the cost of Endocuff is low in the United States compared Next, we actively forced the inspection times in the 4 study
with the cost of colonoscopy and would be unlikely to arms to be equal, because withdrawal time is well known to
adversely affect the cost-effectiveness of improving the qual- influence detection,23 and failure to control inspection
ity of adenoma detection.21,22 time can disrupt the interpretation of a detection trial.23
The reasons EndoRings did not match Endocuff with re- Limitations of our study were primarily that the recruit-
gard to detection are not clear. From a mucosal exposure ment was uneven across the sites, and there were some dif-
perspective, the ability of EndoRings to deflect folds seems ferences between sites with regard to detection. These
comparable with Endocuff. In the left side of the colon, differences suggest some operator dependence applies to
EndoRings seems to have even more of a tendency than these devices, such as the very large increase in APCs with
Endocuff to straighten the lumen and flatten the haustral Endocuff relative to other devices in New York. However,
folds. However, the mucosal gripping properties of many of the trends seen in the overall study were consistent
EndoRings seem to cause it to jump back 2 or 3 folds across the individual sites, including the detection of ade-
at times during withdrawal through the sigmoid, and it nomas and serrated lesions and insertion times. Certainly,
can be difficult to reinsert the instrument to the point direct comparisons between mucosal exposure devices by
where slippage began. In any case, our data suggest that other investigators could be informative. However, we
EndoRings creates greater problems for colonoscope inser- acknowledge that the operator dependence demonstrated
tion than Endocuff, which certainly relates to its larger in the study indicates that some caution is appropriate in
diameter and bulkier profile. Taken together, our data concluding generalizability. Finally, endoscopists were not
suggest that Endocuff is a more effective and easier to blinded to which device was in use. This is a consistent prob-
use device than EndoRings. lem with colonoscopy detection studies, and these studies
Strengths of our study include large size, the use of depend on the investigating endoscopists approaching the
multiple centers, and the testing of multiple devices. This use of each device without bias.
design allowed a comparison of available devices in a The version of Endocuff that we used is no longer
fashion not previously available to practicing colonoscop- commercially available and has been replaced by Endocuff
ists. Further, we used the best available versions of each Vision (Arc Medical Design). Endocuff Vision has fingers
technology throughout the study. We did not see evidence that are 3 mm longer than those on Endocuff, and there
that successive generations of FUSE or EndoRings were is only 1 ring of fingers. There are no direct comparative
associated with increasing detection, suggesting that our studies of Endocuff Vision and Endocuff. Our anecdotal
results apply to the latest generations of these devices. impression of the fold flattening achieved with Endocuff

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Rex et al Comparing HD colonoscopy, Endocuff, EndoRings, and FUSE system

Vision is that it is as or more effective than Endocuff, with no reduction of insertion capability that was clinically
no reduction of insertability. We upgraded the EndoRings important. Finally, our results indicate that the design of
and FUSE colonoscopes as upgrades became available dur- Endocuff is superior to the design of EndoRings as a
ing the study. Although the use of upgraded devices makes mucosal exposure device for colonoscopy.
study interpretation more challenging, we considered that
failure to upgrade and using only older devices would also
subject the study to criticism. Again, we saw no significant REFERENCES
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the EndoRings or FUSE arms, suggesting that our conclu- 2015;60:639-46.
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To the extent that our results endorse the routine use of 1795-803.
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of colorectal cancer and death. N Engl J Med 2014;370:1298-306.
ested in our impressions of how the device affects actual 4. Rex DK. Colonoscopic withdrawal technique is associated with ade-
colonoscopy performance. Our collective impression is noma miss rates. Gastrointest Endosc 2000;51:33-6.
that the use of Endocuff in routine colonoscopic examina- 5. Subramanian V, Mannath J, Hawkey CJ, et al. High definition colonos-
tion is easy for experienced endoscopists to learn and does copy vs. standard video endoscopy for the detection of colonic polyps:
not adversely affect the performance of routine polypecto- a meta-analysis. Endoscopy 2011;43:499-505.
6. Barclay RL, Vicari JJ, Greenlaw RL. Effect of a time-dependent colono-
mies. We suspect it may have the potential to make the scopic withdrawal protocol on adenoma detection during screening
process of examining the proximal sides of folds faster, colonoscopy. Clin Gastroenterol Hepatol 2008;6:1091-8.
as has been suggested in retrospective uncontrolled evalu- 7. Coe SG, Crook JE, Diehl NN, et al. An endoscopic quality improvement
ations24 but which has not been tested as a primary program improves detection of colorectal adenomas. Am J Gastroen-
endpoint of randomized trials. We did not routinely or terol 2013;108:219-26; quiz 27.
8. Pohl J, Schneider A, Vogell H, et al. Pancolonic chromoendoscopy
systematically attempt terminal intubation during the study, with indigo carmine versus standard colonoscopy for detection of
but our impression was that Endocuff does reduce the ease neoplastic lesions: a randomised two-centre trial. Gut 2011;60:
and success rate of terminal ileal intubation, consistent with 485-90.
the results of other studies.25 Finally, attention to difficult 9. Kahi CJ, Anderson JC, Waxman I, et al. High-definition chromocolono-
sigmoid colons is needed in considering use of Endocuff. In scopy vs. high-definition white light colonoscopy for average-risk colo-
rectal cancer screening. Am J Gastroenterol 2010;105:1301-7.
the current study, about 1.5% of subjects had sigmoid 10. Leung WK, Lo OS, Liu KS, et al. Detection of colorectal adenoma by nar-
colons that did not allow passage of Endocuff, and at row band imaging (HQ190) vs. high-definition white light colonos-
Indianapolis about 2% of screened subjects were excluded copy: a randomized controlled trial. Am J Gastroenterol 2014;109:
before randomization because of known diverticular disease 855-63.
that might have made sigmoid passage with Endocuff or 11. Shimoda R, Sakata Y, Fujise T, et al. The adenoma miss rate of blue-
laser imaging vs. white-light imaging during colonoscopy: a random-
EndoRings difficult or impossible. We note that the ized tandem trial. Endoscopy 2017;49:186-90.
detection gains found in this study with Endocuff were 12. Chin M, Karnes W, Jamal MM, et al. Use of the Endocuff during routine
largely in diminutive lesions (Supplementary Table 1), and colonoscopy examination improves adenoma detection: a meta-
the clinical significance of detection gains in diminutive analysis. World J Gastroenterol 2016;22:9642-9.
lesions remains uncertain. Improved detection of 13. Dik VK, Gralnek IM, Segol O, et al. Multicenter, randomized, tandem
evaluation of EndoRings colonoscopydresults of the CLEVER study.
diminutive lesions may be generally associated with Endoscopy 2015;47:1151-8.
improved detections of large lesions, but that suggestion is 14. Gralnek IM, Siersema PD, Halpern Z, et al. Standard forward-viewing
not proven true by these data. Further, we did not perform colonoscopy versus full-spectrum endoscopy: an international, multi-
a formal cost analysis of Endocuff use and have not centre, randomised, tandem colonoscopy trial. Lancet Oncol 2014;15:
evaluated the cost-effectiveness of using Endocuff routinely 353-60.
15. Gonzalez-Fernandez C, Garcia-Rangel D, Aguilar-Olivos NE, et al. Higher
in colonoscopy. adenoma detection rate with the endocuff: a randomized trial. Endos-
In conclusion, in a prospective randomized controlled copy 2017;49:1061-8.
trial we demonstrated that detection with HD forward- 16. Baek MD, Jackson CS, Lunn J, et al. Endocuff assisted colonoscopy
viewing colonoscopes is superior to a very-wide-angle co- significantly increases sessile serrated adenoma detection in veterans.
lonoscope system, which in all in its iterations had what J Gastrointest Oncol 2017;8:636-42.
17. Triantafyllou K, Polymeros D, Apostolopoulos P, et al. Endocuff-assisted
seemed to be recognizably inferior image resolution. colonoscopy is associated with a lower adenoma miss rate: a multi-
Thus, in the hands of high-level detectors, image resolu- center randomized tandem study. Endoscopy 2017;49:1051-60.
tion trumps angle of view for adenoma detection during 18. Bhattacharyya R, Chedgy F, Kandiah K, et al. Endocuff-assisted vs. stan-
colonoscopy. Next, we showed that use of an adjunct (En- dard colonoscopy in the fecal occult blood test-based UK Bowel Can-
docuff) on the end of an HD forward-viewing colonoscope cer Screening Programme (E-cap study): a randomized trial. Endoscopy
2017;49:1043-50.
produced gains in adenoma detection even in the hands of 19. Hassan C, Senore C, Radaelli F, et al. Full-spectrum (FUSE) versus stan-
examiners who are very skilled with standard instruments dard forward-viewing colonoscopy in an organised colorectal cancer
lacking adjunctive devices. Further, Endocuff produced screening programme. Gut 2016;66:1949-55.

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20. Snover D, Ahnen DJ, Burt RW, et al. Serrated polyps of the colon financial relationships relevant to this publication: D. K. Rex: Research
and rectum and serrated (“hyperplastic”) polyposis. In: Bozman FT, support recipient from Boston Scientific, Medivators, EndoChoice,
Carneiro F, Hruban RH, et al, editors. WHO classification of tumours. EndoAid, Braintree Laboratories, Medtronic, Colonary Solutions,
Pathology and genetics. Tumours of the digestive system, 4th ed. PAION, and US Endoscopy; consultant for Boston Scientific and
Berlin, Germany: Springer-Verlag; 2010. p. 160–5. Olympus. A. Repici, S. A. Gross: Consultant for Cook Medical, Boston
21. Hassan C, Rex DK, Zullo A, et al. Efficacy and cost-effectiveness of Scientific, Olympus, and Medivators. C. Hassan: Research support:
screening colonoscopy according to the adenoma detection rate. Endochoice, EndoAid, Norgine, and Fujifilm. All other authors
United Eur Gastroenterol J 2015;3:200-7. disclosed no financial relationships relevant to this publication.
22. Meester RG, Doubeni CA, Lansdorp-Vogelaar I, et al. Variation in ade-
See CME section; p. 397.
noma detection rate and the lifetime benefits and cost of colorectal
cancer screening: a microsimulation model. JAMA 2015;313:2349-58. Copyright ª 2018 by the American Society for Gastrointestinal Endoscopy
23. Leufkens AM, DeMarco DC, Rastogi A, et al. Effect of a retrograde- 0016-5107/$36.00
viewing device on adenoma detection rate during colonoscopy: the https://doi.org/10.1016/j.gie.2018.02.043
TERRACE study. Gastrointest Endosc 2011;73:480-9.
Received November 1, 2017. Accepted February 28, 2018.
24. Tsiamoulos ZP, Misra R, Rameshshanker R, et al. Impact of a new distal
attachment on colonoscopy performance in an academic screening Current affiliations: Division of Gastroenterology/Hepatology (1),
center. Gastrointest Endosc 2018;87:280-7. Department of Biostatistics (5), Indiana University School of Medicine,
25. Gonzalez-Fernandez C, Garcia-Rangel D, Aguilar-Olivos NE, et al. Higher Indianapolis, Indiana, USA; Department of Gastroenterology, Humanitas
adenoma detection rate with the Endocuff: a randomized trial. Endos- Research Hospital & Humanitas University via Manzoni, Milan, Italy (2),
copy 2017;49:1061-8. Department of Gastroenterology, Tisch Hospital, NYU Langone Medical
Center, New York, New York, USA (3), Department of Gastroenterology,
Abbreviations: ADR, adenoma detection rate; APC, adenoma per Nuovo Regina Margherita Hospital, Rome, Italy (4), Department of Public
colonoscopy; FUSE, full spectrum endoscopy; HD, high definition. Health and Preventative Medicine, St. George’s University, Grenada,
West Indies (6).
DISCLOSURE: The following author received a gift for this study from the
Indiana University Foundation from Scott Schurz of Bloomington, Reprint request: Douglas K. Rex, MD, Indiana University Hospital, 550 North
Indiana: D. K. Rex. In addition, the following authors disclosed University Boulevard, Suite 4100, Indianapolis, IN 46202.

344 GASTROINTESTINAL ENDOSCOPY Volume 88, No. 2 : 2018 www.giejournal.org

Rex et al Comparing HD colonoscopy, Endocuff, EndoRings, and FUSE system

SUPPLEMENTARY TABLE 1. Numbers of histologically proven conventional adenomas and sessile serrated polyps by size and location in the 4
study arms

Study arm
Control Endocuff EndoRings Full spectrum
Location Size (n [ 295) (n [ 299) (n [ 295) endoscopy (n [ 299)
Conventional adenomas

All All 445 543 463 385

1-5 mm 336 (76) 424 (78) 342 (74) 299 (78)
6-9 mm 73 (16) 83 (15) 79 (17) 63 (16)

10 mm 36 (8) 36 (7) 42 (9) 23 (6)
Distal to the hepatic flexure All 240 290 250 191
1-5 mm 176 (73) 225 (76) 180 (72) 154 (81)
6-9 mm 45 (19) 46 (16) 48 (19) 28 (15)

10 mm 19 (8) 19 (7) 22 (9) 9 (5)
Right side of the colon All 205 253 213 194
1-5 mm 160 (78) 199 (79) 162 (76) 145 (75)
6-9 mm 28 (14) 37 (15) 31 (15) 35 (18)

10 mm 17 (7) 17 (7) 20 (9) 14 (7)

Sessile serrated polyps

All All 51 50 57 53
1-5 mm 28 (55) 20 (40) 21 (37) 21 (43)
6-9 mm 14 (27) 13 (26) 16 (28) 13 (32)

10 mm 9 (18) 17 (34) 20 (35) 19 (36)
Distal to the hepatic flexure All 31 18 28 28
1-5 mm 19 (49) 9 (50) 13 (46) 12 (43)
6-9 mm 8 (26) 3 (17) 8 (29) 9 (32)

10 mm 4 (13) 6 (33) 7 (25) 7 (25)
Right side of the colon All 20 32 29 25
1-5 mm 9 (45) 11 (34) 8 (28) 9 (36)
6-9 mm 6 (30) 10 (31) 8 (28) 4 (16)

10 mm 5 (25) 11 (34) 13 (45) 12 (48)
Values are number of polyps with percent of all polyps in this location that are in this size group in parentheses. Right side of the colon includes the cecum, ascending colon,
and hepatic flexure.

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Comparing HD colonoscopy, Endocuff, EndoRings, and FUSE system Rex et al

SUPPLEMENTARY TABLE 2. Detection endpoints in the per protocol analysis

Study arm
Control Endocuff EndoRings Full spectrum
(n [ 295) (n [ 299) (n [ 295) endoscopy (n [ 299)

Adenomas per colonoscopy

All sites* 1.53 (2.33)y 1.84 (2.59) 1.57 (2.43) 1.30 (1.96)
Indianapolis 1.89 (2.69) 2.21 (2.88) 1.98 (2.78) 1.59 (2.18)
Milan .83 (1.18) .80 (1.25) .72 (1.18) .68 (1.19)
New Yorkz .92 (1.15) 2.07 (2.35) .82 (0.96) .83 (1.34)
Adenoma detection rate
All sitesx 166 (56%){ 191 (65%) 165 (57%) 154 (52%)
Indianapolis 117 (61%) 137 (71%) 126 (65%) 115 (58%)
Milan 37 (47%) 35 (47%) 28 (38%) 28 (37%)
New York 12 (48%) 19 (70%) 11 (50%) 11 (46%)
Sessile serrated polyp per colonoscopy
All sitesk .17 (.54)y .17 (.54) .20 (.82) .18 (.54)
Indianapolis .24 (.64) .23 (.63) .30 (.98) .25 (.89)
Milan .03 (.16) .04 (.26) .01 (.12) .03 (.16)
New York .04 (.20) .07 (.27) .05 (.21) .04 (.20)
Sessile serrated polyp detection rate
All sites** 36 (12%){ 33 (11%) 33 (11%) 30 (10%)
Indianapolis 33 (17%) 29 (15%) 31 (16%) 27 (14%)
Milan 2 (3%) 2 (3%) 1 (1%) 2 (3%)
New York 1 (4%) 2 (7%) 1 (5%) 1 (4%)
Polyp detection rate
All sitesyy 22 (77%)y 247 (84%) 229 (79%) 213 (71%)
Indianapoliszz 163 (85%) 174 (90%) 171 (89%) 156 (78%)
Milan 46 (59%) 50 (68%) 41 (55%) 38 (51%)
New York 19 (76%) 23 (85%) 17 (77%) 19 (79%)
*Standard, Endocuff, and EndoRings higher than FUSE (all P < .001). Endocuff > EndoRings (P Z .048) and standard (P Z .004).
yDesignated polyp type per colonoscopy (standard deviation).
zEndocuff > EndoRings (P Z .011), FUSE (P Z .010), and standard (P Z .018) in New York; no difference in study arms for APCa at Indianapolis (P Z .16) or Milan (P Z .845).
xEndocuff (P < .001), EndoRings (P Z .004), and standard (P Z .007) all higher than FUSE. Endocuff higher than EndoRings (P < .001) and standard (P Z .004). No differences in
ADR by site.
{Number of patients with designated polyp type (%).
kEndoRings higher than FUSE (P < .001) and standard (P < .001); FUSE higher than standard (P < .001).
**Endocuff (P Z .002), EndoRings (P Z .041), and standard (P < .001) higher than FUSE. Standard higher than EndoRings (P Z .015).
yyEndocuff (P < .001), EndoRings (P Z .009), and standard (P < .001) higher than FUSE. Endocuff higher than EndoRings (P Z 0.16) and standard (P < .001).
zzAt Indianapolis Endocuff (P Z .003) and EndoRings (P Z .007) higher than FUSE.

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