Surg Endosc DOI 10.1007/s00464-014-3500-3
and Other Interventional Techniques
Short-duration virtual reality simulation training positively impacts performance during laparoscopic colectomy in animal model: results of a single-blinded randomized trial VR warm-up for laparoscopic colectomy Sergio E. A. Araujo • Conor P. Delaney • Victor E. Seid Antonio R. Imperiale • Alexandre B. Bertoncini • Sergio C. Nahas • Ivan Cecconello
•
Received: 10 December 2013 / Accepted: 17 February 2014 Ó Springer Science+Business Media New York 2014
Abstract Background Several studies have demonstrated skills transfer after virtual reality (VR) simulation training in laparoscopic surgery. However, the impact of VR simulation training on transfer of skills related to laparoscopic colectomy remains not investigated. The present study aimed at determining the impact of VR simulation warm-up on performance during laparoscopic colectomy in the porcine model. Methods Fourteen residents naive to laparoscopic colectomy as surgeons were randomly assigned in block to two groups. Seven trainees completed a 2-h VR simulator training in the laparoscopic sigmoid colectomy module (study group). The remaining seven surgeons (control
S. E. A. Araujo S. C. Nahas I. Cecconello Department of Gastroenterology, University of Sao Paulo Medical School, Sa˜o Paulo, Brazil S. E. A. Araujo V. E. Seid A. R. Imperiale A. B. Bertoncini S. C. Nahas Colorectal Surgery Division, University of Sao Paulo Medical Center, Sa˜o Paulo, SP, Brazil S. E. A. Araujo (&) Av. Dr. Eneas de Carvalho Aguiar, 255, Sa˜o Paulo, SP 05403-000, Brazil e-mail: [email protected]
group) underwent no intervention. On the same day, all participants performed a sigmoid colectomy with anastomosis on a pig. All operations were video recorded. Two board-certified expert colorectal surgeons independently assessed performance during the colectomy on the swine. Examiners were blinded to group assignment. The two examiners used a previously validated clinical instrument specific to laparoscopic colectomy. The primary outcome was the generic and specific skills score values. Results Surgeons undergoing short-duration training on the VR simulator performed significantly better during laparoscopic colectomy on the pig regarding general and specific technical skills evaluation. The average score of generic skills was 17.2 (16.5–18) for the control group and 20.1 (16.5–22) for the study group (p = 0.002). The specific skills average score for the control group was 20.2 (19–21.5) and 24.2 (21–27.5) for the study group (p = 0.001). There was acceptable concordance (Kendall’s W) regarding the video assessment of generic (W = 0.78) and specific skills (W = 0.84) between the two examiners. Conclusions A single short-duration VR simulator practice positively impacted surgeons’ generic and specific skills performance required to accomplish laparoscopic colectomy in the swine model.
C. P. Delaney Case Western Reserve University Center for Skills and Simulation, Cleveland, OH, USA
Keywords Laparoscopy Colectomy Colonic neoplasms Education Credentialing Clinical skills
C. P. Delaney Digestive Health Institute University Hospitals Case Medical Center, Case Western Reserve University, Cleveland, OH, USA
Skills transfer in surgery follows a traditional model where the trainee surgeon works as an apprentice. Known in the United States and Europe as Halsted’s model, it was introduced at Johns Hopkins University in 1889 and served well to conventional surgery for more than one century [1]. However, laparoscopic surgery has challenged this
I. Cecconello Digestive Surgery Division, University of Sao Paulo Medical Center, Sa˜o Paulo, SP, Brazil
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traditional model. The need to acquire specific skills dissimilar to those used during conventional surgery was imposed. Nowadays, trainee surgeons are required to gather more technical skills in less time, adding stress to an already busy clinical practice [2]. Minimally invasive and endoluminal surgical techniques demand a completely new set of psychomotor skills. The role of simulation in the development of technical skills is being extensively evaluated in recent years [3, 4]. In 1993, Satava [5] proposed the adoption of training in a virtual reality (VR) simulator as a tool for skills transfer with a potential to reduce patient risks. The construction of a realistic scene graph, the possibility of task repetition, unsupervised training, and to record performance variables represent the main advantages of this tool. As result, with the advancement of desktop computing, commercially available VR-based surgical simulators were developed. The LapMentorTM (Simbionix USA Corp., Cleveland, OH) is a high-fidelity and computer-aided simulator. It enables laparoscopic training of basic skills and advanced procedures (such as laparoscopic sigmoidectomy). Moreover, the simulator provides feedback to the trainee at the completion of the task or procedure regarding operative time, efficiency of motion, and safety. Improved training and objective result assessment would be the key strategies for accomplishing less medical errors. It was first demonstrated that training in a VR simulator improves performance in the simulator environment activities [6, 7]. Then, other studies have demonstrated that the achieved improved performance can be observed during a real laparoscopic task [8]. Ultimately, some authors have shown that the adoption of VR practice during surgical training improves operating room performance [9–11]. However, the adoption of VR simulation training by the surgical community remains still investigational. The main reasons are: the characteristics of uni-institutional small sample sizes in the mentioned studies, the recruitment of residents as research subjects and, above all, the relatively low-risk nature of the studied operations for which trainee surgeons were being prepared, i.e., laparoscopic cholecystectomy [4]. The results of non-inferiority of laparoscopic colectomy compared to conventional surgery in the curative surgical treatment of colon [12–15] and rectal cancer [15] were clearly demonstrated. However, the high level of technical complexity associated to laparoscopic colectomies was held partially responsible (associated to socioeconomic factors [16]) for its relatively low adoption rate [17] by surgical community when compared to other laparoscopic operations. In colorectal surgery, the evidence regarding the implementation of simulation-based training into clinical practice remains undetermined [18] partially due to the fact that specialty surgeons rather practice minimally
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invasive colorectal surgery in a cadaver model rather than in a simulator [19]. Furthermore, simulation-based training may require some investment in resources and faculty, which may be balanced against traditional surgical education [20]. A potential application of simulation-based training into surgical practice may include a form of warm-up. A VR simulation warm-up module is performed just before undertaking the real procedure. It was demonstrated that a 15–20-min warm-up led to a 33 % overall technical errors reduction in a series of exercises that simulated surgical skills [21]. Moreover, the positive effect for experienced surgeons on specific psychomotor skills performing cholecystectomies after the warm-up were recently demonstrated in two randomized trials [20, 22]. In colorectal surgery, there is little or virtually no evidence examining the potential of simulation for warm-up training before carrying out a minimally invasive procedure. Therefore, in the present study, we hypothesized that a shortduration (warm-up) skills training in a VR simulator could positively impact the performance of surgical residents. To verify this hypothesis, we undertook a single-blinded randomized trial using technical performance during a colectomy in the swine model as the main outcome.
Materials and methods Subjects Fourteen residents of a university-affiliated hospital with the same level of clinical experience in laparoscopic colorectal surgery were recruited. Virtual reality simulatorbased training is currently not available for surgical education in our hospital. All the surgeons included in the study stated that had not previously joined a laparoscopic colectomy course. Study design Our Institutional Review Board approved all details of the present study. All recruited surgeons gave informed consent. The experimental anesthesia and surgical procedure protocols were approved by a review committee and met the guidelines of Brazilian national responsible agency, strictly followed in the animal laboratory where this study was conducted. This was a randomized and single-blinded study. Randomization was performed en block. Seven residents were assigned to the control group (no VR simulator-based warm-up) and seven, to the study group (VR-based simulator training).
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Fig. 1 Study design
The eligibility criteria were the availability to participate in the study and lack of previous laparoscopic colectomy training. For all participants, the outcome was performance measured during an operation of laparoscopic sigmoid resection in the animal model (swine). This was assessed using the score for generic and specific skill associated to the sigmoid colectomy as previously reported [2]. The study flow diagram [23] is in Fig. 1. VR simulator training (warm-up) The warm-up training was conducted in the LAPMentor (Simbionix, Cleveland, OH, USA) VR simulator (laparoscopic sigmoid resection) with a 2-h duration. Although we did not register the simulator practice time in the present study, all recruited subjects were able to complete were able to complete the sigmoid colectomy on the simulator before 2 h. The sigmoidectomy module constructed in the simulator was developed in accordance with SAGES (Society of American Gastrointestinal and Endoscopic Surgeons) guidelines and through close collaboration with a group of
experts—Dr. Amid Szold (Surgical Endoscopy Unit, Medical Center Sorasky, Israel), Masahiko Watanabe (Department of Surgery, Kitasato University, Japan), Yukihito Kokuba (Department of Laparoscopic Surgery for Digestive Diseases, University of Kyoto, Japan), and Conor Delaney (Department of Surgery, Case Western Reserve University, United States) . Before training, all participants were briefed during a 15-min presentation on the simulator about its functioning and the characteristics of the sigmoid resection module. The participants should complete sigmoid resection and anastomosis. Evaluation of performance and study outcomes All participants completed a laparoscopic sigmoid resection in the swine. The procedure was preceded by a 15-min video presentation on the operation technical details. The surgeon under evaluation and two assistant surgeons composed the surgical team. All residents within the study were supervised by a senior surgeon responsible for the study design and blinded to the surgeon’s status of warm-up. All 14 operations were video recorded. Two Brazilian board-certified colorectal surgeons with personal experience
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Surg Endosc Table 1 Laparoscopic generic technical skills score [2] Generic technical skills Likert ratings
1
2
3
4
5
Handling and dissection of tissues
Unnecessary force on tissues, causing frequent damage to tissues
Careful handling of tissue but occasionally caused inadvertent damage
Consistently handled tissues appropriately with minimal damage
Dexterity
Many unnecessary moves
Efficient time/motion but some unnecessary moves
Economy of movement and maximum efficiency
Instrument and material handling
Repeatedly makes tentative or awkward moves with instrument or material
Competent use of instruments/ material although occasionally awkward
Fluid moves with instruments/ material and no awkwardness
Use of instruments and material
Frequently used inappropriate instruments and materials
Used appropriate instrument and materials for the task or subtask
Expertly used appropriate instruments and materials
Exposure of technical field
Consistently poor exposure
Good exposure most of the time
Expert exposure
Hemostasis
Poor control of bleeding, inappropriate methods used
Competent and controlled bleeding appropriately
Very little bleeding, anticipating possible bleeding areas
Completion and flow of tasks and subtasks
Frequently stopped operating or hesitant in next task or subtask
Forward planning with steady progression of tasks and subtasks
Effortless flow from one task to subtask
Table 2 Laparoscopic specific technical skills score related to the sigmoid colectomy [2] Specific technical skills global ratings
1
2
3
4
5
Access and port insertion
Created clumsy and with difficulty
Created adequately
Created quickly and skillfully
Retraction, dissection, exposure, and mobilization at inferior mesenteric pedicle
Poor retraction, dissection, exposure, and mobilization at inferior mesenteric pedicle, large amount of bleeding
Satisfactory retraction, dissection, exposure, and mobilization at inferior mesenteric pedicle, small amount of bleeding
Expert retraction, dissection, exposure, and mobilization at inferior mesenteric pedicle, minimal amount of bleeding
Clipping and transection of inferior mesenteric artery
Clips not placed accurately, large amount of bleeding
Clips placed proximally and distally adequately, minimal bleeding
Clips placed expertly, proximally and distally, with adequate length, no bleeding
Mobilize colon along Toldt’s fascia on left side of colon
Poor mobilization
Satisfactory mobilization
Expert mobilization
Identify left ureter
Left ureter not identified or transected
Left ureter adequately identified
Left ureter clearly identified
Transection of colon
Clumsily done
Adequately done
Expertly and smoothly done
Extraction of colonic specimen
Clumsily done
Adequately done with little trauma
Smoothly done with minimal trauma
Colonic anastomosis
Clumsily done, with discrepancy in blood supply
Adequately done with little trauma, good blood supply
Expertly and smoothly done, good blood supply
over 300 laparoscopic colectomies analyzed all DVDs. The examiners were blinded to the surgeons’ identities. The examiners used the instrument for surgical performance evaluation validated by Sarker et al. [2]. for assessment of generic and specific technical skills during a laparoscopic sigmoid colectomy. This instrument was used after free English to Portuguese translation and adapted to sigmoid colectomy in the swine model. Regarding generic skills, score results ranged from 7 to 35 (Table 1); and from
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8 to 40 for specific skills (Table 2). For control and study groups, a mean value for generic and specific skills was obtained. These values were compared. Since operating time did not represent an evaluation parameter, according to Sarker’s [2] instrument, time until completion of the colectomy in the animal model was not recorded in the present study. Regarding data analysis and study outcomes, the primary outcome measure was performance quality during
Surg Endosc Table 3 Results of generic and specific skills score [2] for control and study group during a laparoscopic sigmoid resection in the swine according to two evaluators Generic technical skills score results
Control group (N = 7) Mean (range)
Study group (N = 7) Mean (range)
Handling and dissection of tissues
2.5 (2–3)
3 (2–4)
Dexterity
2.1 (2–4)
3 (2–4)
Instrument and material handling
2.3 (2–3)
2.8 (2–4)
Use of instruments and material
2.5 (2–3)
2.5 (2–4)
Exposure of technical field
2.5 (2–4)
2.8 (3–4)
Hemostasis
2.8 (3–4)
3 (3–4)
Completion and flow of tasks and subtasks
2.5 (2–4)
3 (2–4)
Generic technical skills score
17.2 (16.5–18)
20.1 (16.5–22)
Access and port insertion
2.4 (2–4)
3 (3–4)
Retraction, dissection, exposure, and mobilization at inferior mesenteric pedicle
2.3 (2–5)
2.8 (1–4)
Clipping and transection of inferior mesenteric artery
2.7 (2–4)
3.4 (3–4)
mobilize colon along Toldt’s fascia on left side of colon
2.4 (2–4)
3 (2–4)
Identify left ureter
2.7 (2–4)
2.8 (2–4)
Transection of colon
2.3 (2–4)
3.5 (3–5)
Extraction of colonic specimen
2.7 (2–4)
2.8 (2–4)
Colonic anastomosis
2.7 (2–4)
2.9 (2–4)
Specific technical skills score
20.2 (19–21.5)
24.2 (21–27.5)
a
p
Fig. 2 Mean and standard deviation values for generic and specific skills scores in control and study groups 0.002a
0.001a
Student’s t test
colectomy in the swine model according to (1) the generic and (2) the specific skills score. The Student’s t test was used to compare mean score values. Kendall’s coefficient of concordance (W) statistic was used to ensure reliability of the video-based assessment scores between the two expert surgeons (VES and ARI). A value of p \ 0.05 was considered statistically significant.
Fig. 3 Distribution of 28 scores of generic and specific skills during a laparoscopic sigmoid colectomy in the swine model according to study group
was 20.1 (16.5–22)—p = 0.002 (Student’s t test). Regarding specific skills, the mean score was 20.2 (19–21.5) in the control group and 24.2 (21–27.5) in the study group (p = 0.001—Student’s t test). These results are evinced in Table 3 and depicted in Figs. 2 and 3. The mean values of Kendall’s coefficient of concordance (W) for the video assessment conducted by the two expert examiners were 0.78 for generic skills, and 0.84 for specific skills. These results indicate that the reliability of the video-based assessment was acceptable (W [ 0.75).
Results Discussion All participating surgeons completed the study. In each group, there was one female surgeon. All surgeons were right-handed. Data from video recordings were available for all 14 participating surgeons. In the control group, the mean score for generic skills was 17.2 (16.5–18). In the study group, it
Minimally invasive surgery requires specific psychomotor capabilities. These capabilities may be acquired through training [24]. We hypothesized that a short-duration (warm-up) skills training in a VR simulator could positively impact the performance of surgeons not experienced
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in laparoscopic colorectal surgery during a laparoscopic colectomy in the swine model. In the present randomized study, it was demonstrated that a pre-procedural warm-up in a VR simulator improves the performance of novice surgeons conducting a laparoscopic colectomy in the swine model. Although the current study has not demonstrated transference of laparoscopic skills into the real clinical setting, it was the first study to demonstrate the impact of a warm-up for minimally invasive colorectal surgery. Current evidence regarding skills transfer during laparoscopic surgery after a pre-procedural warm-up remains restricted to two main findings. First, brief warm-up laparoscopic exercises conducted in VR simulators improved laparoscopic skills verified on a simulator task [21, 25]. Therefore, this finding generated limited evidence whether a positive warm-up effect could be moved to patients in the real clinical setting. The second category of findings represents the rationale for the present study. Calatayud et al. [20] and Moldovanu et al. [22] have demonstrated a significant beneficial impact of warming-up in a VR simulator on laparoscopic performance during cholecystectomies in the OR. Lee et al. [26] observed that cognitive and psychomotor performed skills were significantly better after a preoperative warm-up using box trainer and VR simulation for surgeons serving as their controls and scheduled to perform clinical laparoscopic renal surgery. The extent to which these findings [20, 22, 24] can be generalized to other procedures remains unknown. Regarding the study design, two limitations of the present study are related to the research subjects. First, the study may be underpowered due to a small sample size. Availability of research subjects of presumably the same skills level was the first impediment factor. Moreover, although highly desirable, a multicenter study could not be accomplished using the proposed methodology. Unavailability of the VR simulators for a multi-institutional trial was the second impediment factor. As result, conclusions may be of limited clinical value. Second, although all included surgeons were first-year residents of digestive tract surgery at the same University hospital, there could have been baseline differences in the level of overall surgical proficiency among the individuals. Therefore, it would have been ideal for each resident to perform a pre-intervention colectomy followed by a postintervention procedure. Therefore, research subjects would serve as their own controls. However, the use of live animals precludes the use of this design in our institution. Another interesting approach would be to obtain a preintervention performance of all the residents by measuring baseline scores on the VR simulator. Ultimately, It is possible that, in the present study, randomization may have helped reducing variable skills levels among research subjects.
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Instead of using a combination of tasks of the basic module of the VR simulator, we chose, after a short briefing about how the simulator works, to warm-up the surgeons in the sigmoid colectomy module. It was our intention to train the naı¨ve surgeons in the steps they should be following during the colectomy in the animal model. Although the swine is less reliable for the laparoscopic colectomy education than the cadaver model [18], training in the live animal model requires the trainee surgeon to simulate OR environment, to follow the flow of predetermined tasks and to manage commonly used equipment and instrumentals specific to laparoscopic colectomy. Evaluation of surgical performance is cumbersome. Several tools have been used in published research studies, although none has been taken up for broad use in technical skills assessments. Moreover, the clinical significance of a measured difference in scores between two or more surgeons of after an educational intervention remains challenging to be addressed. Laparoscopic colorectal surgery is a relatively new specialty. Sarker et al. [27]. have studied hierarchical task analysis to identify key steps during operations to construct Likert scales for generic and specific technical skills assessment. After evaluating 84 live real operations conducted by six consultants and eight trainees using a specific tool [2], they observed that all consultants performed better in both generic and specific technical skills when compared to their trainees. Therefore, it was demonstrated that the proposed assessment tool of generic and specific technical skills in advanced laparoscopic colorectal surgery was reliable. It was our belief that using the instrument validated by this group [2] would be the most accurate way to assess generic and specific skills during a laparoscopic colectomy, even if performed in the swine model. As far as we can ascertain, this study was the first to do so. Moreover, similarly to other studies in the literature, we used two independent observers [20, 22, 26]. It was demonstrated in this study that a short-duration (warm-up) VR simulator training led to improved performance of generic and specific skills during a laparoscopic colectomy in the animal model. These data should be interpreted with caution, especially regarding the potential benefits of warming-up for surgeons more experienced than the research subjects in the present study. Further studies should include more surgeons with different degrees of experience in laparoscopic colorectal surgery. Moreover, clinical tutoring may play a role in the surgical education of non-beginner surgeons to accomplish technical and nontechnical skills transfer. There might be two plausible explanations to the main finding of the present study. First, in most studies, VR simulator practice consisted of tasks repetitions performed in the basic module [20, 21]. In contrast, in this study, the
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warm-up was conducted in the advanced module (laparoscopic sigmoid resection). Second, generic and specific skills may require different time intervals to be incorporated. Generic skills perhaps require more time and are acquired throughout training, for example, during an entire medical residency in surgery [2]. On the other hand, specific skills, although technically sophisticated, are required for the completion of one particular procedure, therefore, requiring less time and effort to be achieved. In the present study, the difference for generic skills mean scores between the groups was slightly lower than that observed for specific skills. These data suggest that training one specific operation in the VR simulator, even for a short interval of time, may enable the trainee surgeon to perform that task more effectively. On the other hand, the impact of a warmup on the set of generic skills is perchance least. The present randomized single-blinded study raises important evidence about the role of VR simulator training for skills transfer in laparoscopic colorectal surgery. However, determining the timing and extent to which this practice should be implemented in the surgical curriculum remains a challenge to be addressed by future research. Although no other studies have tested the concept of warming-up in the real clinical setting of minimally invasive colectomy, the present evidence may shed light on the role of VR simulation training for the education of surgeons involved in the minimally invasive treatment of colorectal diseases.
Disclosures Drs. Sergio Eduardo Alonso Araujo, Conor Patrick Delaney, Victor Edmond Seid, Antonio Rocco Imperiale, Alexandre Bruno Bertoncini, Sergio Carlos Nahas, and Ivan Cecconello have no conflicts of interest or financial ties to disclose.
References 1. Scott DJ, Cendan JC, Pugh CM, Minter RM, Dunnington GL, Kozar RA (2008) The changing face of surgical education: simulation as the new paradigm. J Surg Res 147:189–193 2. Sarker SK, Kumar I, Delaney C (2010) Assessing operative performance in advanced laparoscopic colorectal surgery. World J Surg 34:1594–1603 3. Larsen CR, Oestergaard J, Ottesen BS, Soerensen JL (2012) The efficacy of virtual reality simulation training in laparoscopy: a systematic review of randomized trials. Acta Obstet Gynecol Scand 91:1015–1028 4. Zendejas B, Brydges R, Hamstra SJ, Cook DA (2013) State of the evidence on simulation-based training for laparoscopic surgery: a systematic review. Ann Surg 257:586–593 5. Satava RM (1993) Virtual reality surgical simulator: the first steps. Surg Endosc 7:203–205 6. Grantcharov TP, Kristiansen VB, Bendix J, Bardram L, Rosenberg J, Funch-Jensen P (2004) Randomized clinical trial of virtual reality simulation for laparoscopic skills training. Br J Surg 91:146–150
7. Gallagher AG, Seymour NE, Jordan-Black J-A, Bunting BP, McGlade K, Satava RM (2013) Prospective, randomized assessment of transfer of training (ToT) and transfer effectiveness ratio (TER) of virtual reality simulation training for laparoscopic skill acquisition. Ann Surg 257:1025–1031 8. Torkington J, Smith SG, Rees BI, Darzi A (2001) Skill transfer from virtual reality to a real laparoscopic task. Surg Endosc 15:1076–1079 9. Seymour NE, Gallagher AG, Roman SA, O’Brien MK, Bansal VK, Andersen DK, Stava RM (2002) Virtual reality training improves operating room performance: results of a randomized, double-blinded study. Ann Surg 236:458–463 10. Andreatta PB, Woodrum DT, Birkmeyer JD, Yellamanchilli RK, Doherty GM, Gauger PG, Minter RM (2006) Laparoscopic skills are improved with LapMentor training: results of a randomized, double-blinded study. Ann Surg 243:854–860 11. Ahlberg G, Enochsson L, Gallagher AG, Hedman L, Hogman C, McClusky DA 3rd, Ramel S, Smith CD, Arvidsson D (2007) Proficiency-based virtual reality training significantly reduces the error rate for residents during their first 10 laparoscopic cholecystectomies. Am J Surg 193:797–804 12. Colon Cancer Laparoscopic or Open Resection Study Group, Buunen M, Veldkamp R, Hop WCJ, Kuhry E, Jeekel J, Haglind E, Pa˚hlman L, Cuesta MA, Msika S, Morino M, Lacy A, Bonjer HJ (2009) Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol 10:44–52 13. Lacy AM, Delgado S, Castells A, Prins HA, Arroyo V, Ibarzabal A, Pique JM (2008) The long-term results of a randomized clinical trial of laparoscopy-assisted versus open surgery for colon cancer. Ann Surg 248:1–7 14. Fleshman J, Sargent DJ, Green E, Anvari M, Stryker SJ, Beart RW Jr, Hellinger M, Flanagan R Jr, Peters W, Nelson H (2007) Laparoscopic colectomy for cancer is not inferior to open surgery based on 5-year data from the COST Study Group trial. Ann Surg 246:655–662 15. Jayne DG, Guillou PJ, Thorpe H, Quirke P, Copeland J, Smith AMH, Heath RM, Brown JM (2007) Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial Group. J Clin Oncol 25:3061–3068 16. Bardakcioglu O, Khan A, Aldridge C, Chen J (2013) Growth of laparoscopic colectomy in the United States: analysis of regional and socioeconomic factors over time. Ann Surg 258:270–274 17. Kemp JA, Finlayson SRG (2008) Nationwide trends in laparoscopic colectomy from 2000 to 2004. Surg Endosc 22(5):1181–1187 18. Miskovic D, Wyles SM, Ni M, Darzi AW, Hanna GB (2010) Systematic review on mentoring and simulation in laparoscopic colorectal surgery. Ann Surg 252:943–951 19. LeBlanc F, Champagne BJ, Augestad KM, Neary PC, Senagore AJ, Ellis CN, Delaney CP (2010) A comparison of human cadaver and augmented reality simulator models for straight laparoscopic colorectal skills acquisition training. J Am Coll Surg 211:250–255 20. Calatayud D, Arora S, Aggarwal R, Kruglikova I, Schulze S, Funch-Jensen P, Grantcharov T (2010) Warm-up in a virtual reality environment improves performance in the operating room. Ann Surg 251:1181–1185 21. Kahol K, Satava RM, Ferrara J, Smith ML (2009) Effect of shortterm pretrial practice on surgical proficiency in simulated environments: a randomized trial of the ‘‘preoperative warm-up’’ effect. J Am Coll Surg 208:255–268 22. Moldovanu R, Taˆrcoveanu E, Dimofte G, Lupas¸ cu C, Bradea C (2011) Preoperative warm-up using a virtual reality simulator. JSLS 15:533–538 23. Schulz KF, Altman DG, Moher D (2010) CONSORT Group CONSORT 2010 statement: updated guidelines for reporting parallel group randomized trials. Ann Intern Med 152:726–732
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Surg Endosc 24. Aggarwal R, Grantcharov T, Moorthy K, Hance J, Darzi A (2006) A competency-based virtual reality training curriculum for the acquisition of laparoscopic psychomotor skill. Am J Surg 191:128–133 25. Do AT, Cabbad MF, Kerr A, Serur E, Robertazzi RR, Stankovic MR (2006) A warm-up laparoscopic exercise improves the subsequent laparoscopic performance of Ob-Gyn residents: a lowcost laparoscopic trainer. JSLS 10:297–301
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26. Lee JY, Mucksavage P, Kerbl DC, Osann KE, Winfield HN, Kahol K, McDougall EM (2012) Laparoscopic warm-up exercises improve performance of senior-level trainees during laparoscopic renal surgery. J Endourol Endourol Soc 26:545–550 27. Sarker SK, Chang A, Vincent C, Darzi SA (2006) Development of assessing generic and specific technical skills in laparoscopic surgery. Am J Surg 191:238–244
and Other Interventional Techniques
Short-duration virtual reality simulation training positively impacts performance during laparoscopic colectomy in animal model: results of a single-blinded randomized trial VR warm-up for laparoscopic colectomy Sergio E. A. Araujo • Conor P. Delaney • Victor E. Seid Antonio R. Imperiale • Alexandre B. Bertoncini • Sergio C. Nahas • Ivan Cecconello
•
Received: 10 December 2013 / Accepted: 17 February 2014 Ó Springer Science+Business Media New York 2014
Abstract Background Several studies have demonstrated skills transfer after virtual reality (VR) simulation training in laparoscopic surgery. However, the impact of VR simulation training on transfer of skills related to laparoscopic colectomy remains not investigated. The present study aimed at determining the impact of VR simulation warm-up on performance during laparoscopic colectomy in the porcine model. Methods Fourteen residents naive to laparoscopic colectomy as surgeons were randomly assigned in block to two groups. Seven trainees completed a 2-h VR simulator training in the laparoscopic sigmoid colectomy module (study group). The remaining seven surgeons (control
S. E. A. Araujo S. C. Nahas I. Cecconello Department of Gastroenterology, University of Sao Paulo Medical School, Sa˜o Paulo, Brazil S. E. A. Araujo V. E. Seid A. R. Imperiale A. B. Bertoncini S. C. Nahas Colorectal Surgery Division, University of Sao Paulo Medical Center, Sa˜o Paulo, SP, Brazil S. E. A. Araujo (&) Av. Dr. Eneas de Carvalho Aguiar, 255, Sa˜o Paulo, SP 05403-000, Brazil e-mail: [email protected]
group) underwent no intervention. On the same day, all participants performed a sigmoid colectomy with anastomosis on a pig. All operations were video recorded. Two board-certified expert colorectal surgeons independently assessed performance during the colectomy on the swine. Examiners were blinded to group assignment. The two examiners used a previously validated clinical instrument specific to laparoscopic colectomy. The primary outcome was the generic and specific skills score values. Results Surgeons undergoing short-duration training on the VR simulator performed significantly better during laparoscopic colectomy on the pig regarding general and specific technical skills evaluation. The average score of generic skills was 17.2 (16.5–18) for the control group and 20.1 (16.5–22) for the study group (p = 0.002). The specific skills average score for the control group was 20.2 (19–21.5) and 24.2 (21–27.5) for the study group (p = 0.001). There was acceptable concordance (Kendall’s W) regarding the video assessment of generic (W = 0.78) and specific skills (W = 0.84) between the two examiners. Conclusions A single short-duration VR simulator practice positively impacted surgeons’ generic and specific skills performance required to accomplish laparoscopic colectomy in the swine model.
C. P. Delaney Case Western Reserve University Center for Skills and Simulation, Cleveland, OH, USA
Keywords Laparoscopy Colectomy Colonic neoplasms Education Credentialing Clinical skills
C. P. Delaney Digestive Health Institute University Hospitals Case Medical Center, Case Western Reserve University, Cleveland, OH, USA
Skills transfer in surgery follows a traditional model where the trainee surgeon works as an apprentice. Known in the United States and Europe as Halsted’s model, it was introduced at Johns Hopkins University in 1889 and served well to conventional surgery for more than one century [1]. However, laparoscopic surgery has challenged this
I. Cecconello Digestive Surgery Division, University of Sao Paulo Medical Center, Sa˜o Paulo, SP, Brazil
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traditional model. The need to acquire specific skills dissimilar to those used during conventional surgery was imposed. Nowadays, trainee surgeons are required to gather more technical skills in less time, adding stress to an already busy clinical practice [2]. Minimally invasive and endoluminal surgical techniques demand a completely new set of psychomotor skills. The role of simulation in the development of technical skills is being extensively evaluated in recent years [3, 4]. In 1993, Satava [5] proposed the adoption of training in a virtual reality (VR) simulator as a tool for skills transfer with a potential to reduce patient risks. The construction of a realistic scene graph, the possibility of task repetition, unsupervised training, and to record performance variables represent the main advantages of this tool. As result, with the advancement of desktop computing, commercially available VR-based surgical simulators were developed. The LapMentorTM (Simbionix USA Corp., Cleveland, OH) is a high-fidelity and computer-aided simulator. It enables laparoscopic training of basic skills and advanced procedures (such as laparoscopic sigmoidectomy). Moreover, the simulator provides feedback to the trainee at the completion of the task or procedure regarding operative time, efficiency of motion, and safety. Improved training and objective result assessment would be the key strategies for accomplishing less medical errors. It was first demonstrated that training in a VR simulator improves performance in the simulator environment activities [6, 7]. Then, other studies have demonstrated that the achieved improved performance can be observed during a real laparoscopic task [8]. Ultimately, some authors have shown that the adoption of VR practice during surgical training improves operating room performance [9–11]. However, the adoption of VR simulation training by the surgical community remains still investigational. The main reasons are: the characteristics of uni-institutional small sample sizes in the mentioned studies, the recruitment of residents as research subjects and, above all, the relatively low-risk nature of the studied operations for which trainee surgeons were being prepared, i.e., laparoscopic cholecystectomy [4]. The results of non-inferiority of laparoscopic colectomy compared to conventional surgery in the curative surgical treatment of colon [12–15] and rectal cancer [15] were clearly demonstrated. However, the high level of technical complexity associated to laparoscopic colectomies was held partially responsible (associated to socioeconomic factors [16]) for its relatively low adoption rate [17] by surgical community when compared to other laparoscopic operations. In colorectal surgery, the evidence regarding the implementation of simulation-based training into clinical practice remains undetermined [18] partially due to the fact that specialty surgeons rather practice minimally
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invasive colorectal surgery in a cadaver model rather than in a simulator [19]. Furthermore, simulation-based training may require some investment in resources and faculty, which may be balanced against traditional surgical education [20]. A potential application of simulation-based training into surgical practice may include a form of warm-up. A VR simulation warm-up module is performed just before undertaking the real procedure. It was demonstrated that a 15–20-min warm-up led to a 33 % overall technical errors reduction in a series of exercises that simulated surgical skills [21]. Moreover, the positive effect for experienced surgeons on specific psychomotor skills performing cholecystectomies after the warm-up were recently demonstrated in two randomized trials [20, 22]. In colorectal surgery, there is little or virtually no evidence examining the potential of simulation for warm-up training before carrying out a minimally invasive procedure. Therefore, in the present study, we hypothesized that a shortduration (warm-up) skills training in a VR simulator could positively impact the performance of surgical residents. To verify this hypothesis, we undertook a single-blinded randomized trial using technical performance during a colectomy in the swine model as the main outcome.
Materials and methods Subjects Fourteen residents of a university-affiliated hospital with the same level of clinical experience in laparoscopic colorectal surgery were recruited. Virtual reality simulatorbased training is currently not available for surgical education in our hospital. All the surgeons included in the study stated that had not previously joined a laparoscopic colectomy course. Study design Our Institutional Review Board approved all details of the present study. All recruited surgeons gave informed consent. The experimental anesthesia and surgical procedure protocols were approved by a review committee and met the guidelines of Brazilian national responsible agency, strictly followed in the animal laboratory where this study was conducted. This was a randomized and single-blinded study. Randomization was performed en block. Seven residents were assigned to the control group (no VR simulator-based warm-up) and seven, to the study group (VR-based simulator training).
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Fig. 1 Study design
The eligibility criteria were the availability to participate in the study and lack of previous laparoscopic colectomy training. For all participants, the outcome was performance measured during an operation of laparoscopic sigmoid resection in the animal model (swine). This was assessed using the score for generic and specific skill associated to the sigmoid colectomy as previously reported [2]. The study flow diagram [23] is in Fig. 1. VR simulator training (warm-up) The warm-up training was conducted in the LAPMentor (Simbionix, Cleveland, OH, USA) VR simulator (laparoscopic sigmoid resection) with a 2-h duration. Although we did not register the simulator practice time in the present study, all recruited subjects were able to complete were able to complete the sigmoid colectomy on the simulator before 2 h. The sigmoidectomy module constructed in the simulator was developed in accordance with SAGES (Society of American Gastrointestinal and Endoscopic Surgeons) guidelines and through close collaboration with a group of
experts—Dr. Amid Szold (Surgical Endoscopy Unit, Medical Center Sorasky, Israel), Masahiko Watanabe (Department of Surgery, Kitasato University, Japan), Yukihito Kokuba (Department of Laparoscopic Surgery for Digestive Diseases, University of Kyoto, Japan), and Conor Delaney (Department of Surgery, Case Western Reserve University, United States) . Before training, all participants were briefed during a 15-min presentation on the simulator about its functioning and the characteristics of the sigmoid resection module. The participants should complete sigmoid resection and anastomosis. Evaluation of performance and study outcomes All participants completed a laparoscopic sigmoid resection in the swine. The procedure was preceded by a 15-min video presentation on the operation technical details. The surgeon under evaluation and two assistant surgeons composed the surgical team. All residents within the study were supervised by a senior surgeon responsible for the study design and blinded to the surgeon’s status of warm-up. All 14 operations were video recorded. Two Brazilian board-certified colorectal surgeons with personal experience
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Surg Endosc Table 1 Laparoscopic generic technical skills score [2] Generic technical skills Likert ratings
1
2
3
4
5
Handling and dissection of tissues
Unnecessary force on tissues, causing frequent damage to tissues
Careful handling of tissue but occasionally caused inadvertent damage
Consistently handled tissues appropriately with minimal damage
Dexterity
Many unnecessary moves
Efficient time/motion but some unnecessary moves
Economy of movement and maximum efficiency
Instrument and material handling
Repeatedly makes tentative or awkward moves with instrument or material
Competent use of instruments/ material although occasionally awkward
Fluid moves with instruments/ material and no awkwardness
Use of instruments and material
Frequently used inappropriate instruments and materials
Used appropriate instrument and materials for the task or subtask
Expertly used appropriate instruments and materials
Exposure of technical field
Consistently poor exposure
Good exposure most of the time
Expert exposure
Hemostasis
Poor control of bleeding, inappropriate methods used
Competent and controlled bleeding appropriately
Very little bleeding, anticipating possible bleeding areas
Completion and flow of tasks and subtasks
Frequently stopped operating or hesitant in next task or subtask
Forward planning with steady progression of tasks and subtasks
Effortless flow from one task to subtask
Table 2 Laparoscopic specific technical skills score related to the sigmoid colectomy [2] Specific technical skills global ratings
1
2
3
4
5
Access and port insertion
Created clumsy and with difficulty
Created adequately
Created quickly and skillfully
Retraction, dissection, exposure, and mobilization at inferior mesenteric pedicle
Poor retraction, dissection, exposure, and mobilization at inferior mesenteric pedicle, large amount of bleeding
Satisfactory retraction, dissection, exposure, and mobilization at inferior mesenteric pedicle, small amount of bleeding
Expert retraction, dissection, exposure, and mobilization at inferior mesenteric pedicle, minimal amount of bleeding
Clipping and transection of inferior mesenteric artery
Clips not placed accurately, large amount of bleeding
Clips placed proximally and distally adequately, minimal bleeding
Clips placed expertly, proximally and distally, with adequate length, no bleeding
Mobilize colon along Toldt’s fascia on left side of colon
Poor mobilization
Satisfactory mobilization
Expert mobilization
Identify left ureter
Left ureter not identified or transected
Left ureter adequately identified
Left ureter clearly identified
Transection of colon
Clumsily done
Adequately done
Expertly and smoothly done
Extraction of colonic specimen
Clumsily done
Adequately done with little trauma
Smoothly done with minimal trauma
Colonic anastomosis
Clumsily done, with discrepancy in blood supply
Adequately done with little trauma, good blood supply
Expertly and smoothly done, good blood supply
over 300 laparoscopic colectomies analyzed all DVDs. The examiners were blinded to the surgeons’ identities. The examiners used the instrument for surgical performance evaluation validated by Sarker et al. [2]. for assessment of generic and specific technical skills during a laparoscopic sigmoid colectomy. This instrument was used after free English to Portuguese translation and adapted to sigmoid colectomy in the swine model. Regarding generic skills, score results ranged from 7 to 35 (Table 1); and from
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8 to 40 for specific skills (Table 2). For control and study groups, a mean value for generic and specific skills was obtained. These values were compared. Since operating time did not represent an evaluation parameter, according to Sarker’s [2] instrument, time until completion of the colectomy in the animal model was not recorded in the present study. Regarding data analysis and study outcomes, the primary outcome measure was performance quality during
Surg Endosc Table 3 Results of generic and specific skills score [2] for control and study group during a laparoscopic sigmoid resection in the swine according to two evaluators Generic technical skills score results
Control group (N = 7) Mean (range)
Study group (N = 7) Mean (range)
Handling and dissection of tissues
2.5 (2–3)
3 (2–4)
Dexterity
2.1 (2–4)
3 (2–4)
Instrument and material handling
2.3 (2–3)
2.8 (2–4)
Use of instruments and material
2.5 (2–3)
2.5 (2–4)
Exposure of technical field
2.5 (2–4)
2.8 (3–4)
Hemostasis
2.8 (3–4)
3 (3–4)
Completion and flow of tasks and subtasks
2.5 (2–4)
3 (2–4)
Generic technical skills score
17.2 (16.5–18)
20.1 (16.5–22)
Access and port insertion
2.4 (2–4)
3 (3–4)
Retraction, dissection, exposure, and mobilization at inferior mesenteric pedicle
2.3 (2–5)
2.8 (1–4)
Clipping and transection of inferior mesenteric artery
2.7 (2–4)
3.4 (3–4)
mobilize colon along Toldt’s fascia on left side of colon
2.4 (2–4)
3 (2–4)
Identify left ureter
2.7 (2–4)
2.8 (2–4)
Transection of colon
2.3 (2–4)
3.5 (3–5)
Extraction of colonic specimen
2.7 (2–4)
2.8 (2–4)
Colonic anastomosis
2.7 (2–4)
2.9 (2–4)
Specific technical skills score
20.2 (19–21.5)
24.2 (21–27.5)
a
p
Fig. 2 Mean and standard deviation values for generic and specific skills scores in control and study groups 0.002a
0.001a
Student’s t test
colectomy in the swine model according to (1) the generic and (2) the specific skills score. The Student’s t test was used to compare mean score values. Kendall’s coefficient of concordance (W) statistic was used to ensure reliability of the video-based assessment scores between the two expert surgeons (VES and ARI). A value of p \ 0.05 was considered statistically significant.
Fig. 3 Distribution of 28 scores of generic and specific skills during a laparoscopic sigmoid colectomy in the swine model according to study group
was 20.1 (16.5–22)—p = 0.002 (Student’s t test). Regarding specific skills, the mean score was 20.2 (19–21.5) in the control group and 24.2 (21–27.5) in the study group (p = 0.001—Student’s t test). These results are evinced in Table 3 and depicted in Figs. 2 and 3. The mean values of Kendall’s coefficient of concordance (W) for the video assessment conducted by the two expert examiners were 0.78 for generic skills, and 0.84 for specific skills. These results indicate that the reliability of the video-based assessment was acceptable (W [ 0.75).
Results Discussion All participating surgeons completed the study. In each group, there was one female surgeon. All surgeons were right-handed. Data from video recordings were available for all 14 participating surgeons. In the control group, the mean score for generic skills was 17.2 (16.5–18). In the study group, it
Minimally invasive surgery requires specific psychomotor capabilities. These capabilities may be acquired through training [24]. We hypothesized that a short-duration (warm-up) skills training in a VR simulator could positively impact the performance of surgeons not experienced
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in laparoscopic colorectal surgery during a laparoscopic colectomy in the swine model. In the present randomized study, it was demonstrated that a pre-procedural warm-up in a VR simulator improves the performance of novice surgeons conducting a laparoscopic colectomy in the swine model. Although the current study has not demonstrated transference of laparoscopic skills into the real clinical setting, it was the first study to demonstrate the impact of a warm-up for minimally invasive colorectal surgery. Current evidence regarding skills transfer during laparoscopic surgery after a pre-procedural warm-up remains restricted to two main findings. First, brief warm-up laparoscopic exercises conducted in VR simulators improved laparoscopic skills verified on a simulator task [21, 25]. Therefore, this finding generated limited evidence whether a positive warm-up effect could be moved to patients in the real clinical setting. The second category of findings represents the rationale for the present study. Calatayud et al. [20] and Moldovanu et al. [22] have demonstrated a significant beneficial impact of warming-up in a VR simulator on laparoscopic performance during cholecystectomies in the OR. Lee et al. [26] observed that cognitive and psychomotor performed skills were significantly better after a preoperative warm-up using box trainer and VR simulation for surgeons serving as their controls and scheduled to perform clinical laparoscopic renal surgery. The extent to which these findings [20, 22, 24] can be generalized to other procedures remains unknown. Regarding the study design, two limitations of the present study are related to the research subjects. First, the study may be underpowered due to a small sample size. Availability of research subjects of presumably the same skills level was the first impediment factor. Moreover, although highly desirable, a multicenter study could not be accomplished using the proposed methodology. Unavailability of the VR simulators for a multi-institutional trial was the second impediment factor. As result, conclusions may be of limited clinical value. Second, although all included surgeons were first-year residents of digestive tract surgery at the same University hospital, there could have been baseline differences in the level of overall surgical proficiency among the individuals. Therefore, it would have been ideal for each resident to perform a pre-intervention colectomy followed by a postintervention procedure. Therefore, research subjects would serve as their own controls. However, the use of live animals precludes the use of this design in our institution. Another interesting approach would be to obtain a preintervention performance of all the residents by measuring baseline scores on the VR simulator. Ultimately, It is possible that, in the present study, randomization may have helped reducing variable skills levels among research subjects.
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Instead of using a combination of tasks of the basic module of the VR simulator, we chose, after a short briefing about how the simulator works, to warm-up the surgeons in the sigmoid colectomy module. It was our intention to train the naı¨ve surgeons in the steps they should be following during the colectomy in the animal model. Although the swine is less reliable for the laparoscopic colectomy education than the cadaver model [18], training in the live animal model requires the trainee surgeon to simulate OR environment, to follow the flow of predetermined tasks and to manage commonly used equipment and instrumentals specific to laparoscopic colectomy. Evaluation of surgical performance is cumbersome. Several tools have been used in published research studies, although none has been taken up for broad use in technical skills assessments. Moreover, the clinical significance of a measured difference in scores between two or more surgeons of after an educational intervention remains challenging to be addressed. Laparoscopic colorectal surgery is a relatively new specialty. Sarker et al. [27]. have studied hierarchical task analysis to identify key steps during operations to construct Likert scales for generic and specific technical skills assessment. After evaluating 84 live real operations conducted by six consultants and eight trainees using a specific tool [2], they observed that all consultants performed better in both generic and specific technical skills when compared to their trainees. Therefore, it was demonstrated that the proposed assessment tool of generic and specific technical skills in advanced laparoscopic colorectal surgery was reliable. It was our belief that using the instrument validated by this group [2] would be the most accurate way to assess generic and specific skills during a laparoscopic colectomy, even if performed in the swine model. As far as we can ascertain, this study was the first to do so. Moreover, similarly to other studies in the literature, we used two independent observers [20, 22, 26]. It was demonstrated in this study that a short-duration (warm-up) VR simulator training led to improved performance of generic and specific skills during a laparoscopic colectomy in the animal model. These data should be interpreted with caution, especially regarding the potential benefits of warming-up for surgeons more experienced than the research subjects in the present study. Further studies should include more surgeons with different degrees of experience in laparoscopic colorectal surgery. Moreover, clinical tutoring may play a role in the surgical education of non-beginner surgeons to accomplish technical and nontechnical skills transfer. There might be two plausible explanations to the main finding of the present study. First, in most studies, VR simulator practice consisted of tasks repetitions performed in the basic module [20, 21]. In contrast, in this study, the
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warm-up was conducted in the advanced module (laparoscopic sigmoid resection). Second, generic and specific skills may require different time intervals to be incorporated. Generic skills perhaps require more time and are acquired throughout training, for example, during an entire medical residency in surgery [2]. On the other hand, specific skills, although technically sophisticated, are required for the completion of one particular procedure, therefore, requiring less time and effort to be achieved. In the present study, the difference for generic skills mean scores between the groups was slightly lower than that observed for specific skills. These data suggest that training one specific operation in the VR simulator, even for a short interval of time, may enable the trainee surgeon to perform that task more effectively. On the other hand, the impact of a warmup on the set of generic skills is perchance least. The present randomized single-blinded study raises important evidence about the role of VR simulator training for skills transfer in laparoscopic colorectal surgery. However, determining the timing and extent to which this practice should be implemented in the surgical curriculum remains a challenge to be addressed by future research. Although no other studies have tested the concept of warming-up in the real clinical setting of minimally invasive colectomy, the present evidence may shed light on the role of VR simulation training for the education of surgeons involved in the minimally invasive treatment of colorectal diseases.
Disclosures Drs. Sergio Eduardo Alonso Araujo, Conor Patrick Delaney, Victor Edmond Seid, Antonio Rocco Imperiale, Alexandre Bruno Bertoncini, Sergio Carlos Nahas, and Ivan Cecconello have no conflicts of interest or financial ties to disclose.
References 1. Scott DJ, Cendan JC, Pugh CM, Minter RM, Dunnington GL, Kozar RA (2008) The changing face of surgical education: simulation as the new paradigm. J Surg Res 147:189–193 2. Sarker SK, Kumar I, Delaney C (2010) Assessing operative performance in advanced laparoscopic colorectal surgery. World J Surg 34:1594–1603 3. Larsen CR, Oestergaard J, Ottesen BS, Soerensen JL (2012) The efficacy of virtual reality simulation training in laparoscopy: a systematic review of randomized trials. Acta Obstet Gynecol Scand 91:1015–1028 4. Zendejas B, Brydges R, Hamstra SJ, Cook DA (2013) State of the evidence on simulation-based training for laparoscopic surgery: a systematic review. Ann Surg 257:586–593 5. Satava RM (1993) Virtual reality surgical simulator: the first steps. Surg Endosc 7:203–205 6. Grantcharov TP, Kristiansen VB, Bendix J, Bardram L, Rosenberg J, Funch-Jensen P (2004) Randomized clinical trial of virtual reality simulation for laparoscopic skills training. Br J Surg 91:146–150
7. Gallagher AG, Seymour NE, Jordan-Black J-A, Bunting BP, McGlade K, Satava RM (2013) Prospective, randomized assessment of transfer of training (ToT) and transfer effectiveness ratio (TER) of virtual reality simulation training for laparoscopic skill acquisition. Ann Surg 257:1025–1031 8. Torkington J, Smith SG, Rees BI, Darzi A (2001) Skill transfer from virtual reality to a real laparoscopic task. Surg Endosc 15:1076–1079 9. Seymour NE, Gallagher AG, Roman SA, O’Brien MK, Bansal VK, Andersen DK, Stava RM (2002) Virtual reality training improves operating room performance: results of a randomized, double-blinded study. Ann Surg 236:458–463 10. Andreatta PB, Woodrum DT, Birkmeyer JD, Yellamanchilli RK, Doherty GM, Gauger PG, Minter RM (2006) Laparoscopic skills are improved with LapMentor training: results of a randomized, double-blinded study. Ann Surg 243:854–860 11. Ahlberg G, Enochsson L, Gallagher AG, Hedman L, Hogman C, McClusky DA 3rd, Ramel S, Smith CD, Arvidsson D (2007) Proficiency-based virtual reality training significantly reduces the error rate for residents during their first 10 laparoscopic cholecystectomies. Am J Surg 193:797–804 12. Colon Cancer Laparoscopic or Open Resection Study Group, Buunen M, Veldkamp R, Hop WCJ, Kuhry E, Jeekel J, Haglind E, Pa˚hlman L, Cuesta MA, Msika S, Morino M, Lacy A, Bonjer HJ (2009) Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol 10:44–52 13. Lacy AM, Delgado S, Castells A, Prins HA, Arroyo V, Ibarzabal A, Pique JM (2008) The long-term results of a randomized clinical trial of laparoscopy-assisted versus open surgery for colon cancer. Ann Surg 248:1–7 14. Fleshman J, Sargent DJ, Green E, Anvari M, Stryker SJ, Beart RW Jr, Hellinger M, Flanagan R Jr, Peters W, Nelson H (2007) Laparoscopic colectomy for cancer is not inferior to open surgery based on 5-year data from the COST Study Group trial. Ann Surg 246:655–662 15. Jayne DG, Guillou PJ, Thorpe H, Quirke P, Copeland J, Smith AMH, Heath RM, Brown JM (2007) Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial Group. J Clin Oncol 25:3061–3068 16. Bardakcioglu O, Khan A, Aldridge C, Chen J (2013) Growth of laparoscopic colectomy in the United States: analysis of regional and socioeconomic factors over time. Ann Surg 258:270–274 17. Kemp JA, Finlayson SRG (2008) Nationwide trends in laparoscopic colectomy from 2000 to 2004. Surg Endosc 22(5):1181–1187 18. Miskovic D, Wyles SM, Ni M, Darzi AW, Hanna GB (2010) Systematic review on mentoring and simulation in laparoscopic colorectal surgery. Ann Surg 252:943–951 19. LeBlanc F, Champagne BJ, Augestad KM, Neary PC, Senagore AJ, Ellis CN, Delaney CP (2010) A comparison of human cadaver and augmented reality simulator models for straight laparoscopic colorectal skills acquisition training. J Am Coll Surg 211:250–255 20. Calatayud D, Arora S, Aggarwal R, Kruglikova I, Schulze S, Funch-Jensen P, Grantcharov T (2010) Warm-up in a virtual reality environment improves performance in the operating room. Ann Surg 251:1181–1185 21. Kahol K, Satava RM, Ferrara J, Smith ML (2009) Effect of shortterm pretrial practice on surgical proficiency in simulated environments: a randomized trial of the ‘‘preoperative warm-up’’ effect. J Am Coll Surg 208:255–268 22. Moldovanu R, Taˆrcoveanu E, Dimofte G, Lupas¸ cu C, Bradea C (2011) Preoperative warm-up using a virtual reality simulator. JSLS 15:533–538 23. Schulz KF, Altman DG, Moher D (2010) CONSORT Group CONSORT 2010 statement: updated guidelines for reporting parallel group randomized trials. Ann Intern Med 152:726–732
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Surg Endosc 24. Aggarwal R, Grantcharov T, Moorthy K, Hance J, Darzi A (2006) A competency-based virtual reality training curriculum for the acquisition of laparoscopic psychomotor skill. Am J Surg 191:128–133 25. Do AT, Cabbad MF, Kerr A, Serur E, Robertazzi RR, Stankovic MR (2006) A warm-up laparoscopic exercise improves the subsequent laparoscopic performance of Ob-Gyn residents: a lowcost laparoscopic trainer. JSLS 10:297–301
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26. Lee JY, Mucksavage P, Kerbl DC, Osann KE, Winfield HN, Kahol K, McDougall EM (2012) Laparoscopic warm-up exercises improve performance of senior-level trainees during laparoscopic renal surgery. J Endourol Endourol Soc 26:545–550 27. Sarker SK, Chang A, Vincent C, Darzi SA (2006) Development of assessing generic and specific technical skills in laparoscopic surgery. Am J Surg 191:238–244
