Current status of endoscopic submucosal dissection in Latin America

Nicolás González,¹ Adolfo Parra-Blanco,² Vitor Arantes,³ Klaus Mönkemüller⁴

¹ Department of Gastroenterology (Prof Henry Cohen), Hospital de Clínicas, School of Medicine. Montevideo, Uruguay.
² Department of Gastroenterology, Pontificia Universidad Católica de Chile School of Medicine. Santiago, Chile.
³ Department of Gastroenterology, School of Medicine, Federal University of Minas Gerais. Belo Horizonte, Brazil.
⁴ Division of Gastroenterology and Hepatology, Basil I Hirschowitz Endoscopic Center of Excellence, University of Alabama. Birmingham, United States.

Acta Gastroenterol Latinoam 2016;46: 213-219
Recibido: 29/12/2015 / Aprobado: 18/04/2016 / Publicado en www.actagastro.org el 03/10/2016

Collaborators
Walton Albuquerque (Brasil), Andrés Donoso Durante (Chile), Walther Bejarano (Colombia), Denny Javier Cas­tro (Venezuela), Rodrigo Castaño (Colombia), Alfonso Cal­vo (Chile), Sergio Con (Costa Rica), Ricardo Fiszerowicz (Argentina), Jorge Landaeta (Venezuela), Fauze Maluf Fil­ho (Brasil), Daniela Medeiros Milhomem Cardoso (Brasil), John Ospina Nieto (Colombia), Arecio Peñaloza-Ramírez (Colombia), Raúl Pinilla (Colombia), Lix Alfredo Reis de Oliveira (Brasil), Mario Rey Ferro (Colombia), Carlos An­tonio Robles Medranda (Ecuador), María Constanza Ro­dríguez Rubiano (Colombia), Paulo Sakai (Brasil), Gloria Vargas Cárdenas (Perú), Guido Villa-Gómez (Bolivia), Nancy Zambrano H (Venezuela).

Summary

Endoscopic submucosal dissection (ESD) has been performed routinely in Asia for many years, however, in Western coun­tries ESD it is still limited to a few tertiary centers. Objec­tives. To investigate the practice of ESD in Latin America. Methods. An electronic survey was mailed to Latin-Amer­ican endoscopists affiliated with National Societies of Gas­troenterology and Endoscopy under the collaboration of the Interamerican Association of Gastroenterology and the Inte­ramerican Society of Digestive Endoscopy. Endoscopists from Latin America with publications related to ESD until May 2013 were also invited to participate. Results. A total of 37 endoscopists completed the survey, 25 (67%) performed ESD in humans (ESDH). ESDH was performed in 23 cen­ters located in 10 out of 23 countries (43%). A total of 23 operators of ESDH (92%) had previously been trained in animal models performing 936 ESD. A total of 723 ESDH were performed: stomach 62%, esophagus 15%, colorectum 22%. The average number of procedures per endoscopist was 29 (range: 1-73).There were 9.2% complications (4% per­forations, 4.5% postoperative bleedings and 0.7% miscel­laneous). Conclusions. Although the number of endoscopists in Latin America performing ESD is still relatively low, the number of ESDH being performed is significant. The vast majority of operators appear to have received proper train­ing in pig models and attended Japanese referral centers. The outcomes appear to be similar to Eastern publications.

Key words. Endoscopic submucosal dissection, training, learn­ing curve, endoscopic mucosal resection, endoscopic resection.

Situación Actual de la disección endoscópica de la submucosa en América Latina

Resumen

La disección endoscópica de la submucosa (ESD) se reali­za de forma rutinaria en Asia desde hace muchos años; sin embargo, en los países occidentales la práctica de la ESD todavía se limita a unos pocos centros. Objetivos. Conocer la práctica de la ESD en América Latina. Métodos. Una encuesta electrónica fue enviada por correo a los endoscopis­tas latinoamericanos afiliados a las Sociedades Nacionales de Gastroenterología y Endoscopia con la colaboración de la Asociación Interamericana de Gastroenterología y la Socie­dad Interamericana de Endoscopia Digestiva. También se invitó a participar a los endoscopistas de América Latina que tenían publicaciones relacionadas con ESD hasta mayo de 2013. Resultados. Un total de 37 endoscopistas completaron la encuesta, 25 (67%) realizaban ESD en seres humanos (ESDH). ESDH se realizaba en 23 centros ubicados en 10/23 países (43%). Un total de 23 endoscopistas que realizaban ESDH (92%) habían utilizado los modelos animales para su entrenamiento, realizando 936 ESD. Se realizaron 723 ESDH: en estómago 62%, esófago 15%, colon y recto 22%. El número promedio de procedimientos por endoscopista fue de 29 (rango: 1-73). Hubo 9.2% de complicaciones (4% per­foraciones, 4,5% hemorragias postoperatorias y 0,7% misce­láneas). Conclusiones. A pesar que el número de endoscopistas que realiza ESD en Latinoamérica es todavía relativamente bajo, el número total de procedimientos realizados en huma­nos ESDH es significativo. La gran mayoría de los operadores parecen haber recibido formación en modelos porcinos y asis­tido a centros de referencia japoneses. Los resultados parecen ser similares a las publicaciones de países europeos.

Palabras claves. Disección endoscópica de la submucosa, entrenamiento, curva de aprendizaje, resección de la mucosa endoscópica, resección endoscópica.

Abbreviations
ESD: endoscopic submucosal dissection.
ESDH: ESD in humans.
ISI: International Sensitivity Index.

Endoscopic submucosal dissection (ESD) was developed in Japan with the aim of completely resecting neoplastic tumors in one piece and with adequate free margins.^1-3 Al­though, initially ESD was utilized for early gastric cancer, soon afterwards it became evident that early esophageal and superficial colorectal cancer could also be managed effective­ly using this novel technique. In spite of the excellent results obtained in Japan in terms of effectiveness and safety,^{4, 5} the use of ESD in Western countries remains limited to a few referral centers. The major drawbacks to incorporation of ESD are several and include a) the perceived low rate of early tumor detection in Western centers, b) its being a complex procedure and c) the steep and long learning curve associated with the procedure. In countries like Japan and South Korea there is a high prevalence of gastric cancer in the population, and the endoscopists are highly skilled to recognize the tumors in early stages.⁶ The early gastric tumor, particularly when situated in the antrum, is considered the most suitable lesion to be managed by novice ESD operators. Moreover, expert centers in Japan have developed structured training programs for hands-on practice in animal models and training in hu­mans.⁷ Due to its advantages in terms of potential complete resection, the interest in ESD has grown in Europe.⁸ In the Americas a similar movement has been observed. However, there is scarce data about the number of endoscopists involved in ESD practice and the outcome of this procedure in such centers. Knowledge of these data is of paramount importance to the further implementation, refinement and establishment of this technique. The present study aimed to investigate the current status of ESD practice in Latin America.

Material and methods

A survey with specific questions on ESD and its prac­tice was developed (Table 1). The survey was elaborated in both Spanish and Portuguese and the following data were requested: identification, type of institution (academic/pub­lic/private), medical training background, scientific publica­tions or congress presentations related to ESD, characteris­tics of training program, experimental hands-on practice in animal models, number and type of procedures performed in humans, devices utilized, adverse events and outcome.

Table 1. Summary of the results of the survey for human ESD.

This survey was electronically mailed to Latin-Amer­ican endoscopists from 23 countries affiliated with Na­tional Societies of Gastroenterology and Endoscopy with the collaboration of the Interamerican Association of Gastroenterology (AIGE) and the Interamerican Society of Digestive Endoscopy (SIED). In order to find all po­tential individuals performing ESD in Latin America an additional literature search using the PubMed search en­gine up to the year 2013 was performed.

Statistical analysis

Data are presented in descriptive fashion and variables are summarized in absolute frequencies, percentages, means and/or medians, as needed. The software used was SPSS (version 17.0; SPSS Inc, Chicago, Illinois, USA).

ESD survey results in humans

A total of 37 endoscopists from 23 centers distributed in 10/23 countries (43%) adequately answered and re­turned the survey and reported to perform ESD. Twenty five (67%) had performed ESD in humans (ESDH), and 12 (33%) only in animal models. Of the endosco­pists who had studies published in journals indexed on PubMed, 5/6 (83%) completed the questionnaire.

Table 1 shows a summary of the results of the survey for human ESD. The distribution of endoscopists per­forming ESDH per countries can be seen in Table 2.

Table 2. Distribution of endosco­pists performing ESDH per countries.

Practice on animal models had been carried out by 35/37 (95%). Most of the endoscopists who were per­forming ESDH had also practiced on animal models be­fore embarking on human endoscopic resections 23/25 (92%). The majority (18/25 or 78%) used both ex-vivo and in-vivo models, 4 (17%) only in-vivo models, and 1(4%) only ex-vivo. The porcine model was the choice for all cases (100%), and one endoscopist also used the canine model. Six endoscopists (24%) had an animal laboratory to perform ESD practice in living models. In total, the re­ported number of procedures performed on animal models previous to attempting ESDH was 936, with a mean 40,7 per endoscopist (3-200). Eight (35%) endoscopists had performed more than 30 procedures in animal models. In addition most of the endoscopists (21/25: 84%) perform­ing ESDH had visited referral training centers.

The following knives were used: IT- knife 18 (72%), Flush knife 12 (48%), Flex knife 5 (20%), Hook knife 5 (20%), Hybrid knife 3 (12%), Dual knife 3 (12%), Triangle knife 2 (8%). Five endoscopists (20%) had used only one type of knife, 13 (52%) had used two, 4 (16%) had used three, and 3 (12%) had used four.

A total of 723 ESDH were performed: 62% in the stomach, 15% in the esophagus, 15% in the rectum and 7% in the colon (Table 1). The median number of pro­cedures per endoscopist was 29 (1-73). Ten endoscopists (40%) had performed at least 30 ESDH.

Fourteen respondents (56%) were the only endosco­pists performing ESDH at their center, eight (32%) re­ported having two endoscopists performing, and 3 (12%) answered that there were 3 endoscopists in their institu­tion performing ESDH.

Major complications (perforation or bleeding) were reported by 21 (84%) endoscopists. The total number of complications was 68 (9.4%), 30 (44%) were perfora­tions, 33 (48%) bleeding, and 5 (7%) were other compli­cations. There was one fatal complication due to bleed­ing (0.09%). Among the major complications, 65% were treated endoscopically, 17% required surgery and there were no data on the remaining 18%.

Among the endoscopists performing ESDH, 10 (40%) had publications on this technique in scientific journals and 6 (24%) in journals indexed in PubMed. The total number of articles published in scientific journals was 32, of whom 16 (50%) were indexed in PubMed.10-29

Discussion

This is the first report evaluating the prevalence and utilization of ESD in Latin America. The survey indicates that ESD has definitely arrived to the American conti­nent and is being performed in at least 43% (10/23) of the countries. Even though the number of endoscopists performing ESD can be considered relatively low, with only 25 individuals reporting on ESDH, the number of reported cases performed is high. Indeed, the mean num­ber of ESD performed by Latin American endoscopists was higher than the number reported by the European ESD survey (29 versus 11).⁸ It is possible that this larger number reflects the larger number of gastric cancers in some Latin American countries. Nonetheless, 35% of ESDs reported involved the colorectum and esophagus. Thus, it appears that Latin American endoscopists have adopted this technique for lesions of the entire GI tract. In addition, colorectal lesions with an indication for ESD can be a frequent finding in countries such as Uruguay, where the incidence of colorectal cancer is high, and a national screening program exists.

This survey also stands out for having evaluated two additional issues, both of which may have an influence on the quality of practice of ESD: a) previous training and b) publication of results in scientific journals. An inter­esting finding was that the vast majority of endoscopists performing ESDH had previously trained using live or inanimate biologic models and visited expert centers in Japan. These results are encouraging as they reflect a will­ingness to adopt this method under ideal circumstanc­es. Often times, new techniques fail or are abandoned due to improper training.⁹ It is striking to see that Latin American endoscopists performing ESDH had trained on almost 1000 pig stomach resections before attempt­ing this technique in humans. While it is impossible to know from this survey if other endoscopists performing ESDH who did not respond to the questionnaire had an adequate training as well, we believe that this aspect of previous training must be emphasized as a prerequisite for embarking in ESD. ESD is technically demanding and requires a lot of practice to achieve competence. For these reasons, training programs have been developed in different American countries using porcine models, and frequently including Japanese experts as trainers. It has been shown that these courses may help improve the skills in this technique in a relatively short time.⁷

An additional finding of the current survey was that a significant percentage of Latin American endoscopists reported an interest in making their experience available by publishing the results in peer review journals.^10-29 Pre­vious surveys have not evaluated this aspect, which we believe is important as any adoption of new technique should lead to publication of positive or negative results.

ESD is still not a widespread technique outside Japan, Korea and China. Nonetheless, it is clear that ESD allows “en bloc” resection of superficial neoplastic lesions, al­most without any size limit. Its spread in Western coun­tries has been limited, probably because of the technical difficulties and the initial higher risk of complications. However, in experienced hands ESD results in lower complications. The most frequent major complications reported in this study were bleeding (4.5%), and perfo­ration (4%). These results are not different from those obtained in Asian referral centers, which reported com­plication rates of 1-4%.³⁰ The results from the European survey previously mentioned reported over 8% bleedings, and 5% perforations.⁸ Therefore, it could be concluded that the rate of complications by Latin American endos­copists who completed the survey was slightly lower than those reported by western endoscopists.

ESD is a technically demanding method, and cer­tainly not every therapeutic endoscopist should be ex­pected to perform it. Moreover, the number of lesions with a clear indication for ESD in Latin American slow, perhaps explaining the reduced number of expert endos­copists practicing this technique in each country. This approach is supported by results of a previous survey of Japanese experts in colorectal ESD.³⁰ It is encouraging to observe that Latin American endoscopists performing ESDH have gone through a process of training before embarking in human ESD. Regarding the number of ESDs performed per endoscopist in the different gastro­intestinal locations (esophagus, stomach, colorectum) the mean number was 29, and 40% of the endoscopists performed at least 30 procedures, and 24% performed at least 40 cases. Gotoda et al,⁷ and Kakushima et al³² suggested that at least 30 gastric ESDs supervised by an expert were required for the beginner to gain competence in this technique. Choi et al,³³ reported that 20-40 proce­dures would be the ideal number to achieve initial com­petence, considering safety and effectiveness. However, in a recent study Yamamoto et al³⁴ suggested that 30 pro­cedures is an insufficient number to achieve competence in ESD of gastric lesions in any location, and according to another study by the same authors, 40-80 procedures would be required to achieve competence, and over 80 to be able to resect safely and with efficacy lesions of any location.³⁵ Therefore, if the algorithms suggested by the Japanese experts about the learning curve are considered and applied, it can be stated that the number of endos­copists with enough experience is low. Similarly, Dinis- Ribeiro et al³⁶ recommend having performed 20-40 ESD initially in the distal stomach and later in proximal loca­tions before starting to practice esophageal and colorectal ESD. Ohata et al³⁷ propose that at least 30 gastric ESD would be required to achieve enough competence to start colon ESD. However, other recent studies suggest that it would not be necessary to have a lot of competence in gastric dissections before being able to perform colon ESD.³⁸ The number of endoscopists performing human ESD per center was also analyzed. The low number of endsocopists performing ESD per center can be related to the low number of lesions treated per institution, as well as the recommendation from experts in that field that one endoscopist acquire initial experience before starting the training of a second endoscopist, so that the first can be­come the trainer of the second.³¹

With the results obtained in this survey, and consid­ering that ESD is effective and safe in expert hands, the authors consider that well-structured training programs would be required in Latin America and Western coun­tries in general, to increase the implementation of ESD. Such courses should include animal models, with the su­pervision of experts, and this should be complemented by visits to referral centers. The authors believe that these programs should focus also in the detection and evalua­tion of early digestive neoplasms and should be adapted to the needs and possibilities of each region.

We would like to acknowledge the limitations of this study. Any survey study has the potential limitation of inaccuracy of the data, as the reported results are retro­spective, not always based on registries and some endos­copists performing ESD may not have received the survey or did not answer the survey. In spite of this, we know that the vast majority of endoscopists who had publica­tions in PubMed responded to the questionnaire. One other limitation we must mention is that the results of the procedures were not obtained (en bloc resection rates, R0 resection rates), as this was not the objective of this study and the survey did not include questions related to this topic. Nevertheless, our survey provides new find­ings not addressed by previous survey studies, such as the importance of using animal models when practicing this technique and the percentage of endoscopists who have publications in indexed journals.

In summary, this study allows for important conclu­sions regarding ESDH in Latin America. We found that ESD is performed in 40% of Latin American countries. Although the number of endoscopists in Latin America performing ESD is still relatively low, the number of ESD is significant. The great majority of operators appeared to have received proper hands-on training in biologic mod­els and attended Japanese referral centers before embark­ing on ESDH. Despite not knowing the remedial results of these procedures, the reported outcomes in terms of complications and mortality rates appear to be similar to Eastern and European publications.

Our findings support the creation of a closer collabo­ration among the different Latin American centers, with the aim of creating working groups which promote and participate in teaching, research and developing this tech­nique in depth. Forming close relationships with Asian centers and other Western countries is also considered of great importance to achieve technical improvement and allow for clinical application. All these actions should facilitate the smooth introduction and development of ESD, attracting the interest of the companies related to ESD devices and making them understand that it is a use­ful technique. This is appealing to endoscopists but espe­cially important to patients, so that the armamentarium available for ESD in Japan is also made available to Latin American endoscopists.

Acknowledgements. The authors wish to thank: Gastro­enterology and Endoscopy Societies of Latin American coun­tries and American Gastroenterological Association (AIGE) and Inter American Society of Endoscopy (SIED) for facili­tating access of their members to the survey. We also want to thank Dr Carlos Reolon for his contribution designing the electronic questionnaire.

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Correspondencia: Nicolás González
Av Italia 2870 – Piso 4. Montevideo 11600, Uruguay
Fax: +598-2-4808472
Correo electrónico: nicolasendoscopia@yahoo.es

Acta Gastroenterol Latinoam 2016;46(3): 213-219