Animal models for endoscopic training: do we really need them?

• Introduction
• Animal use and the law
• Training in endoscopic hemostasis
• Training in EUS
• Training in ERCP
• Training in ESD
• Summary
• References

Gastrointestinal endoscopy currently includes many therapeutic methods that are technically challenging and frequently associated with a significant risk of complications. Several issues such as the limited number of clinical cases and practice in emergency situations, and technical difficulty may limit the opportunity for training, and increased exposure in more relaxed situations would be desirable. Moreover, providing the patient with the best possible standard of care is a must. Animal models are the most easily available simulators. Training in these models has been recommended for several complex techniques, among which hemostasis, endoscopic ultrasound, endoscopic retrograde cholangiopancreatography, and endoscopic submucosal dissection are reviewed here. Ex vivo models are much easier to set up and, from an ethical standpoint, they should be used for the initial step in training whenever possible before moving on to in vivo models. Although simulation with animal models has been the subject of a good number of studies, very few of them have evaluated the impact on clinical outcomes, and clearly more studies are needed. Nevertheless, available evidence does suggest that practicing on animal models has an influence on the learning curve and facilitates the acquisition of skills in the complex endoscopic techniques reviewed.

Introduction

During the past few decades, endoscopy has evolved and therapeutic procedures have become much more frequent, with some very complex techniques having been incorporated into the armamentarium. Moreover, the importance of proper information, optimal patient care, and quality assurance is clearly recognized by doctors and patients. Such complex and sophisticated procedures – sometimes applied in emergency situations – should clearly be performed by doctors with adequate experience. Teaching and learning in this context can therefore be hampered.

The use of endoscopic simulators (animal models being the most easily available) remains one of the possible strategies to provide initial endoscopic training in technically demanding methods. In this review, we discuss animal models for training in several established endoscopy techniques, including therapeutic interventions: endoscopic hemostasis, endoscopic ultrasound (EUS), endoscopic retrograde cholangiopancreatography (ERCP), and endoscopic submucosal dissection (ESD). Reports on new techniques without a focus on training are beyond the scope of this review.

Animal use and the law

Animal experimentation, including that for endoscopic training, must be carried out according to ethical principles and the law of the country where the work is conducted. In the European Union, animal experimentation with dogs, cats, and non-human primates is not allowed unless the animals have been bred for that purpose (Directive 2010 /63 /EU of the European Parliament) [1]; for primates in particular, restrictions are greater. Whenever possible, ex vivo models should be preferred.

Training in endoscopic hemostasis

Ex vivo organs for endoscopic training in hemostasis have been used since the late 1990 s. Freys et al. proposed a porcine model that included the esophagus, stomach, and duodenum, and which appeared to be adequate for training in diagnostic and therapeutic techniques [2]. Subsequently the Erlangen Endo-Trainer model was introduced by Hochberger and Neumann [3] [4]. This large surgical/endoscopic simulator, with a potential wide spectrum of training possibilities, included realistic spurting bleeding [3] [4] [5] [6]. For this, a perfusion system with a pump and citrated blood (later substituted by artificial red liquid) was used to simulate spurting arterial bleeding in hollow gastrointestinal organs. Initially, this was done by perforating the external gastric wall with a venous cannula, which was connected to the blood circuit. Later, real vessels were attached to the gastric wall and punctured and irrigated.

The modified light version of the Erlangen model, called the compactEASIE (compact Erlangen Active Simulator for Interventional Endoscopy), has been tested extensively, and it has been demonstrated that training using these models improves the performance of fellows in several techniques of nonvariceal and variceal bleeding [6]. Subjective impressions of trainees who used this model were positive [7]. In one collaborative study between Erlangen University and the New York Society of Gastrointestinal Endoscopy, 28 fellows from New York City hospitals were randomized to receive pure clinical training in endoscopic hemostatic techniques at their hospitals (Group 1), or to participate in three full-day workshops with experienced tutors over a 7-month period (Group 2) [8]. In these workshops, the compactEASIE model was used to practice manual skills, treat bleeding with injection therapy, electrocoagulation, and hemoclips in successive stations, and finally to ligate artificially created esophageal varices. Evaluations were performed before and after training in both groups. Only in Group 2 was there a significant improvement in the overall score after training, as rated by blinded and unblinded tutors; the procedural time was also shorter at final evaluation. The injection and electrocoagulation were performed successfully by 57 % of fellows in Group 2 at baseline and by 92 % at the end of the study. After the first training session, all fellows were able to apply the clip successfully. Review of the information recorded about real clinical procedures performed by the fellows during the study period revealed that hemostasis was achieved in a median of 87 % of cases in Group 1 compared with 100 % in Group 2 (P = 0.034), and complications occurred in a median of 0 % and 11 % of cases, respectively. Interestingly, in both groups there was an overestimation of the level of expertise by fellows compared with ratings given by tutors. However, this was reversed in the group trained with the model (Group 2) at the end of the study compared with the group that underwent pure clinical training (Group 1). Therefore, such training might give the fellows a more accurate sense of their level of expertise. In summary, although the relatively low number of participants was a limitation of the study, the usefulness of this model to improve the skill of trainees seems evident.

In a second study, which had a similar design and was performed in France, 35 fellows were randomized and at the end of the study those trained with the model showed significantly superior ratings at blinded evaluation in all four disciplines, and significantly shorter performance times in two disciplines [9]. Therefore, the benefits of this training strategy seem to be independent of the medical educational system. Trainees rated this model as positive and realistic, and reported that participating in training courses with the model was worthwhile and that their practical ability to treat bleeding was improved as a result of the courses [7] [10].

In a third randomized controlled trial, which was conducted in the United Kingdom, 28 participants were randomized to either no training or hands-on training with the Erlangen ex vivo model in four different endoscopic techniques (30-minute sessions per technique) including nonvariceal hemostasis [11]. For the control of bleeding, there was a significant improvement in performance, with trained participants achieving greater improvement than those without the hands-on training.

In one additional recent study, the compactEASIE was used for training in hemostasis and perforation treatment in the stomach [12]. A total of 30 fellows were randomized to either standard clinical training (control group) or training with the animal model (two sessions, with a total practice time of 12 hours including hemostasis and perforation treatment). A blinded evaluation was then performed in both groups. Finally, the fellows recorded their results for the human cases performed within 5 months from the end of the training period. In the group that received animal model training, a significant improvement was observed in successful management of bleeding between baseline and final evaluation (27 % vs. 73 %); however, in the control group there was no improvement (20 % vs. 20 %, respectively). In the 5 months after completion of the training, fellows in the groups with and without training performed a median of 10 and 8 real hemostatic procedures, respectively, with successful hemostasis being achieved in 83 % and 68 %, respectively (although the difference was not significant). Although this study explored the clinical benefit of the course, the numbers were low, and the impact of training with animal models on patient care and complications, and the durability of the benefit in the long term remain to be ascertained. However, the evidence reviewed here suggests that the benefit most likely exists.

Ex vivo models, as illustrated above, have been shown to be useful at least in improving the fellows’ skill and the rate of successful hemostasis in a second evaluation after completion of the training. Such models have advantages over computerized simulators in that they are more realistic, certainly more easily available, and less costly. The other option is using in vivo models, usually porcine or canine.

In real life, the spectrum of nonvariceal bleeding ranges from Dieulafoy lesions, where there is a single vessel almost without any mucosal defect, to large ulcers, in which the vessel location and tissue properties are variable. Especially in chronic ulcers fibrosis, the tissue is hard and this may make endoscopic hemostasis more demanding. Therefore, creating a real ulcer model might be important for more realistic and advanced training.

In this issue of Endoscopy, Camus et al. present a rather simple method of producing bleeding ulcers in an in vivo porcine model by pretreatment with anticoagulants and antiaggregants [13]. Gastric ulcers were created with the grasp and snare mucosectomy technique plus additional biopsy of submucosal vessels if required to trigger bleeding. Bleeding could be reproduced in almost all of the created ulcers in a short time (mean < 4 minutes). Moreover, the ulcers were realistic. The model was validated for training of fellows (with injection, clipping, and electrocoagulation therapy). One intensive half-day course allowed for significant improvement in the three techniques according to the evaluation by the instructors using a scoring system. This model could be considered as a further step in training of hemostasis, theoretically adding realism due to its use of a living pig, with a real ulcer, and with the advantage of being easy to create, and, indeed, to reproduce.

The bleeding type was Forrest Ib in most cases. It is known that bleeding is not abundant in the porcine stomach, and this is overcome in the ex vivo model, where the amount of bleeding can be regulated, and spurting bleeding can be easily provoked. In spite of this, biopsies from submucosal vessels consistently showed large arterioles. Also, the amount of bleeding was considered to be moderate in 62 % and abundant in 17 %, and these numbers do not seem to be easy to improve upon. As discussed by the authors, Doppler ultrasound probes could be used to detect large vessels, although that would make the model more complex. Another issue with this model is that ulcers are hyperacute, whereas in real practice bleeding frequently takes place in lesions that already have fibrosis, which may lead to more difficult application of certain therapies such as hemoclips [14].

In a study comparing several methods of endoscopic hemostasis, Jensen and Machicado successfully produced a chronic gastric ulcer canine model by applying band ligation [14]. Endoscopy at 1 week follow-up showed that of the 70 bands applied, only one did not have a corresponding ulcer, which was likely due to early dislodgement. In 30 % of the sites there was some stigmata of bleeding (Forrest IIa, IIb, IIc) but there was no active bleeding case. Endoscopies in this study were performed by two expert endoscopists, and in spite of their experience, they noticed a learning curve before being able to successfully deploy hemoclips on the fibrotic ulcers.

Therefore, several degrees of difficulty could be incorporated into the learning process of endoscopic hemostasis: first, an ex vivo model where the application of different hemostatic methods can be practiced; then, a more realistic in vivo acute ulcer model; and finally, an in vivo chronic ulcer model with increased difficulty, which might be particularly relevant for training of advanced hemoclip application. One could speculate that in future studies the model presented by Camus et al. could be further examined in a survival study and tested as a chronic ulcer model. It is believable that in a similar way to their acute ulcer model, biopsy sampling of the ulcer base could also trigger bleeding, which would most likely be nonspurting. Nevertheless, for ethical reasons, ex vivo models, which as explained above have proven to be useful, should always be the first choice for training in endoscopic hemostasis; in vivo models could represent a further step after initial skills have been acquired.

Although several animal models for variceal bleeding have been developed, their purpose was to evaluate the efficacy of new devices or pharmaceutical agents [5]. Nonbleeding varices were created in the ex vivo EASIE model by thermal submucosal injection of stained saline. In one study, the effect of training on this model was not clear, as both the group without simulator training and the group with training showed improvement in the scores for variceal ligation at the final evaluation [8]. In the French study of the compactEASIE, the simulator-training group had a nonsignificant greater rate of successful ligation (83 % vs. 69 %) and a significantly greater overall score at the end of the study [9].

Training in EUS

In the past 10 years EUS has undergone an important development and, as with other techniques such as ERCP, it has evolved from a purely diagnostic tool to one that provides a wide range of therapeutic options [15] [16]. The new interventional EUS-assisted procedures are very demanding from a technical standpoint, with long procedural times and potentially higher complication rates. Therefore, it is necessary to design specific training programs in which animal models can play an important role [17]. There is clearly a need for new training programs in such advanced endoscopy techniques [18] [19] [20].

EUS requires specific knowledge and skills – different from those used in standard endoscopic procedures – as it combines endoscopic and ultrasonographic interpretation, and it is a highly operator-dependent technique [21] [22]. Importantly, most heads of training programs in EUS recognize that trainees and even many of the trainers participate in an insufficient number of EUS cases [23]. However, the learning curve of EUS is lengthy, and numerous studies have confirmed the importance of the learning curve in improving EUS accuracy [24]. A minimum of 150 supervised examinations and 50 fine-needle aspiration (FNA) procedures (25 – 30 pancreatic) are considered to be the requirement to reach competence [25] [26]. The interpretation of complex hepatobiliary pathology may require a longer training period, which is longer still for procedures with therapeutic intent [27]. The use of new tools and learning new techniques on real patients are associated with a high rate of complications and ethical problems. Endoscopic simulators offer a good alternative, avoiding the risks or discomfort associated with learning on real patients [19] [20] [28].

Since the development of the first experimental models in the early 1970 s by Classen and Ruppin or by Williams for the practice of colonoscopy, several ex vivo simulators have been described for endoscopic training, including EUS [29] [30] [31] [32]. However, the lack of realism of such models is particularly problematic for their use in EUS training. Their imitation of tissue properties is usually unsatisfactory, and to date, clinical trials or validation studies for use in EUS have not been performed. Nevertheless, it appears that these models may be useful during the initial phase of learning, by helping trainees to become familiar with gray-scale images, the integration of the three-dimensional image, to improve specific movements, and other technical aspects of EUS such as FNA [33]. In addition, they are easy to install, facilitating their use in training courses and also allowing their demonstration and use at meeting workshops.

The EASIE model of Hochberger et al. was subsequently amended by Matsuda et al. for use in training EUS [8] [34]. But as with other ex vivo models, it is not suitable for training in interventional techniques. Skills such as feeling the needle penetration or experiencing complications (bleeding or perforation) cannot be acquired with the model. In vivo animal models allow a more realistic simulation of EUS. However, the higher cost and ethical implications associated with their use limit their general employment in routine practice [35] [36].

The use of live pigs under anesthesia offers the opportunity to obtain EUS images of organs and vascular structures similar to those obtained in human patients. The anatomy of the pig is similar to the human: the five layers of the gut wall can be displayed, the liver presents a similar echostructure, the pancreas and abdominal vessels are easily identifiable, and it also offers the possibility of identifying vascular structures by Doppler [37] [38] [39] [40].

These animal models have also proved to be useful in identifying submucosal lesions after injection of substances to simulate lesions, and in the training of certain therapeutic techniques such as FNA of different organs, pancreatic pseudocyst drainage, or neurolysis of the celiac plexus [39] [40]. A study recently published in Endoscopy used a new animal model for the training of EUS-guided FNA and showed that training with such a model improves performance and student confidence when performing the procedure in real patients [41].

Although the use of animal models has been shown to have a role in EUS training, simulation should not replace the implementation of a sufficient number of clinical examinations in human patients under the supervision of an expert [25]. Most likely, the real role of these animal models is within specific courses that offer initial hands-on training.

The usefulness of animal models in training courses has been evaluated through the use of questionnaires completed by students who attended two training courses for EUS (held in 1997 and 2000), which used in vivo porcine models and were sponsored by the American Society for Gastrointestinal Endoscopy. The course was useful to 95 % of attendees in 1997 and 85 % particularly valued the practical part of the course. Over 90 % of respondents in 2000 believed that participating in the course had improved their skills and 88 % thought that they would be likely to perform EUS in the future [39].

Barthet et al. designed a 17-day course for training in FNA using hilar lymph nodes. After comparing the results before and after the training course, the authors showed that procedural times were significantly reduced and accuracy was increased after training, showing improvement in the skills of trainees using live animal models [40].

Many EUS-guided therapeutic procedures developed in recent years are still under investigation and have been performed only in animal models; such investigations are very important before implementation of the procedures in human patients [28] [42].

Training in ERCP

The technical complexity and potential risk of complications of ERCP are high when compared with the spectrum of endoscopic techniques available nowadays. The importance of training and expertise on the efficacy and safety of ERCP cannot be overstated. However, the case volume of ERCP is limited compared with other endoscopic techniques, and this may impact on the exposure of trainees to the procedure and hence on the time to acquire competence. Therefore, simulation for ERCP seems to be a good idea and should not be neglected. Progress is expected in this field, although training on a simulator is no substitute for supervised practice in real cases [43] [44].

There are several teaching models for the training of ERCP. The significant technical difficulty of ERCP was probably the reason why in 1974, only 1 year after the first endoscopic papillotomy was reported, a canine model for ERCP was developed. A total of 10 mongrel dogs underwent endoscopy with a side-viewing endoscope, and successful papillae cannulation was achieved in 4 [45]. The live porcine model for ERCP was described by Gholson et al. in 1990 [46]. Peculiarities of the canine model for ERCP are that the biliary and pancreatic ducts drain into separate papillae, in a similar way to the pig anatomy; the biliary papilla is located only a few centimeters distal to the pylorus whereas the pancreatic papilla is more distal [47]. The porcine model has been shown to be adaptable to all types of ERCP procedures, making it possible to cannulate, place stents, and pass routine instruments used by conventional duodenoscopes designed for use in humans [46] [47] [48].

The ex vivo Erlangen model was also adapted for training in ERCP [48]. In this model, the esophagus, stomach, duodenum to 15 cm below the pylorus, liver and gallbladder, gallbladder hilum, and bile ducts are harvested. Then, small pebbles can be inserted to the common bile duct though the papilla. The model is frozen. Before use, it is defrosted and appropriately attached to the dummy to maintain realism (e. g. fixing the hilum is required to keep the common bile duct elongated). This model has been used extensively in workshops for training [48] [49]. Sedlack et al. compared the ex vivo (Erlangen Endo-Trainer), in vivo, and virtual simulator (GI Mentor; Simbionix, Cleveland, Ohio, USA) models [49]. In a workshop, 20 endoscopists (10 students, 10 faculty) were surveyed after practicing biliary cannulation and several interventional techniques in the three models. The ex vivo model scored highest on realism, usefulness, and performance, whereas the computer simulator scored lower in most of the realism scores but was considered to be as the most easily incorporated into training programs.

As explained above, several animal models for ERCP training are available, but the impact of practicing on these models on the performance or learning curve of ERCP, either on simulation or in real clinical cases, has not been studied. However, one study evaluated the changes in clinical practice of participants who took part in a 2-day advanced ERCP workshop that included training on an in vivo porcine model with guidance from expert endoscopists [50]. Pre- and post-course surveys were completed by the participants and revealed that after the course the use of needle-knife precut sphincterotomy in clinical practice increased, as did self-confidence when applying the therapeutic techniques of ERCP.

A new simulation system with ex vivo and in vivo models has been proposed for training in endoscopic sphincterotomy and papillectomy [51]. In an interesting feasibility study, which reported on initial experience, an endoscopist who was experienced in ERCP created simulated papillae in porcine explanted stomach and rectum and in living gastric models by injecting 0.4 % hyaluronic acid. The papillae were created by making small cuts with a needle-knife. Papilla-like bulges were created in 76 % of gastric areas in the in vivo stomach, in 81 % in the ex vivo stomach, and in 100 % in the rectum model. Sphincterotomy could be performed in the gastric models without difficulty by the expert whereas the two participating trainees, who had no or limited experience, respectively, in sphincterotomy, experienced variable difficulty with the procedure. In the rectum, sphincterotomy and papillectomy were performed successfully by the three endoscopists. This model does not include training possibilities in real biliary cannulation or guide wire use, but it could be used as a relatively simple method of learning the basic maneuvers of sphincterotomy.

Matthes and Cohen previously reported on a simulated papilla constructed using explanted chicken heart tissue with two porcine arteries attached to resemble the biliary and pancreatic ducts [52]. The papilla was attached to an ex vivo porcine duodenum. The model was evaluated by nine endoscopists who were very experienced in ERCP, and it was rated as high or very high as a realistic tool for ERCP and especially useful as a method to teach and learn basic ERCP. The preparation of the model required approximately 75 minutes.

Training in ESD

ESD has been one of the greatest recent developments of endoscopy and has attracted the attention of the gastroenterological and surgical community because of its complexity, efficacy, and safety in expert hands [53]. How best to train in ESD remains a big and important question because at the beginning of the learning curve the risk of complications is higher and performance is worse [54] [55] [56]. After the circumferential cutting has been completed, submucosal dissection is the step that trainees experience more difficulty in accomplishing [57]. ESD includes lateral cutting, which is not a traditional therapeutic endoscopy maneuver.

When the existence of a learning curve was observed in initial reports of unsupervised ESD performed by beginners in this technique, experts recommended that at least 30 gastric ESDs should be performed on animal models (ideally supervised) before transferring to human cases [58]. In one study, an endoscopist performed 30 ESDs in a porcine model (initially ex vivo, later in vivo), and found that the total ESD time was higher in the first half of the cases, suggesting the existence of a learning curve [59]. In another study, four endoscopists performed a total of 12 ESDs in porcine models (half in isolated stomach, half in living animal), and could finally complete a human gastric ESD without complications [60].

The number of experimental resections that should be performed before performing ESD in human cases should probably be as great as possible in order to reduce the rate of perforations, as it has been shown that even among very expert endoscopists the rate of perforation is significant (around 20 %) at the beginning of the learning curve [61] [62]. In one study with expert endoscopists (mean 15 years experience in endoscopy), who participated in a seminar on ESD including supervised hands-on ESD in living pigs, a perforation rate of 65 % in gastric and 56 % in esophageal resections was observed [63].

Tanimoto et al. evaluated an in vivo canine model for training in gastric and esophageal ESD [64]. The same group demonstrated the feasibility of the canine model for training in circumferential esophageal ESD, and showed the existence of a clear learning curve and therefore the potential usefulness of this model. Among the 10 cases performed, perforations occurred in each one of the initial seven cases, whereas the last three cases were completed uneventfully [65]. The potential implications of starting such a complex technique in an animal model rather than on human cases are self-evident.

Training in esophageal ESD has been assessed in another study using a rather sophisticated ex vivo porcine model, in which two overtubes are used to give more stability to the esophagus, and hence simulating more realistically the human esophagus at ESD [66]. In this study, three endoscopists without any previous experience in esophageal ESD each performed 10 cases in the model described, and the performance in the initial period (first five cases) and the final period (last five cases) was compared. There was a significant reduction in the operation time for two of the endoscopists, and the mean number of injuries to the muscularis propria layer was significantly reduced for the three of them in the final cases. Therefore, this preliminary study suggests that this model can be adequate for the acquisition of basic skills in esophageal ESD.

Colorectal ESD is probably the most challenging location for this technique, and a reliable training model would be highly desirable. In one recent Western report, very good clinical results in terms of efficacy and safety were shown with a relatively simple training strategy that included six gastric ESDs in an ex vivo model (only one of them supervised), visiting an expert center, and performing a rectal ESD with supervision [67]. However, in a survey of experts in colorectal ESD a more intensive training strategy in animal models was suggested [68].

The role of training models in the learning curve of colorectal ESD remains to be clarified. A simple ex vivo porcine model was assessed for training in colorectal ESD [69]. In this preliminary study, a learning curve was suggested: of 10 procedures, the first two resulted in incomplete en bloc resection and perforations occurred, whereas the subsequent eight cases were completed successfully without any perforations. An ex vivo model for training in colorectal ESD, including hemostasis, was proposed by Yoshida et al. using bovine cecum [70].

Summary

In summary, although animal models were proposed for endoscopic training four decades ago, most of the studies validating them and assessing their efficacy and impact on training have been published in the past 15 years. Evidence from available studies consistently shows that training in animal models improves skills; some also found that it facilitates the application of certain techniques in clinical practice and increases self-confidence of the trainees. Future well-designed studies investigating training with simulators – including impact not only on educational and technical outcomes during simulation but also on clinical outcomes of patients treated by those endoscopists thereafter – are awaited. Animal models may prove to be essential to achieve competence in techniques such as ESD in regions such as Western countries where few early gastric cancer cases are observed and where still few experts are available.

Competing interests: None

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Corresponding author

• References

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