Introduction
Worldwide, colorectal cancer (CRC) is the third most common cancer within the category
of newly diagnosed types of cancer and the second leading cause of death related to
cancer. In Mexico, CRC is the fourth most commonly diagnosed type of cancer and the
sixth cause of death related to cancer. In 2018, there were 1,849,518 new cases of
CRC in the world and 880,792 deaths; in Mexico, there were a total of 10,457 newly
diagnosed CRC cases and roughly 5,700 deaths [1].
CRC incidence and mortality rates have stabilized or even declined in a number of
high human development index countries such as the United States, Australia, New Zealand,
and several Western European countries. One of the reasons is the increased early
detection and prevention through diagnostic screening procedures such as colonoscopy
with polypectomy. On the other hand, several countries in Latin America, the Caribbean,
and Asia, with limited health infrastructure and poorer access to early detection
and treatment have reported increasing CRC mortality [2].
There are two main types of precancerous lesions in the colon, namely conventional
adenomas and serrated lesions. Adenomas are the precursors of 70 % of all CRC cases
and are generated in the adenoma-carcinoma sequence, which is believed to take more
than 10 years in completing its growth in sporadic cancers [3]. The U.S. Multi-Society Task Force on Colorectal Cancer recommends offering CRC
screening to average-risk individuals and those without a high-risk family history
of colorectal neoplasia, beginning at the age of 50 years; a colonoscopy every 10
years, annual fecal immunochemical testing (FIT), CT colonography every 5 years, FIT-fecal
DNA every 3 years, flexible sigmoidoscopy every 5 to 10 years, and capsule colonoscopy
every 5 years, all of which are considered appropriate screening tests for the detection
of early CRC or precancerous lesions [3].
The optimal effectiveness of colonoscopy in preventing CRC depends on the quality
of the procedure. This quality can be measured by comparing the performance of an
endoscopist with a standard reference or benchmark [4]. The specific parameter used for comparisons is called a “quality indicator.” The
quality indicators for colonoscopy that have been found to decrease CRC incidence
and mortality rates are: 1. frequency of adequate bowel preparation; 2. use of recommended
surveillance intervals; 3. cecal intubation rate; 4. withdrawal time; and 5. adenoma
detection rate (ADR) [4].
The American Society for Gastrointestinal Endoscopy (ASGE) and the European Society
of Gastrointestinal Endoscopy (ESGE) recommend a minimum target for overall ADR of
at least 25 %, with specific rates of 30 % for men and 20 % for women [4]
[5]. These recommendations aim to improve ADR results, as it has been shown that for
each 1 % increase in ADR there is a 3 % reduction in CRC incidence and a 5 % reduction
in cancer mortality [6]
[7]. Knowledge of the ADR allows improving the quality of colonoscopies through proper
feedback and training of the endoscopists [8].
The increase in CRC incidence and mortality over the past 10 years in Latin American
countries, including Mexico, may be explained by delays in diagnosis, referral, and
treatment, as well as financial constraints [2]. Also, countries with low ADR perform poorly in the identification of patients with
precancerous lesions and increased CRC risk due to failure to clear the colon. Hence,
the objective of this study was to evaluate the current ADR among Mexican endoscopists
with experience in CRC screening and to compare their results with those shown in
published reports from this country.
Patients and methods
Study design and patients
We carried out a retrospective study to analyze the performance of experienced endoscopists
at two endoscopy units from tertiary care private hospitals in Mexico City. The study
protocol was reviewed and approved by the Institutional Review Boards of both centers.
The research included individuals older than 50 years who underwent screening or diagnostic
colonoscopy from July 2012 to June 2014 in center number 1 and from January 2015 to
December 2016 in center number 2. We were not able to include data from 2017 onward
because some of the endoscopists that participated in this study also participated
in other protocols. Patients were excluded if they had previously been diagnosed with
CRC, had suffered any surgical resection of the colon, had history of any polyp syndrome,
Lynch syndrome or inflammatory bowel disease, had indication of a therapeutic procedure,
incomplete colonoscopy, or an inadequate bowel preparation. The latter was defined
as a score of 5 or less in total or 1 or less in any of the segments in accordance
with the Boston Bowel Preparation Scale (BBPS). Patients were also excluded if there
was no available pathology report or the colonoscopy was device-assisted.
Endoscopic procedures
Each physician had performed a minimum of 400 colonoscopies, with an average of more
than 200 general colonoscopies per year, and aside from having received fellowship
training, they were certified by the Mexican Gastroenterology Board. All the procedures
were performed using the EVIS EXERA II CV-180 video processor (Olympus, Tokyo, Japan)
and CF-H180AL model colonoscopes (Olympus, Tokyo, Japan). The procedures were done
under intravenous sedation supervised by an anesthesiologist with Board certification.
No fellows in gastroenterology or gastrointestinal endoscopy participated in the colonoscopies.
Data collection and study outcome
Patient information including socio-demographics, procedure results, and pathology
reports were accessed for this study after careful review of the electronic medical
records. The primary outcome was the ADR analysis in order to compare it with reported
data from Mexico. Secondary outcomes included the polyp detection rate (PDR), the
mean number of adenomas per colonoscopy (APC) and, the advanced adenoma detection
rate (AADR). ADR, PDR and AADR are defined by the proportion of patients aged 50 years
or older undergoing screening or diagnostic colonoscopy with at least one histologically
proven adenoma, polyp, or advanced adenoma, respectively [5]
[9]
[10]. Advanced adenoma was defined as a lesion with villous features, high-grade dysplasia,
or size greater than 10 mm. The APC was defined as the total number of adenomas divided
by the total number of colonoscopies performed [10]. These secondary targets were investigated only in center number 2.
Literature overview
We performed an electronic search in Medline and Google Scholar databases to identify
all the articles that reported ADR in Mexico. We also conducted a manual search looking
for additional relevant articles. Our research went as far as April 30, 2020; articles
in English and Spanish were both included at this stage. All groups of patients and
interventions were analyzed to obtain the individual data needed to calculate a pooled
ADR.
Statistical analysis
Descriptive statistics with frequency and percentages were used to determine socio-demographic
characteristics. ADR, PDR, and AADR were presented as percentages with 95 % confidence
intervals, while APC was described by average estimates. ADR groups comparisons were
made using a chi-square test. P < 0.05 was considered statistically significant. All statistical analyses were performed
using a standard software package (Stata, version. 14.1; StataCorp).
Results
Baseline characteristics
From July 2012 to June 2014, a total of 1,344 colonoscopies were performed at center
number 1 by four practicing endoscopists and from January 2015 to December 2016, a
total of 1,218 colonoscopies were performed at center number 2 by another four practicing
endoscopists. After application of inclusion and exclusion criteria, 879 screening
colonoscopies from center number 1 and 599 screening colonoscopies from center number
2 were included in our study, with a total of 1,478 endoscopic procedures performed
by 8 endoscopists. The median age of the population sample was 64 years and 47 % of
subjects were male. No significant differences were found between the two centers.
Primary outcome
The global ADR of the 1,478 colonoscopies included in the study was 24.6 % (95 %CI,
22.4 %–26.8 %). For center number 1, the mean ADR was 24.0 % (95 %CI, 21.2 %–26.8 %),
and for center number 2, the mean ADR was 25.5 % (95 %CI, 22.1 %–29.0 %). Individually,
ADRs ranged between 19.2 % and 30 % ( [Table 1]). The percentage of adenomas measuring > 10 mm was 4.3 % (95 %CI, 2.9 %–6.3 %) and
CRC was diagnosed in 1.3 % (95 %CI, 0.7 %–2.7 %) of the colonoscopies performed in
center number 2. There is no data regarding polyp size nor CRC prevalence from center
number 1.
Table 1
Adenoma detection rate per endoscopist.
|
Endoscopy unit
|
Endoscopist
|
Colonoscopies (n)
|
Adenoma Detection Rate (%)
|
|
Center 1
|
1
|
300
|
22.6
|
|
2
|
204
|
30.4
|
|
3
|
125
|
19.2
|
|
4
|
250
|
22.8
|
|
Center 2
|
5
|
165
|
24.8
|
|
6
|
144
|
29.2
|
|
7
|
185
|
22.2
|
|
8
|
105
|
27.6
|
As for relevant literature, we found seven articles that reported 11 ADR values ( [Table 2]). The ADR presented a wide range of values, varying from 5.8 % to 30.7 % [11]
[12]
[13]
[14]
[15]
[16]
[17]. Four of these papers were comparative studies, 3 of them compared conventional
versus endocuff-assisted colonoscopies [12]
[13]
[14]; in the fourth one, a tandem design was employed, comparing the index and second
colonoscopies after improvement of colon cleansing according to the BBPS [15]. ADR values from endocuff-assisted colonoscopies were excluded. The average ADR
was 15.2 % (95 %CI, 13.3 %–17.1 %), while the ADR obtained from colonoscopies in our
study was 24.6 % (216/1,422 [15.2 %] vs. 364/1,478 [24.6 %]; P < 0.001) ( [Fig.1]).
Table 2
ADR reported in previously published studies in Mexico.
|
Authors
|
Publishing year
|
Study design
|
Location
|
Fellow participation
|
Inclusion criteria
|
Colonoscopies (n)
|
Mean BBPS
|
Mean age (years)
|
ADR (%)
|
|
Gutiérrez-Serrano RI, et al. [11].
|
2019
|
Retrospective
|
Second-level public hospital
|
NA
|
15 to 85 years old
First colonoscopy
IBS
|
CC 233
|
NA
|
71 % > 50
|
CC 13.3
|
|
Andujar-Amor MA, et al. [12]
|
2018
|
Prospective
Comparative
|
Third-level public hospital
|
Yes
|
> 18 years old
Screening and surveillance colonoscopies
|
CC 50
EAC 50
|
NA
|
CC 46
EAC 44
|
CC 28
EAC 44
|
|
González-Fernandez C, et al. [13]
|
2017
|
Prospective
Comparative
|
Third-level public hospital
|
Yes
|
> 50 years old
Screening colonoscopy
|
CC 163
EAC 174
|
CC 7
EAC 7
|
CC 62
EAC 60
|
CC 13.5
EAC 22.4
|
|
Peniche-Moguel PA et al. [14]
|
2016
|
Prospective
Comparative
|
Third-level public hospital
|
NA
|
> 18 years-old
|
CC 72
EAC 73
|
CC 7.04
EAC 7.11
|
Total 53
|
CC 13.7
EAC 31.9
|
|
Zamora-Morales M, et al. [15]
|
2016
|
Prospective
Comparative
|
Third-level public hospital
|
NA
|
> 50 years-old
FC: BBPS ≤ 5
|
FC 52
SC 52
|
FC 4.37
SC 7.38
|
Total 56
|
FC 5.8
SC 30.7
|
|
García-Osogobio S, et al. [16]
|
2015
|
Prospective
|
Third-level private hospital
|
No
|
40 to 79 years old
First colonoscopy
|
CC 99
|
CC 7.91
|
CC 50
|
17
|
|
Lascurain-Morhan E, et al. [17]
|
2001
|
Retrospective
|
Third-level private hospital
|
No
|
Rectosigmoidoscopy
|
CC 701
|
CC NA
|
CC 55
|
14.7
|
|
ADR, adenoma detection rate; BBPS, Boston Bowel Preparation Scale; CC, conventional
colonoscopy; EAC, Endocuff-assisted colonoscopy; FC, first colonoscopy with fair-poor
BBPS; SC, second colonoscopy with improved BBPS; IBS, irritable bowel syndrome; NA,
data not available.
Fig. 1 Adenoma detection rate (ADR). Comparison of previously reported data with results
from the present study.
Secondary outcomes
The PDR, AADR, and APC were all analyzed by the 4 endoscopists from center number
2 ( [Fig.2]). The PDR was 39.1 % (95 %CI, 35.1 %–43.1 %); advanced adenomas were detected in
31 out of 599 colonoscopies, with an AADR of 5.2 % (95 %CI, 3.5 %–7.3 %); lastly,
a total of 247 adenomas were detected in 599 colonoscopies by the 4 endoscopists from
center number 2, with an APC mean of 0.41 (range 0.33 to 0.53).
Fig. 2 PDR, ADR, and AADR from center number 2.
Discussion
The average ADR in our study was 24.6 %, which almost meets the criteria set in the
latest ESGE and ASGE guidelines [4]
[5]. The ADR from center number 1 was 24.0 %, whereas the ADR from center number 2 was
25.5 %. Center number 2 did fulfill the benchmark for ADR as a quality indicator.
These percentages are derived from the ESGE and ASGE guidelines, both based on data
from western countries. CRC incidence can vary widely between countries, the age-standardized
incidence rate per 100,000 persons according to data derived from the GLOBOCAN 2018
is 11.2 for Mexico, 32.1 for the United Kingdom, 25.6 for the United States, and 4.4
for India [1]. The ADR may be affected by the mentioned CRC incidences. Endoscopists in the United
States of America have reported ADRs as high as 70 % in Endocuff-assisted colonoscopies,
while Indian literature shows an ADR of 6.7 % [18]
[19]. In Mexico Endocuff-assisted colonoscopy has provided an ADR of 44 % [12]. ADR benchmarks need to be defined by country, however information to make this
possible is still missing. We believe that the current ADR benchmark could be different
among countries according CCR incidence; but the information to support this statement
is unavailable. Published studies from Mexico reported an ADR ranging from 5.8 % to
30.7 % ( [Table 2]) [11]
[12]
[13]
[14]
[15]
[16]
[17]. The pooled ADR from colonoscopies in these publications was 15.2 %. These data
would seem indicate that the Mexican population has a low prevalence of adenomas and
CRC. Nevertheless, the ADR in our study was 24.6 %, showing a statistically significant
difference when compared with reported ADRs ( [Fig.1]). It is important to highlight that the studies included in [Table 2] show a significant heterogeneity in terms of the methodological design, characteristics
of the centers, operators and inclusion criteria. This can cause different ADR results
and limit the comparison; however, this information shows us the data from our country,
as a region with low ADRs and, calls for awareness about the urgency of achieving
the goals of CCR screening. CRC is the fourth most commonly diagnosed type of cancer
in Mexico, which makes us believe that the true adenoma prevalence in Mexico is much
higher than reported. The ADR value of 15.2 % found in Mexican studies may reflect
the performance of low-quality colonoscopies carried out in many Mexican centers and
calls for quality improvement actions that could in turn improve the ADR. Further,
competency in colonoscopy is achieved after 400 procedures during a Gastrointestinal
Endoscopy fellowship and by maintaining a colonoscopy volume of over 200 procedures
per year [20]
[21].
In Germany for example, increased awareness of quality control through the German
Screening Colonoscopy Program resulted in an increase in the ADR among 39.6 % of endoscopists
in a 10-year period [22]. Likewise, the feedback with benchmarking using colonoscopy quality indicators resulted
in a sustained annual improvement of 1.5 % in overall ADR in Poland, with 74.5 % of
endoscopists improving their ADR [6]. Endocuff-assisted colonoscopy has shown an improvement in ADR in comparison with
standard colonoscopy without major adverse events, especially for operators with low
to moderate ADRs [23]. We did not include results from colonoscopies using distal attachment devices or
other technologies in this study; however, we would like to underline that the results
of endocuff-assisted colonoscopies from Mexican studies have shown ADRs as high as
44 % [12].
The mortality-to-incidence ratio (MIR) provides a mean to assess the burden of a disease
by presenting mortality after accounting for incidence. The MIR has been found to
be an insightful measure of the efficacy of cancer control programs [24]. Mortality and incidence data derived from the GLOBOCAN 2018 showed that the MIR
of CRC in Latin American countries is higher in comparison with that of high human
development index countries like the United States, Australia, and Western European
countries [1]. The MIR of CRC in Mexico, Brazil, Argentina, and Colombia is 0.55, 0.55, 0.60,
and 0.60 respectively, while in Australia, the United Kingdom, Japan, and the United
States is 0.17, 0.38, 0.41, and 0.42 respectively [1]. The differences in the MIR of CRC between high and low human development index
countries can be explained by the quality of their health care systems and screening
programs. Developing countries may view a CRC screening program based on colonoscopy
as a public health burden [25]. Therefore, before considering a mass screening colonoscopy program, the current
quality of colonoscopies performed in Mexico should be first defined and optimized.
Mexico does not have a unified national CRC screening program; yet, opportunistic
screening colonoscopy is performed by endoscopists in both public and private medical
centers.
Detection and prevention of CRC is one of the most important targets in the practice
of gastrointestinal endoscopists. Precancerous lesions can be identified by colonoscopy
and properly removed, but it is the responsibility of endoscopists to guarantee the
quality of all the procedures that she/he performs. To improve quality in colonoscopy,
endoscopists must first be aware of quality indicators and be able to compare their
performance with that of fellow endoscopists of their country, so they can evaluate
and contrast their performance on any improvement intervention [26]. Benchmarking is the process of comparison based on a certain standard to develop
better or even optimal practices. The motivation is to provide evidence that the physicianʼs
performance is of high quality [27]. Mexican endoscopists who carry out screening colonoscopies are not aware of their
results regarding quality indicators, so they are unable to perform benchmarking,
but also, they fail to keep a systematic record of their evaluations. This led us
to search for a tool to improve our daily practices in colonoscopy procedures. We
thus created an application for mobile devices (App) that registers personal and regional
quality indicator results for colonoscopy screening, including ADR, PDR, APC, as well
as frequency of adequate bowel preparation. The data provided by our App, named ColonApp,
will allow Mexican endoscopists to perform benchmarking and improve the quality of
its colonoscopy procedures.
The PDR is defined as the number of patients with one or more polyps removed during
screening colonoscopy [4]. This performance measure does not require pathology data and may correlate with
the ADR; in fact, conversion rates from PDR to ADR have been proposed [28]. The ESGE recommends a minimum PDR of 40 % [29]. The proposed APC minimum detection benchmark is 0.50 for men and 0.20 for women
[30]
[31]. Currently, there is no AADR benchmark recommended in the ASGE or ESGE guidelines
[4]
[5]. The suggested threshold value for AADR is 5 % to 10 %; however, there is no proof
that these values apply to large-scale screening programs involving centers with lower
adenoma detection rates [32]. The APC and the AADR found in our study surpassed the proposed quality benchmarks,
but no the PDR.
As strengths of our study, all colonoscopies were performed by certified endoscopists
with experience in CRC screening, more than one medical center was included in the
investigation, and other quality indicators, such as adequate bowel preparation, were
considered. The retrospective nature of the study could be considered an advantage
because it reflects real life ADR and is not affected by the performance pressure
of endoscopists enrolled in prospective ADR studies. On the other hand, the limitations
of the study were mainly the inclusion of diagnosis and screening colonoscopies, and
the lack of sufficient data to analyze size of adenomas and other quality indicators,
such as withdrawal time. Further studies with a larger sample size and the inclusion
of more endoscopy units are needed to better evaluate the quality of screening colonoscopy
in Mexico.
Conclusions
In conclusion, the major finding of our research is that the ADR of the endoscopists
working in two tertiary care private hospitals in Mexico City is above that reported
in Mexican studies. Our results suggest that published data in Mexico is related to
poor quality in colonoscopy performance rather than to low adenoma and CRC incidence.
The data from this work can generate awareness regarding the great opportunity of
improving the quality of colonoscopies afforded to countries with economic developments
and health systems similar to Mexico, in the hopes of achieving the expected benefits
of colorectal cancer screening.
