Preventive Medicine 118 (2019) 304–308

Contents lists available at ScienceDirect

Preventive Medicine
journal homepage: www.elsevier.com/locate/ypmed

Risk factors for severe complications of colonoscopy in screening programs T

a a,b a b
Mercedes Vanaclocha-Espi , Josefa Ibáñez , Ana Molina-Barceló , María José Valverde-Roig ,
Elena Pérezb, Andreu Nolascoc, Mariola de la Vegad, Isabel Diez de la Lastra-Boschd,
María Elena Ocejae, Josep Alfons Espinàsf,g, Rebeca Fontf,g, Francisco Pérez-Riquelmeh,i,
⁎
Eunate Arana-Arrij, Isabel Portillok, Dolores Salasa,b, , CRIBEA Group1
a
Cancer and Public Health Area, FISABIO - Public Health, Valencia, Spain
b
General Directorate Public Health, Valencian Community, Spain
c
University of Alicante, Spain
d
General Directorate of Assistance Programs, Canarias, Spain
e
General Directorate Public Health, Cantabria, Spain
f
Catalan Cancer Strategy, Department of Health, Catalonia, Spain
g
Biomedical Research Institute, Bellvitge, (IDIBELL) – L'Hospitalet de LLob, Barcelona, Spain
h
General Directorate Public Health, Murcia, Spain
i
Biomedical Research Institute of Murcia (IMIB-Arrixaca-UMU), University Clinical Hospital Virgen de la Arrixaca, University of Murcia, Spain
j
Biocruces Research Institute, Barakaldo, Spain
k
The Basque Health Service, Basque Country, Spain

A R T I C LE I N FO A B S T R A C T

Keywords: Severe complications (SC) in colonoscopy represent the most important adverse effect of colorectal cancer
CCR screening screening programs (CRCSP). The objective is to evaluate the risk factors for SC in colonoscopy indicated after a
Colonoscopy positive fecal occult blood test in population-based CRCSP. The SC (n = 161) identified from 48,730 diagnostic
Harms colonoscopies performed in a cohort of all the women and men invited from 2000 to 2012 in 6 CRCSP in Spain. A
total of 318 controls were selected, matched for age, sex and period when the colonoscopy was performed.
Conditional logistic regression models were estimated. The analysis was performed separately in groups: im-
mediate-SC (same day of the colonoscopy); late-SC (between 1 and 30 days after); perforation; and bleeding
events. SC occurred in 3.30‰ of colonoscopies. Prior colon disease showed a higher risk of SC (OR = 4.87).
Regular antiplatelet treatment conferred a higher risk of overall SC (OR = 2.80) and late-SC (OR = 9.26), as did
regular anticoagulant therapy (OR = 3.47, OR = 7.36). A history of pelvic-surgery or abdominal-radiotherapy
was a risk factor for overall SC (OR = 5.03), immediate-SC (OR = 8.49), late-SC (OR = 4.65) and perforation
(OR = 21.59). A finding of adenoma or cancer also showed a higher risk of overall SC (OR = 8.71), immediate-
SC (OR = 12.67), late-SC (OR = 4.08), perforation (OR = 4.69) and bleeding (OR = 17.02). The risk of SC
doesn't vary depending on the type of preparation or type of anesthesia. Knowing the clinical history of patients
such as regular previous medication and history of surgery or radiotherapy, as well as the severity of the findings
during the colonoscopy process could help to focus prevention measures in order to minimize SC in CRCSP.

Abbreviations: SC, Severe complication; CRC, Colorectal Cancer; CRCSP, Colorectal cancer screening programs
⁎
Corresponding author at: General Directorate Public Health, Valencian Community, Spain & Cancer and Public Health Area, FISABIO – Public Health, Avda.
Catalunya, 21., 46020, Valencia, Spain.
E-mail address: salas_dol@gva.es (D. Salas).
1
Dolores Salas; Josefa Ibáñez; Elena Pérez; Ana Molina; Mª José Valverde; Susana Castan; Mercedes Andrés; Gloria Teruel; Maria Girones; J. Ramón Moles; Marta
Ponce; Mercedes Vanaclocha; Rebeca Font; Álvaro González de Aledo; Mariola de La Vega Prieto; Isabel Regina Díez de la Lastra; Francisco Pérez-Riquelme; Jose
Cruzado; María Elena Oceja Setién; Mª Antonia Muñoz Laví; Josep A Espinàs; Amaia Bacigalupe de la Hera; Ana Samper Izarra; Begoña Uranga Mugica; Enrique
Ojembarrena Martínez; Eunate Arana-Arri; Fidencio Bao Pérez; Inés Gil Lasa; Isabel Idígoras Rubio; Isabel Portillo Villares; Javier Fernández Fernández; José Luís
Hurtado Mendoza; Maria Eugenia Alkiza Eizagirre; Montserrat Calvo Sánchez; Raquel Pérez Garay; Santiago Esnaola Suquia; Marià Carulla; Xavier Castells; Jaume
Grau; Raquel Legido; Montse Llorens.

https://doi.org/10.1016/j.ypmed.2018.11.010
Received 1 June 2018; Received in revised form 5 October 2018; Accepted 7 November 2018
Available online 08 November 2018
0091-7435/ © 2018 Elsevier Inc. All rights reserved.
M. Vanaclocha-Espi et al. Preventive Medicine 118 (2019) 304–308

1. Introduction CRCSP. Participating CRCSP are population-based screening programs

targeting men and women aged 50 to 69 years. The screening test is
Colorectal cancer (CRC) is the second cause of mortality from cancer biennial FOBT and diagnostic confirmation is through colonoscopy.
in developed countries in both men and women (Ferlay et al., 2015). This study was approved by the Ethics Committee for Clinical Research.
The World Health Organization and the European Union recommend The study was performed in accordance with the principles of the de-
population-based colorectal cancer screening programs (CRCSP) claration of Helsinki and the Spanish legal requirements of con-
(Ferlay et al., 2015; Council Recommendation, 2003). The aim of these fidentiality.
programs is to reduce mortality and the incidence of CRC through early The CRIBEA study designed a common database for the CRCSP
detection of these tumors and elimination of adenomatous polyps (Pan containing information on 1,995,719 invitations sent to 1,320,300
et al., 2016; Hardcastle et al., 1996). There is evidence of the effec- people (Vanaclocha-Espi et al., 2017; Portillo et al., 2017). Within this
tiveness of various screening tests, such as the fecal occult blood test project, a case-control study was designed to study the adverse effects
(FOBT), sigmoidoscopy, colonoscopy and the combination of FOBT and of CRCSP related to the complications of colonoscopy. Cases and con-
colonoscopy (Segnan et al., 2010). In view of the recommendations of trols were selected from the cohort participating in the CRIBEA study,
the World Health Organization and the European Union (Ferlay et al., specifically among participants with a positive FOBT and diagnostic
2015; Council Recommendation, 2003), CRCSP have been implemented colonoscopies. Follow-up colonoscopies were not included. The total
since 2000 in various autonomous communities of Spain (Salas Trejo number of diagnostic colonoscopies conducted was 48,730. All patients
et al., 2017). These CRCSP use the FOBT as the screening test and co- provided informed consent to undergo colonoscopy and received an
lonoscopy for diagnostic confirmation (Salas Trejo et al., 2017). information sheet on preparation for the procedure indicating the need
Colonoscopy is considered a safe and effective technique in the to discontinue antiplatelet and anticoagulant therapy days before the
detection and treatment of colorectal lesions (Pignone et al., 2002; examination, depending on the treatment and dosage (Rodrigo, 2011).
Walsh and Terdiman, 2003), but carries a risk of severe complications
(SC), any complication requiring hospital admission or causing death, 2.2. Study design: cases and controls
due to perforation, bleeding requiring transfusion, vagal syndrome or
peritonitis, and occurring between 0 and 30 days after colonoscopy, Cases consisted of all SC related to diagnostic colonoscopy identified
which represent an adverse effect of CRCSP (Segnan et al., 2010). In in the participating population that underwent diagnostic colonoscopy
population-based CRCSP with guaiac FOBT, the estimated rate of per- in the cohort analyzed in the CRIBEA project. Following the criteria
foration and serious hemorrhagic is between 0.5% and 1.6% of subjects established by the European guidelines for quality of colorectal cancer
undergoing colonoscopy (Segnan et al., 2010). The large-scale im- screening, we defined SC as any complication requiring hospital ad-
plementation of CRCSP has created the need to evaluate the benefits mission or causing death due to perforation, bleeding requiring trans-
and possible harms of these programs. Specifically, one type of adverse fusion, vagal syndrome or peritonitis, and occurring between 0 and
effect is the complications of diagnostic colonoscopy, which is some- 30 days after colonoscopy (Segnan et al., 2010). We distinguished
times carried out for therapeutic purposes (resection of polyps and among SC according to time of onset, as follows: immediate-SC were
cancer) in these programs. those occurring on the same day as colonoscopy and late-SC were those
Previous studies have demonstrated that the risk of an SC is higher occurring between 1 and 30 days after colonoscopy.
after colonoscopy with polypepctomy (Rutter et al., 2012; Levin et al., SC were identified through the endoscopic report of the CRCSP or
2006; Ko et al., 2010). Some polyp characteristics have also been stu- through linking of the information on the colonoscopies performed in
died, such as size, type and localization, and patient characteristics, the CRCSP and the information on hospital admissions in the period
such as body mass index and sex, are risk factors for bleeding compli- between the performance of the colonoscopy and up to 30 days later.
cations after polypectomy (Kim et al., 2007; Zhang et al., 2014; Blanks All SC in the study population were identified. Specifically, perforations
et al., 2015; Kwon et al., 2015) and perforation or death during and and bleeding events requiring transfusion were detected, while there
after colonoscopy (Heldwein et al., 2005). Several studies have related were no cases of vagal syndrome or peritonitis. There was one death
the quality of colonoscopy to the risk of complications; specifically, one that resulted from a perforation.
study reported that inadequate bowel preparation increased the risk of Controls were selected from diagnostic colonoscopies without SC,
complications (Chan et al., 2015), while others have associated the and were matched by age (in 5-year strata), sex, CRCSP, and the period
endoscopist's experience with the quality of the process (Jover et al., when the colonoscopy was performed (before 2010/ from 2010 to
2016; Rajasekhar et al., 2016; Cardin et al., 2012). The occurrence of 2013).
post-colonoscopy bleeding is more common in patients taking antic- Two controls were selected for each case, we excluded cases and
oagulants (Tong et al., 2015; Hui et al., 2004). controls with colonoscopies performed in private centers and with non-
Given that it is important to determine risk factors for SC to mini- severe complications and finally, cases were matched with 1 or 2
mize the adverse effects of CRCSP and that the complications of colo- controls (Table 1). The total number of cases and controls varied ac-
noscopy can be associated with patients' personal history and char- cording to whether they were immediate or late and according to
acteristics of the procedure, the aim of this study was to evaluate the whether the SC consisted of a perforation or bleeding event.
risk factors for SC in colonoscopy through a case-control study to esti-
mate the risks of SC depending on personal history, procedural char- 2.3. Exposure variables
acteristics and colonoscopy findings.
An active search was made in the clinical histories of cases and
2. Methods controls and information was gathered on personal history, the char-
acteristics of the procedure and the findings of the test, specifically:
2.1. CRIBEA project
- History of symptoms (6 months prior to the colonoscopy): change in
The CRIBEA project is a retrospective study of a cohort of all the bowel habits; rectorrhagia, melena and/or anemia.
men and women invited to screening between 2000 and 2012 in 6 - History of investigations performed (last 5 years): colonoscopy and/
CRCSP implemented in the autonomous communities of the Canary or sigmoidoscopy.
Islands, Cantabria, Catalonia, Murcia, the Basque Country, and the - History of prior disease: colon disease (chronic inflammatory dis-
Valencian Community in Spain. The project aims to identify the factors ease, colorectal polyps, presence of diverticula); coagulation dis-
that can influence the balance between the benefits and harms of orders; lung disease; heart disease; diabetes mellitus; alcoholism and

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other addictions. treatment with sedation and hypnotics. Overall SC, immediate, late and
- History of regular treatment prior to colonoscopy: antiplatelet perforation-related SC were more common in patients with prior pelvic-
agents (eg, clopidogrel, ASPIRIN at antiplatelet doses); antic- surgery or abdominal-radiotherapy (PA above 0.98).
oagulants (SINTROM, heparins or others); oral iron therapy; seda- Procedural characteristics in cases and controls are shown in
tives or hypnotics. Table 4. The percentage of persons who were poorly informed was
- History of Abdominal-pelvic-surgery and/or abdominal-radio- higher in cases with hemorrhagic-SC (PA = 0.91). For overall SC, im-
therapy. mediate, late, perforation-related and hemorrhagic SC, there was a high
- Characteristics of the procedure: information on bowel cleansing PA with the professional performing the sedation, the quality of bowel
(better/worse); type of cleansing (magnesium-citrate/disodium cleansing, and the type of colonoscopy (PA higher than 0.93). The
phosphate/polyethylene-glycol); type of sedation and analgesia percentage of SC was lower when the professional performing the se-
(none/deep/superficial); health professional administering the se- dation was an endoscopist, when the quality of bowel cleansing was
dation (anestesiologist/endoscopist/nurse/others); quality of excellent and when the colonoscopy was purely diagnostic (PA higher
cleaning (excellent/good/acceptable/poor or inadequate); type of than 0.84). The number of polyps found showed a PA above 0.99 with
colonoscopy (diagnostic without polypectomy/diagnostic with overall SC, late, perforation and hemorrhagic SC, the final diagnosis
polypectomy). showed PA = 1 with overall SC, and immediate, late and perforation-
- Colonoscopy findings: number of extirpated polyps; final diagnosis related SC and PA = 0.82 with hemorrhagic-SC.
(normal for screening or low-risk adenoma/medium-high-risk ade- The results of multivariate models are shown in Table 5. Variables
noma or CCR). of previous diseases that had a high PA with patients' regular treatment
were not included. The models included the most relevant predictors
2.4. Statistical analysis and provided the most precise estimates. The OR for the occurrence of a
SC was 5.35(CI 1.40–20.46) in patients with colon disease, 3.83(CI
The study population and the number of SC are described by age, 1.62–9.05) in patients taking regular antiplatelet therapy versus those
sex, and period when the colonoscopy was performed, and the rate of not receiving this treatment, OR = 3.56(CI 1.21–10.43) for antic-
SC was calculated as the proportion of participants developing a SC oagulant therapy, OR = 5.45(CI 2.78–10.70) for a history of pelvic-
among diagnostic colonoscopies performed among participants with a surgery or abdominal-radiotherapy, and OR = 9.36(CI 4.44–19.69) for
positive FOBT between 2000 and 2012. Rates are expressed per 1000 a diagnosis of adenoma or CRC, colonoscopy type was not statistically
diagnostic colonoscopies. significant. The risk of an immediate-SC was higher if there was a
To analyze the association between an exposure factor and SC, data history of pelvic-surgery or abdominal-radiotherapy, OR = 8.49(CI
were described through contingency tables. The statistical technique 3.52–20.52), and if the diagnosis was adenoma or CRC, OR = 12.67(CI
used to analyze the relationship between two variables was based on 4.32–38.65), colonoscopy type was not statistically significant. The risk
Bayes' theorem, calculating the probability of association (PA) as pos- of a late-SC was higher in patients taking regular antiplatelet therapy
teriori probability of the null hypothesis (H0: relationship between the versus those not receiving this treatment, OR = 9.26(CI 3.10–27.65), in
two variables) being valid, given the difference observed giving rise to those taking anticoagulants, OR = 7.36(CI 1.60–33.87), in those with a
the data (d0), that is, calculating: P(H0/d0) (Albert, 2007), In this study, history of pelvic-surgery or abdominal-radiotherapy OR = 4.65(CI
high probability was defined when values above 0.8. Conditional lo- 1.70–12.70), in those with a diagnosis was adenoma or CRC,
gistic regression models were adjusted for SC. The models included OR = 4.08(CI 1.69–9.84) and if the colonoscopy was diagnostic-ther-
those exposure factors showing a high a posteriori PA. We excluded apeutic OR = 2.59(CI 1.29–5.20). The risk of perforation was higher in
those variables with an expected frequency of less than 5 in at least one patients with a history of pelvic-surgery or abdominal-radiotherapy,
of its categories. A multivariate model was adjusted for each of the case- OR = 21.59(CI 7.99–58.32), if the diagnosis was adenoma or CRC,
control groups. The conditional model allowed control of the correla- OR = 4.69(CI 2.07–10.61) and if the type of colonoscopy was diag-
tion between matched data. The results are shown as odds ratios (OR) nostic-therapeutic OR = 2.77(CI 1.02–7.51), while the risk of perfora-
and 95% confidence intervals. The data analysis was performed using tion was lower in patients receiving regular treatment with sedatives or
the R program. hypnotics, OR = 0.34(CI 0.12–0.93). A high risk of hemorrhage was
conferred by regular antiplatelet therapy, OR = 3.74(CI 1.27–11.01),
3. Results anticoagulants, OR = 10.34(CI 1.82–58.80) and a diagnosis of ade-
noma or CRC, OR = 17.02(CI 4.13–70.23), while the risk of hemor-
SC occurred in 3.3‰ of diagnostic colonoscopies; 3.56‰ in men rhage was lower in patients who were better informed about bowel
and 2.95‰ in women, 2.42‰ in participants aged 50–59 years and cleansing, OR = 0.18(CI 0.04–0.79). Like the model for overall SC and
4.07‰ in those aged 60–70 years. SC occurred in 3.09‰ of colo- immediate SC, in the model for bleeding, colonoscopy type was not
noscopies performed between 2000 and 2009 and in 3.33‰ of those statistically significant when other factors were considered
carried out between 2010 and 2013 (Table 2). OR = 1.09(CI 0.25–4.80).
A total of 83 SC were immediate. Of these, 75.9% were perforations
and 24.1% were bleeding events requiring transfusion. There were 78 4. Discussion
late-SC, of which 44.9% were perforations occurring at a mean of
3.3 ± 4.6 days after the colonoscopy, and 55.1% were bleeding events This study shows that risk factors for SC in screening colonoscopy
with 6.0 ± 5.6 days after the procedure. are a prior pelvic-surgery or abdominal-radiotherapy, colonoscopy with
The characteristics of personal antecedents are shown in Table 3. polypectomy, detection of adenoma or CRC and regular antiplatelet and
There was a very low probability of an association between SC and anticoagulant therapies. The study also shows that the factors influen-
symptoms 6 months before colonoscopy and investigations performed cing the appearance of late-SC differ from those influencing immediate-
in the last 5 years. Overall SC, and late and hemorrhagic SC were more SC, with a history of regular antiplatelet and anticoagulant use before
common in persons with prior colonic disease, coagulation disorders, colonoscopy and diagnostic-therapeutic colonoscopy increasing the risk
and heart disease (PA above 0.87), these complications were more of late-SC. The factors influencing the development of perforations and
frequent when the patient was taking regular anticoagulant therapy (PA bleeding events also differ, regular antiplatelet and anticoagulant
above 0.83). Overall SC, late, perforation-related and hemorrhagic SC treatment before colonoscopy increased bleeding risk the type of in-
were more frequent in patients taking regular antiplatelet therapy (PA formation on bowel preparation was a protective factor for bleeding,
above 0.89). Perforation-related SC showed a PA = 0.84 with regular while diagnostic-therapeutic colonoscopy and pelvic-abdominal

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surgery increased perforation risk. Unlike other studies, we found no relationship between the type of
The overall rate of SC in our study was 3.3‰ (in the context of a preparation and SC. One study analyzed the type of preparation in
population-based screening program using guaiac or immunological bowel cleansing and reported a higher percentage of adverse effects
FOBT and colonoscopy for diagnostic confirmation), which is lower such as nausea, vomiting and abdominal pain after colonoscopy in the
than the rates reported in European guideline ranging between 5‰ and group using “Fleet Phospho-Soda” than in groups using “Klean-Prep”
16‰ in subjects undergoing colonoscopy in screening programs using and “Endofalk” (Ell et al., 2003).
guaiac FOBT (Segnan et al., 2010). There is no information on SC rates Our study is limited by the low frequencies in the categories of some
in screening programs using immunological FOBT. One study found an exposure variables that could not be analyzed in greater depth, speci-
SC rate of 4.7% of colonoscopies in the population screened with dif- fically variables such as the health professional administering sedation
ferent methods (Rutter et al., 2012). The fact that patients who undergo and the quality of bowel preparation. In the descriptive analysis, we
colonoscopy after a positive FOBT have a higher risk of having ade- found a relationship between SC and the quality of the procedure, with
nomas or CRC could explain why the rate in our study was higher than the number of complications being lower when the quality was ex-
that in other studies analyzing the SC rate in healthcare colonoscopies cellent according to the Aronchick scale. One study found an associa-
rather than screening colonoscopies (Singh et al., 2009; Ko et al., 2010). tion between colonoscopy quality and complications (Rajasekhar et al.,
As expected, a higher number of extirpated lesions were associated 2016).
with a higher complications risk, consistent with a study showing that Another limitation was the impossibility of including body mass
patients with 2 or more polyps had a higher risk of complications than index as a risk factor as well as certain variables related to the char-
patients with 1 polyp (Heldwein et al., 2005). In this study, more ad- acteristics of extirpated polyps, since this information was not always
vanced adenomas conferred a higher risk of complications. Several recorded in the clinical histories.
studies have shown that age, the number of polyps, and polyp size are Our study shows that lesions diagnosed at colonoscopy as adenoma
risk factors for a finding of more advanced lesions (Portillo et al., 2017). or CRC confer a higher risk of complications than if no lesions are
Few studies have evaluated the association between colonoscopy found. One of the aims of CRCSP is to detect early-stage tumors or
type (diagnostic/diagnostic-therapeutic) and the appearance of com- precursor lesions. The cohort analyzed in this study included data from
plications. As expected, diagnostic colonoscopy with polypectomy the start of CRCSP to 2012 and it could be expected that more advanced
conferred a higher risk of complications, in agreement with Chan, AO lesions would be detected in the first screening round than in successive
(Chan et al., 2015; Rutter et al., 2012). Although most studies have rounds. A study showed that the complication rate decreases with time
analyzed complications in colonoscopies with polypectomy only and that some of this decrease was due to a reduction in the complexity
(Heldwein et al., 2005; Hui et al., 2004). Like other studies, we found of the procedure (Blanks et al., 2015), probably because successive
that patients under regular anticoagulant therapy had a higher risk of rounds identified earlier-stage disease.
late bleeding (Tong et al., 2015; Yousfi et al., 2004). Although Hui et al. SC are an infrequent but important adverse effect of CRCSP that
studied the effect of ASPIRIN use and found no relationship with should be minimized. Our study provides information on the factors
bleeding events after polypectomy, in the present study we found an influencing the occurrence of these complications and has analyzed
association between prior antiplatelet treatment and the appearance of differences between risk factors associated with immediate-SC and late-
late-SC. A possible reason for this discrepancy is that this study included SC independently, as well as risk factors for different types of compli-
ASPIRIN as an antiplatelet agent only when the dose was sufficiently cations. The results could help to target prevention measures, bearing in
high to have an antiplatelet effect. Another study also analyzed the mind certain patient-related and procedural factors that could help to
association of post-polypectomy bleeding and the use of prior ASPIRIN minimize the risk of SC by adopting organizational and information
administration and concluded that there was no significant association measures that take account of the patient's risk of having an SC during
(Yousfi et al., 2004). colonoscopy and the next 30 days. Immediate-SC are more frequently
Prior regular use of sedatives-hypnotics was a protective factor consisted of perforations and to occur in patients with a history of
against perforation. According to the clinical practice guidelines for surgery or radiotherapy and in patients with adenoma or CRC. Late-SC
quality of colonoscopy in CRCSP, sedation is recommended during the are also influenced by prior medication, specifically regular antiplatelet
procedure as it improves patients' experience and can make endoscopic and anticoagulant therapy and type of colonoscopy. Knowledge of the
examination easier (Rodrigo, 2011). Sedatives-hypnotics make patients medical history of persons undergoing colonoscopy is needed for post-
feel calm or sedated and, possibly because of this effect, patients re- procedural follow-up.
ceiving regular prior sedative-hypnotic therapy have a lower risk of
perforation. Funding
Patients receiving poorer information on bowel cleansing before
colonoscopy had a higher bleeding risk, which could be because in- This Project was funded by the Instituto de Salud Carlos III with co-
formation on screening, the informed consent form and instructions for funding from FEDER [PI12/00944].
bowel cleansing are components of colonoscopy quality (Rodrigo,
2011). Ethics considerations
We found no relationship between SC and the type of sedation-an-
algesia (None/Deep sedation/Superficial sedation). Unlike our study, This study was performed in accordance with the principles of the
Wernli et al. compared patients with anesthesia administered by the declaration of Helsinki and the Spanish legal requirements of con-
anesthesia service (which is similar to what we consider to be deep fidentiality.
sedation) and patients with standard sedation (superficial sedation) and
found a higher risk of SC in patients with sedation administered by the Conflict of interest statement
anesthesia service (Wernli et al., 2016). We did find a relationship with
the health professional administering the sedation and with the quality The authors disclose no conflicts interests.
of bowel cleansing, with the percentage of SC being lower when seda-
tion was administered by an endoscopist rather than by an anesthe- Acknowledgments
siologist or nurse and when the quality of bowel cleansing was ex-
cellent. Another study concluded that administration by an anesthesia The authors thank the health professionals working in the cancer
professional did not appear to confer a safety benefit to patients un- screening programs for their contribution to early cancer detection and
dergoing colonoscopy (Vargo et al., 2017). improving the population's health.

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This article is part of the Doctoral Dissertation of Mercedes Pan, J., Xin, L., Ma, Y.F., et al., 2016. Colonoscopy reduces colorectal cancer incidence
Vanaclocha Espi at the University of Alicante, Spain. and mortality in patients with non-malignant findings: a meta-analysis. Am. J.
Gastroenterol. 111, 355–365.
Pignone, M., Rich, M., Teutsch, S.M., et al., 2002. Screening for colorectal cancer in adults
References at average risk: a summary of the evidence for the U.S. Preventive Services Task
Force. Ann. Intern. Med. 137, 132–141.
Portillo, Villares I., Arana-Arri, E., Idigoras, Rubio I., et al., 2017. Lesions detected in six
Albert, J., 2007. Bayesian Computation With R, 2 ed. Springer-Verlag, New York.
Spanish colorectal cancer screening population based programmes. CRIBEA Project.
Blanks, R.G., Nickerson, C., Patnick, J., et al., 2015. Evaluation of colonoscopy perfor-
Spain. Rev. Esp. Salud Publica 91.
mance based on post-procedure bleeding complications:application of procedure
Rajasekhar, P.T., Rees, C.J., Nixon, C., et al., 2016. Factors influencing change in clinical
complexity-adjusted model. Endoscopy 47, 910–916.
practice: a qualitative evaluation of the implementation of the quality improvement
Cardin, F., Minicuci, N., Campigotto, F., et al., 2012. Difficult colonoscopies in the pro-
in colonoscopy study. Int. J. Health Care Qual. Assur. 29, 5–15.
pofol era. BMC Surg. 12 (Suppl1), S9.
Rodrigo, J. (Ed.), 2011. Clinical Practice Guidelines: Quality of Colonoscopy in Colorectal
Chan, A.O., Lee, L.N., Chan, A.C., et al., 2015. Predictive factors for colonoscopy com-
Cancer Screening Spanish Society of Gastrointestinal Endoscopy and the Spanish
plications. Hong Kong Med. J. 21, 23–29.
Association of Gastroenterology.
Council Recommendation of 2 December 2003 on Cancer Screening (2003/878/EC),
Rutter, C.M., Johnson, E., Miglioretti, D.L., et al., 2012. Adverse events after screening
2003. Off. J. Eur. Union L 327, 34–38. https://ec.europa.eu/jrc/sites/default/files/2_
and follow-up colonoscopy. Cancer Causes Control 23 (2), 289–296.
December_2003%2020cancer%2020screening.pdf (16.02.2003.In).
Salas Trejo, D., Portillo Villares, I., Espinas Pinol, J.A., et al., 2017. Implementation of
Ell, C., Fischbach, W., Keller, R., et al., 2003. A randomized, blinded, prospective trial to
colorectal cancer screening in Spain: main results 2006–2011. Eur. J. Cancer Prev.
compare the safety and efficacy of three bowel-cleansing solutions for colonoscopy
26, 17–26.
(HSG-01*). Endoscopy 35, 300–304.
Segnan, N., Patnick, J., Karsa, Lv, 2010. et al. In: European Guidelines for Quality
Ferlay, J., Soerjomataram, I., Dikshit, R., et al., 2015. Cancer incidence and mortality
Assurance in Colorectal Cancer Screening and Diagnosis, 1. ed. Office for Official
worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer
Publications of the European Communities, Luxembourg.
136, E359–E386.
Singh, H., Penfold, R.B., DeCoster, C., et al., 2009. Colonoscopy and its complications
Hardcastle, J.D., Chamberlain, J.O., Robinson, M.H., et al., 1996. Randomised controlled
across a Canadian regional health authority. Gastrointest. Endosc. 69 (3), 665–671.
trial of faecal-occult-blood screening for colorectal cancer. Lancet 348, 1472–1477.
Tong, M.C., Tadros, M., Vaziri, H., 2015. Endoscopy in neutropenic and/or thrombocy-
Heldwein, W., Dollhopf, M., Rosch, T., et al., 2005. The Munich Polypectomy Study
topenic patients. World J. Gastroenterol. 21, 13166–13,176.
(MUPS): prospective analysis of complications and risk factors in 4000 colonic snare
Vanaclocha-Espi, M., Ibanez, J., Molina-Barcelo, A., et al., 2017. Factors influencing
polypectomies. Endoscopy 37, 1116–1122.
participation in colorectal cancer screening programs in Spain. Prev. Med. 105,
Hui, A.J., Wong, R.M., Ching, J.Y., et al., 2004. Risk of colonoscopic polypectomy
190–196.
bleeding with anticoagulants and antiplatelet agents: analysis of 1657 cases.
Vargo, J.J., Niklewski, P.J., Williams, J.L., et al., 2017. Patient safety during sedation by
Gastrointest. Endosc. 59, 44–48.
anesthesia professionals during routine upper endoscopy and colonoscopy: an ana-
Jover, R., Zapater, P., Bujanda, L., et al., 2016. Endoscopist characteristics that influence
lysis of 1.38 million procedures. Gastrointest. Endosc. 85, 101–108.
the quality of colonoscopy. Endoscopy 48, 241–247.
Walsh, J.M., Terdiman, J.P., 2003. Colorectal cancer screening: scientific review. JAMA
Kim, D.H., Lee, S.Y., Choi, K.S., et al., 2007. The usefulness of colonoscopy as a screening
289, 1288–1296.
test for detecting colorectal polyps. Hepato-Gastroenterology 54, 2240–2242.
Wernli, K.J., Brenner, A.T., Rutter, C.M., et al., 2016. Risks associated with anesthesia
Ko, C.W., Riffle, S., Michaels, L., et al., 2010. Serious complications within 30 days of
services during colonoscopy. Gastroenterology 150 (4), 888–894.
screening and surveillance colonoscopy are uncommon. Clin. Gastroenterol. Hepatol.
Yousfi, M., Gostout, C.J., Baron, T.H., et al., 2004. Postpolypectomy lower gastro-
8 (2), 166–173.
intestinal bleeding: potential role of aspirin. Am. J. Gastroenterol. 99, 1785–1789.
Kwon, M.J., Kim, Y.S., Bae, S.I., et al., 2015. Risk factors for delayed post-polypectomy
Zhang, Q., An, S., Chen, Z., et al., 2014. Assessment of risk factors for delayed colonic
bleeding. Intestinal Res. 13, 160–165.
post-polypectomy hemorrhage: a study of 15,553 polypectomies from 2005 to 2013.
Levin, T.R., Zhao, W., Conell, C., et al., 2006. Complications of colonoscopy in an in-
PLoS One 9, e108290.
tegrated health care delivery system. Ann. Intern. Med. 145 (12), 880–886.

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