ORIGINAL PAPER DOI: http://dx.doi.org/10.

15403/jgld-5059

Upper Gastrointestinal Endoscopy Quality in Italy: A Nationwide Study

Angelo Zullo1,Vincenzo De Francesco2*, Arnaldo Amato3, Irene Bergna3, Emanuele Bendia4, Giorgia Giorgini4,
Elisabetta Buscarini5, Guido Manfredi5, Sergio Cadoni6, Renato Cannizzaro7, Stefano Realdon7, Mario Ciuffi8, Orazio
Ignomirelli8, Paola Da Massa Carrara9, Giovanni Finucci9, Antonietta Di Somma10, Chiara Frandina11, Mariafrancesca
Loria11, Francesca Galeazzi12, Francesco Ferrara12, Carlo Gemme13, Noemi Sara Bertetti13, Federica Gentili14, Antonio
Lotito14, Bastianello Germanà15, Nunzia Russo15, Giuseppe Grande16, Rita Conigliaro16, Federico Cravero17, Giovanna
Venezia17, Riccardo Marmo18, Piera Senneca18, Angelo Milano19, Konstantinos Efthymakis19, Fabio Monica10,20, Paolo
Montalto21, Mario Lombardi21, Olivia Morelli22, Danilo Castellani22, Daniela Nigro23, Roberto Festa23, Sergio Peralta24,
Maria Grasso24, Antonello Privitera25, Maria Emanuela Distefano25, Giuseppe Scaccianoce26, Mariangela Loiacono26,
Sergio Segato27, Marco Balzarini27, Paolo Usai Satta28, Mariantonia Lai28, Raffaele Manta9

See Authors affiliations at the ABSTRACT

end of the paper.
Background & Aims: International guidelines advise improving esophagogastroduodenoscopy (EGD)
quality in Western countries, where gastric cancer is still diagnosed in advanced stages. This nationwide study
investigated some indicators for the quality of EGD performed in endoscopic centers in Italy.
Methods: Clinical, endoscopic, and procedural data of consecutive EGDs performed in one month in the
Address for correspondence: participating centers were reviewed and collected in a specific database. Some quality indicators before and
Dr. Angelo Zullo, during endoscopic procedures were evaluated.
Gastroenterologia, PTP Nuovo Results: A total of 3,219 EGDs performed by 172 endoscopists in 28 centers were reviewed. Data found that
Regina Margherita, some relevant information (family history for GI cancer, smoking habit, use of proton pump inhibitors) were
Via Emilio Morosini, not collected before endoscopy in 58.5-80.7% of patients. Pre-endoscopic preparation for gastric cleaning was
3000153 Roma, Italia. routinely performed in only 2 (7.1%) centers. Regarding the procedure, sedation was not performed in 17.6%
angelozullo66@yahoo.it of patients, and virtual chromoendoscopy was frequently (>75%) used in only one (3.6%) center. An adequate
sampling of the gastric mucosa (i.e., antral and gastric body specimens) was heterogeneously performed, and
it was routinely performed only by 23% of endoscopists, and in 14.3% centers.
Conclusions: Our analysis showed that the quality of EGD performed in clinical practice in Italy deserves to
be urgently improved in different aspects.

Key words: esophagogastroduodenoscopy − quality indicators − biopsies.

Received: 04.06.2023 Abbreviations: ESD: esophagogastroduodenoscopy; H. pylori: Helicobacter pylori; PPI: proton pump inhibitor.
Accepted: 02.08.2023

INTRODUCTION some international guidelines advise an urgent need for

improving EGD quality in Western countries [1, 5-9], where
Esophagogastroduodeno- detection of gastric cancer in its early stages still remains
scopy (EGD) is largely used disappointingly low [10], with a dismal prognosis for patients.
in clinical practice in patients Several actions were advised to improve this endoscopic
with different symptoms for examination, including pre-, during, and post-procedure
the diagnosis and surveillance measures [1, 5-9]. Among them, taking an adequate sample
of relevant gastroduodenal of gastric mucosa is essential for Helicobacter pylori (H.
diseases [1, 2]. More than 2.5 pylori) diagnosis as well as for the detection and staging of
million EGDs were performed precancerous lesions and, consequently, to evaluate gastric
in Italy in 2007, mostly as open- cancer risk and schedule an appropriate surveillance [1, 11-
access procedures [3]. A recent 14]. Indeed, the implementation of different measures able
systematic review estimated a to improve EGD quality were found to increase detection
21.7% inappropriate rate of EGD of precancerous lesions on gastric mucosa [15]. As a result,
indications, with values as high assessing current EGDs practice is critical in identifying
as 55%-65% reported in some potential corrective aspects to implement. With this aim, we
Italian studies [4]. On the other designed this multicenter study on EGD practice in endoscopic
hand, mirroring colonoscopy, units of public hospitals through Italy.

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434 Zullo et al.

METHODS meet inclusion criteria. The EGD was the first examination in
1,431 (44.4%) patients, a successive control in 1,258 (39.1%),
Patients and information was lacking for the remaining 530 (16.5%)
For the purpose of this study, we have chosen a retrospective cases. There were 172 endoscopists involved in the centers
design to avoid the ‘Hawthorne effect’ in reporting data and to (median: 6; range: 2-16), and the median number of endoscopic
unaffectedly describe the real setting [16]. Clinical, endoscopic, examinations performed per center was 102 (range: 49-245).
and histological data of consecutive patients referred for EGD In detail, there were 87 endoscopists who executed >15
in the participating centers between October 1 and October EGDs during the study period. At endoscopy, there were 16
31, 2022, were anonymously reviewed and collected in a esophageal cancers (15 adenocarcinomas, 1 squamous), 27
specific Excel database. We investigated whether information gastric neoplasia (25 cancers, 1 lymphoma, 1 neuroendocrine
on some risk factors for gastric cancer (first-degree family tumor), and 2 duodenal tumors (1 adenocarcinoma, 1
history and smoking habit) and ongoing proton pump inhibitor lymphoma). At histological assessment of patients with
(PPI) therapy were systematically recorded. Furthermore, we adequate gastric biopsies sampling, a precancerous lesion
explored if gastric cleaning was adopted before endoscopy was detected in 362 (22.3%) patients, including 193 cases
and if chromoendoscopy and adequate biopsy sampling were with atrophic/metaplastic gastritis confined in the antrum,
performed during the examination. An adequate gastric mucosa 144 with atrophic pangastritis, and 25 with corpus-restricted
sampling was considered to be accomplished when at least atrophic gastritis.
two antral and two gastric body biopsies were collected in two Regarding the pre-procedure data, information on first-
different vials beyond those on endoscopic lesions, as suggested degree upper gastrointestinal cancers was lacking in 2,160
in guidelines [11-14]. Only data from patients referred by their (67.1%) cases, and smoking habit (current or previous) was
general practitioners were collected to better describe routine uninvestigated in 2,598 (80.7%) cases. Data on previous H.
clinical practice. Data from in-patients or EGDs performed pylori eradication, ongoing proton pump inhibitor (PPI)
in an emergency, as well as incomplete examinations for any therapy, and ongoing anti-thrombotic therapy were not
reason, were excluded. For the main considered parameters, the collected in 1,886 (58.5%), 1,281 (39.8%), and 1,213 (37.7%)
comparisons among different endoscopists were restricted to patients, respectively. Before endoscopy, gastric cleaning
those who performed at least 15 EGDs during the study period. preparation was routinely given in only 2 (7.1%) centers,
This cut-off was arbitrarily chosen to limit the probability of a and sedation was not performed in 568 (17.6%) patients.
potential selection bias (β-type error). Since no identification of Concerning the intra-procedure phase, an image-enhanced
patients was allowed, no experimental drugs were administered, endoscopy technique was overall applied in 498 (15.5%) EGDs,
no additional costs or procedures for the patients were required, being used in >75% of cases in only one center, between 50%
and no funds were received, the Investigational Review Boards and 25% in 4, between 25% and 5% in 10, and less than 5% in
waived formal approval for this retrospective analysis. the remaining 13 centers.
Overall, adequate biopsy sampling of gastric mucosa (i.e.,
Statistical Analysis antral and gastric body specimens) was achieved in 1,625
Frequencies and means or medians with their 95% (50.5%) cases, at least one biopsy in further in 540 (16.8%),
confidence intervals (CI) were calculated for the main while no biopsy at all was performed in 1,054 (32.7%)
observations. Comparison among subgroups was performed EGDs. By considering data of only the 87 endoscopists
using the Chi-square test or Fisher’s exact test, as appropriate. who performed at least 15 EGDs, an adequate biopsy
A P value less than 0.05 was considered statistically significant sampling was heterogeneously performed, and only 20 (23%)
operators accomplished this procedure in more than 75% of
RESULTS their consecutive endoscopic examinations, with 6 (6.9%)
endoscopists taking adequate biopsies in less than 10% of
A total of 3,219 patients (males 1,387; mean age: 58.9 ± procedures (Fig. 1A). Moreover, in only 4 (14.3%) centres all
16.2 years) who underwent EGD in the 28 participating centers the operators routinely were taking both antral and gastric

Fig. 1. Rates of adequate (2 antral plus 2 gastric body) gastric mucosa sampling performed by
different gastroenterologists (A), and in different centers (B).

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Upper gastrointestinal endoscopy quality in Italy 435

Table I. Rate of adequate sampling of gastric mucosa in different settings

Setting Comparison (n, %) p
Examination; (first vs successive) 812/1431 (56.7) vs 571/1,258 (45.3) <0.0001
Age; (<50 vs >50 years) 476/856 (55.6) vs 1149/2,363 (48.6) <0.001
Family history of GI cancer; (yes vs not) 72/101 (71.2) vs 486/ 958 (50.7) <0.001
Current smoking habit; (yes vs not) 44/131 (33.5) vs 180/490 (36.7) 0.5
Ongoing PPI therapy; (yes vs not) 487/1,042 (46.7) vs 418/896 (46.6) 1
Previous H. pylori therapy; (yes vs not) 122/217 (56.2) vs 574/1,116 (51.4) 0.2
GI: gastrointestinal; PPI: Proton pump inhibitor; H. pylori: Helicobacter pylori.

body biopsies in >75% of their performed procedures (Fig. significantly increase the risk of gastric precancerous lesions
1B). The rate of adequate gastric biopsy sampling according and cancer onset [18-20]. Moreover, information on therapy
patients’ age, first-degree family history for cancer, smoking with PPIs was not enquired in more than 1 every 3 patients,
habits, ongoing PPI therapy, previous H. pylori therapy and even though it was highlighted that their current use reduces
type of examination were provided in Table I. The main results the detection of both H. pylori infection and endoscopic
of the study were summarized in Fig. 2. lesions [21, 22], and delayed gastric cancer diagnosis [23].
Information on previous therapy for H. pylori (namely the
DISCUSSION pathogen involved in the majority of gastric diseases) was not
investigated in more than half patients. All these observations
The implementation of organized gastric cancer screening suggest that prior to EGD, some clinical information was not
in Western countries is largely prevented by unfavorable collected in a significant percentage of patients. This easily
cost-efficacy profiles [17]. Therefore, improving EGD quality obtained and free information – including family history,
is the only practicable way to reduce gastric cancer mortality smoking habits, and ongoing PPI therapy – could be used
through the detection of early-stage lesions. Several indicators as ‘red flags’ alerting the operator about a higher pre-test
were suggested for the assessment of EGD quality in the likelihood of upper gastrointestinal lesions.
different international consensus [1, 5-9]. For the present Another relevant finding from our study was that sedation is
study, we evaluated whether data on some pre-procedure not performed in 1 every 5 patients who undergo EGD in clinical
quality indicators (indication, family history, smoking habit, practice. The use of sedation is recommended to achieve greater
previous examinations, administration of gastric preparation) collaboration by the patient during EGD, higher satisfaction
were collected, as well as whether sedation, use of virtual with the procedure and willingness to repeat it in the future,
chromoendoscopy, and standard sampling of gastric mucosa and higher diagnostic yield [1]. We also found that gastric
were performed during the procedure. cleaning preparation was routinely used in only 2 (7%) out the
Overall, our investigation revealed some relevant gaps in participating centers. It has been found that administration of
both the pre-procedure phase and the endoscopic examination. a solution with acetylcysteine and simethicone before EGD
In as many as 67.1%-80% of patients, no information was significantly improves the visualization of gastric mucosa,
gathered on both first-degree family history of upper GI cancers allowing better detection of subtle mucosal lesions, that may be
and smoking habits, which are two independent factors that missed in the stomach at standard examination [24]. Indeed, a

Fig. 2. The main results of the study according to current Italian guidelines on esophagogastroscopy quality [1].
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436 Zullo et al.

systematic review found a 10% missing rate for gastric cancer, so Endoscopy Unit, Riuniti Hospitals, Foggia; 3) Gastroenterology Unit,
that a more rigorous protocol for endoscopy and biopsy should A. Manzoni Hospital, Lecco; 4) Digestive Endoscopy Unit,, Riuniti
be implemented worldwide [25]. In detail, an adequate sampling Hospital, Ancona; 5) Gastroenterology and Endoscopy Unit, Maggiore
of gastric mucosa, i.e, both antral and gastric body specimens, Hospital, Crema (CR); 6) Gastroenterology Unit, CTO Hospital,
should be consistently performed during EGD, according to Iglesias; 7) Experimental Oncological Gastroenterology Unit, CRO
several guidelines [1, 11-14]. Overall, our data found that an Hospital, Aviano (PN); 8) Endoscopy Unit, IRCCS CROB Hospital,
adequate biopsy sampling was achieved in 50% of EGDs, but Rionero in Vulture (PZ); 9) Gastroenterology Unit, ASL Toscana
it was routinely performed by only a minority of operators Nord-Ovest, San Luca Hospital, Lucca; 10) Gastroenterology Unit,
and centers involved in the study, with 23% of endoscopists San Giovanni di Dio Hospital, Gorizia; 11) Gastroenterology Unit,
taking adequate gastric biopsies in <25% of their EGDs. In S. Giovanni di Dio Hospital, Crotone; 12) Gastroenterology Unit,
detail, we found that the endoscopists distinctly increased the University Hospital, Padua; 13) Gastroenterology Unit, SS. Antonio,
rate of correct gastric sampling only when facing with patients Biagio e Cesare Arrigo Hospital, Alessandria; 14) Gastroenterology
with a family history of upper GI cancers (approaching 70%), Unit, Santa Maria Hospital, Terni; 15) Gastroenterology and
whilst the role current smoking was not considered. However, Endoscopy Unit, San Martino Hospital, Belluno; 16) Gastroenterology
previous Italian studies found an 1.8-2.6 increased risk in first- Unit, Civile Baggiovara Hospital, Modena; 17) Gastroenterology Unit,
degree relatives of gastric cancer patients [18], a value largely Santa Croce e Carle Hospital, Cuneo; 18) Gastroenterology Unit, L.
overlapping with 1.5-2.5 increased risk reported in smoking Curto Hospital, Polla (SA); 19) Gastroenterology and Endoscopy Unit,
subjects [20, 26]. Disappointingly, the role of patient’s age was SS. Annunziata Hospital, Hospital, Chieti; 20) Gastroenterology and
less considered by endoscopists, with adequate gastric biopsy Endoscopy Unit, Cattinara Hospital, Trieste; 21) Gastroenterology
sampling performed even less frequently in more aged patients, Unit, ASL Toscana Centro, Pistoia; 22) Gastroenterology Unit, Santa
despite the probability of finding both H. pylori infection and Maria della Misericordia Hospital, Perugia; 23) Gastroenterology
precancerous lesions in the stomach increases in the over 50-old Unit, San Carlo Hospital, Melfi (PZ); 24) Gastroenterology Unit,
years subjects [27]. As compared to standard biopsy sampling, AOU Policlinico Hospital, Palermo; 25) Gastroenterology Unit,
taking only 1 to 3 specimens was found to significantly reduce Cannizzaro Hospital, Catania; 26) Gastroenterology Unit, Giovanni
the probability of finding both atrophy and intestinal metaplasia Paolo II IRCCS, Bari; 27) Gastroenterology Unit, ASST dei Sette
in the gastric mucosa [28]. All these observations indicate that Laghi Hospital, Varese; 28) Gastroenterology Unit, Brotzu ARNAS,
endoscopists can miss important factors (i.e., smoking habits, Cagliari, Italy.
patient’s age) that increase the possibility of both diagnosing
H. pylori infection and finding precancerous lesions in the Author,s contribution: A.Z. and V. De F. conceived the study and
stomach, so that a correct endoscopic follow-up may be design the methodology. All the authors collected data. A.Z. and V.
scheduled in high-risk patients [13]. De F. analyzed the data and drafted the manuscript. R.M. critically
Another concern emerged in the present study was the revised the manuscript. All the authors approved the final version.
scanty use of image-enhanced endoscopy, despite its efficacy
in detection and staging of intestinal metaplasia on gastric
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